Neuroscience in peripheral cancers: tumors hijacking nerves and neuroimmune crosstalk

Hua-Yang Fan , Xin-Hua Liang , Ya-Ling Tang

MedComm ›› 2024, Vol. 5 ›› Issue (11) : e784

PDF
MedComm ›› 2024, Vol. 5 ›› Issue (11) : e784 DOI: 10.1002/mco2.784
REVIEW

Neuroscience in peripheral cancers: tumors hijacking nerves and neuroimmune crosstalk

Author information +
History +
PDF

Abstract

Cancer neuroscience is an emerging field that investigates the intricate relationship between the nervous system and cancer, gaining increasing recognition for its importance. The central nervous system governs the development of the nervous system and directly affects brain tumors, and the peripheral nervous system (PNS) shapes the tumor microenvironment (TME) of peripheral tumors. Both systems are crucial in cancer initiation and progression, with recent studies revealing a more intricate role of the PNS within the TME. Tumors not only invade nerves but also persuade them through remodeling to further promote malignancy, creating a bidirectional interaction between nerves and cancers. Notably, immune cells also contribute to this communication, forming a triangular relationship that influences protumor inflammation and the effectiveness of immunotherapy. This review delves into the intricate mechanisms connecting the PNS and tumors, focusing on how various immune cell types influence nerve–tumor interactions, emphasizing the clinical relevance of nerve–tumor and nerve–immune dynamics. By deepening our understanding of the interplay between nerves, cancer, and immune cells, this review has the potential to reshape tumor biology insights, inspire innovative therapies, and improve clinical outcomes for cancer patients.

Keywords

cancer neuroscience / cancer therapy / neuroimmune crosstalk / peripheral nervous system / tumor microenvironment / tumor–nerve interactions

Cite this article

Download citation ▾
Hua-Yang Fan, Xin-Hua Liang, Ya-Ling Tang. Neuroscience in peripheral cancers: tumors hijacking nerves and neuroimmune crosstalk. MedComm, 2024, 5(11): e784 DOI:10.1002/mco2.784

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Mancusi R, Monje M. The neuroscience of cancer. Nature. 2023; 618(7965): 467-479.

[2]

Hanahan D, Monje M. Cancer hallmarks intersect with neuroscience in the tumor microenvironment. Cancer Cell. 2023; 41(3): 573-580.

[3]

Winkler F, Venkatesh HS, Amit M, et al. Cancer neuroscience: state of the field, emerging directions. Cell. 2023; 186(8): 1689-1707.

[4]

Wu J, Heidelberg RE, Gajjar A. Adolescents and young adults with cancer: CNS tumors. J Clin Oncol. 2024; 42(6): 686-695.

[5]

Magnon C, Hondermarck H. The neural addiction of cancer. Nat Rev Cancer. 2023; 23(5): 317-334.

[6]

Segarra M, Aburto MR, Hefendehl J, Acker-Palmer A. Neurovascular interactions in the nervous system. Annu Rev Cell Dev Biol. 2019; 35: 615-635.

[7]

Liu Q, Ma Z, Cao Q, et al. Perineural invasion-associated biomarkers for tumor development. Biomed Pharmacother. 2022; 155: 113691.

[8]

Schmitd LB, Beesley LJ, Russo N, et al. Redefining perineural invasion: integration of biology with clinical outcome. Neoplasia. 2018; 20(7): 657-667.

[9]

Ayala GE, Dai H, Powell M, et al. Cancer-related axonogenesis and neurogenesis in prostate cancer. Clin Cancer Res. 2008; 14(23): 7593-7603.

[10]

Albo D, Akay CL, Marshall CL, et al. Neurogenesis in colorectal cancer is a marker of aggressive tumor behavior and poor outcomes. Cancer. 2011; 117(21): 4834-4845.

[11]

Park H, Lee CH. The contribution of the nervous system in the cancer progression. BMB Rep. 2024; 57(4): 167-175.

[12]

Pundavela J, Roselli S, Faulkner S, et al. Nerve fibers infiltrate the tumor microenvironment and are associated with nerve growth factor production and lymph node invasion in breast cancer. Mol Oncol. 2015; 9(8): 1626-1635.

[13]

Griffin N, Faulkner S, Jobling P, Hondermarck H. Targeting neurotrophin signaling in cancer: the renaissance. Pharmacol Res. 2018; 135: 12-17.

[14]

Hung YH, Hou YC, Hsu SH, et al. Pancreatic cancer cell-derived semaphorin 3A promotes neuron recruitment to accelerate tumor growth and dissemination. Am J Cancer Res. 2023; 13(8): 3417-3432.

[15]

Hu J, Chen W, Shen L, Chen Z, Huang J. Crosstalk between the peripheral nervous system and breast cancer influences tumor progression. Biochim Biophys Acta Rev Cancer. 2022; 1877(6): 188828.

[16]

Hernandez S, Serrano AG. The role of nerve fibers in the tumor immune microenvironment of solid tumors. Adv Biol. 2022; 6(9): e2200046.

[17]

Khanmammadova N, Islam S, Sharma P, Amit M. Neuro-immune interactions and immuno-oncology. Trends Cancer. 2023; 9(8): 636-649.

[18]

Lyu Y, Xie F, Chen B, et al. The nerve cells in gastrointestinal cancers: from molecular mechanisms to clinical intervention. Oncogene. 2024; 43(2): 77-91.

[19]

Han J, Jiang Q, Ma R, et al. Norepinephrine-CREB1-miR-373 axis promotes progression of colon cancer. Mol Oncol. 2020; 14(5): 1059-1073.

[20]

He B, Gao R, Lv S, et al. Cancer cell employs a microenvironmental neural signal trans-activating nucleus-mitochondria coordination to acquire stemness. Signal Transduct Target Ther. 2023; 8(1): 275.

[21]

Hayakawa Y, Sakitani K, Konishi M, et al. Nerve growth factor promotes gastric tumorigenesis through aberrant cholinergic signaling. Cancer Cell. 2017; 31(1): 21-34.

[22]

Fu Y, Shen K, Wang H, et al. Alpha5 nicotine acetylcholine receptor subunit promotes intrahepatic cholangiocarcinoma metastasis. Signal Transduct Target Ther. 2024; 9(1): 63.

[23]

Montoya A, Varela-Ramirez A, Dickerson E, et al. The beta adrenergic receptor antagonist propranolol alters mitogenic and apoptotic signaling in late stage breast cancer. Biomed J. 2019; 42(3): 155-165.

[24]

Satilmis H, Verheye E, Vlummens P, et al. Targeting the β(2) - adrenergic receptor increases chemosensitivity in multiple myeloma by induction of apoptosis and modulating cancer cell metabolism. J Pathol. 2023; 259(1): 69-80.

[25]

Nuevo-Tapioles C, Santacatterina F, Stamatakis K, et al. Coordinate β-adrenergic inhibition of mitochondrial activity and angiogenesis arrest tumor growth. Nat Commun. 2020; 11(1): 3606.

[26]

Kang Y, Nagaraja AS, Armaiz-Pena GN, et al. Adrenergic stimulation of DUSP1 impairs chemotherapy response in ovarian cancer. Clin Cancer Res. 2016; 22(7): 1713-1724.

[27]

Eng JW, Reed CB, Kokolus KM, et al. Housing temperature-induced stress drives therapeutic resistance in murine tumour models through β2-adrenergic receptor activation. Nat Commun. 2015; 6: 6426.

[28]

Ray R, Al Khashali H, Haddad B, et al. Regulation of cisplatin resistance in lung cancer cells by nicotine, BDNF, and a β-adrenergic receptor blocker. Int J Mol Sci. 2022; 23(21): 12829.

[29]

Globig AM, Zhao S, Roginsky J, et al. The β(1)-adrenergic receptor links sympathetic nerves to T cell exhaustion. Nature. 2023; 622(7982): 383-392.

[30]

Fjæstad KY, Rømer AMA, Goitea V, et al. Blockade of beta-adrenergic receptors reduces cancer growth and enhances the response to anti-CTLA4 therapy by modulating the tumor microenvironment. Oncogene. 2022; 41(9): 1364-1375.

[31]

Chang A, Botteri E, Gillis RD, et al. Beta-blockade enhances anthracycline control of metastasis in triple-negative breast cancer. Sci Transl Med. 2023; 15(693): eadf1147.

[32]

Kraboth Z, Kalman B. ß-Adrenoreceptors in human cancers. Int J Mol Sci. 2023; 24(4): 3671.

[33]

Massalee R, Cao X. Repurposing beta-blockers for combinatory cancer treatment: effects on conventional and immune therapies. Front Pharmacol. 2023; 14: 1325050.

[34]

Nilsson MB, Le X, Heymach JV. β-Adrenergic signaling in lung cancer: a potential role for beta-blockers. J Neuroimmune Pharmacol. 2020; 15(1): 27-36.

[35]

Nie M, Chen N, Pang H, et al. Targeting acetylcholine signaling modulates persistent drug tolerance in EGFR-mutant lung cancer and impedes tumor relapse. J Clin Invest. 2022; 132(20): e160152.

[36]

Kuol N, Davidson M, Karakkat J, et al. Blocking muscarinic receptor 3 attenuates tumor growth and decreases immunosuppressive and cholinergic markers in an orthotopic mouse model of colorectal cancer. Int J Mol Sci. 2022; 24(1): 596.

[37]

Wen YC, Tram VTN, Chen WH, et al. CHRM4/AKT/MYCN upregulates interferon alpha-17 in the tumor microenvironment to promote neuroendocrine differentiation of prostate cancer. Cell Death Dis. 2023; 14(5): 304.

[38]

Gandhi S, Pandey MR, Attwood K, et al. Phase I clinical trial of combination propranolol and pembrolizumab in locally advanced and metastatic melanoma: safety, tolerability, and preliminary evidence of antitumor activity. Clin Cancer Res. 2021; 27(1): 87-95.

[39]

Filippi L, Bruno G, Domazetovic V, Favre C, Calvani M. Current therapies and new targets to fight melanoma: a promising role for the β3-adrenoreceptor. Cancers (Basel). 2020; 12(6): 1415.

[40]

Li W, Wan J, Chen C, et al. Dissecting the role of cell signaling versus CD8(+) T cell modulation in propranolol antitumor activity. J Mol Med. 2022; 100(9): 1299-1306.

[41]

Ferraguti G, Terracina S, Tarani L, et al. Nerve growth factor and the role of inflammation in tumor development. Curr Issues Mol Biol. 2024; 46(2): 965-989.

[42]

Gasparini G, Pellegatta M, Crippa S, et al. Nerves and pancreatic cancer: new insights into a dangerous relationship. Cancers (Basel). 2019; 11(7): 893.

[43]

Romon R, Adriaenssens E, Lagadec C, Germain E, Hondermarck H, Le Bourhis X. Nerve growth factor promotes breast cancer angiogenesis by activating multiple pathways. Mol Cancer. 2010; 9: 157.

[44]

Renz BW, Takahashi R, Tanaka T, et al. β2 adrenergic-neurotrophin feedforward loop promotes pancreatic cancer. Cancer Cell. 2018; 33(1): 75-90.

[45]

Simó M, Navarro X, Yuste VJ, Bruna J. Autonomic nervous system and cancer. Clin Auton Res. 2018; 28(3): 301-314.

[46]

Zahalka AH, Frenette PS. Nerves in cancer. Nat Rev Cancer. 2020; 20(3): 143-157.

[47]

Kamiya A, Hiyama T, Fujimura A, Yoshikawa S. Sympathetic and parasympathetic innervation in cancer: therapeutic implications. Clin Auton Res. 2021; 31(2): 165-178.

[48]

Cui Q, Jiang D, Zhang Y, Chen C. The tumor–nerve circuit in breast cancer. Cancer Metastasis Rev. 2023; 42(2): 543-574.

[49]

Erin N, Akman M, Aliyev E, Tanrıöver G, Korcum AF. Olvanil activates sensory nerve fibers, increases T cell response and decreases metastasis of breast carcinoma. Life Sci. 2022; 291: 120305.

[50]

Darragh LB, Nguyen A, Pham TT, et al. Sensory nerve release of CGRP increases tumor growth in HNSCC by suppressing TILs. Med. 2024; 5(3): 254-270.

[51]

Holland AM, Bon-Frauches AC, Keszthelyi D, Melotte V, Boesmans W. The enteric nervous system in gastrointestinal disease etiology. Cell Mol Life Sci. 2021; 78(10): 4713-4733.

[52]

Vaes N, Schonkeren SL, Rademakers G, et al. Loss of enteric neuronal Ndrg4 promotes colorectal cancer via increased release of Nid1 and Fbln2. EMBO Rep. 2021; 22(6): e51913.

[53]

Zhao CM, Hayakawa Y, Kodama Y, et al. Denervation suppresses gastric tumorigenesis. Sci Transl Med. 2014; 6(250): 250ra115.

[54]

Amit M, Takahashi H, Dragomir MP, et al. Loss of p53 drives neuron reprogramming in head and neck cancer. Nature. 2020; 578(7795): 449-454.

[55]

Perez-Pacheco C, Schmitd LB, Furgal A, et al. Increased nerve density adversely affects outcome in oral cancer. Clin Cancer Res. 2023; 29(13): 2501-2512.

[56]

Hojman P, Gehl J, Christensen JF, Pedersen BK. Molecular mechanisms linking exercise to cancer prevention and treatment. Cell Metab. 2018; 27(1): 10-21.

[57]

Kurz E, Hirsch CA, Dalton T, et al. Exercise-induced engagement of the IL-15/IL-15Rα axis promotes anti-tumor immunity in pancreatic cancer. Cancer Cell. 2022; 40(7): 720-737.

[58]

Wei Y, Liang Y, Lin H, Dai Y, Yao S. Autonomic nervous system and inflammation interaction in endometriosis-associated pain. J Neuroinflammation. 2020; 17(1): 80.

[59]

Eichmann A, Brunet I. Arterial innervation in development and disease. Sci Transl Med. 2014; 6(252): 252ps9.

[60]

Willems JL, Buylaert WA, Lefebvre RA, Bogaert MG. Neuronal dopamine receptors on autonomic ganglia and sympathetic nerves and dopamine receptors in the gastrointestinal system. Pharmacol Rev. 1985; 37(2): 165-216.

[61]

Scott-Solomon E, Boehm E, Kuruvilla R. The sympathetic nervous system in development and disease. Nat Rev Neurosci. 2021; 22(11): 685-702.

[62]

McEwen BS. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev. 2007; 87(3): 873-904.

[63]

Gibbons CH. Basics of autonomic nervous system function. Handb Clin Neurol. 2019; 160: 407-418.

[64]

VanPatten S, Al-Abed Y. The challenges of modulating the ‘rest and digest’ system: acetylcholine receptors as drug targets. Drug Discov Today. 2017; 22(1): 97-104.

[65]

Cole SW, Nagaraja AS, Lutgendorf SK, Green PA, Sood AK. Sympathetic nervous system regulation of the tumour microenvironment. Nat Rev Cancer. 2015; 15(9): 563-572.

[66]

Maestroni GJM. Adrenergic modulation of hematopoiesis. J Neuroimmune Pharmacol. 2020; 15(1): 82-92.

[67]

Insel PA. Structure and function of alpha-adrenergic receptors. Am J Med. 1989; 87(2): 12s-18s.

[68]

Sofuoglu M, Mooney M. Cholinergic functioning in stimulant addiction: implications for medications development. CNS Drugs. 2009; 23(11): 939-952.

[69]

Kolmus K, Tavernier J, Gerlo S. β2-Adrenergic receptors in immunity and inflammation: stressing NF-κB. Brain Behav Immun. 2015; 45: 297-310.

[70]

Simpson RJ, Boßlau TK, Weyh C, et al. Exercise and adrenergic regulation of immunity. Brain Behav Immun. 2021; 97: 303-318.

[71]

Halder N, Lal G. Cholinergic system and its therapeutic importance in inflammation and autoimmunity. Front Immunol. 2021; 12: 660342.

[72]

Dhawan S, Cailotto C, Harthoorn LF, de Jonge WJ. Cholinergic signalling in gut immunity. Life Sci. 2012; 91(21-22): 1038-1042.

[73]

Shah N, Khurana S, Cheng K, Raufman JP. Muscarinic receptors and ligands in cancer. Am J Physiol Cell Physiol. 2009; 296(2): C221-C232.

[74]

Jensen AWP, Carnaz Simões AM, Thor Straten P, Holmen Olofsson G. Adrenergic signaling in immunotherapy of cancer: friend or foe? Cancers (Basel). 2021; 13(3): 394.

[75]

Farooq MA, Ajmal I, Hui X, Chen Y, Ren Y, Jiang W. β2-Adrenergic receptor mediated inhibition of T cell function and its implications for CAR-T cell therapy. Int J Mol Sci. 2023; 24(16): 12837.

[76]

Li XQ, Peng WT, Shan S, et al. β-Arrestin2 regulating β2-adrenergic receptor signaling in hepatic stellate cells contributes to hepatocellular carcinoma progression. J Cancer. 2021; 12(24): 7287-7299.

[77]

Palm D, Lang K, Niggemann B, et al. The norepinephrine-driven metastasis development of PC-3 human prostate cancer cells in BALB/c nude mice is inhibited by beta-blockers. Int J Cancer. 2006; 118(11): 2744-2749.

[78]

Zhi X, Li B, Li Z, et al. Adrenergic modulation of AMPK-dependent autophagy by chronic stress enhances cell proliferation and survival in gastric cancer. Int J Oncol. 2019; 54(5): 1625-1638.

[79]

Zhang X, Zhang Y, He Z, et al. Chronic stress promotes gastric cancer progression and metastasis: an essential role for ADRB2. Cell Death Dis. 2019; 10(11): 788.

[80]

Liu H, Wang C, Xie N, et al. Activation of adrenergic receptor β2 promotes tumor progression and epithelial mesenchymal transition in tongue squamous cell carcinoma. Int J Mol Med. 2018; 41(1): 147-154.

[81]

Nagaraja AS, Dorniak PL, Sadaoui NC, et al. Sustained adrenergic signaling leads to increased metastasis in ovarian cancer via increased PGE2 synthesis. Oncogene. 2016; 35(18): 2390-2397.

[82]

Moretti S, Massi D, Farini V, et al. β-Adrenoceptors are upregulated in human melanoma and their activation releases pro-tumorigenic cytokines and metalloproteases in melanoma cell lines. Lab Invest. 2013; 93(3): 279-290.

[83]

Liu J, Qu L, Wan C, et al. A novel β2-AR/YB-1/β-catenin axis mediates chronic stress-associated metastasis in hepatocellular carcinoma. Oncogenesis. 2020; 9(9): 84.

[84]

Reavis HD, Gysler SM, McKenney GB, et al. Norepinephrine induces anoikis resistance in high-grade serous ovarian cancer precursor cells. JCI Insight. 2024; 9(5): e170961.

[85]

Madden KS, Szpunar MJ, Brown EB. β-Adrenergic receptors (β-AR) regulate VEGF and IL-6 production by divergent pathways in high β-AR-expressing breast cancer cell lines. Breast Cancer Res Treat. 2011; 130(3): 747-758.

[86]

Qin JF, Jin FJ, Li N, et al. Adrenergic receptor β2 activation by stress promotes breast cancer progression through macrophages M2 polarization in tumor microenvironment. BMB Rep. 2015; 48(5): 295-300.

[87]

Caulfield MP. Muscarinic receptors–characterization, coupling and function. Pharmacol Ther. 1993; 58(3): 319-379.

[88]

Schaaf CP. Nicotinic acetylcholine receptors in human genetic disease. Genet Med. 2014; 16(9): 649-656.

[89]

Zahalka AH, Arnal-Estapé A, Maryanovich M, et al. Adrenergic nerves activate an angio-metabolic switch in prostate cancer. Science. 2017; 358(6361): 321-326.

[90]

Wang J, Wei J, Pu T, et al. Cholinergic signaling via muscarinic M1 receptor confers resistance to docetaxel in prostate cancer. Cell Rep Med. 2024; 5(2): 101388.

[91]

Lobbes LA, Schütze MA, Droeser R, et al. Muscarinic acetylcholine receptor M3 expression and survival in human colorectal carcinoma—an unexpected correlation to guide future treatment? Int J Mol Sci. 2023; 24(9): 8198.

[92]

Bele T, Turk T, Križaj I. Nicotinic acetylcholine receptors in cancer: limitations and prospects. Biochim Biophys Acta Mol Basis Dis. 2024; 1870(1): 166875.

[93]

Schaal CM, Bora-Singhal N, Kumar DM, Chellappan SP. Regulation of Sox2 and stemness by nicotine and electronic-cigarettes in non-small cell lung cancer. Mol Cancer. 2018; 17(1): 149.

[94]

He Z, Xu Y, Rao Z, et al. The role of α7-nAChR-mediated PI3K/AKT pathway in lung cancer induced by nicotine. Sci Total Environ. 2024; 912: 169604.

[95]

Takahashi R, Ijichi H, Fujishiro M. The role of neural signaling in the pancreatic cancer microenvironment. Cancers (Basel). 2022; 14(17): 4269.

[96]

Dragomir MP, Moisoiu V, Manaila R, et al. A holistic perspective: exosomes shuttle between nerves and immune cells in the tumor microenvironment. J Clin Med. 2020; 9(11): 3529.

[97]

Jennings MR, Munn D, Blazeck J. Immunosuppressive metabolites in tumoral immune evasion: redundancies, clinical efforts, and pathways forward. J Immunother Cancer. 2021; 9(10): e003013.

[98]

Koop LK, Tadi P. Neuroanatomy, sensory nerves. StatPearls. StatPearls Publishing Copyright © 2024, StatPearls Publishing LLC; 2024.

[99]

Leroux A, Roque M, Casas E, et al. The effect of CGRP and SP and the cell signaling dialogue between sensory neurons and endothelial cells. Biol Res. 2024; 57(1): 65.

[100]

Carr R, Frings S. Neuropeptides in sensory signal processing. Cell Tissue Res. 2019; 375(1): 217-225.

[101]

Salio C, Lossi L, Ferrini F, Merighi A. Neuropeptides as synaptic transmitters. Cell Tissue Res. 2006; 326(2): 583-598.

[102]

Mashaghi A, Marmalidou A, Tehrani M, Grace PM, Pothoulakis C, Dana R. Substance P and pain chronicity. Cell Tissue Res. 2016; 73(22): 4249-4264.

[103]

Zieglgänsberger W. Substance P and pain chronicity. Cell Tissue Res. 2019; 375(1): 227-241

[104]

Russo AF, Hay DL. Physiol Rev. 2023; 103(2): 1565-1644.

[105]

Coveñas R, Muñoz M. Cancer progression and substance P. Histol Histopathol. 2014; 29(7): 881-890.

[106]

Padmanaban V, Keller I, Seltzer ES, Ostendorf BN, Kerner Z, Tavazoie SF. Neuronal substance P drives metastasis through an extracellular RNA-TLR7 axis. Nature. 2024; 633(8028): 207-215.

[107]

Yu H, Huang T, Lu WW, Tong L, Chen D. Osteoarthritis pain. Int J Mol Sci. 2022; 23(9): 4642.

[108]

Balood M, Ahmadi M, Eichwald T, et al. Nociceptor neurons affect cancer immunosurveillance. Nature. 2022; 611(7935): 405-412.

[109]

Erin N, Szallasi A. Carcinogenesis and metastasis: focus on TRPV1-positive neurons and immune cells. Biomolecules. 2023; 13(6): 983.

[110]

Szkutnik-Fiedler D. Pharmacokinetics, pharmacodynamics and drug–drug interactions of new anti-migraine drugs-lasmiditan, gepants, and calcitonin-gene-related peptide (CGRP) receptor monoclonal antibodies. Pharmaceutics. 2020; 12(12): 1180.

[111]

Tu NH, Inoue K, Lewis PK, et al. Calcitonin related polypeptide alpha mediates oral cancer pain. Cells. 2023; 12(13): 1675.

[112]

Mardelle U, Bretaud N, Daher C, Feuillet V. From pain to tumor immunity: influence of peripheral sensory neurons in cancer. Front Immunol. 2024; 15: 1335387.

[113]

Peng L, Agogo GO, Guo J, Yan M. Substance P and fibrotic diseases. Neuropeptides. 2019; 76: 101941.

[114]

Wallrapp A, Chiu IM. Neuroimmune interactions in the intestine. Annu Rev Immunol. 2024; 42(1): 489-519.

[115]

Spencer NJ, Hu H. Enteric nervous system: sensory transduction, neural circuits and gastrointestinal motility. Nat Rev Gastroenterol Hepatol. 2020; 17(6): 338-351.

[116]

Niesler B, Kuerten S, Demir IE, Schäfer KH. Disorders of the enteric nervous system—a holistic view. Nat Rev Gastroenterol Hepatol. 2021; 18(6): 393-410.

[117]

Rademakers G, Vaes N, Schonkeren S, Koch A, Sharkey KA, Melotte V. The role of enteric neurons in the development and progression of colorectal cancer. Biochim Biophys Acta Rev Cancer. 2017; 1868(2): 420-434.

[118]

Wang K, Zhao XH, Liu J, Zhang R, Li JP. Nervous system and gastric cancer. Biochim Biophys Acta Rev Cancer. 2020; 1873(1): 188313.

[119]

Schonkeren SL, Thijssen MS, Vaes N, Boesmans W, Melotte V. The emerging role of nerves and glia in colorectal cancer. Cancers (Basel). 2021; 13(1): 152.

[120]

Liebl F, Demir IE, Mayer K, et al. The impact of neural invasion severity in gastrointestinal malignancies: a clinicopathological study. Ann Surg. 2014; 260(5): 900-907. discussion 907-908.

[121]

Schorn S, Demir IE, Haller B, et al. The influence of neural invasion on survival and tumor recurrence in pancreatic ductal adenocarcinoma—a systematic review and meta-analysis. Surg Oncol. 2017; 26(1): 105-115.

[122]

Zauszkiewicz-Pawlak A, Godlewski J, Kwiatkowski P, Kmiec Z. Ultrastructural characteristics of myenteric plexus in patients with colorectal cancer. Folia Histochem Cytobiol. 2017; 55(1): 6-10.

[123]

Ceyhan GO, Demir IE, Altintas B, et al. Neural invasion in pancreatic cancer: a mutual tropism between neurons and cancer cells. Biochem Biophys Res Commun. 2008; 374(3): 442-447.

[124]

Duchalais E, Guilluy C, Nedellec S, et al. Colorectal cancer cells adhere to and migrate along the neurons of the enteric nervous system. Cell Mol Gastroenterol Hepatol. 2018; 5(1): 31-49.

[125]

Deborde S, Omelchenko T, Lyubchik A, et al. Schwann cells induce cancer cell dispersion and invasion. J Clin Invest. 2016; 126(4): 1538-1554.

[126]

Renz BW, Tanaka T, Sunagawa M, et al. Cholinergic signaling via muscarinic receptors directly and indirectly suppresses pancreatic tumorigenesis and cancer stemness. Cancer Discov. 2018; 8(11): 1458-1473.

[127]

Partecke LI, Käding A, Trung DN, et al. Subdiaphragmatic vagotomy promotes tumor growth and reduces survival via TNFα in a murine pancreatic cancer model. Oncotarget. 2017; 8(14): 22501-22512.

[128]

He K, Wang H, Huo R, Jiang SH, Xue J. Schwann cells and enteric glial cells: emerging stars in colorectal cancer. Biochim Biophys Acta Rev Cancer. 2024; 1879(5): 189160.

[129]

Orange ST, Leslie J, Ross M, Mann DA, Wackerhage H. The exercise IL-6 enigma in cancer. Trends Endocrinol Metab. 2023; 34(11): 749-763.

[130]

Koelwyn GJ, Zhuang X, Tammela T, Schietinger A, Jones LW. Exercise and immunometabolic regulation in cancer. Nat Metab. 2020; 2(9): 849-857.

[131]

Goh J, Kirk EA, Lee SX, Ladiges WC. Exercise, physical activity and breast cancer: the role of tumor-associated macrophages. Exerc Immunol Rev. 2012; 18: 158-176.

[132]

Gustafson MP, Wheatley-Guy CM, Rosenthal AC, et al. Exercise and the immune system: taking steps to improve responses to cancer immunotherapy. J Immunother Cancer. 2021; 9(7).

[133]

Wennerberg E, Lhuillier C, Rybstein MD, et al. Exercise reduces immune suppression and breast cancer progression in a preclinical model. Oncotarget. 2020; 11(4): 452-461.

[134]

Gomes-Santos IL, Amoozgar Z, Kumar AS, et al. Exercise training improves tumor control by increasing CD8(+) T-cell infiltration via CXCR3 signaling and sensitizes breast cancer to immune checkpoint blockade. Cancer Immunol Res. 2021; 9(7): 765-778.

[135]

Schnyder S, Handschin C. Skeletal muscle as an endocrine organ: PGC-1α myokines and exercise. Bone. 2015; 80: 115-125.

[136]

Kim S, Kim K. The effects of exercise and conjugated linoleic acid intake on IGF-1 and pro-inflammatory cytokines in atrophied skeletal muscle of rats. Integr Med Res. 2013; 2(4): 166-173.

[137]

Huang KY, Upadhyay G, Ahn Y, et al. Neuronal innervation regulates the secretion of neurotrophic myokines and exosomes from skeletal muscle. Proc Natl Acad Sci U S A. 2024; 121(19): e2313590121.

[138]

Zeng Q, Cheng Y, Zhu Q, et al. The relationship between overexpression of glial cell-derived neurotrophic factor and its RET receptor with progression and prognosis of human pancreatic cancer. J Int Med Res. 2008; 36(4): 656-664.

[139]

Cintrón-Colón AF, Almeida-Alves G, Boynton AM, Spitsbergen JM. GDNF synthesis, signaling, and retrograde transport in motor neurons. Cell Tissue Res. 2020; 382(1): 47-56.

[140]

Kostrzewa RM, Jacobowitz DM. Pharmacological actions of 6-hydroxydopamine. Pharmacol Rev. 1974; 26(3): 199-288.

[141]

Magnon C, Hall SJ, Lin J, et al. Autonomic nerve development contributes to prostate cancer progression. Science. 2013; 341(6142): 1236361.

[142]

Raju B, Haug SR, Ibrahim SO, Heyeraas KJ. Sympathectomy decreases size and invasiveness of tongue cancer in rats. Neuroscience. 2007; 149(3): 715-725.

[143]

Atherton MA, Park S, Horan NL, et al. Sympathetic modulation of tumor necrosis factor alpha-induced nociception in the presence of oral squamous cell carcinoma. Pain. 2023; 164(1): 27-42.

[144]

Szpunar MJ, Belcher EK, Dawes RP, Madden KS. Sympathetic innervation, norepinephrine content, and norepinephrine turnover in orthotopic and spontaneous models of breast cancer. Brain Behav Immun. 2016; 53: 223-233.

[145]

Horvathova L, Padova A, Tillinger A, Osacka J, Bizik J, Mravec B. Sympathectomy reduces tumor weight and affects expression of tumor-related genes in melanoma tissue in the mouse. Stress. 2016; 19(5): 528-534.

[146]

Shiralkar J, Anthony T, McCallum GA, Durand DM. Neural recordings can differentiate between spontaneously metastasizing melanomas and melanomas with low metastatic potential. PLoS One. 2024; 19(2): e0297281.

[147]

Berthoud HR, Neuhuber WL. Functional and chemical anatomy of the afferent vagal system. Auton Neurosci. 2000; 85(1-3): 1-17.

[148]

Erin N, Zhao W, Bylander J, Chase G, Clawson G. Capsaicin-induced inactivation of sensory neurons promotes a more aggressive gene expression phenotype in breast cancer cells. Breast Cancer Res Treat. 2006; 99(3): 351-364.

[149]

Stopczynski RE, Normolle DP, Hartman DJ, et al. Neuroplastic changes occur early in the development of pancreatic ductal adenocarcinoma. Cancer Res. 2014; 74(6): 1718-1727.

[150]

Schwartz ES, Christianson JA, Chen X, et al. Synergistic role of TRPV1 and TRPA1 in pancreatic pain and inflammation. Gastroenterology. 2011; 140(4): 1283-1291.

[151]

Schwartz ES, La JH, Scheff NN, Davis BM, Albers KM, Gebhart GF. TRPV1 and TRPA1 antagonists prevent the transition of acute to chronic inflammation and pain in chronic pancreatitis. J Neurosci. 2013; 33(13): 5603-5611.

[152]

Saloman JL, Albers KM, Li D, et al. Ablation of sensory neurons in a genetic model of pancreatic ductal adenocarcinoma slows initiation and progression of cancer. Proc Natl Acad Sci U S A. 2016; 113(11): 3078-3083.

[153]

Foster SL, Seehus CR, Woolf CJ, Talbot S. Sense and immunity: context-dependent neuro-immune interplay. Front Immunol. 2017; 8: 1463.

[154]

Zhang Y, Lin C, Liu Z, et al. Cancer cells co-opt nociceptive nerves to thrive in nutrient-poor environments and upon nutrient-starvation therapies. Cell Metab. 2022; 34(12): 1999-2017.

[155]

Baral P, Udit S, Chiu IM. Pain and immunity: implications for host defence. Nat Rev Immunol. 2019; 19(7): 433-447.

[156]

Tsuru S, Ito Y, Matsuda H, et al. RAMP1 signaling in immune cells regulates inflammation-associated lymphangiogenesis. Lab Invest. 2020; 100(5): 738-750.

[157]

Vitorakis N, Gargalionis AN, Papavassiliou KA, Adamopoulos C, Papavassiliou AG. Precision targeting strategies in pancreatic cancer: the role of tumor microenvironment. Cancers (Basel). 2024; 16(16): 2876.

[158]

Zhu YH, Zheng JH, Jia QY, et al. Immunosuppression, immune escape, and immunotherapy in pancreatic cancer: focused on the tumor microenvironment. Cell Oncol. 2023; 46(1): 17-48.

[159]

Fan JQ, Wang MF, Chen HL, Shang D, Das JK, Song J. Current advances and outlooks in immunotherapy for pancreatic ductal adenocarcinoma. Mol Cancer. 2020; 19(1): 32.

[160]

Liu Y, Tian S, Ning B, Huang T, Li Y, Wei Y. Stress and cancer: the mechanisms of immune dysregulation and management. Front Immunol. 2022; 13: 1032294.

[161]

Machelska H, Celik M. Immune cell-mediated opioid analgesia. Immunol Lett. 2020; 227: 48-59.

[162]

Gysler SM, Drapkin R. Tumor innervation: peripheral nerves take control of the tumor microenvironment. J Clin Invest. 2021; 131(11): e147276.

[163]

Heine M, Heck J, Ciuraszkiewicz A, Bikbaev A. Dynamic compartmentalization of calcium channel signalling in neurons. Neuropharmacology. 2020; 169: 107556.

[164]

Prevarskaya N, Skryma R, Shuba Y. Ion channels in cancer: are cancer hallmarks oncochannelopathies? Physiol Rev. 2018; 98(2): 559-621.

[165]

Fan JJ, Huang X. Ion channels in cancer: orchestrators of electrical signaling and cellular crosstalk. Rev Physiol Biochem Pharmacol. 2022; 183: 103-133.

[166]

Kondratskyi A, Kondratska K, Skryma R, Prevarskaya N. Ion channels in the regulation of apoptosis. Biochim Biophys Acta. 2015; 1848(pt B): 2532-2546.

[167]

Anderson KJ, Cormier RT, Scott PM. Role of ion channels in gastrointestinal cancer. World J Gastroenterol. 2019; 25(38): 5732-5772.

[168]

Liu H, Weng J, Huang CL, Jackson AP. Voltage-gated sodium channels in cancers. Biomark Res. 2024; 12(1): 70.

[169]

Giammello F, Biella C, Priori EC, et al. Modulating voltage-gated sodium channels to enhance differentiation and sensitize glioblastoma cells to chemotherapy. Cell Commun Signal. 2024; 22(1): 434.

[170]

Li RQ, Zhao XH, Zhu Q, et al. Exploring neurotransmitters and their receptors for breast cancer prevention and treatment. Theranostics. 2023; 13(3): 1109-1129.

[171]

Erin N, Shurin GV, Baraldi JH, Shurin MR. Regulation of carcinogenesis by sensory neurons and neuromediators. Cancers (Basel). 2022; 14(9): 2333.

[172]

Li D, Hu LN, Zheng SM, et al. High nerve density in breast cancer is associated with poor patient outcome. FASEB Bioadv. 2022; 4(6): 391-401.

[173]

Schmitd LB, Perez-Pacheco C, D’Silva NJ. Nerve density in cancer: less is better. FASEB Bioadv. 2021; 3(10): 773-786.

[174]

Bednarsch J, Kather J, Tan X, et al. Nerve fibers in the tumor microenvironment as a novel biomarker for oncological outcome in patients undergoing surgery for perihilar cholangiocarcinoma. Liver Cancer. 2021; 10(3): 260-274.

[175]

Eckerling A, Ricon-Becker I, Sorski L, Sandbank E, Ben-Eliyahu S. Stress and cancer: mechanisms, significance and future directions. Nat Rev Cancer. 2021; 21(12): 767-785.

[176]

Weeden CE, Hill W, Lim EL, Grönroos E, Swanton C. Impact of risk factors on early cancer evolution. Cell. 2023; 186(8): 1541-1563.

[177]

Wu S, Zhu W, Thompson P, Hannun YA. Evaluating intrinsic and non-intrinsic cancer risk factors. Nat Commun. 2018; 9(1): 3490.

[178]

Vicente-Dueñas C, Hauer J, Cobaleda C, Borkhardt A, Sánchez-García I. Epigenetic priming in cancer initiation. Trends Cancer. 2018; 4(6): 408-417.

[179]

Tiwari RK, Sharma V, Pandey RK, Shukla SS. Nicotine addiction: neurobiology and mechanism. J Pharmacopuncture. 2020; 23(1): 1-7.

[180]

Le Foll B, Piper ME, Fowler CD, et al. Tobacco and nicotine use. Nat Rev Dis Primers. 2022; 8(1): 19.

[181]

Wittenberg RE, Wolfman SL, De Biasi M, Dani JA. Nicotinic acetylcholine receptors and nicotine addiction: a brief introduction. Neuropharmacology. 2020; 177: 108256.

[182]

Zhang L, Pan J, Chen W, Jiang J, Huang J. Chronic stress-induced immune dysregulation in cancer: implications for initiation, progression, metastasis, and treatment. Am J Cancer Res. 2020; 10(5): 1294-1307.

[183]

Lupu M, Caruntu A, Caruntu C, et al. Neuroendocrine factors: the missing link in non-melanoma skin cancer (review). Oncol Rep. 2017; 38(3): 1327-1340.

[184]

Gaillard H, García-Muse T, Aguilera A. Replication stress and cancer. Nat Rev Cancer. 2015; 15(5): 276-289.

[185]

Yasuda MT, Sakakibara H, Shimoi K. Estrogen-and stress-induced DNA damage in breast cancer and chemoprevention with dietary flavonoid. Genes Environ. 2017; 39: 10.

[186]

Lamboy-Caraballo R, Ortiz-Sanchez C, Acevedo-Santiago A, Matta J, Monteiro ANA, Armaiz-Pena GN. Norepinephrine-induced DNA damage in ovarian cancer cells. Int J Mol Sci. 2020; 21(6): 2250.

[187]

Reeder A, Attar M, Nazario L, et al. Stress hormones reduce the efficacy of paclitaxel in triple negative breast cancer through induction of DNA damage. Br J Cancer. 2015; 112(9): 1461-1470.

[188]

Hara MR, Kovacs JJ, Whalen EJ, et al. A stress response pathway regulates DNA damage through β2-adrenoreceptors and β-arrestin-1. Nature. 2011; 477(7364): 349-353.

[189]

Hara MR, Sachs BD, Caron MG, Lefkowitz RJ. Pharmacological blockade of a β(2)AR-β-arrestin-1 signaling cascade prevents the accumulation of DNA damage in a behavioral stress model. Cell Cycle. 2013; 12(2): 219-224.

[190]

Flint MS, Baum A, Chambers WH, Jenkins FJ. Induction of DNA damage, alteration of DNA repair and transcriptional activation by stress hormones. Psychoneuroendocrinology. 2007; 32(5): 470-479.

[191]

Pfitzinger PL, Fangmann L, Wang K, et al. Indirect cholinergic activation slows down pancreatic cancer growth and tumor-associated inflammation. J Exp Clin Cancer Res. 2020; 39(1): 289.

[192]

Shehwana H, Keskus AG, Ozdemir SE, et al. CHRNA5 belongs to the secondary estrogen signaling network exhibiting prognostic significance in breast cancer. Cell Oncol. 2021; 44(2): 453-472.

[193]

Koh M, Takahashi T, Kurokawa Y, et al. Propranolol suppresses gastric cancer cell growth by regulating proliferation and apoptosis. Gastric Cancer. 2021; 24(5): 1037-1049.

[194]

Rousseau B, Murugan S, Palagani A, Sarkar DK. Beta 2 adrenergic receptor and mu opioid receptor interact to potentiate the aggressiveness of human breast cancer cell by activating the glycogen synthase kinase 3 signaling. Breast Cancer Res. 2022; 24(1): 33.

[195]

Sood AK, Armaiz-Pena GN, Halder J, et al. Adrenergic modulation of focal adhesion kinase protects human ovarian cancer cells from anoikis. J Clin Invest. 2010; 120(5): 1515-1523.

[196]

Zhang D, Ma Q, Wang Z, et al. β2-Adrenoceptor blockage induces G1/S phase arrest and apoptosis in pancreatic cancer cells via Ras/Akt/NFκB pathway. Mol Cancer. 2011; 10: 146.

[197]

Chin CC, Li JM, Lee KF, et al. Selective β2-AR blockage suppresses colorectal cancer growth through regulation of EGFR-Akt/ERK1/2 signaling, G1-phase arrest, and apoptosis. J Cell Physiol. 2016; 231(2): 459-472.

[198]

Wu FQ, Fang T, Yu LX, et al. ADRB2 signaling promotes HCC progression and sorafenib resistance by inhibiting autophagic degradation of HIF1α. J Hepatol. 2016; 65(2): 314-324.

[199]

Raufman JP, Chen Y, Cheng K, Compadre C, Compadre L, Zimniak P. Selective interaction of bile acids with muscarinic receptors: a case of molecular mimicry. Eur J Pharmacol. 2002; 457(2-3): 77-84.

[200]

Yu H, Xia H, Tang Q, et al. Acetylcholine acts through M3 muscarinic receptor to activate the EGFR signaling and promotes gastric cancer cell proliferation. Sci Rep. 2017; 7: 40802.

[201]

Pan C, Wu J, Zheng S, et al. Depression accelerates gastric cancer invasion and metastasis by inducing a neuroendocrine phenotype via the catecholamine/β(2)–AR/MACC1 axis. Cancer Commun. 2021; 41(10): 1049-1070.

[202]

Zhou Z, Shu Y, Bao H, et al. Stress-induced epinephrine promotes epithelial-to-mesenchymal transition and stemness of CRC through the CEBPB/TRIM2/P53 axis. J Transl Med. 2022; 20(1): 262.

[203]

Armaiz-Pena GN, Allen JK, Cruz A, et al. Src activation by β-adrenoreceptors is a key switch for tumour metastasis. Nat Commun. 2013; 4: 1403.

[204]

Landen CN, Lin YG, Armaiz-Pena GN, et al. Neuroendocrine modulation of signal transducer and activator of transcription-3 in ovarian cancer. Cancer Res. 2007; 67(21): 10389-10396.

[205]

Choi MJ, Cho KH, Lee S, et al. hTERT mediates norepinephrine-induced Slug expression and ovarian cancer aggressiveness. Oncogene. 2015; 34(26): 3402-3412.

[206]

Lin XH, Liu HH, Hsu SJ, et al. Norepinephrine-stimulated HSCs secrete sFRP1 to promote HCC progression following chronic stress via augmentation of a Wnt16B/β-catenin positive feedback loop. J Exp Clin Cancer Res. 2020; 39(1): 64.

[207]

Du P, Zeng H, Xiao Y, et al. Chronic stress promotes EMT-mediated metastasis through activation of STAT3 signaling pathway by miR-337-3p in breast cancer. Cell Death Dis. 2020; 11(9): 761.

[208]

Pu J, Zhang X, Luo H, Xu L, Lu X, Lu J. Adrenaline promotes epithelial-to-mesenchymal transition via HuR-TGFβ regulatory axis in pancreatic cancer cells and the implication in cancer prognosis. Biochem Biophys Res Commun. 2017; 493(3): 1273-1279.

[209]

Ray R, Goel S, Al Khashali H, et al. Regulation of soluble E-cadherin signaling in non-small-cell lung cancer cells by nicotine, BDNF, and β-adrenergic receptor ligands. Biomedicines. 2023; 11(9): 2555.

[210]

Lutgendorf SK, Cole S, Costanzo E, et al. Stress-related mediators stimulate vascular endothelial growth factor secretion by two ovarian cancer cell lines. Clin Cancer Res. 2003; 9(12): 4514-4521.

[211]

Thaker PH, Han LY, Kamat AA, et al. Chronic stress promotes tumor growth and angiogenesis in a mouse model of ovarian carcinoma. Nat Med. 2006; 12(8): 939-944.

[212]

Yang EV, Kim SJ, Donovan EL, et al. Norepinephrine upregulates VEGF, IL-8, and IL-6 expression in human melanoma tumor cell lines: implications for stress-related enhancement of tumor progression. Brain Behav Immun. 2009; 23(2): 267-275.

[213]

Shan T, Ma J, Ma Q, et al. β2-AR-HIF-1α: a novel regulatory axis for stress-induced pancreatic tumor growth and angiogenesis. Curr Mol Med. 2013; 13(6): 1023-1034.

[214]

Xie H, Li C, He Y, Griffin R, Ye Q, Li L. Chronic stress promotes oral cancer growth and angiogenesis with increased circulating catecholamine and glucocorticoid levels in a mouse model. Oral Oncol. 2015; 51(11): 991-997.

[215]

Yang EV, Sood AK, Chen M, et al. Norepinephrine up-regulates the expression of vascular endothelial growth factor, matrix metalloproteinase (MMP)-2, and MMP-9 in nasopharyngeal carcinoma tumor cells. Cancer Res. 2006; 66(21): 10357-10364.

[216]

Xia Y, Wei Y, Li ZY, et al. Catecholamines contribute to the neovascularization of lung cancer via tumor-associated macrophages. Brain Behav Immun. 2019; 81: 111-121.

[217]

Felten DL, Felten SY. Sympathetic noradrenergic innervation of immune organs. Brain Behav Immun. 1988; 2(4): 293-300.

[218]

Le CP, Nowell CJ, Kim-Fuchs C, et al. Chronic stress in mice remodels lymph vasculature to promote tumour cell dissemination. Nat Commun. 2016; 7: 10634.

[219]

Shi RJ, Ke BW, Tang YL, Liang XH. Perineural invasion: a potential driver of cancer-induced pain. Biochem Pharmacol. 2023; 215: 115692.

[220]

Batsakis JG. Nerves and neurotropic carcinomas. Ann Otol Rhinol Laryngol. 1985; 94(4 pt 1): 426-427.

[221]

Wang H, Zheng Q, Lu Z, et al. Role of the nervous system in cancers: a review. Cell Death Discov. 2021; 7(1): 76.

[222]

Huang D, Su S, Cui X, et al. Nerve fibers in breast cancer tissues indicate aggressive tumor progression. Medicine (Baltimore). 2014; 93(27): e172.

[223]

Maru N, Ohori M, Kattan MW, Scardino PT, Wheeler TM. Prognostic significance of the diameter of perineural invasion in radical prostatectomy specimens. Hum Pathol. 2001; 32(8): 828-833.

[224]

Mitsunaga S, Hasebe T, Kinoshita T, et al. Detail histologic analysis of nerve plexus invasion in invasive ductal carcinoma of the pancreas and its prognostic impact. Am J Surg Pathol. 2007; 31(11): 1636-1644.

[225]

Schweizerhof M, Stösser S, Kurejova M, et al. Hematopoietic colony-stimulating factors mediate tumor–nerve interactions and bone cancer pain. Nat Med. 2009; 15(7): 802-807.

[226]

Selvaraj D, Gangadharan V, Michalski CW, et al. A functional role for VEGFR1 expressed in peripheral sensory neurons in cancer pain. Cancer Cell. 2015; 27(6): 780-796.

[227]

Hirth M, Gandla J, Höper C, et al. CXCL10 and CCL21 promote migration of pancreatic cancer cells toward sensory neurons and neural remodeling in tumors in mice, associated with pain in patients. Gastroenterology. 2020; 159(2): 665-681.

[228]

Swanson BJ, McDermott KM, Singh PK, Eggers JP, Crocker PR, Hollingsworth MA. MUC1 is a counter-receptor for myelin-associated glycoprotein (Siglec-4a) and their interaction contributes to adhesion in pancreatic cancer perineural invasion. Cancer Res. 2007; 67(21): 10222-10229.

[229]

Okada Y, Takeyama H, Sato M, et al. Experimental implication of celiac ganglionotropic invasion of pancreatic-cancer cells bearing c-ret proto-oncogene with reference to glial-cell-line-derived neurotrophic factor (GDNF). Int J Cancer. 1999; 81(1): 67-73.

[230]

Lian EY, Hyndman BD, Moodley S, Maritan SM, Mulligan LM. RET isoforms contribute differentially to invasive processes in pancreatic ductal adenocarcinoma. Oncogene. 2020; 39(41): 6493-6510.

[231]

Roger E, Martel S, Bertrand-Chapel A, et al. Schwann cells support oncogenic potential of pancreatic cancer cells through TGFβ signaling. Cell Death Dis. 2019; 10(12): 886.

[232]

Na’ara S, Amit M, Gil Z. L1CAM induces perineural invasion of pancreas cancer cells by upregulation of metalloproteinase expression. Oncogene. 2019; 38(4): 596-608.

[233]

Bakst RL, Xiong H, Chen CH, et al. Inflammatory monocytes promote perineural invasion via CCL2-mediated recruitment and cathepsin B expression. Cancer Res. 2017; 77(22): 6400-6414.

[234]

Kershner LJ, Choi K, Wu J, et al. Multiple Nf1 Schwann cell populations reprogram the plexiform neurofibroma tumor microenvironment. JCI Insight. 2022; 7(18): e154513.

[235]

Su D, Guo X, Huang L, et al. Tumor-neuroglia interaction promotes pancreatic cancer metastasis. Theranostics. 2020; 10(11): 5029-5047.

[236]

Li J, Kang R, Tang D. Cellular and molecular mechanisms of perineural invasion of pancreatic ductal adenocarcinoma. Cancer Commun (Lond). 2021; 41(8): 642-660.

[237]

Silverman DA, Martinez VK, Dougherty PM, Myers JN, Calin GA, Amit M. Cancer-associated neurogenesis and nerve-cancer cross-talk. Cancer Res. 2021; 81(6): 1431-1440.

[238]

Dobrenis K, Gauthier LR, Barroca V, Magnon C. Granulocyte colony-stimulating factor off-target effect on nerve outgrowth promotes prostate cancer development. Int J Cancer. 2015; 136(4): 982-988.

[239]

McIlvried LA, Atherton MA, Horan NL, Goch TN, Scheff NN. Sensory neurotransmitter calcitonin gene-related peptide modulates tumor growth and lymphocyte infiltration in oral squamous cell carcinoma. Adv Biol. 2022; 6(9): e2200019.

[240]

Pundavela J, Demont Y, Jobling P, et al. ProNGF correlates with Gleason score and is a potential driver of nerve infiltration in prostate cancer. Am J Pathol. 2014; 184(12): 3156-3162.

[241]

Deborde S, Gusain L, Powers A, et al. Reprogrammed Schwann cells organize into dynamic tracks that promote pancreatic cancer invasion. Cancer Discov. 2022; 12(10): 2454-2473.

[242]

Mauffrey P, Tchitchek N, Barroca V, et al. Progenitors from the central nervous system drive neurogenesis in cancer. Nature. 2019; 569(7758): 672-678.

[243]

Aggarwal A. Hypothalamo-pituitary-adrenal axis and brain during stress, yoga and meditation: a review. Int J Health Clin Res. 2020;3(9): 96-103.

[244]

Ehrhart-Bornstein M, Bornstein SR. Cross-talk between adrenal medulla and adrenal cortex in stress. Ann N Y Acad Sci. 2008; 1148: 112-117.

[245]

Kvetnansky R, Sabban EL, Palkovits M. Catecholaminergic systems in stress: structural and molecular genetic approaches. Physiol Rev. 2009; 89(2): 535-606.

[246]

Basarrate S, Monzel AS, Smith JLM, Marsland AL, Trumpff C, Picard M. Glucocorticoid and adrenergic receptor distribution across human organs and tissues: a map for stress transduction. Psychosom Med. 2024; 86(2): 89-98.

[247]

Niedzwiedz CL, Knifton L, Robb KA, Katikireddi SV, Smith DJ. Depression and anxiety among people living with and beyond cancer: a growing clinical and research priority. BMC Cancer. 2019; 19(1): 943.

[248]

Nordin K, Berglund G, Glimelius B, Sjödén PO. Predicting anxiety and depression among cancer patients: a clinical model. Eur J Cancer. 2001; 37(3): 376-384.

[249]

PDQ Supportive Palliative Care Editorial Board. Adjustment to cancer: anxiety and distress (PDQ®): health professional version. PDQ Cancer Information Summaries. Bethesda (MD): National Cancer Institute (US); 2002.

[250]

Brandão T, Tavares R, Schulz MS, Matos PM. Measuring emotion regulation and emotional expression in breast cancer patients: a systematic review. Clin Psychol Rev. 2016; 43: 114-127.

[251]

Giese-Davis J, Collie K, Rancourt KM, Neri E, Kraemer HC, Spiegel D. Decrease in depression symptoms is associated with longer survival in patients with metastatic breast cancer: a secondary analysis. J Clin Oncol. 2011; 29(4): 413-420.

[252]

Schrepf A, Clevenger L, Christensen D, et al. Cortisol and inflammatory processes in ovarian cancer patients following primary treatment: relationships with depression, fatigue, and disability. Brain Behav Immun. 2013(suppl 0): S126-S134.

[253]

Thomson F, Craighead M. Innovative approaches for the treatment of depression: targeting the HPA axis. Neurochem Res. 2008; 33(4): 691-707.

[254]

Zhang H, Yang Y, Cao Y, Guan J. Effects of chronic stress on cancer development and the therapeutic prospects of adrenergic signaling regulation. Biomed Pharmacother. 2024; 175: 116609.

[255]

Cui B, Peng F, Lu J, et al. Cancer and stress: NextGen strategies. Brain Behav Immun. 2021; 93: 368-383.

[256]

Flaherty RL, Falcinelli M, Flint MS. Stress and drug resistance in cancer. Cancer Drug Resist. 2019; 2(3): 773-786.

[257]

Hanns P, Paczulla AM, Medinger M, Konantz M, Lengerke C. Stress and catecholamines modulate the bone marrow microenvironment to promote tumorigenesis. Cell Stress. 2019; 3(7): 221-235.

[258]

Jia Q, Zhou Y, Song L, et al. Baicalin reduces chronic stress-induced breast cancer metastasis via directly targeting β2-adrenergic receptor. J Pharm Anal. 2024; 14(7): 100934.

[259]

Haist M, Stege H, Grabbe S, Bros M. The functional crosstalk between myeloid-derived suppressor cells and regulatory T cells within the immunosuppressive tumor microenvironment. Cancers (Basel). 2021; 13(2): 210.

[260]

Neo SY, Tong L, Chong J, et al. Tumor-associated NK cells drive MDSC-mediated tumor immune tolerance through the IL-6/STAT3 axis. Sci Transl Med. 2024; 16(747): eadi2952.

[261]

Tang J, Li Z, Lu L, Cho CH. β-Adrenergic system, a backstage manipulator regulating tumour progression and drug target in cancer therapy. Semin Cancer Biol. 2013; 23(6 pt B): 533-542.

[262]

Lempesis IG, Georgakopoulou VE, Papalexis P, Chrousos GP, Spandidos DA. Role of stress in the pathogenesis of cancer (review). Int J Oncol. 2023; 63(5): 124.

[263]

Antoni MH, Dhabhar FS. The impact of psychosocial stress and stress management on immune responses in patients with cancer. Cancer. 2019; 125(9): 1417-1431.

[264]

Sandbank E, Eckerling A, Margalit A, Sorski L, Ben-Eliyahu S. Immunotherapy during the immediate perioperative period: a promising approach against metastatic disease. Curr Oncol. 2023; 30(8): 7450-7477.

[265]

Yan J, Chen Y, Luo M, et al. Chronic stress in solid tumor development: from mechanisms to interventions. J Biomed Sci. 2023; 30(1): 8.

[266]

Bakos O, Lawson C, Rouleau S, Tai LH. Combining surgery and immunotherapy: turning an immunosuppressive effect into a therapeutic opportunity. J Immunother Cancer. 2018; 6(1): 86.

[267]

Daher C, Vimeux L, Stoeva R, et al. Blockade of β-adrenergic receptors improves CD8(+) T-cell priming and cancer vaccine efficacy. Cancer Immunol Res. 2019; 7(11): 1849-1863.

[268]

Nissen MD, Sloan EK, Mattarollo SR. β-Adrenergic signaling impairs antitumor CD8(+) T-cell responses to B-cell lymphoma immunotherapy. Cancer Immunol Res. 2018; 6(1): 98-109.

[269]

Bucsek MJ, Qiao G, MacDonald CR, et al. β-Adrenergic signaling in mice housed at standard temperatures suppresses an effector phenotype in CD8(+) T cells and undermines checkpoint inhibitor therapy. Cancer Res. 2017; 77(20): 5639-5651.

[270]

Ma Y, Kroemer G. The cancer-immune dialogue in the context of stress. Nat Rev Immunol. 2024; 24(4): 264-281.

[271]

Shi M, Yang Z, Hu M, et al. Catecholamine-Induced β2-adrenergic receptor activation mediates desensitization of gastric cancer cells to trastuzumab by upregulating MUC4 expression. J Immunol. 2013; 190(11): 5600-5608.

[272]

Liu D, Yang Z, Wang T, et al. β2-AR signaling controls trastuzumab resistance-dependent pathway. Oncogene. 2016; 35(1): 47-58.

[273]

Fearon DT. The expansion and maintenance of antigen-selected CD8(+) T cell clones. Adv Immunol. 2007; 96: 103-139.

[274]

Williams MA, Bevan MJ. Effector and memory CTL differentiation. Annu Rev Immunol. 2007; 25: 171-192.

[275]

Arens R, Schoenberger SP. Plasticity in programming of effector and memory CD8 T-cell formation. Immunol Rev. 2010; 235(1): 190-205.

[276]

Sanders VM, Baker RA, Ramer-Quinn DS, Kasprowicz DJ, Fuchs BA, Street NE. Differential expression of the beta2-adrenergic receptor by Th1 and Th2 clones: implications for cytokine production and B cell help. J Immunol. 1997; 158(9): 4200-4210.

[277]

Mueller SN. Neural control of immune cell trafficking. J Exp Med. 2022; 219(3): e20211604.

[278]

Nakai A, Hayano Y, Furuta F, Noda M, Suzuki K. Control of lymphocyte egress from lymph nodes through β2-adrenergic receptors. J Exp Med. 2014; 211(13): 2583-2598.

[279]

Devi S, Alexandre YO, Loi JK, et al. Adrenergic regulation of the vasculature impairs leukocyte interstitial migration and suppresses immune responses. Immunity. 2021; 54(6): 1219-1230.

[280]

Grebe KM, Hickman HD, Irvine KR, Takeda K, Bennink JR, Yewdell JW. Sympathetic nervous system control of anti-influenza CD8+ T cell responses. Proc Natl Acad Sci U S A. 2009; 106(13): 5300-5305.

[281]

Kohm AP, Sanders VM. Norepinephrine and beta 2-adrenergic receptor stimulation regulate CD4+ T and B lymphocyte function in vitro and in vivo. Pharmacol Rev. 2001; 53(4): 487-525.

[282]

Rosas-Ballina M, Olofsson PS, Ochani M, et al. Acetylcholine-synthesizing T cells relay neural signals in a vagus nerve circuit. Science. 2011; 334(6052): 98-101.

[283]

Shurin MR, Shurin GV, Zlotnikov SB, Bunimovich YL. The neuroimmune axis in the tumor microenvironment. J Immunol. 2020; 204(2): 280-285.

[284]

Wang H, Yu M, Ochani M, et al. Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature. 2003; 421(6921): 384-388.

[285]

Pilatova K, Bencsikova B, Demlova R, Valik D, Zdrazilova-Dubska L. Myeloid-derived suppressor cells (MDSCs) in patients with solid tumors: considerations for granulocyte colony-stimulating factor treatment. Cancer Immunol Immunother. 2018; 67(12): 1919-1929.

[286]

Tcyganov E, Mastio J, Chen E, Gabrilovich DI. Plasticity of myeloid-derived suppressor cells in cancer. Curr Opin Immunol. 2018; 51: 76-82.

[287]

Law AMK, Valdes-Mora F, Gallego-Ortega D. Myeloid-derived suppressor cells as a therapeutic target for cancer. Cells. 2020; 9(3): 561.

[288]

Ma T, Renz BW, Ilmer M, et al. Myeloid-derived suppressor cells in solid tumors. Cells. 2022; 11(2): 310.

[289]

Zhao Y, Wu T, Shao S, Shi B, Zhao Y. Phenotype, development, and biological function of myeloid-derived suppressor cells. Oncoimmunology. 2016; 5(2): e1004983.

[290]

Mohammadpour H, MacDonald CR, McCarthy PL, Abrams SI, Repasky EA. β2-Adrenergic receptor signaling regulates metabolic pathways critical to myeloid-derived suppressor cell function within the TME. Cell Rep. 2021; 37(4): 109883.

[291]

Xiao L, Li X, Fang C, Yu J, Chen T. Neurotransmitters: promising immune modulators in the tumor microenvironment. Front Immunol. 2023; 14: 1118637.

[292]

Mohammadpour H, MacDonald CR, Qiao G, et al. β2 adrenergic receptor-mediated signaling regulates the immunosuppressive potential of myeloid-derived suppressor cells. J Clin Invest. 2019; 129(12): 5537-5552.

[293]

Dantzer R. Neuroimmune interactions: from the brain to the immune system and vice versa. Physiol Rev. 2018; 98(1): 477-504.

[294]

Peng WT, Sun WY, Li XR, Sun JC, Du JJ, Wei W. Emerging roles of G protein-coupled receptors in hepatocellular carcinoma. Int J Mol Sci. 2018; 19(5): 1366.

[295]

Nevin JT, Moussa M, Corwin WL, Srivastava PK. Sympathetic nervous tone limits the development of myeloid-derived suppressor cells. Sci Immunol. 2020; 5(51): eaay9368.

[296]

Singh A, Ranjan A. Adrenergic receptor signaling regulates the CD40-receptor mediated anti-tumor immunity. Front Immunol. 2023; 14: 1141712.

[297]

Zhang Y, Brekken RA. Direct and indirect regulation of the tumor immune microenvironment by VEGF. J Leukoc Biol. 2022; 111(6): 1269-1286.

[298]

Sorrentino C, Miele L, Porta A, Pinto A, Morello S. Myeloid-derived suppressor cells contribute to A2B adenosine receptor-induced VEGF production and angiogenesis in a mouse melanoma model. Oncotarget. 2015; 6(29): 27478-27489.

[299]

Chen SH, Zhang BY, Zhou B, Zhu CZ, Sun LQ, Feng YJ. Perineural invasion of cancer: a complex crosstalk between cells and molecules in the perineural niche. Am J Cancer Res. 2019; 9(1): 1-21.

[300]

Nguyen TM, Ngoc DTM, Choi JH, Lee CH. Unveiling the neural environment in cancer: exploring the role of neural circuit players and potential therapeutic strategies. Cells. 2023; 12(15): 1996.

[301]

Wang W, Li L, Chen N, et al. Nerves in the tumor microenvironment: origin and effects. Front Cell Dev Biol. 2020; 8: 601738.

[302]

Sloan EK, Priceman SJ, Cox BF, et al. The sympathetic nervous system induces a metastatic switch in primary breast cancer. Cancer Res. 2010; 70(18): 7042-7052.

[303]

Partecke LI, Günther C, Hagemann S, et al. Induction of M2-macrophages by tumour cells and tumour growth promotion by M2-macrophages: a quid pro quo in pancreatic cancer. Pancreatology. 2013; 13(5): 508-516.

[304]

Cheng Y, Tang XY, Li YX, et al. Depression-induced neuropeptide Y secretion promotes prostate cancer growth by recruiting myeloid cells. Clin Cancer Res. 2019; 25(8): 2621-2632.

[305]

Zhu Y, Herndon JM, Sojka DK, et al. Tissue-resident macrophages in pancreatic ductal adenocarcinoma originate from embryonic hematopoiesis and promote tumor progression. Immunity. 2017; 47(2): 323-338.

[306]

Borovikova LV, Ivanova S, Zhang M, et al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature. 2000; 405(6785): 458-562.

[307]

Dubeykovskaya Z, Si Y, Chen X, et al. Neural innervation stimulates splenic TFF2 to arrest myeloid cell expansion and cancer. Nat Commun. 2016; 7: 10517.

[308]

Kim JK, Kim YS, Lee HM, et al. GABAergic signaling linked to autophagy enhances host protection against intracellular bacterial infections. Nat Commun. 2018; 9(1): 4184.

[309]

Huang D, Wang Y, Thompson JW, et al. Cancer-cell-derived GABA promotes β-catenin-mediated tumour growth and immunosuppression. Nat Cell Biol. 2022; 24(2): 230-241.

[310]

Spranger S, Dai D, Horton B, Gajewski TF. Tumor-residing Batf3 dendritic cells are required for effector T cell trafficking and adoptive T cell therapy. Cancer Cell. 2017; 31(5): 711-723.

[311]

Zhang B, Vogelzang A, Miyajima M, et al. B cell-derived GABA elicits IL-10(+) macrophages to limit anti-tumour immunity. Nature. 2021; 599(7885): 471-476.

[312]

Wu X, Shen Q, Chang H, Li J, Xing D. Promoted CD4(+) T cell-derived IFN-γ/IL-10 by photobiomodulation therapy modulates neurogenesis to ameliorate cognitive deficits in APP/PS1 and 3xTg-AD mice. J Neuroinflammation. 2022; 19(1): 253.

[313]

Xiong XY, Liu L, Yang QW. Functions and mechanisms of microglia/macrophages in neuroinflammation and neurogenesis after stroke. Prog Neurobiol. 2016; 142: 23-44.

[314]

Gungabeesoon J, Gort-Freitas NA, Kiss M, et al. A neutrophil response linked to tumor control in immunotherapy. Cell. 2023; 186(7): 1448-1464.

[315]

Jaillon S, Ponzetta A, Di Mitri D, Santoni A, Bonecchi R, Mantovani A. Neutrophil diversity and plasticity in tumour progression and therapy. Nat Rev Cancer. 2020; 20(9): 485-503.

[316]

Xue R, Zhang Q, Cao Q, et al. Liver tumour immune microenvironment subtypes and neutrophil heterogeneity. Nature. 2022; 612(7938): 141-147.

[317]

Li J, Che M, Zhang B, Zhao K, Wan C, Yang K. The association between the neuroendocrine system and the tumor immune microenvironment: emerging directions for cancer immunotherapy. Biochim Biophys Acta Rev Cancer. 2023; 1878(6): 189007.

[318]

Shalabi S, Belayachi A, Larrivée B. Involvement of neuronal factors in tumor angiogenesis and the shaping of the cancer microenvironment. Front Immunol. 2024; 15: 1284629.

[319]

Sookhai S, Wang JH, McCourt M, O’Connell D, Redmond HP. Dopamine induces neutrophil apoptosis through a dopamine D-1 receptor-independent mechanism. Surgery. 1999; 126(2): 314-322.

[320]

Burfeind KG, Zhu X, Norgard MA, et al. Circulating myeloid cells invade the central nervous system to mediate cachexia during pancreatic cancer. Elife. 2020;9:e54095.

[321]

Zha C, Meng X, Li L, et al. Neutrophil extracellular traps mediate the crosstalk between glioma progression and the tumor microenvironment via the HMGB1/RAGE/IL-8 axis. Cancer Biol Med. 2020; 17(1): 154-168.

[322]

Gilardi M, Ramos M, Hollern D. B cells secrete GABA, which provokes a pro-tumor immune microenvironment. Cancer Cell. 2022; 40(1): 17-19.

[323]

Zhang X, Lei B, Yuan Y, et al. Brain control of humoral immune responses amenable to behavioural modulation. Nature. 2020; 581(7807): 204-208.

[324]

Shi DD, Guo JA, Hoffman HI, et al. Therapeutic avenues for cancer neuroscience: translational frontiers and clinical opportunities. Lancet Oncol. 2022; 23(2): e62-e74.

[325]

Demir IE, Reyes CM, Alrawashdeh W, et al. Clinically actionable strategies for studying neural influences in cancer. Cancer Cell. 2020; 38(1): 11-14.

[326]

Qiao G, Chen M, Bucsek MJ, Repasky EA, Hylander BL. Adrenergic signaling: a targetable checkpoint limiting development of the antitumor immune response. Front Immunol. 2018; 9: 164.

[327]

Joensuu H, Gligorov J. Adjuvant treatments for triple-negative breast cancers. Ann Oncol. 2012; 23(suppl 6): vi40-vi45.

[328]

Florent R, Poulain L, N’Diaye M. Drug repositioning of the α(1)-adrenergic receptor antagonist naftopidil: a potential new anti-cancer drug? Int J Mol Sci. 2020; 21(15): 5339.

[329]

Wang J, Lu S, Meng Y, Fu W, Zhou X. Beta adrenergic blockade and clinical outcomes in patients with colorectal cancer: a systematic review and meta-analysis. Eur J Pharmacol. 2022; 929: 175135.

[330]

Puzderova B, Belvoncikova P, Grossmannova K, et al. Promising chemosensitizer and candidate for the combined therapy through disruption of tumor microenvironment homeostasis by decreasing the level of carbonic anhydrase IX. Int J Mol Sci. 2023; 24(13): 11094.

[331]

Di Fonte R, Strippoli S, Garofoli M, et al. Cervical cancer benefits from trabectedin combination with the β-blocker propranolol: in vitro and ex vivo evaluations in patient-derived organoids. Front Cell Dev Biol. 2023; 11: 1178316.

[332]

Farhoumand LS, Liu H, Tsimpaki T, et al. Blockade of ß-adrenergic receptors by nebivolol enables tumor control potential for uveal melanoma in 3D tumor spheroids and 2D cultures. Int J Mol Sci. 2023; 24(6): 5894.

[333]

Liang J, Seghiri M, Singh PK, et al. The β2-adrenergic receptor associates with CXCR4 multimers in human cancer cells. Proc Natl Acad Sci U S A. 2024; 121(14): e2304897121.

[334]

Yu J, Li M, Ren B, et al. Unleashing the efficacy of immune checkpoint inhibitors for advanced hepatocellular carcinoma: factors, strategies, and ongoing trials. Front Pharmacol. 2023; 14: 1261575.

[335]

Liu YT, Sun ZJ. Turning cold tumors into hot tumors by improving T-cell infiltration. Theranostics. 2021; 11(11): 5365-5386.

[336]

Montani L, Petrinovic MM. Targeting axonal regeneration: the growth cone takes the lead. J Neurosci. 2014; 34(13): 4443-4444.

[337]

Le TT, Oudin MJ. Understanding and modeling nerve–cancer interactions. Dis Model Mech. 2023; 16(1): dmm049729.

[338]

Sang Q, Sun D, Chen Z, Zhao W. NGF and PI3K/Akt signaling participate in the ventral motor neuronal protection of curcumin in sciatic nerve injury rat models. Biomed Pharmacother. 2018; 103: 1146-1153.

[339]

Peach CJ, Tonello R, Gomez K, et al. Neuropilin-1 is a co-receptor for NGF and TrkA-evoked pain. bioRxiv. 2024.

[340]

Patel TD, Jackman A, Rice FL, Kucera J, Snider WD. Development of sensory neurons in the absence of NGF/TrkA signaling in vivo. Neuron. 2000; 25(2): 345-357.

[341]

Bimonte S, Cascella M, Forte CA, Esposito G, Cuomo A. The role of anti-nerve growth factor monoclonal antibodies in the control of chronic cancer and non-cancer pain. J Pain Res. 2021; 14: 1959-1967.

[342]

Kelleher JH, Tewari D, McMahon SB. Neurotrophic factors and their inhibitors in chronic pain treatment. Neurobiol Dis. 2017; 97: 127-138.

[343]

Lei Y, Tang L, Xie Y, et al. Gold nanoclusters-assisted delivery of NGF siRNA for effective treatment of pancreatic cancer. Nat Commun. 2017; 8: 15130.

[344]

Lillemoe KD, Cameron JL, Kaufman HS, Yeo CJ, Pitt HA, Sauter PK. Chemical splanchnicectomy in patients with unresectable pancreatic cancer. A prospective randomized trial. Ann Surg. 1993; 217(5): 456-457.

[345]

Coarfa C, Florentin D, Putluri N, et al. Influence of the neural microenvironment on prostate cancer. Prostate. 2018; 78(2): 128-139.

[346]

Vudatha V, Herremans KM, Freudenberger DC, Liu C, Trevino JG. In vivo models of pancreatic ductal adenocarcinoma. Adv Cancer Res. 2023; 159: 75-112.

[347]

Guo S, Gao S, Liu R, et al. Oncological and genetic factors impacting PDX model construction with NSG mice in pancreatic cancer. FASEB J. 2019; 33(1): 873-884.

[348]

Lai Y, Wei X, Lin S, Qin L, Cheng L, Li P. Current status and perspectives of patient-derived xenograft models in cancer research. J Hematol Oncol. 2017; 10(1): 106.

[349]

Navari RM, Aapro M. Antiemetic prophylaxis for chemotherapy-induced nausea and vomiting. N Engl J Med. 2016; 374(14): 1356-1367.

[350]

Boutros C, Tarhini A, Routier E, et al. Safety profiles of anti-CTLA-4 and anti-PD-1 antibodies alone and in combination. Nat Rev Clin Oncol. 2016; 13(8): 473-486.

[351]

Fucà G, Galli G, Poggi M, et al. Modulation of peripheral blood immune cells by early use of steroids and its association with clinical outcomes in patients with metastatic non-small cell lung cancer treated with immune checkpoint inhibitors. ESMO Open. 2019; 4(1): e000457.

[352]

Arbour KC, Mezquita L, Long N, et al. Impact of baseline steroids on efficacy of programmed cell death-1 and programmed death-ligand 1 blockade in patients with non-small-cell lung cancer. J Clin Oncol. 2018; 36(28): 2872-2878.

[353]

Scott SC, Pennell NA. Early use of systemic corticosteroids in patients with advanced NSCLC treated with nivolumab. J Thorac Oncol. 2018; 13(11): 1771-1775.

[354]

Boucherit N, Gorvel L, Olive D. 3D tumor models and their use for the testing of immunotherapies. Front Immunol. 2020; 11: 603640.

[355]

Yuan J, Li X, Yu S. Cancer organoid co-culture model system: novel approach to guide precision medicine. Front Immunol. 2022; 13: 1061388.

[356]

Urzì O, Gasparro R, Costanzo E, et al. Three-dimensional cell cultures: the bridge between in vitro and in vivo models. Int J Mol Sci. 2023; 24(15): 12046.

[357]

Li L, Hanahan D. Hijacking the neuronal NMDAR signaling circuit to promote tumor growth and invasion. Cell. 2013; 153(1): 86-100.

[358]

Venkataramani V, Tanev DI, Strahle C, et al. Glutamatergic synaptic input to glioma cells drives brain tumour progression. Nature. 2019; 573(7775): 532-538.

[359]

Venkatesh HS, Morishita W, Geraghty AC, et al. Electrical and synaptic integration of glioma into neural circuits. Nature. 2019; 573(7775): 539-545.

[360]

Stokholm MG, Høyer S, Borre M, et al. Molecular imaging of cholinergic processes in prostate cancer using ¹¹C-donepezil and ¹⁸F-FEOBV. Eur J Nucl Med Mol Imaging. 2016; 43(5): 906-910.

[361]

Werner C, Sauer M, Geis C. Super-resolving microscopy in neuroscience. Chem Rev. 2021; 121(19): 11971-12015.

[362]

Hierro-Bujalance C, Bacskai BJ, Garcia-Alloza M. In vivo imaging of microglia with multiphoton microscopy. Front Aging Neurosci. 2018; 10: 218.

[363]

Richardson DS, Guan W, Matsumoto K, et al. Tissue clearing. Nat Rev Methods Primers. 2021; 1(1): 84.

[364]

Ueda HR, Ertürk A, Chung K, et al. Tissue clearing and its applications in neuroscience. Nat Rev Neurosci. 2020; 21(2): 61-79.

[365]

Tetzlaff SK, Reyhan E, Bengtson CP, et al. Characterizing and targeting glioblastoma neuron-tumor networks with retrograde tracing. bioRxiv. 2024. doi:10.1101/2024.03.18.585565

[366]

Perdyan A, Lawrynowicz U, Horbacz M, Kaminska B, Mieczkowski J. Integration of single-cell RNA sequencing and spatial transcriptomics to reveal the glioblastoma heterogeneity. F1000Res. 2022; 11: 1180.

[367]

Jin Y, Zuo Y, Li G, et al. Advances in spatial transcriptomics and its applications in cancer research. Mol Cancer. 2024; 23(1): 129.

[368]

Masarapu Y, Cekanaviciute E, Andrusivova Z, et al. Spatially resolved multiomics on the neuronal effects induced by spaceflight in mice. Nat Commun. 2024; 15(1): 4778.

RIGHTS & PERMISSIONS

2024 The Author(s). MedComm published by Sichuan International Medical Exchange & Promotion Association (SCIMEA) and John Wiley & Sons Australia, Ltd.

AI Summary AI Mindmap
PDF

294

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/