
Immune mediated support of metastasis: Implication for bone invasion
Zengfeng Xin, Luying Qin, Yang Tang, Siyu Guo, Fangfang Li, Yuan Fang, Gege Li, Yihan Yao, Binbin Zheng, Bicheng Zhang, Dang Wu, Jie Xiao, Chao Ni, Qichun Wei, Ting Zhang
Cancer Communications ›› 2024, Vol. 44 ›› Issue (09) : 967-991.
Immune mediated support of metastasis: Implication for bone invasion
Bone is a common organ affected by metastasis in various advanced cancers, including lung, breast, prostate, colorectal, and melanoma. Once a patient is diagnosed with bone metastasis, the patient’s quality of life and overall survival are significantly reduced owing to a wide range of morbidities and the increasing difficulty of treatment. Many studies have shown that bone metastasis is closely related to bone microenvironment, especially bone immune microenvironment. However, the effects of various immune cells in the bone microenvironment on bone metastasis remain unclear. Here, we described the changes in various immune cells during bone metastasis and discussed their related mechanisms. Osteoblasts, adipocytes, and other non-immune cells closely related to bone metastasis were also included. This review also summarized the existing treatment methods and potential therapeutic targets, and provided insights for future studies of cancer bone metastasis.
bone metastasis / bone microenvironment / cancer / immune cell / therapy
[1] |
Hofbauer LC, Rachner TD, Coleman RE, Jakob F. Endocrine aspects of bone metastases. Lancet Diabetes Endocrinol. 2014; 2(6): 500–512.
CrossRef
Google scholar
|
[2] |
Song H, Arredondo Carrera HM, Sprules A, Ji Y, Zhang T, He J, et al. C-terminal variants of the P2×7 receptor are associated with prostate cancer progression and bone metastasis -evidence from clinical and pre-clinical data. Cancer Commun (Lond). 2023; 43(3): 400–404.
CrossRef
Google scholar
|
[3] |
Invernizzi M, Kim J, Fusco N. Editorial: Quality of Life in Breast Cancer Patients and Survivors. Front Oncol. 2020; 10: 620574.
CrossRef
Google scholar
|
[4] |
Baek YH, Jeon HL, Oh IS, Yang H, Park J, Shin JY. Incidence of skeletal-related events in patients with breast or prostate cancer-induced bone metastasis or multiple myeloma: A 12-year longitudinal nationwide healthcare database study. Cancer Epidemiol. 2019; 61: 104–110.
CrossRef
Google scholar
|
[5] |
Spencer JA, Ferraro F, Roussakis E, Klein A, Wu J, Runnels JM, et al. Direct measurement of local oxygen concentration in the bone marrow of live animals. Nature. 2014; 508(7495): 269–273.
CrossRef
Google scholar
|
[6] |
Hiraga T. Hypoxic Microenvironment and Metastatic Bone Disease. Int J Mol Sci. 2018; 19(11): 3523.
CrossRef
Google scholar
|
[7] |
Yuan FL, Xu MH, Li X, Xinlong H, Fang W, Dong J. The Roles of Acidosis in Osteoclast Biology. Front Physiol. 2016; 7: 222.
CrossRef
Google scholar
|
[8] |
Arnett TR. Acidosis, hypoxia and bone. Arch Biochem Biophys. 2010; 503(1): 103–109.
CrossRef
Google scholar
|
[9] |
Santos-de-Frutos K, Djouder N. When dormancy fuels tumour relapse. Commun Biol. 2021; 4(1): 747.
CrossRef
Google scholar
|
[10] |
Zhang Y, Liang J, Liu P, Wang Q, Liu L, Zhao H. The RANK/RANKL/OPG system and tumor bone metastasis: Potential mechanisms and therapeutic strategies. Front Endocrinol (Lausanne). 2022; 13: 1063815.
CrossRef
Google scholar
|
[11] |
Zhang X. Interactions between cancer cells and bone microenvironment promote bone metastasis in prostate cancer. Cancer Commun (Lond). 2019; 39(1): 76.
CrossRef
Google scholar
|
[12] |
Croucher PI, McDonald MM, Martin TJ. Bone metastasis: the importance of the neighbourhood. Nat Rev Cancer. 2016; 16(6): 373–386.
CrossRef
Google scholar
|
[13] |
Pastushenko I, Brisebarre A, Sifrim A, Fioramonti M, Revenco T, Boumahdi S, et al. Identification of the tumour transition states occurring during EMT. Nature. 2018; 556(7702): 463–468.
CrossRef
Google scholar
|
[14] |
Sistigu A, Di Modugno F, Manic G, Nisticò P. Deciphering the loop of epithelial-mesenchymal transition, inflammatory cytokines and cancer immunoediting. Cytokine Growth Factor Rev. 2017; 36: 67–77.
CrossRef
Google scholar
|
[15] |
Greten FR, Grivennikov SI. Inflammation and Cancer: Triggers, Mechanisms, and Consequences. Immunity. 2019; 51(1): 27–41.
CrossRef
Google scholar
|
[16] |
Fernandes R, Costa C, Fernandes R, Barros AN. Inflammation in Prostate Cancer: Exploring the Promising Role of Phenolic Compounds as an Innovative Therapeutic Approach. Biomedicines. 2023; 11(12): 3140.
CrossRef
Google scholar
|
[17] |
Hofbauer LC, Bozec A, Rauner M, Jakob F, Perner S, Pantel K. Novel approaches to target the microenvironment of bone metastasis. Nat Rev Clin Oncol. 2021; 18(8): 488–505.
CrossRef
Google scholar
|
[18] |
Del Conte A, De Carlo E, Bertoli E, Stanzione B, Revelant A, Bertola M, et al. Bone Metastasis and Immune Checkpoint Inhibitors in Non-Small Cell Lung Cancer (NSCLC): Microenvironment and Possible Clinical Implications. Int J Mol Sci. 2022; 23(12): 6832.
CrossRef
Google scholar
|
[19] |
Zhao E, Xu H, Wang L, Kryczek I, Wu K, Hu Y, et al. Bone marrow and the control of immunity. Cell Mol Immunol. 2012; 9(1): 11–19.
CrossRef
Google scholar
|
[20] |
Ponzetti M, Rucci N. Updates on Osteoimmunology: What’s New on the Cross-Talk Between Bone and Immune System. Front Endocrinol (Lausanne). 2019; 10: 236.
CrossRef
Google scholar
|
[21] |
Zhang W, Bado IL, Hu J, Wan YW, Wu L, Wang H, et al. The bone microenvironment invigorates metastatic seeds for further dissemination. Cell. 2021; 184(9): 2471–2486.e20.
CrossRef
Google scholar
|
[22] |
Juárez P, Guise TA. TGF-β in cancer and bone: implications for treatment of bone metastases. Bone. 2011; 48(1): 23–29.
CrossRef
Google scholar
|
[23] |
Singh T, Kaur V, Kumar M, Kaur P, Murthy RS, Rawal RK. The critical role of bisphosphonates to target bone cancer metastasis: an overview. J Drug Target. 2015; 23(1): 1–15.
CrossRef
Google scholar
|
[24] |
Smith MR, Saad F, Coleman R, Shore N, Fizazi K, Tombal B, et al. Denosumab and bone-metastasis-free survival in men with castration-resistant prostate cancer: results of a phase 3, randomised, placebo-controlled trial. Lancet. 2012; 379(9810): 39–46.
CrossRef
Google scholar
|
[25] |
Laccetti AL, Subudhi SK. Immunotherapy for metastatic prostate cancer: immuno-cold or the tip of the iceberg? Curr Opin Urol. 2017; 27(6): 566–571.
CrossRef
Google scholar
|
[26] |
Landi L, D’Incà F, Gelibter A, Chiari R, Grossi F, Delmonte A, et al. Bone metastases and immunotherapy in patients with advanced non-small-cell lung cancer. J Immunother Cancer. 2019; 7(1): 316.
CrossRef
Google scholar
|
[27] |
Murray PJ, Allen JE, Biswas SK, Fisher EA, Gilroy DW, Goerdt S, et al. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity. 2014; 41(1): 14–20.
CrossRef
Google scholar
|
[28] |
Qian BZ, Pollard JW. Macrophage diversity enhances tumor progression and metastasis. Cell. 2010; 141(1): 39–51.
CrossRef
Google scholar
|
[29] |
Yunna C, Mengru H, Lei W, Weidong C. Macrophage M1/M2 polarization. Eur J Pharmacol. 2020; 877: 173090.
CrossRef
Google scholar
|
[30] |
DeNardo DG, Ruffell B. Macrophages as regulators of tumour immunity and immunotherapy. Nat Rev Immunol. 2019; 19(6): 369–382.
CrossRef
Google scholar
|
[31] |
Azizi E, Carr AJ, Plitas G, Cornish AE, Konopacki C, Prabhakaran S, et al. Single-Cell Map of Diverse Immune Phenotypes in the Breast Tumor Microenvironment. Cell. 2018; 174(5): 1293–1308.e36.
CrossRef
Google scholar
|
[32] |
Zhai K, Huang Z, Huang Q, Tao W, Fang X, Zhang A, et al. Pharmacological inhibition of BACE1 suppresses glioblastoma growth by stimulating macrophage phagocytosis of tumor cells. Nat Cancer. 2021; 2(11): 1136–1151.
CrossRef
Google scholar
|
[33] |
Colegio OR, Chu N-Q, Szabo AL, Chu T, Rhebergen AM, Jairam V, et al. Functional polarization of tumour-associated macrophages by tumour-derived lactic acid. Nature. 2014; 513(7519): 559–563.
CrossRef
Google scholar
|
[34] |
Hibino S, Kawazoe T, Kasahara H, Itoh S, Ishimoto T, Sakata-Yanagimoto M. et al. Inflammation-Induced Tumorigenesis and Metastasis. Int J Mol Sci. 2021; 22(11): 5421.
CrossRef
Google scholar
|
[35] |
Bellavia D, Costa V, De Luca A, Cordaro A, Fini M, Giavaresi G, et al. The Binomial “Inflammation-Epigenetics” in Breast Cancer Progression and Bone Metastasis: IL-1β Actions Are Influenced by TET Inhibitor in MCF-7 Cell Line. Int J Mol Sci. 2022; 23(23): 15422.
CrossRef
Google scholar
|
[36] |
Magliacane Trotta S, Adinolfi A, D’Orsi L, Panico S, Mercadante G, Mehlen P, et al. Cancer-derived exosomal Alu RNA promotes colorectal cancer progression. Exp Mol Med. 2024; 56(3): 700–710.
CrossRef
Google scholar
|
[37] |
Pan Y, Yu Y, Wang X, Zhang T. Tumor-Associated Macrophages in Tumor Immunity. Front Immunol. 2020; 11: 583084.
CrossRef
Google scholar
|
[38] |
Munir MT, Kay MK, Kang MH, Rahman MM, Al-Harrasi A. Choudhury M, et al. Tumor-Associated Macrophages as Multifaceted Regulators of Breast Tumor Growth. Int J Mol Sci. 2021; 22(12): 6526.
CrossRef
Google scholar
|
[39] |
Yuan G, Huang Y, Yang ST, Ng A, Yang S. RGS12 inhibits the progression and metastasis of multiple myeloma by driving M1 macrophage polarization and activation in the bone marrow microenvironment. Cancer Commun (Lond). 2022; 42(1): 60–64.
CrossRef
Google scholar
|
[40] |
Lee JH, Kim HN, Kim KO, Jin WJ, Lee S, Kim HH, et al. CXCL10 promotes osteolytic bone metastasis by enhancing cancer outgrowth and osteoclastogenesis. Cancer Res. 2012; 72(13): 3175–3186.
CrossRef
Google scholar
|
[41] |
Shin SY, Nam JS, Lim Y, Lee YH. TNFα-exposed bone marrow-derived mesenchymal stem cells promote locomotion of MDA-MB-231 breast cancer cells through transcriptional activation of CXCR3 ligand chemokines. J Biol Chem. 2010; 285(40): 30731–30740.
CrossRef
Google scholar
|
[42] |
Midavaine É, Côté J, Sarret P. The multifaceted roles of the chemokines CCL2 and CXCL12 in osteophilic metastatic cancers. Cancer Metastasis Rev. 2021; 40(2): 427–445.
CrossRef
Google scholar
|
[43] |
Shen S, Zhang Y, Chen KG, Luo YL, Wang J. Cationic Polymeric Nanoparticle Delivering CCR2 siRNA to Inflammatory Monocytes for Tumor Microenvironment Modification and Cancer Therapy. Mol Pharm. 2018; 15(9): 3642–3653.
CrossRef
Google scholar
|
[44] |
Alsamraae M, Cook LM. Emerging roles for myeloid immune cells in bone metastasis. Cancer Metastasis Rev. 2021; 40(2): 413–425.
CrossRef
Google scholar
|
[45] |
Jiang P, Gao W, Ma T, Wang R, Piao Y, Dong X, et al. CD137 promotes bone metastasis of breast cancer by enhancing the migration and osteoclast differentiation of monocytes/macrophages. Theranostics. 2019; 9(10): 2950–2966.
CrossRef
Google scholar
|
[46] |
Leconet W, Chentouf M, du Manoir S, Chevalier C, Sirvent A, Aït-Arsa I, et al. Therapeutic Activity of Anti-AXL Antibody against Triple-Negative Breast Cancer Patient-Derived Xenografts and Metastasis. Clin Cancer Res. 2017; 23(11): 2806–2816.
CrossRef
Google scholar
|
[47] |
Ma RY, Zhang H, Li XF, Zhang CB, Selli C, Tagliavini G, et al. Monocyte-derived macrophages promote breast cancer bone metastasis outgrowth. J Exp Med. 2020; 217(11): e20191820.
CrossRef
Google scholar
|
[48] |
Wu J, Yang H, Cheng J, Zhang L, Ke Y, Zhu Y, et al. Knockdown of milk-fat globule EGF factor-8 suppresses glioma progression in GL261 glioma cells by repressing microglial M2 polarization. J Cell Physiol. 2020; 235(11): 8679–8690.
CrossRef
Google scholar
|
[49] |
Soki FN, Koh AJ, Jones JD, Kim YW, Dai J, Keller ET, et al. Polarization of prostate cancer-associated macrophages is induced by milk fat globule-EGF factor 8 (MFG-E8)-mediated efferocytosis. J Biol Chem. 2014; 289(35): 24560–24572.
CrossRef
Google scholar
|
[50] |
Rutkowski MR, Stephen TL, Svoronos N, Allegrezza MJ, Tesone AJ, Perales-Puchalt A. et al. Microbially driven TLR5-dependent signaling governs distal malignant progression through tumor-promoting inflammation. Cancer Cell. 2015; 27(1): 27–40.
CrossRef
Google scholar
|
[51] |
Roca H, Jones JD, Purica MC, Weidner S, Koh AJ, Kuo R, et al. Apoptosis-induced CXCL5 accelerates inflammation and growth of prostate tumor metastases in bone. J Clin Invest. 2018; 128(1): 248–266.
CrossRef
Google scholar
|
[52] |
Yu H, Pardoll D, Jove R. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer. 2009; 9(11): 798–809.
CrossRef
Google scholar
|
[53] |
Coscia M, Quaglino E, Iezzi M, Curcio C, Pantaleoni F, Riganti C, et al. Zoledronic acid repolarizes tumour-associated macrophages and inhibits mammary carcinogenesis by targeting the mevalonate pathway. J Cell Mol Med. 2010; 14(12): 2803–2815.
CrossRef
Google scholar
|
[54] |
Battafarano G, Rossi M, Marampon F, Del Fattore A. Cellular and Molecular Mediators of Bone Metastatic Lesions. Int J Mol Sci. 2018; 19(6): 1709.
CrossRef
Google scholar
|
[55] |
Huang Z, Zhang Z, Jiang Y, Zhang D, Chen J, Dong L, et al. Targeted delivery of oligonucleotides into tumor-associated macrophages for cancer immunotherapy. J Control Release. 2012; 158(2): 286–292.
CrossRef
Google scholar
|
[56] |
Ma S, Li X, Mai Y, Guo J, Zuo W, Yang J. Immunotherapeutic treatment of lung cancer and bone metastasis with a mPLA/mRNA tumor vaccine. Acta Biomater. 2023; 169: 489–499.
CrossRef
Google scholar
|
[57] |
Jiang J, Mei J, Yi S, Feng C, Ma Y, Liu Y, et al. Tumor associated macrophage and microbe: The potential targets of tumor vaccine delivery. Adv Drug Deliv Rev. 2022; 180: 114046.
CrossRef
Google scholar
|
[58] |
Ge YW, Liu XL, Yu DG, Zhu ZA, Ke QF, Mao YQ, et al. Graphene-modified CePO4 nanorods effectively treat breast cancer-induced bone metastases and regulate macrophage polarization to improve osteo-inductive ability. J Nanobiotechnology. 2021; 19(1): 11.
CrossRef
Google scholar
|
[59] |
Bliss SA, Sinha G, Sandiford OA, Williams LM, Engelberth DJ, Guiro K, et al. Mesenchymal Stem Cell-Derived Exosomes Stimulate Cycling Quiescence and Early Breast Cancer Dormancy in Bone Marrow. Cancer Res. 2016; 76(19): 5832–5844.
CrossRef
Google scholar
|
[60] |
Sosa MS, Bragado P, Aguirre-Ghiso JA. Mechanisms of disseminated cancer cell dormancy: an awakening field. Nat Rev Cancer. 2014; 14(9): 611–622.
CrossRef
Google scholar
|
[61] |
Hosseini H, Obradović MMS, Hoffmann M, Harper KL, Sosa MS, Werner-Klein M. et al. Early dissemination seeds metastasis in breast cancer. Nature. 2016; 540(7634): 552–558.
CrossRef
Google scholar
|
[62] |
Walker ND, Elias M, Guiro K, Bhatia R, Greco SJ, Bryan M, et al. Exosomes from differentially activated macrophages influence dormancy or resurgence of breast cancer cells within bone marrow stroma. Cell Death Dis. 2019; 10(2): 59.
CrossRef
Google scholar
|
[63] |
Choi SH, Kim AR, Nam JK, Kim JM, Kim JY, Seo HR, et al. Tumour-vasculature development via endothelial-to-mesenchymal transition after radiotherapy controls CD44v6(+) cancer cell and macrophage polarization. Nat Commun. 2018; 9(1): 5108.
CrossRef
Google scholar
|
[64] |
Boyce BF. Advances in the regulation of osteoclasts and osteoclast functions. J Dent Res. 2013; 92(10): 860–867.
CrossRef
Google scholar
|
[65] |
Jacome-Galarza CE, Percin GI, Muller JT, Mass E, Lazarov T, Eitler J, et al. Developmental origin, functional maintenance and genetic rescue of osteoclasts. Nature. 2019; 568(7753): 541–545.
CrossRef
Google scholar
|
[66] |
Maurizi A, Rucci N. The Osteoclast in Bone Metastasis: Player and Target. Cancers (Basel). 2018; 10(7): 218.
CrossRef
Google scholar
|
[67] |
Kim JM, Lin C, Stavre Z, Greenblatt MB, Shim JH. Osteoblast-Osteoclast Communication and Bone Homeostasis. Cells. 2020; 9(9): 2073.
CrossRef
Google scholar
|
[68] |
Sun Y, Li J, Xie X, Gu F, Sui Z, Zhang K, et al. Macrophage-Osteoclast Associations: Origin, Polarization, and Subgroups. Front Immunol. 2021; 12: 778078.
CrossRef
Google scholar
|
[69] |
Kuo PL, Liao SH, Hung JY, Huang MS, Hsu YL. MicroRNA-33a functions as a bone metastasis suppressor in lung cancer by targeting parathyroid hormone related protein. Biochim Biophys Acta. 2013; 1830(6): 3756–3766.
CrossRef
Google scholar
|
[70] |
Esposito M, Mondal N, Greco TM, Wei Y, Spadazzi C, Lin SC, et al. Bone vascular niche E-selectin induces mesenchymal-epithelial transition and Wnt activation in cancer cells to promote bone metastasis. Nat Cell Biol. 2019; 21(5): 627–639.
CrossRef
Google scholar
|
[71] |
Celià-Terrassa T, Kang Y. Metastatic niche functions and therapeutic opportunities. Nat Cell Biol. 2018; 20(8): 868–877.
CrossRef
Google scholar
|
[72] |
Todd VM, Johnson RW. Hypoxia in bone metastasis and osteolysis. Cancer Lett. 2020; 489: 144–154.
CrossRef
Google scholar
|
[73] |
Yuan X, Qian N, Ling S, Li Y, Sun W, Li J, et al. Breast cancer exosomes contribute to pre-metastatic niche formation and promote bone metastasis of tumor cells. Theranostics. 2021; 11(3): 1429–1445.
CrossRef
Google scholar
|
[74] |
Yu L, Sui B, Fan W, Lei L, Zhou L, Yang L, et al. Exosomes derived from osteogenic tumor activate osteoclast differentiation and concurrently inhibit osteogenesis by transferring COL1A1-targeting miRNA-92a-1-5p. J Extracell Vesicles. 2021; 10(3): e12056.
CrossRef
Google scholar
|
[75] |
Wang K, Donnelly CR, Jiang C, Liao Y, Luo X, Tao X, et al. STING suppresses bone cancer pain via immune and neuronal modulation. Nat Commun. 2021; 12(1): 4558.
CrossRef
Google scholar
|
[76] |
Wang K, Gu Y, Liao Y, Bang S, Donnelly CR, Chen O, et al. PD-1 blockade inhibits osteoclast formation and murine bone cancer pain. J Clin Invest. 2020; 130(7): 3603–3620.
CrossRef
Google scholar
|
[77] |
Khan UA, Hashimi SM, Bakr MM, Forwood MR, Morrison NA. CCL2 and CCR2 are Essential for the Formation of Osteoclasts and Foreign Body Giant Cells. J Cell Biochem. 2016; 117(2): 382–389.
CrossRef
Google scholar
|
[78] |
Gao YJ, Cheng JK, Zeng Q, Xu ZZ, Decosterd I, Xu X, et al. Selective inhibition of JNK with a peptide inhibitor attenuates pain hypersensitivity and tumor growth in a mouse skin cancer pain model. Exp Neurol. 2009; 219(1): 146–155.
CrossRef
Google scholar
|
[79] |
Abbadie C, Bhangoo S, De Koninck Y, Malcangio M, Melik-Parsadaniantz S. White FA. Chemokines and pain mechanisms. Brain Res Rev. 2009; 60(1): 125–134.
CrossRef
Google scholar
|
[80] |
Xie RG, Gao YJ, Park CK, Lu N, Luo C, Wang WT, et al. Spinal CCL2 Promotes Central Sensitization, Long-Term Potentiation. and Inflammatory Pain via CCR2: Further Insights into Molecular, Synaptic, and Cellular Mechanisms. Neurosci Bull. 2018; 34(1): 13–21.
CrossRef
Google scholar
|
[81] |
Yue Z, Niu X, Yuan Z, Qin Q, Jiang W, He L, et al. RSPO2 and RANKL signal through LGR4 to regulate osteoclastic premetastatic niche formation and bone metastasis. J Clin Invest. 2022; 132(2): e144579.
CrossRef
Google scholar
|
[82] |
Zeeuwen PL, Cheng T, Schalkwijk J. The biology of cystatin M/E and its cognate target proteases. J Invest Dermatol. 2009; 129(6): 1327–1338.
CrossRef
Google scholar
|
[83] |
Jin L, Zhang Y, Li H, Yao L, Fu D, Yao X, et al. Differential secretome analysis reveals CST6 as a suppressor of breast cancer bone metastasis. Cell Res. 2012; 22(9): 1356–1373.
CrossRef
Google scholar
|
[84] |
Rivenbark AG, Jones WD, Coleman WB. DNA methylation-dependent silencing of CST6 in human breast cancer cell lines. Lab Invest. 2006; 86(12): 1233–1242.
CrossRef
Google scholar
|
[85] |
Li X, Liang Y, Lian C, Peng F, Xiao Y, He Y, et al. CST6 protein and peptides inhibit breast cancer bone metastasis by suppressing CTSB activity and osteoclastogenesis. Theranostics. 2021; 11(20): 9821–9832.
CrossRef
Google scholar
|
[86] |
Cocucci E, Meldolesi J. Ectosomes and exosomes: shedding the confusion between extracellular vesicles. Trends Cell Biol. 2015; 25(6): 364–372.
CrossRef
Google scholar
|
[87] |
Savci-Heijink CD, Halfwerk H, Hooijer GK, Horlings HM, Wesseling J, van de Vijver MJ. Retrospective analysis of metastatic behaviour of breast cancer subtypes. Breast Cancer Res Treat. 2015; 150(3): 547–557.
CrossRef
Google scholar
|
[88] |
Ouchida M, Kanzaki H, Ito S, Hanafusa H, Jitsumori Y, Tamaru S, et al. Novel direct targets of miR-19a identified in breast cancer cells by a quantitative proteomic approach. PLoS One. 2012; 7(8): e44095.
CrossRef
Google scholar
|
[89] |
Wu K, Feng J, Lyu F, Xing F, Sharma S, Liu Y, et al. Exosomal miR-19a and IBSP cooperate to induce osteolytic bone metastasis of estrogen receptor-positive breast cancer. Nat Commun. 2021; 12(1): 5196.
CrossRef
Google scholar
|
[90] |
Kang Y. Dissecting Tumor-Stromal Interactions in Breast Cancer Bone Metastasis. Endocrinol Metab (Seoul). 2016; 31(2): 206–212.
CrossRef
Google scholar
|
[91] |
Fournier PG, Juárez P, Jiang G, Clines GA, Niewolna M, Kim HS, et al. The TGF-β Signaling Regulator PMEPA1 Suppresses Prostate Cancer Metastases to Bone. Cancer Cell. 2015; 27(6): 809–821.
CrossRef
Google scholar
|
[92] |
Sethi N, Dai X, Winter CG, Kang Y. Tumor-derived JAGGED1 promotes osteolytic bone metastasis of breast cancer by engaging notch signaling in bone cells. Cancer Cell. 2011; 19(2): 192–205.
CrossRef
Google scholar
|
[93] |
Javelaud D, Mohammad KS, McKenna CR, Fournier P, Luciani F, Niewolna M, et al. Stable overexpression of Smad7 in human melanoma cells impairs bone metastasis. Cancer Res. 2007; 67(5): 2317–2324.
CrossRef
Google scholar
|
[94] |
Mohammad KS, Javelaud D, Fournier PG, Niewolna M, McKenna CR, Peng XH, et al. TGF-beta-RI kinase inhibitor SD-208 reduces the development and progression of melanoma bone metastases. Cancer Res. 2011; 71(1): 175–184.
CrossRef
Google scholar
|
[95] |
Danielpour D. Advances and Challenges in Targeting TGF-β Isoforms for Therapeutic Intervention of Cancer: A Mechanism-Based Perspective. Pharmaceuticals (Basel). 2024; 17(4): 533.
CrossRef
Google scholar
|
[96] |
Kang J, La Manna F, Bonollo F, Sampson N, Alberts IL, Mingels C, et al. Tumor microenvironment mechanisms and bone metastatic disease progression of prostate cancer. Cancer Lett. 2022; 530: 156–169.
CrossRef
Google scholar
|
[97] |
Özdemir BC, Hensel J, Secondini C, Wetterwald A, Schwaninger R, Fleischmann A, et al. The molecular signature of the stroma response in prostate cancer-induced osteoblastic bone metastasis highlights expansion of hematopoietic and prostate epithelial stem cell niches. PLoS One. 2014; 9(12): e114530.
CrossRef
Google scholar
|
[98] |
Lin SC, Yu-Lee LY. Lin SH. Osteoblastic Factors in Prostate Cancer Bone Metastasis. Curr Osteoporos Rep. 2018; 16(6): 642–647.
CrossRef
Google scholar
|
[99] |
Keller ET, Brown J. Prostate cancer bone metastases promote both osteolytic and osteoblastic activity. J Cell Biochem. 2004; 91(4): 718–729.
CrossRef
Google scholar
|
[100] |
Abe E, Yamamoto M, Taguchi Y, Lecka-Czernik B. O’Brien CA, Economides AN, et al. Essential requirement of BMPs-2/4 for both osteoblast and osteoclast formation in murine bone marrow cultures from adult mice: antagonism by noggin. J Bone Miner Res. 2000; 15(4): 663–673.
CrossRef
Google scholar
|
[101] |
Lawson MA, McDonald MM, Kovacic N, Hua Khoo W, Terry RL, Down J, et al. Osteoclasts control reactivation of dormant myeloma cells by remodelling the endosteal niche. Nat Commun. 2015; 6: 8983.
CrossRef
Google scholar
|
[102] |
Kan C, Vargas G, Pape FL, Clézardin P. Cancer Cell Colonisation in the Bone Microenvironment. Int J Mol Sci. 2016; 17(10): 1674.
CrossRef
Google scholar
|
[103] |
Price TT, Burness ML, Sivan A, Warner MJ, Cheng R, Lee CH, et al. Dormant breast cancer micrometastases reside in specific bone marrow niches that regulate their transit to and from bone. Sci Transl Med. 2016; 8(340): 340ra73.
CrossRef
Google scholar
|
[104] |
Shen Y, Lv Y. Dual targeted zeolitic imidazolate framework nanoparticles for treating metastatic breast cancer and inhibiting bone destruction. Colloids Surf B Biointerfaces. 2022; 219: 112826.
CrossRef
Google scholar
|
[105] |
Veglia F, Gabrilovich DI. Dendritic cells in cancer: the role revisited. Curr Opin Immunol. 2017; 45: 43–51.
CrossRef
Google scholar
|
[106] |
Wooster AL, Girgis LH, Brazeale H, Anderson TS, Wood LM, Lowe DB. Dendritic cell vaccine therapy for colorectal cancer. Pharmacol Res. 2021; 164: 105374.
CrossRef
Google scholar
|
[107] |
Zong J, Keskinov AA, Shurin GV, Shurin MR. Tumor-derived factors modulating dendritic cell function. Cancer Immunol Immunother. 2016; 65(7): 821–833.
CrossRef
Google scholar
|
[108] |
Brown RD, Pope B, Murray A, Esdale W, Sze DM, Gibson J, et al. Dendritic cells from patients with myeloma are numerically normal but functionally defective as they fail to up-regulate CD80 (B7-1) expression after huCD40LT stimulation because of inhibition by transforming growth factor-beta1 and interleukin-10. Blood. 2001; 98(10): 2992–2998.
CrossRef
Google scholar
|
[109] |
Tucci M, Stucci S, Strippoli S, Dammacco F, Silvestris F. Dendritic cells and malignant plasma cells: an alliance in multiple myeloma tumor progression? Oncologist. 2011; 16(7): 1040–1048.
CrossRef
Google scholar
|
[110] |
Nguyen-Pham TN, Lee YK, Lee HJ, Kim MH, Yang DH, Kim HJ, et al. Cellular immunotherapy using dendritic cells against multiple myeloma. Korean J Hematol. 2012; 47(1): 17–27.
CrossRef
Google scholar
|
[111] |
Schatz A, Mian BM. Current and emerging trends in prostate cancer immunotherapy. Asian J Androl. 2017; 21(1): 6–11.
CrossRef
Google scholar
|
[112] |
Fuessel S, Meye A, Schmitz M, Zastrow S, Linné C, Richter K, et al. Vaccination of hormone-refractory prostate cancer patients with peptide cocktail-loaded dendritic cells: results of a phase I clinical trial. Prostate. 2006; 66(8): 811–821.
CrossRef
Google scholar
|
[113] |
Jackson AM, Mulcahy LA, Zhu XW, O’Donnell D, Patel PM. Tumour-mediated disruption of dendritic cell function: inhibiting the MEK1/2-p44/42 axis restores IL-12 production and Th1-generation. Int J Cancer. 2008; 123(3): 623–632.
CrossRef
Google scholar
|
[114] |
Kraeber-Bodéré F, Campion L, Rousseau C, Bourdin S, Chatal JF, Resche I. Treatment of bone metastases of prostate cancer with strontium-89 chloride: efficacy in relation to the degree of bone involvement. Eur J Nucl Med. 2000; 27(10): 1487–1493.
CrossRef
Google scholar
|
[115] |
Liu J, Li J, Fan Y, Chang K, Yang X, Zhu W, et al. Concurrent dendritic cell vaccine and strontium-89 radiation therapy in the management of multiple bone metastases. Ir J Med Sci. 2015; 184(2): 457–461.
CrossRef
Google scholar
|
[116] |
De Silva NH, Akazawa T, Wijewardana V, Inoue N, Oyamada M, Ohta A, et al. Development of effective tumor immunotherapy using a novel dendritic cell-targeting Toll-like receptor ligand. PLoS One. 2017; 12(11): e0188738.
CrossRef
Google scholar
|
[117] |
Akazawa T, Ohashi T, Nakajima H, Nishizawa Y, Kodama K, Sugiura K, et al. Development of a dendritic cell-targeting lipopeptide as an immunoadjuvant that inhibits tumor growth without inducing local inflammation. Int J Cancer. 2014; 135(12): 2847–2856.
CrossRef
Google scholar
|
[118] |
Simons JW, Sacks N. Granulocyte-macrophage colony-stimulating factor-transduced allogeneic cancer cellular immunotherapy: the GVAX vaccine for prostate cancer. Urol Oncol. 2006; 24(5): 419–424.
CrossRef
Google scholar
|
[119] |
Stary G, Bangert C, Tauber M, Strohal R, Kopp T, Stingl G. Tumoricidal activity of TLR7/8-activated inflammatory dendritic cells. J Exp Med. 2007; 204(6): 1441–1451.
CrossRef
Google scholar
|
[120] |
Drobits B, Holcmann M, Amberg N, Swiecki M, Grundtner R, Hammer M, et al. Imiquimod clears tumors in mice independent of adaptive immunity by converting pDCs into tumor-killing effector cells. J Clin Invest. 2012; 122(2): 575–585.
CrossRef
Google scholar
|
[121] |
Xiao W, Chan A, Waarts MR, Mishra T, Liu Y, Cai SF, et al. Plasmacytoid dendritic cell expansion defines a distinct subset of RUNX1-mutated acute myeloid leukemia. Blood. 2021; 137(10): 1377–1391.
CrossRef
Google scholar
|
[122] |
Sawant A, Hensel JA, Chanda D, Harris BA, Siegal GP, Maheshwari A, et al. Depletion of plasmacytoid dendritic cells inhibits tumor growth and prevents bone metastasis of breast cancer cells. J Immunol. 2012; 189(9): 4258–4265.
CrossRef
Google scholar
|
[123] |
Sax MJ, Gasch C, Athota VR, Freeman R, Rasighaemi P, Westcott DE, et al. Cancer cell CCL5 mediates bone marrow independent angiogenesis in breast cancer. Oncotarget. 2016; 7(51): 85437–85449.
CrossRef
Google scholar
|
[124] |
Fujimoto H, Sangai T, Ishii G, Ikehara A, Nagashima T, Miyazaki M, et al. Stromal MCP-1 in mammary tumors induces tumor-associated macrophage infiltration and contributes to tumor progression. Int J Cancer. 2009; 125(6): 1276–1284.
CrossRef
Google scholar
|
[125] |
Chaperot L, Perrot I, Jacob MC, Blanchard D, Salaun V, Deneys V, et al. Leukemic plasmacytoid dendritic cells share phenotypic and functional features with their normal counterparts. Eur J Immunol. 2004; 34(2): 418–426.
CrossRef
Google scholar
|
[126] |
Budhwar S, Verma P, Verma R, Rai S, Singh K. The Yin and Yang of Myeloid Derived Suppressor Cells. Front Immunol. 2018; 9: 2776.
CrossRef
Google scholar
|
[127] |
Ling Z, Yang C, Tan J, Dou C, Chen Y. Beyond immunosuppressive effects: dual roles of myeloid-derived suppressor cells in bone-related diseases. Cell Mol Life Sci. 2021; 78(23): 7161–7183.
CrossRef
Google scholar
|
[128] |
Nakamura K, Smyth MJ. Myeloid immunosuppression and immune checkpoints in the tumor microenvironment. Cell Mol Immunol. 2020; 17(1): 1–12.
CrossRef
Google scholar
|
[129] |
Hegde S, Leader AM, Merad M. MDSC: Markers, development, states, and unaddressed complexity. Immunity. 2021; 54(5): 875–884.
CrossRef
Google scholar
|
[130] |
Tesi RJ. MDSC; the Most Important Cell You Have Never Heard Of. Trends Pharmacol Sci. 2019; 40(1): 4–7.
CrossRef
Google scholar
|
[131] |
Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol. 2009; 9(3): 162–174.
CrossRef
Google scholar
|
[132] |
Hinshaw DC, Shevde LA. The Tumor Microenvironment Innately Modulates Cancer Progression. Cancer Res. 2019; 79(18): 4557–4566.
CrossRef
Google scholar
|
[133] |
Chen C, Huang R, Zhou J, Guo L, Xiang S. Formation of pre-metastatic bone niche in prostate cancer and regulation of traditional chinese medicine. Front Pharmacol. 2022; 13: 897942.
CrossRef
Google scholar
|
[134] |
Wang Y, Ding Y, Guo N, Wang S. MDSCs: Key Criminals of Tumor Pre-metastatic Niche Formation. Front Immunol. 2019; 10: 172.
CrossRef
Google scholar
|
[135] |
Zhao W, Xu Y, Xu J, Wu D, Zhao B, Yin Z, et al. Subsets of myeloid-derived suppressor cells in hepatocellular carcinoma express chemokines and chemokine receptors differentially. Int Immunopharmacol. 2015; 26(2): 314–321.
CrossRef
Google scholar
|
[136] |
Korbecki J, Simińska D, Kojder K, Grochans S, Gutowska I, Chlubek D, et al. Fractalkine/CX3CL1 in Neoplastic Processes. Int J Mol Sci. 2020; 21(10): 3723.
CrossRef
Google scholar
|
[137] |
Danilin S, Merkel AR, Johnson JR, Johnson RW, Edwards JR, Sterling JA. Myeloid-derived suppressor cells expand during breast cancer progression and promote tumor-induced bone destruction. Oncoimmunology. 2012; 1(9): 1484–1494.
CrossRef
Google scholar
|
[138] |
Van Valckenborgh E, Schouppe E, Movahedi K, De Bruyne E, Menu E, De Baetselier P, et al. Multiple myeloma induces the immunosuppressive capacity of distinct myeloid-derived suppressor cell subpopulations in the bone marrow. Leukemia. 2012; 26(11): 2424–2428.
CrossRef
Google scholar
|
[139] |
Wang G, Lu X, Dey P, Deng P, Wu CC, Jiang S, et al. Targeting YAP-Dependent MDSC Infiltration Impairs Tumor Progression. Cancer Discov. 2016; 6(1): 80–95.
CrossRef
Google scholar
|
[140] |
Wen J, Huang G, Liu S, Wan J, Wang X, Zhu Y, et al. Polymorphonuclear MDSCs are enriched in the stroma and expanded in metastases of prostate cancer. J Pathol Clin Res. 2020; 6(3): 171–177.
CrossRef
Google scholar
|
[141] |
Sawant A, Deshane J, Jules J, Lee CM, Harris BA, Feng X, et al. Myeloid-derived suppressor cells function as novel osteoclast progenitors enhancing bone loss in breast cancer. Cancer Res. 2013; 73(2): 672–682.
CrossRef
Google scholar
|
[142] |
Sawant A, Ponnazhagan S. Myeloid-derived suppressor cells as osteoclast progenitors: a novel target for controlling osteolytic bone metastasis. Cancer Res. 2013; 73(15): 4606–4610.
CrossRef
Google scholar
|
[143] |
Sawant A, Ponnazhagan S. Myeloid-derived suppressor cells as a novel target for the control of osteolytic bone disease. Oncoimmunology. 2013; 2(5): e24064.
CrossRef
Google scholar
|
[144] |
Sinha P, Clements VK, Bunt SK, Albelda SM, Ostrand-Rosenberg S. Cross-talk between myeloid-derived suppressor cells and macrophages subverts tumor immunity toward a type 2 response. J Immunol. 2007; 179(2): 977–983.
CrossRef
Google scholar
|
[145] |
Rosales C, Lowell CA, Schnoor M, Uribe-Querol E. Neutrophils: Their Role in Innate and Adaptive Immunity 2017. J Immunol Res. 2017; 2017: 9748345.
CrossRef
Google scholar
|
[146] |
Amulic B, Cazalet C, Hayes GL, Metzler KD, Zychlinsky A. Neutrophil function: from mechanisms to disease. Annu Rev Immunol. 2012; 30: 459–489.
CrossRef
Google scholar
|
[147] |
Kolaczkowska E, Kubes P. Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol. 2013; 13(3): 159–175.
CrossRef
Google scholar
|
[148] |
Liang W, Ferrara N. The Complex Role of Neutrophils in Tumor Angiogenesis and Metastasis. Cancer Immunol Res. 2016; 4(2): 83–91.
CrossRef
Google scholar
|
[149] |
Mantovani A. The yin-yang of tumor-associated neutrophils. Cancer Cell. 2009; 16(3): 173–174.
CrossRef
Google scholar
|
[150] |
Piccard H, Muschel RJ, Opdenakker G. On the dual roles and polarized phenotypes of neutrophils in tumor development and progression. Crit Rev Oncol Hematol. 2012; 82(3): 296–309.
CrossRef
Google scholar
|
[151] |
Fridlender ZG, Sun J, Kim S, Kapoor V, Cheng G, Ling L, et al. Polarization of tumor-associated neutrophil phenotype by TGF-beta: “N1” versus “N2” TAN. Cancer Cell. 2009; 16(3): 183–194.
CrossRef
Google scholar
|
[152] |
Luca M, Huang S, Gershenwald JE, Singh RK, Reich R, Bar-Eli M. Expression of interleukin-8 by human melanoma cells up-regulates MMP-2 activity and increases tumor growth and metastasis. Am J Pathol. 1997; 151(4): 1105–1113.
|
[153] |
De Larco JE, Wuertz BR, Rosner KA, Erickson SA, Gamache DE, Manivel JC, et al. A potential role for interleukin-8 in the metastatic phenotype of breast carcinoma cells. Am J Pathol. 2001; 158(2): 639–646.
CrossRef
Google scholar
|
[154] |
Borregaard N, Sørensen OE, Theilgaard-Mönch K. Neutrophil granules: a library of innate immunity proteins. Trends Immunol. 2007; 28(8): 340–345.
CrossRef
Google scholar
|
[155] |
De Larco JE, Wuertz BR, Furcht LT. The potential role of neutrophils in promoting the metastatic phenotype of tumors releasing interleukin-8. Clin Cancer Res. 2004; 10(15): 4895–4900.
CrossRef
Google scholar
|
[156] |
Lin Q, Fang X, Liang G, Luo Q, Cen Y, Shi Y, et al. Silencing CTNND1 Mediates Triple-Negative Breast Cancer Bone Metastasis via Upregulating CXCR4/CXCL12 Axis and Neutrophils Infiltration in Bone. Cancers (Basel). 2021; 13(22): 5703.
CrossRef
Google scholar
|
[157] |
Kolonin MG, Sergeeva A, Staquicini DI, Smith TL, Tarleton CA, Molldrem JJ, et al. Interaction between Tumor Cell Surface Receptor RAGE and Proteinase 3 Mediates Prostate Cancer Metastasis to Bone. Cancer Res. 2017; 77(12): 3144–3150.
CrossRef
Google scholar
|
[158] |
Taguchi A, Blood DC, del Toro G, Canet A, Lee DC, Qu W, et al. Blockade of RAGE-amphoterin signalling suppresses tumour growth and metastases. Nature. 2000; 405(6784): 354–360.
CrossRef
Google scholar
|
[159] |
Yin C, Wang M, Wang Y, Lin Q, Lin K, Du H, et al. BHLHE22 drives the immunosuppressive bone tumor microenvironment and associated bone metastasis in prostate cancer. J Immunother Cancer. 2023; 11(3): e005532.
CrossRef
Google scholar
|
[160] |
Albrengues J, Shields MA, Ng D, Park CG, Ambrico A, Poindexter ME, et al. Neutrophil extracellular traps produced during inflammation awaken dormant cancer cells in mice. Science. 2018; 361(6409): eaao4227.
CrossRef
Google scholar
|
[161] |
Koga Y, Matsuzaki A, Suminoe A, Hattori H, Hara T. Neutrophil-derived TNF-related apoptosis-inducing ligand (TRAIL): a novel mechanism of antitumor effect by neutrophils. Cancer Res. 2004; 64(3): 1037–1043.
CrossRef
Google scholar
|
[162] |
Costanzo-Garvey DL, Keeley T, Case AJ, Watson GF, Alsamraae M, Yu Y, et al. Neutrophils are mediators of metastatic prostate cancer progression in bone. Cancer Immunol Immunother. 2020; 69(6): 1113–1130.
CrossRef
Google scholar
|
[163] |
Ma X, Fan Y, Chen Z, Zhang Y, Wang S, Yu J. Blood biomarkers of bone metastasis in digestive tract malignant tumors. Future Oncol. 2021; 17(12): 1507–1518.
CrossRef
Google scholar
|
[164] |
Thio Q, Goudriaan WA, Janssen SJ, Paulino Pereira NR, Sciubba DM, Rosovksy RP, et al. Prognostic role of neutrophil-to-lymphocyte ratio and platelet-to-lymphocyte ratio in patients with bone metastases. Br J Cancer. 2018; 119(6): 737–743.
CrossRef
Google scholar
|
[165] |
Weller PF, Spencer LA. Functions of tissue-resident eosinophils. Nat Rev Immunol. 2017; 17(12): 746–760.
CrossRef
Google scholar
|
[166] |
Chusid MJ. Eosinophils: Friends or Foes? J Allergy Clin Immunol Pract. 2018; 6(5): 1439–1444.
CrossRef
Google scholar
|
[167] |
Grisaru-Tal S, Itan M, Grass DG, Torres-Roca J. Eschrich SA, Gordon Y, et al. Primary tumors from mucosal barrier organs drive unique eosinophil infiltration patterns and clinical associations. Oncoimmunology. 2020; 10(1): 1859732.
CrossRef
Google scholar
|
[168] |
Grisaru-Tal S, Rothenberg ME, Munitz A. Eosinophil-lymphocyte interactions in the tumor microenvironment and cancer immunotherapy. Nat Immunol. 2022; 23(9): 1309–1316.
CrossRef
Google scholar
|
[169] |
Zaynagetdinov R, Sherrill TP, Gleaves LA, McLoed AG, Saxon JA, Habermann AC, et al. Interleukin-5 facilitates lung metastasis by modulating the immune microenvironment. Cancer Res. 2015; 75(8): 1624–1634.
CrossRef
Google scholar
|
[170] |
Ikutani M, Yanagibashi T, Ogasawara M, Tsuneyama K, Yamamoto S, Hattori Y, et al. Identification of innate IL-5-producing cells and their role in lung eosinophil regulation and antitumor immunity. J Immunol. 2012; 188(2): 703–713.
CrossRef
Google scholar
|
[171] |
Li F, Du X, Lan F, Li N, Zhang C, Zhu C, et al. Eosinophilic inflammation promotes CCL6-dependent metastatic tumor growth. Sci Adv. 2021; 7(22): eabb5943.
CrossRef
Google scholar
|
[172] |
Miyake K, Ito J, Karasuyama H. Role of Basophils in a Broad Spectrum of Disorders. Front Immunol. 2022; 13: 902494.
CrossRef
Google scholar
|
[173] |
Liu Q, Luo D, Cai S, Li Q, Li X. Circulating basophil count as a prognostic marker of tumor aggressiveness and survival outcomes in colorectal cancer. Clin Transl Med. 2020; 9(1): 6.
CrossRef
Google scholar
|
[174] |
Wang C, Chen YG, Gao JL, Lyu GY, Su J, Zhang QI, et al. Low local blood perfusion, high white blood cell and high platelet count are associated with primary tumor growth and lung metastasis in a 4T1 mouse breast cancer metastasis model. Oncol Lett. 2015; 10(2): 754–760.
CrossRef
Google scholar
|
[175] |
Sektioglu IM, Carretero R, Bulbuc N, Bald T, Tüting T, Rudensky AY, et al. Basophils Promote Tumor Rejection via Chemotaxis and Infiltration of CD8+ T Cells. Cancer Res. 2017; 77(2): 291–302.
CrossRef
Google scholar
|
[176] |
Lakshmi Narendra B, Eshvendar Reddy K, Shantikumar S, Ramakrishna S. Immune system: a double-edged sword in cancer. Inflamm Res. 2013; 62(9): 823–834.
CrossRef
Google scholar
|
[177] |
Chen ML, Pittet MJ, Gorelik L, Flavell RA, Weissleder R, von Boehmer H, et al. Regulatory T cells suppress tumor-specific CD8 T cell cytotoxicity through TGF-beta signals in vivo. Proc Natl Acad Sci U S A. 2005; 102(2): 419–424.
CrossRef
Google scholar
|
[178] |
Knutson KL, Disis ML, Salazar LG. CD4 regulatory T cells in human cancer pathogenesis. Cancer Immunol Immunother. 2007; 56(3): 271–285.
CrossRef
Google scholar
|
[179] |
Marshall EA, Ng KW, Kung SH, Conway EM, Martinez VD, Halvorsen EC, et al. Emerging roles of T helper 17 and regulatory T cells in lung cancer progression and metastasis. Mol Cancer. 2016; 15(1): 67.
CrossRef
Google scholar
|
[180] |
Choi Y, Woo KM, Ko SH, Lee YJ, Park SJ, Kim HM, et al. Osteoclastogenesis is enhanced by activated B cells but suppressed by activated CD8(+) T cells. Eur J Immunol. 2001; 31(7): 2179–2188.
CrossRef
Google scholar
|
[181] |
Grcević D, Lukić IK, Kovacić N, Ivcević S, Katavić V, Marusić A. Activated T lymphocytes suppress osteoclastogenesis by diverting early monocyte/macrophage progenitor lineage commitment towards dendritic cell differentiation through down-regulation of receptor activator of nuclear factor-kappaB and c-Fos. Clin Exp Immunol. 2006; 146(1): 146–158.
CrossRef
Google scholar
|
[182] |
Monteiro AC, Leal AC, Gonçalves-Silva T, Mercadante AC, Kestelman F, Chaves SB, et al. T cells induce pre-metastatic osteolytic disease and help bone metastases establishment in a mouse model of metastatic breast cancer. PLoS One. 2013; 8(7): e68171.
CrossRef
Google scholar
|
[183] |
Monteiro AC, Bonomo A. CD8(+) T cells from experimental in situ breast carcinoma interfere with bone homeostasis. Bone. 2021; 150: 116014.
CrossRef
Google scholar
|
[184] |
Sato K, Suematsu A, Okamoto K, Yamaguchi A, Morishita Y, Kadono Y, et al. Th17 functions as an osteoclastogenic helper T cell subset that links T cell activation and bone destruction. J Exp Med. 2006; 203(12): 2673–2682.
CrossRef
Google scholar
|
[185] |
Kfoury Y, Baryawno N, Severe N, Mei S, Gustafsson K, Hirz T, et al. Human prostate cancer bone metastases have an actionable immunosuppressive microenvironment. Cancer Cell. 2021; 39(11): 1464–1478.e8.
CrossRef
Google scholar
|
[186] |
Santini D, Barni S, Intagliata S, Falcone A, Ferraù F, Galetta D, et al. Natural History of Non-Small-Cell Lung Cancer with Bone Metastases. Sci Rep. 2015; 5: 18670.
CrossRef
Google scholar
|
[187] |
Nigam R, Field M, Harris G, Barton M, Carolan M, Metcalfe P, et al. Automated detection, delineation and quantification of whole-body bone metastasis using FDG-PET/CT images. Phys Eng Sci Med. 2023; 46(2): 851–863.
CrossRef
Google scholar
|
[188] |
Liang H, Chen Q, Hu Z, Zhou L, Meng Q, Zhang T, et al. Siglec15 facilitates the progression of non-small cell lung cancer and is correlated with spinal metastasis. Ann Transl Med. 2022; 10(6): 281.
CrossRef
Google scholar
|
[189] |
Yang XR, Pi C, Zhang YC, Chen ZH, Zhang XC, Zhu DQ, et al. Heterogeneity in the immune microenvironment of bone metastasis in driver-positive non-small cell lung cancer. Mol Carcinog. 2023; 62(7): 1001–1008.
CrossRef
Google scholar
|
[190] |
Wu H, Xia L, Jia D, Zou H, Jin G, Qian W, et al. PD-L1(+) regulatory B cells act as a T cell suppressor in a PD-L1-dependent manner in melanoma patients with bone metastasis. Mol Immunol. 2020; 119: 83–91.
CrossRef
Google scholar
|
[191] |
Zuo H, Wan Y. Inhibition of myeloid PD-L1 suppresses osteoclastogenesis and cancer bone metastasis. Cancer Gene Ther. 2022; 29(10): 1342–1354.
CrossRef
Google scholar
|
[192] |
Barrueto L, Caminero F, Cash L, Makris C, Lamichhane P, Deshmukh RR. Resistance to Checkpoint Inhibition in Cancer Immunotherapy. Transl Oncol. 2020; 13(3): 100738.
CrossRef
Google scholar
|
[193] |
Mehdi A, Attias M, Arakelian A, Piccirillo CA, Szyf M, Rabbani SA. Co-Targeting Luminal B Breast Cancer with S-Adenosylmethionine and Immune Checkpoint Inhibitor Reduces Primary Tumor Growth and Progression, and Metastasis to Lungs and Bone. Cancers (Basel). 2022; 15(1): 48.
CrossRef
Google scholar
|
[194] |
Alsaab HO, Sau S, Alzhrani R, Tatiparti K, Bhise K, Kashaw SK, et al. PD-1 and PD-L1 Checkpoint Signaling Inhibition for Cancer Immunotherapy: Mechanism, Combinations, and Clinical Outcome. Front Pharmacol. 2017; 8: 561.
CrossRef
Google scholar
|
[195] |
Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012; 12(4): 252–264.
CrossRef
Google scholar
|
[196] |
Xu Y, Mao Y, Lv Y, Tang W, Xu J. B cells in tumor metastasis: friend or foe? Int J Biol Sci. 2023; 19(8): 2382–2393.
CrossRef
Google scholar
|
[197] |
Helmink BA, Reddy SM, Gao J, Zhang S, Basar R, Thakur R, et al. B cells and tertiary lymphoid structures promote immunotherapy response. Nature. 2020; 577(7791): 549–555.
CrossRef
Google scholar
|
[198] |
Perricone MA, Smith KA, Claussen KA, Plog MS, Hempel DM, Roberts BL, et al. Enhanced efficacy of melanoma vaccines in the absence of B lymphocytes. J Immunother. 2004; 27(4): 273–281.
CrossRef
Google scholar
|
[199] |
Meylan M, Petitprez F, Becht E, Bougoüin A, Pupier G, Calvez A, et al. Tertiary lymphoid structures generate and propagate anti-tumor antibody-producing plasma cells in renal cell cancer. Immunity. 2022; 55(3): 527–541.e5.
CrossRef
Google scholar
|
[200] |
Roato I, Brunetti G, Gorassini E, Grano M, Colucci S, Bonello L, et al. IL-7 up-regulates TNF-alpha-dependent osteoclastogenesis in patients affected by solid tumor. PLoS One. 2006; 1(1): e124.
CrossRef
Google scholar
|
[201] |
Gauthier L, Morel A, Anceriz N, Rossi B, Blanchard-Alvarez A. Grondin G, et al. Multifunctional Natural Killer Cell Engagers Targeting NKp46 Trigger Protective Tumor Immunity. Cell. 2019; 177(7): 1701–1713.e16.
CrossRef
Google scholar
|
[202] |
Liu S, Galat V, Galat Y, Lee YKA, Wainwright D, Wu J. NK cell-based cancer immunotherapy: from basic biology to clinical development. J Hematol Oncol. 2021; 14(1): 7.
CrossRef
Google scholar
|
[203] |
Li T, Yang Y, Hua X, Wang G, Liu W, Jia C, et al. Hepatocellular carcinoma-associated fibroblasts trigger NK cell dysfunction via PGE2 and IDO. Cancer Lett. 2012; 318(2): 154–161.
CrossRef
Google scholar
|
[204] |
Wu Y, Kuang DM, Pan WD, Wan YL, Lao XM, Wang D, et al. Monocyte/macrophage-elicited natural killer cell dysfunction in hepatocellular carcinoma is mediated by CD48/2B4 interactions. Hepatology. 2013; 57(3): 1107–1116.
CrossRef
Google scholar
|
[205] |
Pal S, Perrien DS, Yumoto T, Faccio R, Stoica A, Adams J, et al. The microbiome restrains melanoma bone growth by promoting intestinal NK and Th1 cell homing to bone. J Clin Invest. 2022; 132(12): e157340.
CrossRef
Google scholar
|
[206] |
Wu Q, Tian P, He D, Jia Z, He Y, Luo W, et al. SCUBE2 mediates bone metastasis of luminal breast cancer by modulating immune-suppressive osteoblastic niches. Cell Res. 2023; 33(6): 464–478.
CrossRef
Google scholar
|
[207] |
Miki T, Yano S, Hanibuchi M, Kanematsu T, Muguruma H, Sone S. Parathyroid hormone-related protein (PTHrP) is responsible for production of bone metastasis, but not visceral metastasis, by human small cell lung cancer SBC-5 cells in natural killer cell-depleted SCID mice. Int J Cancer. 2004; 108(4): 511–515.
CrossRef
Google scholar
|
[208] |
Miki T, Yano S, Hanibuchi M, Sone S. Bone metastasis model with multiorgan dissemination of human small-cell lung cancer (SBC-5) cells in natural killer cell-depleted SCID mice. Oncol Res. 2000; 12(5): 209–217.
CrossRef
Google scholar
|
[209] |
Zhang H, Yano S, Miki T, Goto H, Kanematsu T, Muguruma H, et al. A novel bisphosphonate minodronate (YM529) specifically inhibits osteolytic bone metastasis produced by human small-cell lung cancer cells in NK-cell depleted SCID mice. Clin Exp Metastasis. 2003; 20(2): 153–159.
|
[210] |
Rautela J, Baschuk N, Slaney CY, Jayatilleke KM, Xiao K, Bidwell BN, et al. Loss of Host Type-I IFN Signaling Accelerates Metastasis and Impairs NK-cell Antitumor Function in Multiple Models of Breast Cancer. Cancer Immunol Res. 2015; 3(11): 1207–1217.
CrossRef
Google scholar
|
[211] |
Deauvieau F, Ollion V, Doffin AC, Achard C, Fonteneau JF, Verronese E, et al. Human natural killer cells promote cross-presentation of tumor cell-derived antigens by dendritic cells. Int J Cancer. 2015; 136(5): 1085–1094.
CrossRef
Google scholar
|
[212] |
Zarrer J, Haider MT, Smit DJ, Taipaleenmäki H. Pathological Crosstalk between Metastatic Breast Cancer Cells and the Bone Microenvironment. Biomolecules. 2020; 10(2): 337.
CrossRef
Google scholar
|
[213] |
Conte M, Martucci M, Sandri M, Franceschi C, Salvioli S. The Dual Role of the Pervasive “Fattish” Tissue Remodeling With Age. Front Endocrinol (Lausanne). 2019; 10: 114.
CrossRef
Google scholar
|
[214] |
Wu Q, Li B, Sun S, Sun S. Unraveling Adipocytes and Cancer Links: Is There a Role for Senescence? Front Cell Dev Biol. 2020; 8: 282.
CrossRef
Google scholar
|
[215] |
Yao H, He S. Multi faceted role of cancer associated adipocytes in the tumor microenvironment (Review). Mol Med Rep. 2021; 24(6): 866.
CrossRef
Google scholar
|
[216] |
Herroon MK, Rajagurubandara E, Diedrich JD, Heath EI, Podgorski I. Adipocyte-activated oxidative and ER stress pathways promote tumor survival in bone via upregulation of Heme Oxygenase 1 and Survivin. Sci Rep. 2018; 8(1): 40.
CrossRef
Google scholar
|
[217] |
Diedrich JD, Rajagurubandara E, Herroon MK, Mahapatra G, Hüttemann M, Podgorski I. Bone marrow adipocytes promote the Warburg phenotype in metastatic prostate tumors via HIF-1α activation. Oncotarget. 2016; 7(40): 64854–64877.
CrossRef
Google scholar
|
[218] |
Hardaway AL, Herroon MK, Rajagurubandara E, Podgorski I. Marrow adipocyte-derived CXCL1 and CXCL2 contribute to osteolysis in metastatic prostate cancer. Clin Exp Metastasis. 2015; 32(4): 353–368.
CrossRef
Google scholar
|
[219] |
Sato S, Hiruma T, Koizumi M, Yoshihara M, Nakamura Y, Tadokoro H, et al. Bone marrow adipocytes induce cancer-associated fibroblasts and immune evasion, enhancing invasion and drug resistance. Cancer Sci. 2023; 114(6): 2674–2688.
CrossRef
Google scholar
|
[220] |
Dirat B, Bochet L, Dabek M, Daviaud D, Dauvillier S, Majed B, et al. Cancer-associated adipocytes exhibit an activated phenotype and contribute to breast cancer invasion. Cancer Res. 2011; 71(7): 2455–2465.
CrossRef
Google scholar
|
[221] |
Fairfield H, Dudakovic A, Khatib CM, Farrell M, Costa S, Falank C, et al. Myeloma-Modified Adipocytes Exhibit Metabolic Dysfunction and a Senescence-Associated Secretory Phenotype. Cancer Res. 2021; 81(3): 634–647.
CrossRef
Google scholar
|
[222] |
Delgado-Calle J, Bellido T. Osteocytes and Skeletal Pathophysiology. Curr Mol Biol Rep. 2015; 1(4): 157–167.
CrossRef
Google scholar
|
[223] |
Grimaud E, Soubigou L, Couillaud S, Coipeau P, Moreau A, Passuti N, et al. Receptor activator of nuclear factor kappaB ligand (RANKL)/osteoprotegerin (OPG) ratio is increased in severe osteolysis. Am J Pathol. 2003; 163(5): 2021–2031.
CrossRef
Google scholar
|
[224] |
Wang H, Yu C, Gao X, Welte T, Muscarella AM, Tian L, et al. The osteogenic niche promotes early-stage bone colonization of disseminated breast cancer cells. Cancer Cell. 2015; 27(2): 193–210.
CrossRef
Google scholar
|
[225] |
Jung Y, Wang J, Schneider A, Sun YX, Koh-Paige AJ. Osman NI, et al. Regulation of SDF-1 (CXCL12) production by osteoblasts; a possible mechanism for stem cell homing. Bone. 2006; 38(4): 497–508.
CrossRef
Google scholar
|
[226] |
Johnson RW, Finger EC, Olcina MM, Vilalta M, Aguilera T, Miao Y, et al. Induction of LIFR confers a dormancy phenotype in breast cancer cells disseminated to the bone marrow. Nat Cell Biol. 2016; 18(10): 1078–1089.
CrossRef
Google scholar
|
[227] |
Decker AM, Jung Y, Cackowski FC, Yumoto K, Wang J, Taichman RS. Sympathetic Signaling Reactivates Quiescent Disseminated Prostate Cancer Cells in the Bone Marrow. Mol Cancer Res. 2017; 15(12): 1644–1655.
CrossRef
Google scholar
|
[228] |
Sosnoski DM, Norgard RJ, Grove CD, Foster SJ, Mastro AM. Dormancy and growth of metastatic breast cancer cells in a bone-like microenvironment. Clin Exp Metastasis. 2015; 32(4): 335–344.
CrossRef
Google scholar
|
[229] |
Hu W, Zhang L, Dong Y, Tian Z, Chen Y, Dong S. Tumour dormancy in inflammatory microenvironment: A promising therapeutic strategy for cancer-related bone metastasis. Cell Mol Life Sci. 2020; 77(24): 5149–5169.
CrossRef
Google scholar
|
[230] |
Dai R, Liu M, Xiang X, Xi Z, Xu H. Osteoblasts and osteoclasts: an important switch of tumour cell dormancy during bone metastasis. J Exp Clin Cancer Res. 2022; 41(1): 316.
CrossRef
Google scholar
|
[231] |
Wu AC, He Y, Broomfield A, Paatan NJ, Harrington BS, Tseng HW, et al. CD169(+) macrophages mediate pathological formation of woven bone in skeletal lesions of prostate cancer. J Pathol. 2016; 239(2): 218–230.
CrossRef
Google scholar
|
[232] |
Delgado-Calle J, Bellido T. The osteocyte as a signaling cell. Physiol Rev. 2022; 102(1): 379–410.
CrossRef
Google scholar
|
[233] |
Uda Y, Azab E, Sun N, Shi C, Pajevic PD. Osteocyte Mechanobiology. Curr Osteoporos Rep. 2017; 15(4): 318–325.
CrossRef
Google scholar
|
[234] |
Riquelme MA, Cardenas ER, Jiang JX. Osteocytes and Bone Metastasis. Front Endocrinol (Lausanne). 2020; 11: 567844.
CrossRef
Google scholar
|
[235] |
Myers TJ, Longobardi L, Willcockson H, Temple JD, Tagliafierro L, Ye P, et al. BMP2 Regulation of CXCL12 Cellular, Temporal, and Spatial Expression is Essential During Fracture Repair. J Bone Miner Res. 2015; 30(11): 2014–2027.
CrossRef
Google scholar
|
[236] |
Liu S, Fan Y, Chen A, Jalali A, Minami K, Ogawa K, et al. Osteocyte-Driven Downregulation of Snail Restrains Effects of Drd2 Inhibitors on Mammary Tumor Cells. Cancer Res. 2018; 78(14): 3865–3876.
CrossRef
Google scholar
|
[237] |
Zhou H, Zhang W, Li H, Xu F, Yinwang E, Xue Y, et al. Osteocyte mitochondria inhibit tumor development via STING-dependent antitumor immunity. Sci Adv. 2024; 10(3): eadi4298.
CrossRef
Google scholar
|
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