Multiplex analysis of cancer cells treated with induced mesenchymal stem cell membrane vesicles

Sevindzh K. Kletukhina , Marina O. Gomzikova

Genes & Cells ›› 2024, Vol. 19 ›› Issue (4) : 441 -452.

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Genes & Cells ›› 2024, Vol. 19 ›› Issue (4) : 441 -452. DOI: 10.17816/gc609563
Original Study Articles
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Multiplex analysis of cancer cells treated with induced mesenchymal stem cell membrane vesicles

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Abstract

BACKGROUND: Extracellular vesicles (EVs) are membrane-derived vesicles secreted by cells into the extracellular space. They play an important role in intercellular communication and regulate various biological processes. Vesicles are found in tumor tissue where they mediate signaling between tumor cells and surrounding cells in the microenvironment. Like parental mesenchymal stem cells (MSCs), EVs exert dual effects on tumorogenesis. Some studies have shown that MSC-EVs promote tumor growth, while others have demonstrated their inhibitory role.

AIM: The aim of the study was to evaluate the effect of MSC membrane vesicles (MVs) on the molecular composition of cancer cells.

MATERIALS AND METHODS: Induced membrane vesicles (iMVs) were obtained from MSCs previously isolated from adipose tissue by treatment with cytochalasin B. To simulate intercellular communication between tumor cells and MSCs, iMVs with different protein concentrations were applied to recipient cells (SH-SY5Y, PC3, MCF7). A bicinchoninic acid technique was used to measure total protein isolated from human cells/iMVs. The molecular composition of the recipient cells was then analyzed by multiplex analysis. The cells were pre-treated with MSC iMVs.

RESULTS: Applying MSC MVs to cancer cells induces significant changes in the expression of many biologically active molecules, including cytokines, chemokines, and growth factors. For example, increased levels of the growth factor FGF-2, cytokines G-CSF, fractalkine, IL-12p40, IL-9, IL-4, IL-6, IL-8, chemokines IP-10, MCP-1, and others were detected. In addition, the majority of these molecules are found to be associated with cell proliferation, migration and immune response.

CONCLUSION: MSC MVs are able to alter the molecular profile of cancer cells, increasing the levels of molecules associated with cell survival and migration.

Keywords

membrane vesicles / cytochalasin B-induced membrane vesicles / mesenchymal stem cells / multipotent stromal cells

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Sevindzh K. Kletukhina, Marina O. Gomzikova. Multiplex analysis of cancer cells treated with induced mesenchymal stem cell membrane vesicles. Genes & Cells, 2024, 19(4): 441-452 DOI:10.17816/gc609563

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References

[1]

Akers JC, Gonda D, Kim R, et al. Biogenesis of extracellular vesicles (EV): exosomes, microvesicles, retrovirus-like vesicles, and apoptotic bodies. J Neurooncol. 2013;113(1):1–11. doi: 10.1007/s11060-013-1084-8

[2]

Akers J.C., Gonda D., Kim R., et al. Biogenesis of extracellular vesicles (EV): exosomes, microvesicles, retrovirus-like vesicles, and apoptotic bodies // J Neurooncol. 2013. Vol. 113, N. 1. P. 1–11. doi: 10.1007/s11060-013-1084-8

[3]

Akyurekli C, Le Y, Richardson RB, et al. A systematic review of preclinical studies on the therapeutic potential of mesenchymal stromal cell-derived microvesicles. Stem Cell Rev and Rep. 2015;11(1):150–160. doi: 10.1007/s12015-014-9545-9

[4]

Akyurekli C., Le Y., Richardson R.B., et al. A systematic review of preclinical studies on the therapeutic potential of mesenchymal stromal cell-derived microvesicles // Stem Cell Rev Rep. 2015. Vol. 11, N. 1. P. 150–160. doi: 10.1007/s12015-014-9545-9

[5]

Teng X, Chen L, Chen W, et al. Mesenchymal stem cell-derived exosomes improve the microenvironment of infarcted myocardium contributing to angiogenesis and anti-inflammation. Cell Physiol Biochem. 2015;37(6):2415–2424. doi: 10.1159/000438594

[6]

Teng X., Chen L., Chen W., et al. Mesenchymal stem cell-derived exosomes improve the microenvironment of infarcted myocardium contributing to angiogenesis and anti-inflammation // Cell Physiol Biochem. 2015. Vol. 37, N. 6. P. 2415–2424. doi: 10.1159/000438594

[7]

Zhang Y, Chopp M, Meng Y, et al. Effect of exosomes derived from multipluripotent mesenchymal stromal cells on functional recovery and neurovascular plasticity in rats after traumatic brain injury. J Neurosurg. 2015;122(4):856–867. doi: 10.3171/2014.11.JNS14770

[8]

Zhang Y., Chopp M., Meng Y., et al. Effect of exosomes derived from multipluripotent mesenchymal stromal cells on functional recovery and neurovascular plasticity in rats after traumatic brain injury // 2015. Vol. 122, N. 4. P. 856–867. doi: 10.3171/2014.11.JNS14770

[9]

Zhang Y, Xu J, Liu S, et al. Embryonic stem cell-derived extracellular vesicles enhance the therapeutic effect of mesenchymal stem cells. Theranostics. 2019;9(23):6976–6990. doi: 10.7150/thno.35305

[10]

Zhang Y., Xu J., Liu S., et al. Embryonic stem cell-derived extracellular vesicles enhance the therapeutic effect of mesenchymal stem cells // Theranostics. 2019. Vol. 9, N. 23. P. 6976–6990. doi: 10.7150/thno.35305

[11]

Wang N, Chen C, Yang D, et al. Mesenchymal stem cells-derived extracellular vesicles, via miR-210, improve infarcted cardiac function by promotion of angiogenesis. Biochim Biophys Acta Mol Basis Dis. 2017;1863(8):2085–2092. doi: 10.1016/j.bbadis.2017.02.023

[12]

Wang N., Chen C., Yang D., et al. Mesenchymal stem cells-derived extracellular vesicles, via miR-210, improve infarcted cardiac function by promotion of angiogenesis // Biochim Biophys Acta Mol Basis Dis. 2017. Vol. 1863, N. 8. P. 2085–2092. doi: 10.1016/j.bbadis.2017.02.023

[13]

Di Trapani M, Bassi G, Midolo M, et al. Differential and transferable modulatory effects of mesenchymal stromal cell-derived extracellular vesicles on T, B and NK cell functions. Sci Rep. 2016;6:24120. doi: 10.1038/srep24120

[14]

Di Trapani M., Bassi G., Midolo M., et al. Differential and transferable modulatory effects of mesenchymal stromal cell-derived extracellular vesicles on T, B and NK cell functions // Sci Rep. 2016. Vol. 6. P. 24120. doi: 10.1038/srep24120

[15]

Seo Y, Kim HS, Hong IS. Stem cell-derived extracellular vesicles as immunomodulatory therapeutics. Stem Cells Int. 2019;2019:5126156. doi: 10.1155/2019/5126156

[16]

Seo Y., Kim H.S., Hong I.S. Stem cell-derived extracellular vesicles as immunomodulatory therapeutics // Stem Cells Int. 2019. Vol. 2019. P. 5126156. doi: 10.1155/2019/5126156

[17]

Syromiatnikova V, Prokopeva A, Gomzikova M. Methods of the large-scale production of extracellular vesicles. Int J Mol Sci. 2022;23(18):10522. doi: 10.3390/ijms231810522

[18]

Syromiatnikova V., Prokopeva A., Gomzikova M. Methods of the large-scale production of extracellular vesicles // Int J Mol Sci. 2022. Vol. 23, N. 18. P. 10522. doi: 10.3390/ijms231810522

[19]

Pick H, Schmid EL, Tairi AP, et al. Investigating cellular signaling reactions in single attoliter vesicles. J Am Chem Soc. 2005;127(9):2908–2912. doi: 10.1021/ja044605x

[20]

Pick H., Schmid E.L., Tairi A.P., et al. Investigating cellular signaling reactions in single attoliter vesicles // J Am Chem Soc. 2005. Vol. 127, N. 9. P. 2908–2912. doi: 10.1021/ja044605x

[21]

Fox JE, Austin CD, Boyles JK, Steffen PK. Role of the membrane skeleton in preventing the shedding of procoagulant-rich microvesicles from the platelet plasma membrane. J Cell Biol. 1990;111(2):483–493. doi: 10.1083/jcb.111.2.483

[22]

Fox J.E., Austin C.D., Boyles J.K., Steffen P.K. Role of the membrane skeleton in preventing the shedding of procoagulant-rich microvesicles from the platelet plasma membrane // J Cell Biol. 1990. Vol. 111, N. 2. P. 483–493. doi: 10.1083/jcb.111.2.483

[23]

Choi DS, Yang JS, Choi EJ, et al. The protein interaction network of extracellular vesicles derived from human colorectal cancer cells. J Proteome Res. 2012;11(2):1144–1151. doi: 10.1021/pr200842h

[24]

Choi D.S., Yang J.S., Choi E.J., et al. The protein interaction network of extracellular vesicles derived from human colorectal cancer cells // J Proteome Res. 2012. Vol. 11, N. 2. P. 1144–1151. doi: 10.1021/pr200842h

[25]

Atanassoff AP, Wolfmeier H, Schoenauer R, et al. Microvesicle shedding and lysosomal repair fulfill divergent cellular needs during the repair of streptolysin O-induced plasmalemmal damage. PLoS One. 2014;9(2):e89743. doi: 10.1371/journal.pone.0089743

[26]

Atanassoff A.P., Wolfmeier H., Schoenauer R., et al. Microvesicle shedding and lysosomal repair fulfill divergent cellular needs during the repair of streptolysin O-induced plasmalemmal damage // PLoS One. 2014. Vol. 9, N. 2. P. e89743. doi: 10.1371/journal.pone.0089743

[27]

EL Andaloussi S, Mäger I, Breakefield XO, Wood MJA. Extracellular vesicles: biology and emerging therapeutic opportunities. Nat Rev Drug Discov. 2013;12(5):347–357. doi: 10.1038/nrd3978

[28]

EL Andaloussi S., Mäger I., Breakefield X.O., Wood M.J. Extracellular vesicles: biology and emerging therapeutic opportunities // Nat Rev Drug Discov. 2013. Vol. 12, N. 5. P. 347–357. doi: 10.1038/nrd3978

[29]

Gomzikova M, Kletukhina S, Kurbangaleeva S, Rizvanov A. Evaluation of cytochalasin b-induced membrane vesicles fusion specificity with target cells. Biomed Res Int. 2018;2018:7053623. doi: 10.1155/2018/7053623

[30]

Gomzikova M., Kletukhina S., Kurbangaleeva S., Rizvanov A. Evaluation of cytochalasin B-induced membrane vesicles fusion specificity with target cells // Biomed Res Int. 2018. Vol. 2018. P. 7053623. doi: 10.1155/2018/7053623

[31]

Gomzikova MO, Zhuravleva MN, Vorobev VV, et al. Angiogenic activity of cytochalasin b-induced membrane vesicles of human mesenchymal stem cells. Cells. 2019;9(1):95. doi: 10.3390/cells9010095

[32]

Gomzikova M.O., Zhuravleva M.N., Vorobev V.V., et al. Angiogenic activity of cytochalasin b-induced membrane vesicles of human mesenchymal stem cells // Cells. 2019. Vol. 9, N. 1. P. 95. doi: 10.3390/cells9010095

[33]

Kurbangaleeva SV, Syromiatnikova VY, Prokopeva AE, et al. Increased yield of extracellular vesicles after cytochalasin b treatment and vortexing. Curr Issues Mol Biol. 2023;45(3):2431–2443. doi: 10.3390/cimb45030158

[34]

Kurbangaleeva S.V., Syromiatnikova V.Y., Prokopeva A.E., et al. Increased yield of extracellular vesicles after cytochalasin b treatment and vortexing // Curr Issues Mol Biol. 2023. Vol. 45, N. 3. P. 2431–2443. doi: 10.3390/cimb45030158

[35]

Ciccarone V, Spengler BA, Meyers MB, et al. Phenotypic diversification in human neuroblastoma cells: expression of distinct neural crest lineages. Cancer Res. 1989;49(1):219–225.

[36]

Ciccarone V., Spengler B.A., Meyers M.B., et al. Phenotypic diversification in human neuroblastoma cells: expression of distinct neural crest lineages // Cancer Res. 1989. Vol. 49, N. 1. P. 219–225.

[37]

Horwitz KB, Costlow ME, McGuire WL. MCF-7: a human breast cancer cell line with estrogen, progesterone, and glucocorticoid receptors. Steroids. 1975;26(6):785–795. doi: 10.1016/0039-128x(75)90110-5

[38]

Horwitz K.B., Costlow M.E., McGuire W.L. MCF-7; a human breast cancer cell line with estrogen, androgen, progesterone, and glucocorticoid receptors // Steroids. 1975. Vol. 26, N. 6. P. 785–795. doi: 10.1016/0039-128x(75)90110-5

[39]

Anait S, Jordan VC. MCF-7: the first hormone-responsive breast cancer cell line. Canc Res. 1997;57(15):3071–3078.

[40]

Anait S., Jordan V.C. MCF-7: the first hormone-responsive breast cancer cell line // Cancer Res. 1997. Vol. 57, N. 15. P. 3071–3078.

[41]

Zhang K, Waxman DJ. PC3 prostate tumor-initiating cells with molecular profile FAM65Bhigh/MFI2low/LEF1low increase tumor angiogenesis. Mol Cancer. 2010;29:319. doi: 10.1186/1476-4598-9-319

[42]

Zhang K., Waxman D.J. PC3 prostate tumor-initiating cells with molecular profile FAM65Bhigh/MFI2low/LEF1low increase tumor angiogenesis // Mol Cancer. 2010. Vol. 9. P. 319. doi: 10.1186/1476-4598-9-319

[43]

Grivennikov S, Karin M. Autocrine IL-6 signaling: A key event in tumorigenesis? Cancer Cell. 2008;13(1):7–9. doi: 10.1016/j.ccr.2007.12.020

[44]

Grivennikov S., Karin M. Autocrine IL-6 signaling: a key event in tumorigenesis? // Cancer Cell. 2008. Vol. 13, N. 1. P. 7–9. doi: 10.1016/j.ccr.2007.12.020

[45]

Lin R, Wang S, Zhao RC. Exosomes from human adipose-derived mesenchymal stem cells promote migration through Wnt signaling pathway in a breast cancer cell model. Mol Cell Biochem. 2013;383(1-2):13–20. doi: 10.1007/s11010-013-1746-z

[46]

Lin R., Wang S., Zhao R.C. Exosomes from human adipose-derived mesenchymal stem cells promote migration through WNT signaling pathway in a breast cancer cell model // Mol Cell Biochem. 2013. Vol. 383, N. 1-2. P. 13–20. doi: 10.1007/s11010-013-1746-z

[47]

Vallabhaneni KC, Penfornis P, Dhule S, et al. Extracellular vesicles from bone marrow mesenchymal stem/stromal cells transport tumor regulatory microRNA, proteins, and metabolites. Oncotarget. 2015;6(7):4953–4967. doi: 10.18632/oncotarget.3211

[48]

Vallabhaneni K.C., Penfornis P., Dhule S., et al. Extracellular vesicles from bone marrow mesenchymal stem/stromal cells transport tumor regulatory microRNA, proteins, and metabolites // Oncotarget. 2015. Vol. 6, N. 7. P. 4953–4967. doi: 10.18632/oncotarget.3211

[49]

Zhu W, Huang L, Li Y, et al. Exosomes derived from human bone marrow mesenchymal stem cells promote tumor growth in vivo. Cancer Lett. 2012;315(1):28–37. doi: 10.1016/j.canlet.2011.10.002

[50]

Zhu W., Huang L., Li Y., et al. Exosomes derived from human bone marrow mesenchymal stem cells promote tumor growth in vivo // Cancer Lett. 2012. Vol. 315, N. 1. P. 28–37. doi: 10.1016/j.canlet.2011.10.002

[51]

Du T, Ju G, Wu S, et al. Microvesicles derived from human wharton’s jelly mesenchymal stem cells promote human renal cancer cell growth and aggressiveness through induction of hepatocyte growth factor. PLoS One. 2014;9(5):e96836. doi: 10.1371/journal.pone.0096836

[52]

Du T., Ju G., Wu S., et al. Microvesicles derived from human wharton’s jelly mesenchymal stem cells promote human renal cancer cell growth and aggressiveness through induction of hepatocyte growth factor // PLoS One. 2014. Vol. 9, N. 5. P. e96836. doi: 10.1371/journal.pone.0096836

[53]

Bromberg J, Wang TC. Inflammation and cancer: IL-6 and STAT3 complete the link. Cancer Cell. 2009;15(2):79–80. doi: 10.1016/j.ccr.2009.01.009

[54]

Bromberg J., Wang T.C. Inflammation and cancer: IL-6 and STAT3 complete the link // Cancer Cell. 2009. Vol. 15, N. 2. P. 79–80. doi: 10.1016/j.ccr.2009.01.009

[55]

Kumari N, Dwarakanath BS, Das A, Bhatt AN. Role of interleukin-6 in cancer progression and therapeutic resistance. Tumour Biol. 2016;37(9):11553–11572. doi: 10.1007/s13277-016-5098-7

[56]

Kumari N., Dwarakanath B.S., Das A., Bhatt A.N. Role of interleukin-6 in cancer progression and therapeutic resistance // Tumour Biol. 2016. Vol. 37, N. 9. P. 11553–11572. doi: 10.1007/s13277-016-5098-7

[57]

Ghandadi M, Sahebkar A. Interleukin-6: a critical cytokine in cancer multidrug resistance. Curr Pharm Des. 2016;22(5):518–526. doi: 10.2174/1381612822666151124234417

[58]

Ghandadi M., Sahebkar A. Interleukin-6: a critical cytokine in cancer multidrug resistance // Curr Pharm Des. 2016. Vol. 22, N. 5. P. 518–526. doi: 10.2174/1381612822666151124234417

[59]

Valdembri D, Serini G, Vacca A, et al. In vivo activation of JAK2/STAT-3 pathway during angiogenesis induced by GM-CSF. FASEB J. 2002;16(2):225–227. doi: 10.1096/fj.01-0633fje

[60]

Valdembri D., Serini G., Vacca A., Ribatti D., et al. In vivo activation of JAK2/STAT-3 pathway during angiogenesis induced by GM-CSF // FASEB J. 2002. Vol. 16, N. 2. P. 225–227. doi: 10.1096/fj.01-0633fje

[61]

Zgheib A, Lamy S, Annabi B. Epigallocatechin gallate targeting of membrane type 1 matrix metalloproteinase-mediated Src and janus kinase/signal transducers and activators of transcription 3 signaling inhibits transcription of colony-stimulating factors 2 and 3 in mesenchymal stromal cells. J Biol Chem. 2013;288(19):13378–13386. doi: 10.1074/jbc.M113.456533

[62]

Zgheib A., Lamy S., Annabi B. Epigallocatechin gallate targeting of membrane type 1 matrix metalloproteinase-mediated Src and Janus kinase/signal transducers and activators of transcription 3 signaling inhibits transcription of colony-stimulating factors 2 and 3 in mesenchymal stromal cells // J Biol Chem. 2013. Vol. 288, N. 19. P. 13378–13386. doi: 10.1074/jbc.M113.456533

[63]

Adeegbe DO, Nishikawa H. Natural and induced T regulatory cells in cancer. Front Immunol. 2013;4:190. doi: 10.3389/fimmu.2013.00190

[64]

Adeegbe D.O., Nishikawa H. Natural and induced T regulatory cells in cancer // Front Immunol. 2013. Vol. 4. P. 190. doi: 10.3389/fimmu.2013.00190

[65]

Hori S, Miyake M, Onishi S, et al. Evaluation of pro- and anti-tumor effects induced by three colony-stimulating factors, G-CSF, GM-CSF and M-CSF, in bladder cancer cells: Is G-CSF a friend of bladder cancer cells? Int J Oncol. 2019;54(6):2237–2249. doi: 10.3892/ijo.2019.4772

[66]

Hori S., Miyake M., Onishi S., et al. Evaluation of pro- and anti-tumor effects induced by three colony-stimulating factors, G-CSF, GM-CSF and M-CSF, in bladder cancer cells: Is G-CSF a friend of bladder cancer cells // Int J Oncol. 2019. Vol. 54, N. 6. P. 2237–2249. doi: 10.3892/ijo.2019.4772

[67]

Espinoza-Sánchez NA, Vadillo E, Balandrán JC, et al. Evidence of lateral transmission of aggressive features between different types of breast cancer cells. Int J Oncol. 2017;51(5):1482–1496. doi: 10.3892/ijo.2017.4128

[68]

Espinoza-Sánchez N.A., Vadillo E., Balandrán J.C., et al. Evidence of lateral transmission of aggressive features between different types of breast cancer cells // Int J Oncol. 2017. Vol. 51, N. 5. P. 1482–1496. doi: 10.3892/ijo.2017.4128

[69]

Lazarus H, Rowe JM. Clinical use of hematopoietic growth factors in allogeneic bone marrow transplantation. Blood Reviews. 1994;8(3):169–178. doi: 10.1016/0268-960x(94)90078-v

[70]

Lazarus H., Rowe J.M. Clinical use of hematopoietic growth factors in allogeneic bone marrow transplantation // Blood Rev. 1994. Vol. 8, N. 3. P. 169–178. doi: 10.1016/0268-960x(94)90078-V

[71]

Van Pelt LJ, De Craen AJM, Langeveld NE, Weening RS. Granulocyte-macrophage colony-stimulating factor (GM-CSF) ameliorates chemotherapy-induced neutropenia in children with solid tumors. Pediatr Hematol Oncol. 1997;14(6):539–545. doi: 10.3109/08880019709030910

[72]

Van Pelt L.J., De Craen A.J., Langeveld N.E., Weening R.S. Granulocyte-macrophage colony-stimulating factor (GM-CSF) ameliorates chemotherapy-induced neutropenia in children with solid tumors // Pediatr Hematol Oncol. 1997. Vol. 14, N. 6. P. 539–545. doi: 10.3109/08880019709030910

[73]

Mehta HM, Malandra M, Corey SJ. G-CSF and GM-CSF in neutropenia. J Immunol. 2015;195(4):1341–1349. doi: 10.4049/jimmunol.1500861

[74]

Mehta H.M., Malandra M., Corey S.J. G-CSF and GM-CSF in neutropenia // J Immunol. 2015. Vol. 195, N. 4. P. 1341–1349. doi: 10.4049/jimmunol.1500861

[75]

Feleszko W, Giermasz A, Gołatb J, et al. Granulocyte-macrophage colony-stimulating factor accelerates growth of Lewis lung carcinoma in mice. Cancer Lett. 1996;101(2):193–197. doi: 10.1016/0304-3835(96)04134-1

[76]

Feleszko W., Giermasz A., Gołatb J., et al. Granulocyte-macrophage colony-stimulating factor accelerates growth of Lewis lung carcinoma in mice // Cancer Lett. 1996. Vol. 101, N. 2. P. 193–197. doi: 10.1016/0304-3835(96)04134-1

[77]

Obermueller E, Vosseler S, Fusenig NE, Mueller MM. Cooperative autocrine and paracrine functions of granulocyte colony-stimulating factor and granulocyte-macrophage colony-stimulating factor in the progression of skin carcinoma cells. Cancer Res. 2004;64(21):7801–7812. doi: 10.1158/0008-5472.CAN-03-3301

[78]

Obermueller E., Vosseler S., Fusenig N.E., Mueller M.M. Cooperative autocrine and paracrine functions of granulocyte colony-stimulating factor and granulocyte-macrophage colony-stimulating factor in the progression of skin carcinoma cells // Cancer Res. 2004. Vol. 64, N. 21. P. 7801–7812. doi: 10.1158/0008-5472.CAN-03-3301

[79]

Gutschalk CM, Herold-Mende CC, Fusenig NE, Mueller MM. Granulocyte colony-stimulating factor and granulocyte-macrophage colony-stimulating factor promote malignant growth of cells from head and neck squamous cell carcinomas in vivo. Cancer Res. 2006;66(16):8026–8036. doi: 10.1158/0008-5472.CAN-06-0158

[80]

Gutschalk C.M., Herold-Mende C.C., Fusenig N.E., Mueller M.M. Granulocyte colony-stimulating factor and granulocyte-macrophage colony-stimulating factor promote malignant growth of cells from head and neck squamous cell carcinomas in vivo // Cancer Res. 2006. Vol. 66, N. 16. P. 8026–8036. doi: 10.1158/0008-5472.CAN-06-0158

[81]

Gutschalk CM, Yanamandra AK, Linde N, et al. GM-CSF enhances tumor invasion by elevated MMP-2, -9, and -26 expression. Cancer Med. 2013;2(2):117–129. doi: 10.1002/cam4.20

[82]

Gutschalk C.M., Yanamandra A.K., Linde N., et al. GM-CSF enhances tumor invasion by elevated MMP-2, -9, and -26 expression // Cancer Med. 2013. Vol. 2, N. 2. P. 117–129. doi: 10.1002/cam4.20

[83]

Qiu L, Lai R, Lin Q, et al. Autocrine release of interleukin-9 promotes Jak3-dependent survival of ALK+ anaplastic large-cell lymphoma cells. Blood. 2006;108(7):2407–2415. doi: 10.1182/blood-2006-04-020305

[84]

Qiu L., Lai R., Lin Q., et al. Autocrine release of interleukin-9 promotes Jak3-dependent survival of ALK+ anaplastic large-cell lymphoma cells // Blood. 2006. Vol. 108, N. 7. P. 2407–2415. doi: 10.1182/blood-2006-04-020305

[85]

Allegra A, Musolino C, Tonacci A, et al. Clinico-biological implications of modified levels of cytokines in chronic lymphocytic leukemia: a possible therapeutic role. Cancers (Basel). 2020;12(2):524. doi: 10.3390/cancers12020524

[86]

Allegra A., Musolino C., Tonacci A., et al. Clinico-biological implications of modified levels of cytokines in chronic lymphocytic leukemia: a possible therapeutic role // Cancers (Basel). 2020. Vol. 12, N. 2. P. 524. doi: 10.3390/cancers12020524

[87]

Teng KY, Han J, Zhang X, et al. Blocking the CCL2–CCR2 axis using CCL2-neutralizing antibody is an effective therapy for hepatocellular cancer in a mouse model. Molecular Cancer Therapeutics. 2017;16(2):312–322. doi: 10.1158/1535-7163.MCT-16-0124

[88]

Teng K.Y., Han J., Zhang X., et al. Blocking the CCL2–CCR2 axis using CCL2-neutralizing antibody is an effective therapy for hepatocellular cancer in a mouse model // Molecular Cancer Therapeutics. 2017. Vol. 16, N. 2. P. 312–322. doi: 10.1158/1535-7163.MCT-16-0124

[89]

Fridlender ZG, Kapoor V, Buchlis G, et al. Monocyte chemoattractant protein-1 blockade inhibits lung cancer tumor growth by altering macrophage phenotype and activating CD8+ cells. Am J Respir Cell Mol Biol. 2011;44(2):230–237. doi: 10.1165/rcmb.2010-0080OC

[90]

Fridlender Z.G., Kapoor V., Buchlis G., et al. Monocyte chemoattractant protein-1 blockade inhibits lung cancer tumor growth by altering macrophage phenotype and activating CD8+ cells // Am J Respir Cell Mol Biol. 2011. Vol. 44, N. 2. P. 230–237. doi: 10.1165/rcmb.2010-0080OC

[91]

Loberg RD, Ying C, Craig M, et al. CCL2 as an important mediator of prostate cancer growth in vivo through the regulation of macrophage infiltration. Neoplasia. 2007;9(7):556–562. doi: 10.1593/neo.07307

[92]

Loberg R.D., Ying C., Craig M., et al. CCL2 as an important mediator of prostate cancer growth in vivo through the regulation of macrophage infiltration // Neoplasia. 2007. Vol. 9, N. 7. P. 556–562. doi: 10.1593/neo.07307

[93]

Qian BZ, Li J, Zhang H, et al. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature. 2011;475(7355):222–225. doi: 10.1038/nature10138

[94]

Qian B.Z., Li J., Zhang H., et al. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis // Nature. 2011. Vol. 475, N. 7355. P. 222–225. doi: 10.1038/nature10138

[95]

Sun C, Li X, Guo E, et al. MCP-1/CCR-2 axis in adipocytes and cancer cell respectively facilitates ovarian cancer peritoneal metastasis. Oncogene. 2020;39(8):1681–1695. doi: 10.1038/s41388-019-1090-1

[96]

Sun C., Li X., Guo E., et al. MCP-1/CCR-2 axis in adipocytes and cancer cell respectively facilitates ovarian cancer peritoneal metastasis // Oncogene. 2020. Vol. 39, N. 8. P. 1681–1695. doi: 10.1038/s41388-019-1090-1

[97]

Ueno T, Toi M, Saji H, et al. Significance of macrophage chemoattractant protein-1 in macrophage recruitment, angiogenesis, and survival in human breast cancer. Clin Cancer Res. 2000;6(8):3282–3289.

[98]

Ueno T., Toi M., Saji H., et al. Significance of macrophage chemoattractant protein-1 in macrophage recruitment, angiogenesis, and survival in human breast cancer // Clin Cancer Res. 2000. Vol. 6, N. 8. P. 3282–3289.

[99]

Kuziel G, Thompson V, D’Amato JV, Arendt LM. Stromal CCL2 signaling promotes mammary tumor fibrosis through recruitment of myeloid-lineage cells. Cancers (Basel). 2020;12(8):2083. doi: 10.3390/cancers12082083

[100]

Kuziel G., Thompson V., D’Amato J.V., Arendt L.M. Stromal CCL2 signaling promotes mammary tumor fibrosis through recruitment of myeloid-lineage cells // Cancers (Basel). 2020. Vol. 12, N. 8. P. 2083. doi: 10.3390/cancers12082083

[101]

Cho HR, Kumari N, Thi Vu H, et al. Increased antiangiogenic effect by blocking CCL2-dependent macrophages in a rodent glioblastoma model: correlation study with dynamic susceptibility contrast perfusion MRI. Sci Rep. 2019;9(1):11085. doi: 10.1038/s41598-019-47438-4

[102]

Cho H.R., Kumari N., Thi Vu H., et al. Increased antiangiogenic effect by blocking CCL2-dependent macrophages in a rodent glioblastoma model: correlation study with dynamic susceptibility contrast perfusion MRI // Sci Rep. 2019. Vol. 9, N. 1. P. 11085. doi: 10.1038/s41598-019-47438-4

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