miRNAs Delivery for Cancer-associated Fibroblasts’ Activation and Drug Resistance in Cancer Microenvironment

Page: [333 - 347] Pages: 15

  • * (Excluding Mailing and Handling)

Abstract

Cancer-associated fibroblasts (CAFs) as a major component of cancer stroma contribute to diverse procedures of most solid tumors and might be a targeted cancer therapy approach. Their specified features, related signaling pathways, distinct biomarkers, and sub-populations need to be deciphered. There is a need for CAF extraction or induction for in vitro investigations. Some miRNAs could activate CAF-like phenotype and they also interfere in CAF-mediated drug resistance, aggressiveness, and metastatic behaviors of several cancer cell types. Due to the complex relevance of miRNA and CAFs, these non-coding oligonucleotides may serve as attractive scope for anti-cancer targeted therapies, but the lack of an efficient delivery system is still a major hurdle. Here, we have summarized the investigated information on CAF features, isolation, and induction procedures, and highlighted the miRNA-CAF communications, providing special insight into nano-delivery systems.

Graphical Abstract

[1]
Kalluri, R. The biology and function of fibroblasts in cancer. Nat. Rev. Cancer, 2016, 16(9), 582-598.
[http://dx.doi.org/10.1038/nrc.2016.73] [PMID: 27550820]
[2]
Mohla, S. Tumor microenvironment. J. Cell. Biochem., 2007, 101(4), 801-804.
[http://dx.doi.org/10.1002/jcb.21320] [PMID: 17407156]
[3]
Whiteside, T.L. The tumor microenvironment and its role in promoting tumor growth. Oncogene, 2008, 27(45), 5904-5912.
[http://dx.doi.org/10.1038/onc.2008.271] [PMID: 18836471]
[4]
Galbo, P.M., Jr; Zang, X.; Zheng, D. Molecular features of cancer-associated fibroblast subtypes and their implication on cancer pathogenesis, prognosis, and immunotherapy resistance. Clin. Cancer Res., 2021, 27(9), 2636-2647.
[http://dx.doi.org/10.1158/1078-0432.CCR-20-4226] [PMID: 33622705]
[5]
Anari, F.; Ramamurthy, C.; Zibelman, M. Impact of tumor microenvironment composition on therapeutic responses and clinical outcomes in cancer. Future Oncol., 2018, 14(14), 1409-1421.
[http://dx.doi.org/10.2217/fon-2017-0585] [PMID: 29848096]
[6]
Chen, X.; Song, E. Turning foes to friends: Targeting cancer-associated fibroblasts. Nat. Rev. Drug Discov., 2019, 18(2), 99-115.
[http://dx.doi.org/10.1038/s41573-018-0004-1] [PMID: 30470818]
[7]
Barker, H.E.; Cox, T.R.; Erler, J.T. The rationale for targeting the LOX family in cancer. Nat. Rev. Cancer, 2012, 12(8), 540-552.
[http://dx.doi.org/10.1038/nrc3319] [PMID: 22810810]
[8]
Liu, T.; Zhou, L.; Li, D.; Andl, T.; Zhang, Y. Cancer-associated fibroblasts build and secure the tumor microenvironment. Front. Cell Dev. Biol., 2019, 7, 60.
[http://dx.doi.org/10.3389/fcell.2019.00060] [PMID: 31106200]
[9]
Paterlini-Bréchot, P. About seed and soil. Cancer Microenviron., 2014, 7(3), 91-93.
[http://dx.doi.org/10.1007/s12307-014-0163-5] [PMID: 25512049]
[10]
Neophytou, C.M.; Panagi, M.; Stylianopoulos, T.; Papageorgis, P. The role of tumor microenvironment in cancer metastasis: Molecular mechanisms and therapeutic opportunities. Cancers, 2021, 13(9), 2053.
[http://dx.doi.org/10.3390/cancers13092053]
[11]
Flier, J.S.; Underhill, L.H.; Dvorak, H.F. Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound heal-ing. N. Engl. J. Med., 1986, 315(26), 1650-1659.
[http://dx.doi.org/10.1056/NEJM198612253152606] [PMID: 3537791]
[12]
Liu, T.; Han, C.; Wang, S.; Fang, P.; Ma, Z.; Xu, L.; Yin, R. Cancer-associated fibroblasts: An emerging target of anti-cancer immunotherapy. J. Hematol. Oncol., 2019, 12(1), 86.
[http://dx.doi.org/10.1186/s13045-019-0770-1] [PMID: 31462327]
[13]
Rieske, P.; Krynska, B.; Azizi, S.A. Human fibroblast-derived cell lines have characteristics of embryonic stem cells and cells of neuro-ectodermal origin. Differentiation, 2005, 73(9-10), 474-483.
[http://dx.doi.org/10.1111/j.1432-0436.2005.00050.x] [PMID: 16351691]
[14]
D’Arcangelo, E.; Wu, N.C.; Cadavid, J.L.; McGuigan, A.P. The life cycle of cancer-associated fibroblasts within the tumour stroma and its importance in disease outcome. Br. J. Cancer, 2020, 122(7), 931-942.
[http://dx.doi.org/10.1038/s41416-019-0705-1] [PMID: 31992854]
[15]
Polanska, U.M.; Acar, A.; Orimo, A. Experimental generation of carcinoma-associated fibroblasts (CAFs) from human mammary fibro-blasts. J. Vis. Exp., 2011, (56), e3201.
[PMID: 22064505]
[16]
Dourado, R.C.; Porto, L.P.A.; Leitão, Á.C.G.H.; Cerqueira, P.S.G.; dos Santos, J.N.; Ramalho, L.M.P.; Xavier, F.C.A. Immunohistochemical characterization of cancer-associated fibroblasts in oral squamous cell carcinoma. Appl. Immunohistochem. Mol. Morphol., 2018, 26(9), 640-647.
[http://dx.doi.org/10.1097/PAI.0000000000000486] [PMID: 28968269]
[17]
Katoh, M. Genomic testing, tumor microenvironment and targeted therapy of Hedgehog-related human cancers. Clin. Sci., 2019, 133(8), 953-970.
[http://dx.doi.org/10.1042/CS20180845] [PMID: 31036756]
[18]
Di Mauro, C; Rosa, R; Amato, VD; Ciciola, P; Servetto, A; Marciano, R Hedgehog signalling pathway orchestrates angiogenesis in triple-negative breast cancers. Br. J. Cancer, 2017, 116(11), 1425-1435.
[http://dx.doi.org/10.1038/bjc.2017.116]
[19]
Chinchilla, P; Xiao, L; Kazanietz, MG; Riobo, NA Hedgehog proteins activate pro-angiogenic responses in endothelial cells through non-canonical signaling pathways. Cell Cycle, 2010, 9(3), 570-579.
[http://dx.doi.org/10.4161/cc.9.3.10591]
[20]
Cazet, A.S.; Hui, M.N.; Elsworth, B.L.; Wu, S.Z.; Roden, D.; Chan, C.L.; Skhinas, J.N.; Collot, R.; Yang, J.; Harvey, K.; Johan, M.Z.; Cooper, C.; Nair, R.; Herrmann, D.; McFarland, A.; Deng, N.; Ruiz-Borrego, M.; Rojo, F.; Trigo, J.M.; Bezares, S.; Caballero, R.; Lim, E.; Timpson, P.; O’Toole, S.; Watkins, D.N.; Cox, T.R.; Samuel, M.S.; Martín, M.; Swarbrick, A. Targeting stromal remodeling and cancer stem cell plasticity overcomes chemoresistance in triple negative breast cancer. Nat. Commun., 2018, 9(1), 2897.
[http://dx.doi.org/10.1038/s41467-018-05220-6] [PMID: 30042390]
[21]
Doldi, V.; Callari, M.; Giannoni, E.; D’Aiuto, F.; Maffezzini, M.; Valdagni, R.; Chiarugi, P.; Gandellini, P.; Zaffaroni, N. Integrated gene and miRNA expression analysis of prostate cancer associated fibroblasts supports a prominent role for interleukin-6 in fibroblast activa-tion. Oncotarget, 2015, 6(31), 31441-31460.
[http://dx.doi.org/10.18632/oncotarget.5056] [PMID: 26375444]
[22]
Yoshida, G.J. Regulation of heterogeneous cancer-associated fibroblasts: the molecular pathology of activated signaling pathways. J. Exp. Clin. Cancer Res., 2020, 39(1), 112.
[http://dx.doi.org/10.1186/s13046-020-01611-0] [PMID: 32546182]
[23]
Sahai, E.; Astsaturov, I.; Cukierman, E.; DeNardo, D.G.; Egeblad, M.; Evans, R.M.; Fearon, D.; Greten, F.R.; Hingorani, S.R.; Hunter, T.; Hynes, R.O.; Jain, R.K.; Janowitz, T.; Jorgensen, C.; Kimmelman, A.C.; Kolonin, M.G.; Maki, R.G.; Powers, R.S.; Puré, E.; Ramirez, D.C.; Scherz-Shouval, R.; Sherman, M.H.; Stewart, S.; Tlsty, T.D.; Tuveson, D.A.; Watt, F.M.; Weaver, V.; Weeraratna, A.T.; Werb, Z. A frame-work for advancing our understanding of cancer-associated fibroblasts. Nat. Rev. Cancer, 2020, 20(3), 174-186.
[http://dx.doi.org/10.1038/s41568-019-0238-1] [PMID: 31980749]
[24]
Duluc, C.; Moatassim-Billah, S.; Chalabi-Dchar, M.; Perraud, A.; Samain, R.; Breibach, F.; Gayral, M.; Cordelier, P.; Delisle, M.B.; Bousquet-Dubouch, M.P.; Tomasini, R.; Schmid, H.; Mathonnet, M.; Pyronnet, S.; Martineau, Y.; Bousquet, C. Pharmacological targeting of the protein synthesis MTOR/4E‐ BP 1 pathway in cancer‐associated fibroblasts abrogates pancreatic tumour chemoresistance. EMBO Mol. Med., 2015, 7(6), 735-753.
[http://dx.doi.org/10.15252/emmm.201404346] [PMID: 25834145]
[25]
Brechbuhl, H.M.; Finlay-schultz, J.; Yamamoto, T.M.; Gillen, A.E.; Cittelly, D.M.; Tan, A. Fibroblast subtypes regulate responsiveness of luminal breast cancer to estrogen. Clin. Cancer. Res., 2017, 146(7), 1710-1722.
[26]
Rhim, A.D.; Oberstein, P.E.; Thomas, D.H.; Mirek, E.T.; Palermo, C.F.; Sastra, S.A.; Dekleva, E.N.; Saunders, T.; Becerra, C.P.; Tattersall, I.W.; Westphalen, C.B.; Kitajewski, J.; Fernandez-Barrena, M.G.; Fernandez-Zapico, M.E.; Iacobuzio-Donahue, C.; Olive, K.P.; Stanger, B.Z. Stromal elements act to restrain, rather than support, pancreatic ductal adenocarcinoma. Cancer. Cell., 2014, 25(6), 735-747.
[http://dx.doi.org/10.1016/j.ccr.2014.04.021] [PMID: 24856585]
[27]
Özdemir, B.C.; Pentcheva-Hoang, T.; Carstens, J.L.; Zheng, X.; Wu, C.C.; Simpson, T.R.; Laklai, H.; Sugimoto, H.; Kahlert, C.; Novitskiy, S.V.; De Jesus-Acosta, A.; Sharma, P.; Heidari, P.; Mahmood, U.; Chin, L.; Moses, H.L.; Weaver, V.M.; Maitra, A.; Allison, J.P.; LeBleu, V.S.; Kalluri, R. Depletion of carcinoma-associated fibroblasts and fibrosis induces immunosuppression and accelerates pancreas cancer with reduced survival. Cancer. Cell, 2014, 25(6), 719-734.
[http://dx.doi.org/10.1016/j.ccr.2014.04.005] [PMID: 24856586]
[28]
Gieniec, K.A.; Butler, L.M.; Worthley, D.L.; Woods, S.L. Cancer-associated fibroblasts—heroes or villains? Br. J. Cancer, 2019, 121(4), 293-302.
[http://dx.doi.org/10.1038/s41416-019-0509-3] [PMID: 31289350]
[29]
Pelon, F.; Bourachot, B.; Kieffer, Y.; Magagna, I.; Mermet-Meillon, F.; Bonnet, I.; Costa, A.; Givel, A.M.; Attieh, Y.; Barbazan, J.; Bonneau, C.; Fuhrmann, L.; Descroix, S.; Vignjevic, D.; Silberzan, P.; Parrini, M.C.; Vincent-Salomon, A.; Mechta-Grigoriou, F. Cancer-associated fibroblast heterogeneity in axillary lymph nodes drives metastases in breast cancer through complementary mechanisms. Nat. Commun., 2020, 11(1), 404.
[http://dx.doi.org/10.1038/s41467-019-14134-w] [PMID: 31964880]
[30]
Flach, E.H.; Rebecca, V.W.; Herlyn, M.; Smalley, K.S.M.; Anderson, A.R.A. Fibroblasts contribute to melanoma tumor growth and drug resistance. Mol. Pharm., 2011, 8(6), 2039-2049.
[http://dx.doi.org/10.1021/mp200421k] [PMID: 22067046]
[31]
Lazard, D.; Sastre, X.; Frid, M.G.; Glukhova, M.A.; Thiery, J.P.; Koteliansky, V.E. Expression of smooth muscle-specific proteins in my-oepithelium and stromal myofibroblasts of normal and malignant human breast tissue. Proc. Natl. Acad. Sci., 1993, 90(3), 999-1003.
[http://dx.doi.org/10.1073/pnas.90.3.999] [PMID: 8430113]
[32]
Vered, M.; Shnaiderman-Shapiro, A.; Zlotogorski-Hurvitz, A.; Salo, T.; Yahalom, R. Cancer-associated fibroblasts in the tumor microenvironment of tongue carcinoma is a heterogeneous cell population. Acta Histochem., 2019, 121(8), 151446.
[http://dx.doi.org/10.1016/j.acthis.2019.151446] [PMID: 31604589]
[33]
Su, S.; Chen, J.; Yao, H.; Liu, J.; Yu, S.; Lao, L.; Wang, M.; Luo, M.; Xing, Y.; Chen, F.; Huang, D.; Zhao, J.; Yang, L.; Liao, D.; Su, F.; Li, M.; Liu, Q.; Song, E. CD10+GPR77+ cancer-associated fibroblasts promote cancer formation and chemoresistance by sustaining cancer stemness. Cell, 2018, 172(4), 841-856.e16.
[http://dx.doi.org/10.1016/j.cell.2018.01.009] [PMID: 29395328]
[34]
Ishibashi, M.; Neri, S.; Hashimoto, H.; Miyashita, T.; Yoshida, T.; Nakamura, Y.; Udagawa, H.; Kirita, K.; Matsumoto, S.; Umemura, S.; Yoh, K.; Niho, S.; Tsuboi, M.; Masutomi, K.; Goto, K.; Ochiai, A.; Ishii, G. CD200-positive cancer associated fibroblasts augment the sensitivity of epidermal growth factor receptor mutation-positive lung adenocarcinomas to EGFR Tyrosine kinase inhibitors. Sci. Rep., 2017, 7(1), 46662.
[http://dx.doi.org/10.1038/srep46662] [PMID: 28429795]
[35]
Costa, A.; Kieffer, Y.; Scholer-Dahirel, A.; Pelon, F.; Bourachot, B.; Cardon, M.; Sirven, P.; Magagna, I.; Fuhrmann, L.; Bernard, C.; Bonneau, C.; Kondratova, M.; Kuperstein, I.; Zinovyev, A.; Givel, A.M.; Parrini, M.C.; Soumelis, V.; Vincent-Salomon, A.; Mechta-Grigoriou, F. Fibroblast heterogeneity and immunosuppressive environment in human breast cancer. Cancer. Cell., 2018, 33(3), 463-479.e10.
[http://dx.doi.org/10.1016/j.ccell.2018.01.011] [PMID: 29455927]
[36]
Sandberg, T.P.; Stuart, M.P.M.E.; Oosting, J.; Tollenaar, R.A.E.M.; Sier, C.F.M.; Mesker, W.E. Increased expression of cancer-associated fibroblast markers at the invasive front and its association with tumor-stroma ratio in colorectal cancer. BMC Cancer, 2019, 19(1), 284.
[http://dx.doi.org/10.1186/s12885-019-5462-2] [PMID: 30922247]
[37]
Sitia, L.; Bonizzi, A.; Mazzucchelli, S.; Negri, S.; Sottani, C.; Grignani, E.; Rizzuto, M.A.; Prosperi, D.; Sorrentino, L.; Morasso, C.; Allevi, R.; Sevieri, M.; Silva, F.; Truffi, M.; Corsi, F. Selective targeting of cancer-associated fibroblasts by engineered h-ferritin nanocages loaded with navitoclax. Cells, 2021, 10(2), 328.
[http://dx.doi.org/10.3390/cells10020328] [PMID: 33562504]
[38]
Cui, Y.; Wang, D.; Xie, M. Tumor-derived extracellular vesicles promote activation of carcinoma-associated fibroblasts and facilitate invasion and metastasis of ovarian cancer by carrying miR-630. Front. Cell Dev. Biol., 2021, 9, 652322.
[http://dx.doi.org/10.3389/fcell.2021.652322] [PMID: 34277601]
[39]
Domogauer, J.D.; de Toledo, S.M.; Howell, R.W.; Azzam, E.I. Acquired radioresistance in cancer associated fibroblasts is concomitant with enhanced antioxidant potential and DNA repair capacity. Cell Commun. Signal., 2021, 19(1), 30.
[http://dx.doi.org/10.1186/s12964-021-00711-4] [PMID: 33637118]
[40]
Zhu, G.; Cao, B.; Liang, X.; Li, L.; Hao, Y.; Meng, W.; He, C.; Wang, L.; Li, L. Small extracellular vesicles containing miR-192/215 mediate hypoxia-induced cancer-associated fibroblast development in head and neck squamous cell carcinoma. Cancer Lett., 2021, 506(55), 11-22.
[http://dx.doi.org/10.1016/j.canlet.2021.01.006] [PMID: 33639203]
[41]
Wang, H.; Wei, H.; Wang, J.; Li, L.; Chen, A.; Li, Z. MicroRNA-181d-5p-containing exosomes derived from CAFs promote EMT by regulating CDX2/HOXA5 in breast cancer. Mol. Ther. Nucleic Acids, 2020, 19(150), 654-667.
[http://dx.doi.org/10.1016/j.omtn.2019.11.024] [PMID: 31955007]
[42]
Wang, H.; Liu, H.; Sun, C.; Liu, C.; Jiang, T.; Yin, Y.; Xu, A.; Pang, Z.; Zhang, B.; Hu, Y. Nanoparticles dual targeting both myeloma cells and cancer-associated fibroblasts simultaneously to improve multiple myeloma treatment. Pharmaceutics, 2021, 13(2), 274.
[http://dx.doi.org/10.3390/pharmaceutics13020274] [PMID: 33670464]
[43]
Awaji, M.; Futakuchi, M.; Heavican, T.; Iqbal, J.; Singh, R.K. Cancer-associated fibroblasts enhance survival and progression of the ag-gressive pancreatic tumor via FGF-2 and CXCL8. Cancer Microenviron., 2019, 12(1), 37-46.
[http://dx.doi.org/10.1007/s12307-019-00223-3] [PMID: 31025289]
[44]
Yu, Y.; Xiao, C-H.; Tan, L-D.; Wang, Q-S.; Li, X-Q.; Feng, Y-M. Cancer-associated fibroblasts induce epithelial–mesenchymal transition of breast cancer cells through paracrine TGF-β signalling. Br. J. Cancer, 2014, 110(3), 724-732.
[http://dx.doi.org/10.1038/bjc.2013.768] [PMID: 24335925]
[45]
Kong, J.; Zhao, H.; Shang, Q.; Ma, Z.; Kang, N.; Tan, J.; Ahmed Ibrahim Alraimi, H.; Liu, T. Establishment and characterization of a carcinoma-associated fibroblast cell line derived from a human salivary gland adenoid cystic carcinoma. Cell Commun. Adhes., 2018, 24(1), 11-18.
[http://dx.doi.org/10.1080/15419061.2018.1464000] [PMID: 29734861]
[46]
Neri, S.; Ishii, G.; Hashimoto, H.; Kuwata, T.; Nagai, K.; Date, H.; Ochiai, A. Podoplanin-expressing cancer-associated fibroblasts lead and enhance the local invasion of cancer cells in lung adenocarcinoma. Int. J. Cancer, 2015, 137(4), 784-796.
[http://dx.doi.org/10.1002/ijc.29464] [PMID: 25648219]
[47]
Li, Q.; Zhang, D.; Wang, Y.; Sun, P.; Hou, X.; Larner, J.; Xiong, W.; Mi, J. MiR-21/Smad 7 signaling determines TGF-β1-induced CAF formation. Sci. Rep., 2013, 3(1), 2038.
[http://dx.doi.org/10.1038/srep02038]
[48]
Nguyen, M.; De Ninno, A.; Mencattini, A.; Mermet-Meillon, F.; Fornabaio, G.; Evans, S.S.; Cossutta, M.; Khira, Y.; Han, W.; Sirven, P.; Pelon, F.; Di Giuseppe, D.; Bertani, F.R.; Gerardino, A.; Yamada, A.; Descroix, S.; Soumelis, V.; Mechta-Grigoriou, F.; Zalcman, G.; Camonis, J.; Martinelli, E.; Businaro, L.; Parrini, M.C. Dissecting effects of anti-cancer drugs and cancer-associated fibroblasts by on-chip reconstitution of immunocompetent tumor microenvironments. Cell Rep., 2018, 25(13), 3884-3893.e3.
[http://dx.doi.org/10.1016/j.celrep.2018.12.015] [PMID: 30590056]
[49]
Kim, K.; Sohn, Y.J.; Lee, R.; Yoo, H.J.; Kang, J.Y.; Choi, N.; Na, D.; Yeon, J.H. Cancer-associated fibroblasts differentiated by exosomes isolated from cancer cells promote cancer cell invasion. Int. J. Mol. Sci., 2020, 21(21), 8153.
[http://dx.doi.org/10.3390/ijms21218153] [PMID: 33142759]
[50]
Shi, H.; Jiang, H.; Wang, L.; Cao, Y.; Liu, P.; Xu, X.; Wang, Y.; Sun, L.; Niu, H. Overexpression of monocarboxylate anion transporter 1 and 4 in T24-induced cancer-associated fibroblasts regulates the progression of bladder cancer cells in a 3D microfluidic device. Cell Cycle, 2015, 14(19), 3058-3065.
[http://dx.doi.org/10.1080/15384101.2015.1053666] [PMID: 26125467]
[51]
Chen, C.P.; Sun, Z.L.; Lu, X.; Wu, W.X.; Guo, W.L.; Lu, J.J.; Han, C.; Huang, J.Q.; Fang, Y. miR-340 suppresses cell migration and invasion by targeting MYO10 in breast cancer. Oncol. Rep., 2016, 35(2), 709-716.
[http://dx.doi.org/10.3892/or.2015.4411] [PMID: 26573744]
[52]
Nii, T.; Makino, K.; Tabata, Y. A cancer invasion model combined with cancer-associated fibroblasts aggregates incorporating gelatin hydrogel microspheres containing a p53 Inhibitor. Tissue. Eng. Part. C. Methods., 2019, 25(12), 711-720.
[http://dx.doi.org/10.1089/ten.tec.2019.0189] [PMID: 31621504]
[53]
Es, H.A.; Cox, T.R.; Sarafraz-Yazdi, E.; Thiery, J.P.; Warkiani, M.E. Pirfenidone reduces epithelial–mesenchymal transition and spheroid formation in breast carcinoma through targeting cancer-associated fibroblasts (Cafs). Cancers , 2021, 13(20), 5118.
[http://dx.doi.org/10.3390/cancers13205118] [PMID: 34680267]
[54]
Brancato, V.; Gioiella, F.; Profeta, M.; Imparato, G.; Guarnieri, D.; Urciuolo, F.; Melone, P.; Netti, P.A. 3D tumor microtissues as an In vitro testing platform for microenvironmentally-triggered drug delivery systems. Acta Biomater., 2017, 57, 47-58.
[http://dx.doi.org/10.1016/j.actbio.2017.05.004] [PMID: 28483691]
[55]
Brancato, V.; Comunanza, V.; Imparato, G.; Corà, D.; Urciuolo, F.; Noghero, A.; Bussolino, F.; Netti, P.A. Bioengineered tumoral microtissues recapitulate desmoplastic reaction of pancreatic cancer. Acta Biomater., 2017, 49, 152-166.
[http://dx.doi.org/10.1016/j.actbio.2016.11.072] [PMID: 27916739]
[56]
Brancato, V.; Gioiella, F.; Imparato, G.; Guarnieri, D.; Urciuolo, F.; Netti, P.A. 3D breast cancer microtissue reveals the role of tumor microenvironment on the transport and efficacy of free-doxorubicin In vitro. Acta Biomater., 2018, 75, 200-212.
[http://dx.doi.org/10.1016/j.actbio.2018.05.055] [PMID: 29864516]
[57]
Aboulkheyr Es, H.; Zhand, S.; Thiery, J.P.; Warkiani, M.E. Pirfenidone reduces immune-suppressive capacity of cancer-associated fibroblasts through targeting CCL17 and TNF-beta. Integr. Biol., 2020, 12(7), 188-197.
[http://dx.doi.org/10.1093/intbio/zyaa014] [PMID: 32638026]
[58]
Zhao, L.; Sun, Y.; Hou, Y.; Peng, Q.; Wang, L.; Luo, H.; Tang, X.; Zeng, Z.; Liu, M. MiRNA expression analysis of cancer-associated fibroblasts and normal fibroblasts in breast cancer. Int. J. Biochem. Cell Biol., 2012, 44(11), 2051-2059.
[http://dx.doi.org/10.1016/j.biocel.2012.08.005] [PMID: 22964023]
[59]
Wu, H.J.; Hao, M.; Yeo, S.K.; Guan, J.L. FAK signaling in cancer-associated fibroblasts promotes breast cancer cell migration and metastasis by exosomal miRNAs-mediated intercellular communication. Oncogene, 2020, 39(12), 2539-2549.
[http://dx.doi.org/10.1038/s41388-020-1162-2] [PMID: 31988451]
[60]
Tang, X.; Tu, G.; Yang, G.; Wang, X.; Kang, L.; Yang, L.; Zeng, H.; Wan, X.; Qiao, Y.; Cui, X.; Liu, M.; Hou, Y. Autocrine TGF-β1/miR-200s/miR-221/DNMT3B regulatory loop maintains CAF status to fuel breast cancer cell proliferation. Cancer Lett., 2019, 452, 79-89.
[http://dx.doi.org/10.1016/j.canlet.2019.02.044] [PMID: 30851420]
[61]
Tao, S.; Li, H.; Ma, X.; Ma, Y.; He, J.; Gao, Y.; Li, J. Elevating microRNA-1-3p shuttled by cancer-associated fibroblasts-derived extracellular vesicles suppresses breast cancer progression and metastasis by inhibiting GLIS1. Cancer Gene Ther., 2021, 28(6), 634-648.
[http://dx.doi.org/10.1038/s41417-020-00244-x] [PMID: 33154575]
[62]
Fang, Z.; Xu, J.; Zhang, B.; Wang, W.; Liu, J.; Liang, C.; Hua, J.; Meng, Q.; Yu, X.; Shi, S. The promising role of noncoding RNAs in cancer-associated fibroblasts: An overview of current status and future perspectives. J. Hematol. Oncol., 2020, 13(1), 154.
[http://dx.doi.org/10.1186/s13045-020-00988-x] [PMID: 33213510]
[63]
Du, Y.; Tu, G.; Yang, G.; Li, G.; Yang, D.; Lang, L.; Xi, L.; Sun, K.; Chen, Y.; Shu, K.; Liao, H.; Liu, M.; Hou, Y. MiR-205/YAP1 in activated fibroblasts of breast tumor promotes VEGF-independent angiogenesis through STAT3 signaling. Theranostics, 2017, 7(16), 3972-3988.
[http://dx.doi.org/10.7150/thno.18990] [PMID: 29109792]
[64]
You, J.; Li, M.; Tan, Y.; Cao, L.; Gu, Q.; Yang, H.; Hu, C. Snail1-expressing cancer-associated fibroblasts induce lung cancer cell epithelial-mesenchymal transition through miR-33b. Oncotarget, 2017, 8(70), 114769-114786.
[http://dx.doi.org/10.18632/oncotarget.23082] [PMID: 29383119]
[65]
Zhang, J.; Han, L.; Yu, J.; Li, H.; Li, Q. miR-224 aggravates cancer-associated fibroblast-induced progression of non-small cell lung cancer by modulating a positive loop of the SIRT3/AMPK/mTOR/HIF-1α axis. Aging , 2021, 13(7), 10431-10449.
[http://dx.doi.org/10.18632/aging.202803] [PMID: 33819917]
[66]
Lee, S.; Hong, J.H.; Kim, J.S.; Yoon, J.S.; Chun, S.H.; Hong, S.A.; Kim, E.J.; Kang, K.; Lee Kang, J.; Ko, Y.H.; Ahn, Y.H. Cancer-associated fibroblasts activated by miR-196a promote the migration and invasion of lung cancer cells. Cancer Lett., 2021, 508, 92-103.
[http://dx.doi.org/10.1016/j.canlet.2021.03.021] [PMID: 33775710]
[67]
Kabir, T.D.; Leigh, R.J.; Tasena, H.; Mellone, M.; Coletta, R.D.; Parkinson, E.K.; Prime, S.S.; Thomas, G.J.; Paterson, I.C.; Zhou, D.; McCall, J.; Speight, P.M.; Lambert, D.W. A miR-335/COX-2/PTEN axis regulates the secretory phenotype of senescent cancer-associated fibroblasts. Aging, 2016, 8(8), 1608-1635.
[http://dx.doi.org/10.18632/aging.100987] [PMID: 27385366]
[68]
Melling, G.E.; Flannery, S.E.; Abidin, S.A.; Clemmens, H.; Prajapati, P.; Hinsley, E.E.; Hunt, S.; Catto, J.W.F.; Coletta, R.D.; Mellone, M.; Thomas, G.J.; Parkinson, E.K.; Prime, S.S.; Paterson, I.C.; Buttle, D.J.; Lambert, D.W. A miRNA-145/TGF-β1 negative feedback loop regulates the cancer-associated fibroblast phenotype. Carcinogenesis, 2018, 39(6), 798-807.
[http://dx.doi.org/10.1093/carcin/bgy032] [PMID: 29506142]
[69]
He, L.; Guo, J.; Fan, Z.; Yang, S.; Zhang, C.; Cheng, B.; Xia, J. Exosomal miR-146b-5p derived from cancer-associated fibroblasts pro-motes progression of oral squamous cell carcinoma by downregulating HIPK3. Cell. Signal., 2023, 106, 110635.
[http://dx.doi.org/10.1016/j.cellsig.2023.110635] [PMID: 36813147]
[70]
Yang, J.; Lu, Y.; Lin, Y.Y.; Zheng, Z.Y.; Fang, J.H.; He, S.; Zhuang, S.M. Vascular mimicry formation is promoted by paracrine TGF-β and SDF1 of cancer-associated fibroblasts and inhibited by miR-101 in hepatocellular carcinoma. Cancer Lett., 2016, 383(1), 18-27.
[http://dx.doi.org/10.1016/j.canlet.2016.09.012] [PMID: 27693460]
[71]
Eun, J.W.; Ahn, H.R.; Baek, G.O.; Yoon, M.G.; Son, J.A.; Weon, J.H.; Yoon, J.H.; Kim, H.S.; Han, J.E.; Kim, S.S.; Cheong, J.Y.; Kim, B.; Cho, H.J. Aberrantly expressed micrornas in cancer-associated fibroblasts and their target oncogenic signatures in hepatocellular carcinoma. Int. J. Mol. Sci., 2023, 24(5), 4272.
[http://dx.doi.org/10.3390/ijms24054272] [PMID: 36901700]
[72]
Zhao, M; Zhuang, A; Fang, Y Cancer-associated fibroblast-derived exosomal miRNA-320a promotes macrophage M2 polarization In vitro by regulating PTEN/PI3K γ signaling in pancreatic cancer. J. Oncol., 2022, 2022, 9514697.
[73]
Mandys, V; Popov, A; Gürlich, R; Havr, J; Pfeiferov, L; Kol, M Expression of selected mirnas in normal and cancer-associated fibro-blasts and in BxPc3 and MIA PaCa-2 Cell lines of pancreatic ductal adenocarcinoma. Int. J. Mol. Sci., 2023, 24(4), 3617.
[http://dx.doi.org/10.3390/ijms24043617]
[74]
Mitra, A.K.; Zillhardt, M.; Hua, Y.; Tiwari, P.; Murmann, A.E.; Peter, M.E.; Lengyel, E. MicroRNAs reprogram normal fibroblasts into cancer-associated fibroblasts in ovarian cancer. Cancer Discov., 2012, 2(12), 1100-1108.
[http://dx.doi.org/10.1158/2159-8290.CD-12-0206] [PMID: 23171795]
[75]
Han, Q.; Tan, S.; Gong, L.; Li, G.; Wu, Q.; Chen, L.; Du, S.; Li, W.; Liu, X.; Cai, J.; Wang, Z. Omental cancer‐associated fibroblast‐derived exosomes with low microRNA‐29c‐3p promote ovarian cancer peritoneal metastasis. Cancer Sci., 2023, 114(5), 1929-1942. Epub ahead of print
[http://dx.doi.org/10.1111/cas.15726] [PMID: 36644823]
[76]
Liu, Y; Fu, W; Cao, X; Li, S; Xiong, T; Zhang, X. Delivery of miR-224-5p by exosomes from cancer-associated fibroblasts potentiates progression of clear cell renal cell carcinoma. Comput. Math. Methods. Med., 2021, 2021
[http://dx.doi.org/10.1155/2021/5517747]
[77]
Zhang, N.; Wang, Y.; Liu, H.; Shen, W. Extracellular vesicle encapsulated microRNA-320a inhibits endometrial cancer by suppression of the HIF1α/VEGFA axis. Exp. Cell Res., 2020, 394(2), 112113.
[http://dx.doi.org/10.1016/j.yexcr.2020.112113] [PMID: 32473223]
[78]
Zhang, X.; Wang, Y.; Wang, X.; Zou, B.; Mei, J.; Peng, X.; Wu, Z. Extracellular vesicles-encapsulated microRNA-10a-5p shed from cancer-associated fibroblast facilitates cervical squamous cell carcinoma cell angiogenesis and tumorigenicity via Hedgehog signaling pathway. Cancer Gene Ther., 2021, 28(5), 529-542.
[http://dx.doi.org/10.1038/s41417-020-00238-9] [PMID: 33235271]
[79]
Wang, X; Wang, X; Xu, M; Sheng, W; Higgins, PJ; Czekay, R-P Effects of CAF-derived MicroRNA on tumor biology and clinical applications. Cancers, 2021, 13(13), 3160.
[http://dx.doi.org/10.3390/cancers13133160]
[80]
Kunita, A.; Morita, S.; Irisa, T.U.; Goto, A.; Niki, T.; Takai, D.; Nakajima, J.; Fukayama, M. MicroRNA-21 in cancer-associated fibroblasts supports lung adenocarcinoma progression. Sci. Rep., 2018, 8(1), 8838.
[http://dx.doi.org/10.1038/s41598-018-27128-3] [PMID: 29892003]
[81]
Mohammadi-Yeganeh, S.; Mansouri, A.; Paryan, M. Targeting of miR9/NOTCH1 interaction reduces metastatic behavior in triple-negative breast cancer. Chem. Biol. Drug Des., 2015, 86(5), 1185-1191.
[http://dx.doi.org/10.1111/cbdd.12584] [PMID: 25963903]
[82]
Baroni, S.; Romero-Cordoba, S.; Plantamura, I.; Dugo, M.; D’Ippolito, E.; Cataldo, A.; Cosentino, G.; Angeloni, V.; Rossini, A.; Daidone, M.G.; Iorio, M.V. Exosome-mediated delivery of miR-9 induces cancer-associated fibroblast-like properties in human breast fibroblasts. Cell Death Dis., 2016, 7(7), e2312.
[http://dx.doi.org/10.1038/cddis.2016.224] [PMID: 27468688]
[83]
kia, V.; Paryan, M.; Mortazavi, Y.; Biglari, A.; Mohammadi-Yeganeh, S. Evaluation of exosomal miR‐9 and miR‐155 targeting PTEN and DUSP14 in highly metastatic breast cancer and their effect on low metastatic cells. J. Cell. Biochem., 2019, 120(4), 5666-5676.
[http://dx.doi.org/10.1002/jcb.27850] [PMID: 30335891]
[84]
Cosentino, G.; Romero-Cordoba, S.; Plantamura, I.; Cataldo, A.; Iorio, M.V. miR-9-mediated inhibition of EFEMP1 contributes to the acquisition of pro-tumoral properties in normal fibroblasts. Cells, 2020, 9(9), 2143.
[http://dx.doi.org/10.3390/cells9092143] [PMID: 32972039]
[85]
Vu, L.T.; Peng, B.; Zhang, D.X.; Ma, V.; Mathey-Andrews, C.A.; Lam, C.K.; Kiomourtzis, T.; Jin, J.; McReynolds, L.; Huang, L.; Grimson, A.; Cho, W.C.; Lieberman, J.; Le, M.T. Tumor-secreted extracellular vesicles promote the activation of cancer-associated fibroblasts via the transfer of microRNA-125b. J. Extracell. Vesicles, 2019, 8(1), 1599680.
[http://dx.doi.org/10.1080/20013078.2019.1599680] [PMID: 31044053]
[86]
Pang, W.; Su, J.; Wang, Y.; Feng, H.; Dai, X.; Yuan, Y.; Chen, X.; Yao, W. Pancreatic cancer‐secreted miR‐155 implicates in the conversion from normal fibroblasts to cancer‐associated fibroblasts. Cancer Sci., 2015, 106(10), 1362-1369.
[http://dx.doi.org/10.1111/cas.12747] [PMID: 26195069]
[87]
Fang, T.; Lv, H.; Lv, G.; Li, T.; Wang, C.; Han, Q.; Yu, L.; Su, B.; Guo, L.; Huang, S.; Cao, D.; Tang, L.; Tang, S.; Wu, M.; Yang, W.; Wang, H. Tumor-derived exosomal miR-1247-3p induces cancer-associated fibroblast activation to foster lung metastasis of liver cancer. Nat. Commun., 2018, 9(1), 191.
[http://dx.doi.org/10.1038/s41467-017-02583-0] [PMID: 29335551]
[88]
Shen, P.; Fillatreau, S.; Thase, M.E.; Mahableshwarkar, A.R.; Dragheim, M.; Loft, H. A meta-analysis of randomized, placebo-controlled trials of vortioxetine for the treatment of major depressive disorder in adults. Eur. Neuropsychopharmacol., 2015, 26(6), 1-15. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0924977X16300050%5Cnhttp://www.ncbi.nlm.nih.gov/pubmed/27139079
[89]
Mo, Y.; Leung, L.L.; Mak, C.S.L.; Wang, X.; Chan, W.S.; Hui, L.M.N.; Tang, H.W.M.; Siu, M.K.Y.; Sharma, R.; Xu, D.; Tsui, S.K.W.; Ngan, H.Y.S.; Yung, M.M.H.; Chan, K.K.L.; Chan, D.W. Tumor-secreted exosomal miR-141 activates tumor-stroma interactions and controls premetastatic niche formation in ovarian cancer metastasis. Mol. Cancer, 2023, 22(1), 4.
[http://dx.doi.org/10.1186/s12943-022-01703-9] [PMID: 36624516]
[90]
Zhang, H.; Deng, T.; Liu, R.; Ning, T.; Yang, H.; Liu, D.; Zhang, Q.; Lin, D.; Ge, S.; Bai, M.; Wang, X.; Zhang, L.; Li, H.; Yang, Y.; Ji, Z.; Wang, H.; Ying, G.; Ba, Y. CAF secreted miR-522 suppresses ferroptosis and promotes acquired chemo-resistance in gastric cancer. Mol. Cancer, 2020, 19(1), 43.
[http://dx.doi.org/10.1186/s12943-020-01168-8] [PMID: 32106859]
[91]
Moradi-Chaleshtori, M.; Hashemi, S.M.; Soudi, S.; Bandehpour, M.; Mohammadi-Yeganeh, S. Tumor‐derived exosomal microRNAs and proteins as modulators of macrophage function. J. Cell. Physiol., 2019, 234(6), 7970-7982.
[http://dx.doi.org/10.1002/jcp.27552] [PMID: 30378104]
[92]
Sansone, P.; Berishaj, M.; Rajasekhar, V.K.; Ceccarelli, C.; Chang, Q.; Strillacci, A.; Savini, C.; Shapiro, L.; Bowman, R.L.; Mastroleo, C.; De Carolis, S.; Daly, L.; Benito-Martin, A.; Perna, F.; Fabbri, N.; Healey, J.H.; Spisni, E.; Cricca, M.; Lyden, D.; Bonafé, M.; Bromberg, J. Evolution of cancer stem-like cells in endocrine-resistant metastatic breast cancers is mediated by stromal microvesicles. Cancer Res., 2017, 77(8), 1927-1941.
[http://dx.doi.org/10.1158/0008-5472.CAN-16-2129] [PMID: 28202520]
[93]
Shan, G; Zhou, X; Gu, J; Zhou, D; Cheng, W; Wu, H. Downregulated exosomal microRNA-148b-3p in cancer associated fibroblasts enhance chemosensitivity of bladder cancer cells by downregulating the Wnt / β -catenin pathway and upregulating PTEN. 2021, 44, 45-59.
[94]
Qin, X; Guo, H; Wang, X; Zhu, X; Yan, M; Wang, X Exosomal miR-196a derived from cancer-associated fibroblasts confers cisplatin resistance in head and neck cancer through targeting CDKN1B and ING5. Genome Biol., 2019, 20(1), 12.
[95]
Yao, F; Wu, S; Xu, M Exosomal miR-196a-5p enhances radioresistance in lung cancer cells by downregulating NFKBIA. Kaohsiung J. Med. Sci., 2022, 39(6), 554-564.
[96]
Wang, H; Huang, H; Wang, L; Liu, Y; Wang, M; Zhao, S Cancer-associated fibroblasts secreted miR-103a-3p suppresses apoptosis and promotes cisplatin resistance in non-small cell lung cancer. Aging , 2021, 13(10), 14456-14468.
[http://dx.doi.org/10.18632/aging.103556]
[97]
Zhang, H; Shi, Y; Wang, JLH; Wang, P; Wu, Z; Li, L Cancer-associated fibroblast-derived exosomal microRNA-24-3p enhances colon cancer cell resistance to MTX by down-regulating CDX2/HEPH axis. J. Cell. Mol. Med., 2020, 25(8), 3699-3713.
[98]
Liu, W.; Wang, S.; Zhou, S.; Yang, F.; Jiang, W.; Zhang, Q.; Wang, L. A systems biology approach to identify microRNAs contributing to cisplatin resistance in human ovarian cancer cells. Mol. Biosyst., 2017, 13(11), 2268-2276.
[http://dx.doi.org/10.1039/C7MB00362E] [PMID: 28861582]
[99]
Han, X.; Li, Q.; Liu, C.; Wang, C.; Li, Y. Overexpression miR‐24‐3p repressed Bim expression to confer tamoxifen resistance in breast cancer. J. Cell. Biochem., 2019, 120(8), 12966-12976.
[http://dx.doi.org/10.1002/jcb.28568] [PMID: 31001849]
[100]
Zhang, L; Yao, J; Li, W; Zhang, C Micro-RNA-21 regulates cancer-associated fibroblast-mediated drug resistance in pancreatic cancer. Oncol. Res., 2018, 26(6), 827-835.
[101]
Zhao, Q.; Huang, L.; Qin, G.; Qiao, Y.; Ren, F.; Shen, C.; Wang, S.; Liu, S.; Lian, J.; Wang, D.; Yu, W.; Zhang, Y. Cancer-associated fibro-blasts induce monocytic myeloid-derived suppressor cell generation via IL-6/exosomal miR-21-activated STAT3 signaling to promote cisplatin resistance in esophageal squamous cell carcinoma. Cancer Lett., 2021, 518, 35-48.
[http://dx.doi.org/10.1016/j.canlet.2021.06.009] [PMID: 34139285]
[102]
Chen, X.; Liu, Y.; Zhang, Q.; Liu, B.; Cheng, Y.; Zhang, Y.; Sun, Y.; Liu, J. Exosomal miR-590-3p derived from cancer-associated fibro-blasts confers radioresistance in colorectal cancer. Mol. Ther. Nucleic Acids, 2021, 24(127), 113-126.
[http://dx.doi.org/10.1016/j.omtn.2020.11.003] [PMID: 33738143]
[103]
Takahashi, R.; Prieto-Vila, M.; Kohama, I.; Ochiya, T. Development of mi RNA ‐based therapeutic approaches for cancer patients. Cancer Sci., 2019, 110(4), 1140-1147.
[http://dx.doi.org/10.1111/cas.13965] [PMID: 30729639]
[104]
Shah, M.Y.; Ferrajoli, A.; Sood, A.K.; Lopez-Berestein, G.; Calin, G.A. microRNA therapeutics in cancer: An emerging concept. EBioMedicine, 2016, 12, 34-42.
[http://dx.doi.org/10.1016/j.ebiom.2016.09.017] [PMID: 27720213]
[105]
Boca, S.; Gulei, D.; Zimta, A.A.; Onaciu, A.; Magdo, L.; Tigu, A.B.; Ionescu, C.; Irimie, A.; Buiga, R.; Berindan-Neagoe, I. Nanoscale delivery systems for microRNAs in cancer therapy. Cell. Mol. Life Sci., 2020, 77(6), 1059-1086.
[http://dx.doi.org/10.1007/s00018-019-03317-9] [PMID: 31637450]
[106]
Safarzadeh, M.; Mohammadi-Yeganeh, S.; Ghorbani-Bidkorbeh, F.; Haji Molla Hoseini, M. Chitosan based nanoformulation expressing miR-155 as a promising adjuvant to enhance Th1-biased immune responses. Life Sci., 2022, 297, 120459.
[http://dx.doi.org/10.1016/j.lfs.2022.120459] [PMID: 35248524]
[107]
Cheng, C.J.; Bahal, R.; Babar, I.A.; Pincus, Z.; Barrera, F.; Liu, C.; Svoronos, A.; Braddock, D.T.; Glazer, P.M.; Engelman, D.M.; Saltzman, W.M.; Slack, F.J. MicroRNA silencing for cancer therapy targeted to the tumour microenvironment. Nature, 2015, 518(7537), 107-110.
[http://dx.doi.org/10.1038/nature13905] [PMID: 25409146]
[108]
Alhussan, A.; Bromma, K.; Bozdoğan, E.P.D.; Metcalfe, A.; Karasinska, J.; Beckham, W.; Alexander, A.S.; Renouf, D.J.; Schaeffer, D.F.; Chithrani, D.B. Investigation of nano-bio interactions within a pancreatic tumor microenvironment for the advancement of nanomedicine in cancer treatment. Curr. Oncol., 2021, 28(3), 1962-1979.
[http://dx.doi.org/10.3390/curroncol28030183] [PMID: 34073974]
[109]
Teng, C.; Zhang, B.; Yuan, Z.; Kuang, Z.; Chai, Z.; Ren, L.; Qin, C.; Yang, L.; Han, X.; Yin, L. Fibroblast activation protein-α-adaptive micelles deliver anti-cancer drugs and reprogram stroma fibrosis. Nanoscale, 2020, 12(46), 23756-23767.
[http://dx.doi.org/10.1039/D0NR04465B] [PMID: 33231238]
[110]
Shoucair, I.; Weber Mello, F.; Jabalee, J.; Maleki, S.; Garnis, C. The role of cancer-associated fibroblasts and extracellular vesicles in tu-morigenesis. Int. J. Mol. Sci., 2020, 21(18), 6837.
[http://dx.doi.org/10.3390/ijms21186837] [PMID: 32957712]
[111]
Shojaei, S.; Hashemi, S.M.; Ghanbarian, H.; Salehi, M.; Mohammadi-Yeganeh, S. Effect of mesenchymal stem cells‐derived exosomes on tumor microenvironment: Tumor progression versus tumor suppression. J. Cell. Physiol., 2019, 234(4), 3394-3409.
[http://dx.doi.org/10.1002/jcp.27326] [PMID: 30362503]
[112]
Lee, S.W.L.; Paoletti, C.; Campisi, M.; Osaki, T.; Adriani, G.; Kamm, R.D.; Mattu, C.; Chiono, V. MicroRNA delivery through nanoparticles. J. Control. Release, 2019, 313, 80-95.
[http://dx.doi.org/10.1016/j.jconrel.2019.10.007] [PMID: 31622695]
[113]
Lee, H.K.; Finniss, S.; Cazacu, S.; Bucris, E.; Ziv-Av, A.; Xiang, C.; Bobbitt, K.; Rempel, S.A.; Hasselbach, L.; Mikkelsen, T.; Slavin, S.; Brodie, C. Mesenchymal stem cells deliver synthetic microRNA mimics to glioma cells and glioma stem cells and inhibit their cell migration and self-renewal. Oncotarget, 2013, 4(2), 346-361.
[http://dx.doi.org/10.18632/oncotarget.868] [PMID: 23548312]
[114]
Naito, Y.; Yamamoto, Y.; Sakamoto, N.; Shimomura, I.; Kogure, A.; Kumazaki, M.; Yokoi, A.; Yashiro, M.; Kiyono, T.; Yanagihara, K.; Takahashi, R.; Hirakawa, K.; Yasui, W.; Ochiya, T. Cancer extracellular vesicles contribute to stromal heterogeneity by inducing chemo kines in cancer-associated fibroblasts. Oncogene, 2019, 38(28), 5566-5579.
[http://dx.doi.org/10.1038/s41388-019-0832-4] [PMID: 31147602]