Endothelial exosomes contribute to the antitumor response during breast cancer neoadjuvant chemotherapy via microRNA transfer

Oncotarget

Volumn 6, Issue 12, 2015, Pages 10253-10266

  Bovy, Nicolas ^a   Blomme, Benoît ^a   Frères, Pierre ^a   Dederen, Stella ^a   Nivelles, Olivier ^a   Lion, Michelle ^a   Carnet, Oriane ^a   Martial, Joseph A ^a   Noël, Agnès ^a   Thiry, Marc ^a   Jérusalem, Guy ^b   Josse, Claire ^a   Bours, Vincent ^a   Tabruyn, Sébastien P ^a   Struman, Ingrid ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

Angiogenesis; Cancer; Exosomes; microRNAs; miR 503

Indexed keywords

CYCLIN D2; CYCLIN D3; CYCLOPHOSPHAMIDE; DOCETAXEL; EPIRUBICIN; FLUOROURACIL; MICRORNA; MICRORNA 503; PACLITAXEL; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; CANCER ADJUVANT THERAPY; CANCER CELL; CANCER PATIENT; CELL CULTURE; CELL INVASION; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; EXOSOME; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; PROTEIN TARGETING; RNA ANALYSIS; RNA TRANSPORT; TUMOR CELL; ADJUVANT CHEMOTHERAPY; BREAST NEOPLASMS; GENE EXPRESSION REGULATION; GENETICS; HCT 116 CELL LINE; METABOLISM; NEOADJUVANT THERAPY; PATHOLOGY; TUMOR CELL LINE; UMBILICAL VEIN ENDOTHELIAL CELL;

BREAST NEOPLASMS; CELL LINE, TUMOR; CHEMOTHERAPY, ADJUVANT; ENDOTHELIAL CELLS; EXOSOMES; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HCT116 CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MICRORNAS; NEOADJUVANT THERAPY;

EID: 84929603438     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3520     Document Type: Article

References (41)

1. Suzuki HI, Katsura A, Matsuyama H, Miyazono K. MicroRNA regulons in tumor microenvironment. Oncogene. 2014.
2. Goubran HA, Kotb RR, Stakiw J, Emara ME, Burnouf T. Regulation of tumor growth and metastasis: the role of tumor microenvironment. Cancer Growth Metastasis. 2014; 7: 9-18.
3. Carmeliet P. Angiogenesis in life, disease and medicine. Nature. 2005; 438: 932-936.
4. Ebos JM, Kerbel RS. Antiangiogenic therapy: impact on invasion, disease progression, and metastasis. Nat Rev Clin Oncol. 2011; 8: 210-221.
5. Li M, Li J, Ding X, He M, Cheng SY. microRNA and cancer. AAPS J. 2010; 12: 309-317.
6. Zhang C. MicroRNAs in vascular biology and vascular disease. J Cardiovasc Transl Res. 2010; 3: 235-240.
7. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009; 136: 215-233.
8. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004; 116: 281-297.
9. Taylor DD, Gercel-Taylor C. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol Oncol. 2008; 110: 13-21.
10. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007; 9: 654-659.
11. Mathivanan S, Ji H, Simpson RJ. Exosomes: extracellular organelles important in intercellular communication. J Proteomics. 2010; 73: 1907-1920.
12. Kharaziha P, Ceder S, Li Q, Panaretakis T. Tumor cellderived exosomes: a message in a bottle. Biochim Biophys Acta. 2012; 1826: 103-111.
13. Mittelbrunn M, Gutierrez-Vazquez C, Villarroya-Beltri C, Gonzalez S, Sanchez-Cabo F, Gonzalez MA, Bernad A, Sanchez-Madrid F. Unidirectional transfer of microRNAloaded exosomes from T cells to antigen-presenting cells. Nat Commun. 2011; 2: 282.
14. Halkein J, Tabruyn SP, Ricke-Hoch M, Haghikia A, Nguyen NQ, Scherr M, Castermans K, Malvaux L, Lambert V, Thiry M, Sliwa K, Noel A, Martial JA, et al. MicroRNA-146a is a therapeutic target and biomarker for peripartum cardiomyopathy. J Clin Invest. 2013; 123: 2143-2154.
15. Hergenreider E, Heydt S, Treguer K, Boettger T, Horrevoets AJ, Zeiher AM, Scheffer MP, Frangakis AS, Yin X, Mayr M, Braun T, Urbich C, Boon RA, et al. Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs. Nat Cell Biol. 2012; 14:249-256.
16. Wang J, Huang SK, Zhao M, Yang M, Zhong JL, Gu YY, Peng H, Che YQ, Huang CZ. Identification of a circulating microRNA signature for colorectal cancer detection. PLoS One. 2014; 9: e87451.
17. Freres P, Josse C, Bovy N, Boukerroucha M, Struman I, Bours V, Jerusalem G. Neoadjuvant chemotherapy in breast cancer patients induces miR-34a and miR-122 expression. J Cell Physiol. 2014.
18. Fu Z, Qian F, Yang X, Jiang H, Chen Y, Liu S. Circulating miR-222 in plasma and its potential diagnostic and prognostic value in gastric cancer. Med Oncol. 2014; 31:164.
19. Kahlert C, Kalluri R. Exosomes in tumor microenvironment influence cancer progression and metastasis. J Mol Med (Berl). 2013; 91: 431-437.
20. Kucharzewska P, Belting M. Emerging roles of extracellular vesicles in the adaptive response of tumour cells to microenvironmental stress. J Extracell Vesicles. 2013; 2.
21. Webber J, Steadman R, Mason MD, Tabi Z, Clayton A. Cancer exosomes trigger fibroblast to myofibroblast differentiation. Cancer Res. 2010; 70: 9621-9630.
22. Zhuang G, Wu X, Jiang Z, Kasman I, Yao J, Guan Y, Oeh J, Modrusan Z, Bais C, Sampath D, Ferrara N. Tumoursecreted miR-9 promotes endothelial cell migration and angiogenesis by activating the JAK-STAT pathway. EMBO J. 2012; 31: 3513-3523.
23. Hessvik NP, Phuyal S, Brech A, Sandvig K, Llorente A. Profiling of microRNAs in exosomes released from PC-3 prostate cancer cells. Biochim Biophys Acta. 2012; 1819:1154-1163.
24. Carmeliet P, Jain RK. Molecular mechanisms and clinical applications of angiogenesis. Nature. 2011; 473: 298-307.
25. Qiu T, Zhou L, Wang T, Xu J, Wang J, Chen W, Zhou X, Huang Z, Zhu W, Shu Y, Liu P. miR-503 regulates the resistance of non-small cell lung cancer cells to cisplatin by targeting Bcl-2. Int J Mol Med. 2013; 32: 593-598.
26. Xiao F, Zhang W, Chen L, Chen F, Xie H, Xing C, Yu X, Ding S, Chen K, Guo H, Cheng J, Zheng S, Zhou L. MicroRNA-503 inhibits the G1/S transition by downregulating cyclin D3 and E2F3 in hepatocellular carcinoma. J Transl Med. 2013; 11: 195.
27. Yang Y, Liu L, Zhang Y, Guan H, Wu J, Zhu X, Yuan J, Li M. MiR-503 targets PI3K p85 and IKK-beta and suppresses progression of non-small cell lung cancer. Int J Cancer. 2014; 135: 1531-1542.
28. Van Balkom BW, de Jong OG, Smits M, Brummelman J, den Ouden K, de Bree PM, van Eijndhoven MA, Pegtel DM, Stoorvogel W, Wurdinger T, Verhaar MC. Endothelial cells require miR-214 to secrete exosomes that suppress senescence and induce angiogenesis in human and mouse endothelial cells. Blood. 2013; 121: 3997-4006, S1-15.
29. Sharghi-Namini S, Tan E, Ong LL, Ge R, Asada HH. Dll4- containing exosomes induce capillary sprout retraction in a 3D microenvironment. Sci Rep. 2014; 4: 4031.
30. Lee JK, Park SR, Jung BK, Jeon YK, Lee YS, Kim MK, Kim YG, Jang JY, Kim CW. Exosomes derived from mesenchymal stem cells suppress angiogenesis by downregulating VEGF expression in breast cancer cells. PLoS One. 2013; 8: e84256.
31. Zhu W, Huang L, Li Y, Zhang X, Gu J, Yan Y, Xu X, Wang M, Qian H, Xu W. Exosomes derived from human bone marrow mesenchymal stem cells promote tumor growth in vivo. Cancer Lett. 2012; 315: 28-37.
32. Zitvogel L, Regnault A, Lozier A, Wolfers J, Flament C, Tenza D, Ricciardi-Castagnoli P, Raposo G, Amigorena S. Eradication of established murine tumors using a novel cellfree vaccine: dendritic cell-derived exosomes. Nat Med. 1998; 4: 594-600.
33. Caporali A, Meloni M, Vollenkle C, Bonci D, Sala-Newby GB, Addis R, Spinetti G, Losa S, Masson R, Baker AH, Agami R, le Sage C, Condorelli G, et al. Deregulation of microRNA-503 contributes to diabetes mellitusinduced impairment of endothelial function and reparative angiogenesis after limb ischemia. Circulation. 2011; 123:282-291.
34. Sarkar S, Dey BK, Dutta A. MiR-322/424 and -503 are induced during muscle differentiation and promote cell cycle quiescence and differentiation by down-regulation of Cdc25A. Mol Biol Cell. 2010; 21: 2138-2149.
35. Zhou B, Ma R, Si W, Li S, Xu Y, Tu X, Wang Q. MicroRNA-503 targets FGF2 and VEGFA and inhibits tumor angiogenesis and growth. Cancer Lett. 2013; 333:159-169.
36. Wagner-Ecker M, Schwager C, Wirkner U, Abdollahi A, Huber PE. MicroRNA expression after ionizing radiation in human endothelial cells. Radiat Oncol. 2010; 5: 25.
37. Soultati A, Mountzios G, Avgerinou C, Papaxoinis G, Pectasides D, Dimopoulos M-A, Papadimitriou C. Endothelial vascular toxicity from chemotherapeutic agents:preclinical evidence and clinical implications. Cancer Treatment Reviews. 2012; 38: 473-83.
38. Nie Y, Han BM, Liu XB, Yang JJ, Wang F, Cong XF, Chen X. Identification of MicroRNAs involved in hypoxia- and serum deprivation-induced apoptosis in mesenchymal stem cells. Int J Biol Sci. 2011; 7: 762-768.
39. Rissland OS, Hong SJ, Bartel DP. MicroRNA destabilization enables dynamic regulation of the miR-16 family in response to cell-cycle changes. Mol Cell. 2011; 43: 993-1004.
40. Tabruyn SP, Memet S, Ave P, Verhaeghe C, Mayo KH, Struman I, Martial JA, Griffioen AW. NF-kappaB activation in endothelial cells is critical for the activity of angiostatic agents. Mol Cancer Ther. 2009; 8: 2645-2654.
41. Correa de Sampaio P, Auslaender D, Krubasik D, Failla A V, Skepper JN, Murphy G, English WR. A heterogeneous in vitro three dimensional model of tumour-stroma interactions regulating sprouting angiogenesis. PLoS One. 2012; 7: e30753.