Exosomes derived from human bone marrow mesenchymal stem cells promote tumor growth in vivo

Cancer Letters

Volumn 315, Issue 1, 2012, Pages 28-37

  Zhu, Wei ^a   Huang, Ling ^a   Li, Yahong ^a   Zhang, Xu ^a   Gu, Jianmei ^a   Yan, Yongmin ^a   Xu, Xiaomeng ^a   Wang, Mei ^a   Qian, Hui ^a   Xu, Wenrong ^a,b  

^a JIANGSU UNIVERSITY   (China)

^b AFFILIATED HOSPITAL OF JIANGSU UNIVERSITY   (China)

Author keywords

Exosome; MAPK pathway; Mesenchymal stem cell; Tumor growth; Xenograft model

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE 1; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL ACTIVITY; CELL CYCLE PHASE; CELL INTERACTION; CELL ISOLATION; CELL LEVEL; CELL SECRETION; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DISEASE ACTIVITY; ENZYME ACTIVATION; ENZYME INHIBITION; EXOSOME; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR CELL;

ANIMALS; BONE MARROW CELLS; CELL DIFFERENTIATION; CELL GROWTH PROCESSES; EXOSOMES; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MESENCHYMAL STEM CELLS; MICE; MICE, INBRED BALB C; NEOPLASMS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 81955167406     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2011.10.002     Document Type: Article

References (35)

1. Pittenger M.F., Mackay A.M., Beck S.C., Jaiswal R.K., Douglas R., Mosca J.D., Moorman M.A., Simonetti D.W., Craig S., Marshak D.R. Multilineage potential of adult human mensenchymal stem cells. Science 1999, 284:143-147.
2. Studeny M., Marini F.C., Champlin R.E., Zompetta C., Fidler I.J., Andreeff M. Bone marrow-derived mesenchymal stem cells as vehicles for interferon-beta delivery into tumors. Cancer Res. 2002, 62:3603-3608.
3. Studeny M., Marini F.C., Dembinski J.L., Zompetta C., Cabreira-Hansen M., Bekele B.N., Champlin R.E., Andreeff M. Mesenchymal stem cells: potential precursors for tumor stroma and targeted-delivery vehicles for anticancer agents. J. Natl. Cancer Inst. 2004, 96:1593-1603.
4. Roorda B.D., ter Elst A., Kamps W.A., de Bont E.S. Bone marrow-derived cells and tumor growth: contribution of bone marrow-derived cells to tumor micro-environments with special focus on mesenchymal stem cells. Crit. Rev. Oncol. Hematol. 2009, 69:187-198.
5. Zhu W., Xu W., Jiang R., Qian H., Chen M., Hu J., Cao W., Han C., Chen Y. Mesenchymal stem cells derived from bone marrow favor tumor cell growth in vivo. Exp. Mol. Pathol. 2006, 80:267-274.
6. Karnoub A.E., Dash A.B., Vo A.P., Sullivan A., Brooks M.W., Bell G.W., Richardson A.L., Polyak K., Tubo R., Weinberg R.A. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 2007, 449:557-563.
7. Shinagawa K., Kitadai Y., Tanaka M., Sumida T., Kodama M., Higashi Y., Tanaka S., Yasui W., Chayama K. Mesenchymal stem cells enhance growth and metastasis of colon cancer. Int. J. Cancer 2010, 127:2323-2333.
8. Cao H., Xu W., Qian H., Zhu W., Yan Y., Zhou H., Zhang X., Xu X., Li J., Chen Z., Xu X. Mesenchymal stem cell-like cells derived from human gastric cancer tissues. Cancer Lett. 2009, 274:61-71.
9. Djouad F., Plence P., Bony C., Tropel P., Apparailly F., Sany J., Noël D., Jorgensen C. Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood 2003, 102:3837-3844.
10. Rubio D., Garcia S., De la Cueva T., Paz M.F., Lloyd A.C., Bernad A., Garcia-Castro J. Human mesenchymal stem cell transformation is associated with a mesenchymal-epithelial transition. Exp. Cell Res. 2008, 314:691-698.
11. Spaeth E.L., Dembinski J.L., Sasser A.K., Watson K., Klopp A., Hall B., Andreeff M., Marini F. Mesenchymal stem cell transition to tumor-associated fibroblasts contributes to fibrovascular network expansion and tumor progression. PLoS One 2009, 4:e4992.
12. Bouffi C., Djouad F., Mathieu M., Noël D., Jorgensen C., cells Multipotent mesenchymal stromal, benefit? rheumatoid arthritis: risk or Rheumatology (Oxford) 2009, 48:1185-1189.
13. Pap E., Pállinger E., Pásztói M., Falus A. Highlights of a new type of intercellular communication: microvesicle-based information transfer. Inflamm. Res. 2009, 58:1-8.
14. Al-Nedawi K., Meehan B., Rak J. Microvesicles: messengers and mediators of tumor progression. Cell Cycle 2009, 8:2014-2018.
15. Simons M., Raposo G. Exosomes-vesicular carriers for intercellular communication. Curr. Opin. Cell Biol. 2009, 21:575-581.
16. Angelot F., Seillès E., Biichlé S., Berda Y., Gaugler B., Plumas J., Chaperot L., Dignat-George F., Tiberghien P., Saas P., Garnache-Ottou F. Endothelial cell-derived microparticles induce plasmacytoid dendritic cell maturation: potential implications in inflammatory diseases. Haematologica 2009, 94:1502-1512.
17. Raposo G., Nijman H.W., Stoorvogel W., Liejendekker R., Harding C.V., Melief C.J., Geuze H.J. B lymphocytes secrete antigen-presenting vesicles. J. Exp. Med. 1996, 183:1161-1172.
18. Camussi G., Deregibus M.C., Tetta C. Paracrine/endocrine mechanism of stem cells on kidney repair: role of microvesicle-mediated transfer of genetic information. Curr. Opin. Nephrol. Hypertens. 2010, 19:7-12.
19. Bruno S., Grange C., Deregibus M.C., Calogero R.A., Saviozzi S., Collino F., Morando L., Busca A., Falda M., Bussolati B., Tetta C., Camussi G. Mesenchymal stem cell-derived microvesicles protect against acute tubular injury. J. Am. Soc. Nephrol. 2009, 20:1053-1067.
20. Xu W., Zhang X., Qian H., Zhu W., Sun X., Hu J., Zhou H., Chen Y. Mesenchymal stem cells from adult human bone marrow differentiate into a cardiomyocyte phenotype in vitro. Exp. Biol. Med. (Maywood) 2004, 229:623-631.
21. Qu J.L., Qu X.J., Zhao M.F., Teng Y.E., Zhang Y., Hou K.Z., Jiang Y.H., Yang X.H., Liu Y.P. Gastric cancer exosomes promote tumour cell proliferation through PI3K/Akt and MAPK/ERK activation. Dig. Liver Dis. 2009, 41:875-880.
22. Tomayko M.M., Reynolds C.P. Determination of subcutaneous tumor size in athymic (nude) mice. Cancer Chemother. Pharmacol. 1989, 24:148-154.
23. Beckermann B.M., Kallifatidis G., Groth A., Frommhold D., Apel A., Mattern J., Salnikov A.V., Moldenhauer G., Wagner W., Diehlmann A., Saffrich R., Schubert M., Ho A.D., Giese N., Büchler M.W., Friess H., Büchler P., Herr I. EGF expression by mesenchymal stem cells contributes to angiogenesis in pancreatic carcinoma. Br. J. Cancer 2008, 99:622-631.
24. Roorda B.D., Elst A., Boer T.G., Kamps W.A., De Bont E.S. Mesenchymal stem cells contribute to tumor cell proliferation by direct cell-cell contact interactions. Cancer Invest. 2010, 28:526-534.
25. Lai R.C., Arslan F., Lee M.M., Sze N.S., Choo A., Chen T.S., Salto-Tellez M., Timmers L., Lee C.N., El Oakley R.M., Pasterkamp G., de Kleijn D.P., Lim S.K. Exosome secreted by MSC reduces myocardial ischemia/reperfusion injury. Stem Cell Res. 2010, 4:214-222.
26. Ma B., Ren J., Jiang H.F., Jia J. Antitumor activities against hepatocellular carcinoma induced by bone marrow mesenchymal stem cells pulsed with tumor-derived exosomes. Beijing Da Xue Xue Bao 2008, 40:494-499.
27. Hood J.L., Pan H., Lanza G.M., Wickline S.A. Consortium for Translational Research in Advanced Imaging and Nanomedicine (C-TRAIN), Paracrine induction of endothelium by tumor exosomes. Lab. Invest. 2009, 89:1317-1328.
28. Weber J.D., Raben D.M., Phillips P.J., Baldassare J.J. Sustained activation of extracellular-signal-regulated kinase 1 (ERK1) is required for the continued expression of cyclin D1 in G1 phase. Biochem. J. 1997, 326:61-68.
29. Balmanno K., Cook S.J. Sustained MAP kinase activation is required for the expression of cyclin D1, p21Cip1 and a subset of AP-1 proteins in CCL39 cells. Oncogene 1999, 18:3085-3097.
30. Hao L., Zhang C., Qiu Y., Wang L., Luo Y., Jin M., Zhang Y., Guo T.B., Matsushima K., Zhang Y. Recombination of CXCR4, VEGF, and MMP-9 predicting lymph node metastasis in human breast cancer. Cancer Lett. 2007, 253:34-42.
31. Liang Z., Brooks J., Willard M., Liang K., Yoon Y., Kang S., Shim H. VEGF-mediated tumor angiogenesis through Akt signaling pathway. Biochem. Biophys. Res. Commun. 2007, 359:716-722.
32. Walczak C., Gaignier F., Gilet A., Zou F., Thornton S.N., Ropars A. Aldosterone increases VEGF-A production in human neutrophils through PI3K, ERK1/2 and p38 pathways. Biochim. Biophys. Acta. 2011, 23.
33. Essafi-Benkhadir K., Pouyssegur J., Pages G. Implication of the ERK pathway on the post-transcriptional regulation of VEGF mRNA stability. Methods Mol. Biol. 2010, 661:451-469.
34. Bi S., Liu J.R., Li Y., Wang Q., Liu H.K., Yan Y.G., Chen B.Q., Sun W.G. Gamma-Tocotrienol modulates the paracrine secretion of VEGF induced by cobalt(II) chloride via ERK signaling pathway in gastric adenocarcinoma SGC-7901 cell line. Toxicology 2010, 274:27-33.
35. Yoshino Y., Aoyagi M., Tamaki M., Duan L., Morimoto T., Ohno K. Activation of p38 MAPK and/or JNK contributes to increased levels of VEGF secretion in human malignant glioma cells. Int. J. Oncol. 2006, 29:981-987.