Prostate tumor-induced angiogenesis is blocked by exosomes derived from menstrual stem cells through the inhibition of reactive oxygen species

Oncotarget

Volumn 7, Issue 28, 2016, Pages 44462-44477

  Alcayaga Miranda, Francisca ^a,b   González, Paz L ^a,b   Lopez Verrilli, Alejandra ^b   Varas Godoy, Manuel ^a   Aguila Díaz, Carolina ^c   Contreras, Luis ^a   Khoury, Maroun ^a,b,c  

^a UNIVERSIDAD DE LOS ANDES   (Chile)

^b Chilean Consortium for Regenerative Medicine   (Chile)

^c Clínica Universidad de los Andes ^*  (Chile)

Author keywords

Exosomes; Mesenchymal stem cells; Prostate cancer; ROS pathway; Tumor angiogenesis

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR RECEPTOR; HEMOGLOBIN; HYPOXIA INDUCIBLE FACTOR 1BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; REACTIVE OXYGEN METABOLITE; VASCULOTROPIN; VASCULOTROPIN A;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW DERIVED MESENCHYMAL STEM CELL; CAPILLARY DENSITY; CASE REPORT; CONTROLLED STUDY; EXOSOME; HEMOGLOBIN DETERMINATION; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MENSTRUAL STEM CELL; MOUSE; NONHUMAN; PROSTATE CANCER; PROTEIN SECRETION; STEM CELL; STEM CELL TRANSPLANTATION; TUMOR GROWTH; TUMOR VASCULARIZATION; TUMOR XENOGRAFT; ANIMAL; BLOOD; CELL CULTURE; COCULTURE; DRUG SCREENING; FEMALE; GENETICS; KNOCKOUT MOUSE; MCF-7 CELL LINE; MENSTRUATION; MESENCHYMAL STROMA CELL; METABOLISM; MIDDLE AGED; NEOVASCULARIZATION (PATHOLOGY); NONOBESE DIABETIC MOUSE; PATHOLOGY; PROCEDURES; PROSTATE TUMOR; SCID MOUSE; TUMOR CELL LINE; VASCULARIZATION;

ADULT; AGED; ANIMALS; CELL LINE, TUMOR; CELLS, CULTURED; COCULTURE TECHNIQUES; EXOSOMES; FEMALE; HUMANS; MALE; MCF-7 CELLS; MENSTRUATION; MESENCHYMAL STROMAL CELLS; MICE, INBRED NOD; MICE, KNOCKOUT; MICE, SCID; MIDDLE AGED; NEOVASCULARIZATION, PATHOLOGIC; PROSTATIC NEOPLASMS; REACTIVE OXYGEN SPECIES; VASCULAR ENDOTHELIAL GROWTH FACTOR A; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84978695674     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.9852     Document Type: Article

References (51)

1. Koch S, Tugues S, Li X, Gualandi L, Claesson-Welsh L. Signal transduction by vascular endothelial growth factor receptors. The Biochemical journal. 2011; 437:169-183.
2. Kim YW, Byzova TV. Oxidative stress in angiogenesis and vascular disease. Blood. 2014; 123:625-631.
3. Wang Y, Zang QS, Liu Z, Wu Q, Maass D, Dulan G, Shaul PW, Melito L, Frantz DE, Kilgore JA, Williams NS, Terada LS, Nwariaku FE. Regulation of VEGF-induced endothelial cell migration by mitochondrial reactive oxygen species. American journal of physiology Cell physiology. 2011; 301:C695-704.
4. Szatrowski TP, Nathan CF. Production of large amounts of hydrogen peroxide by human tumor cells. Cancer research. 1991; 51:794-798.
5. Xia C, Meng Q, Liu LZ, Rojanasakul Y, Wang XR, Jiang BH. Reactive oxygen species regulate angiogenesis and tumor growth through vascular endothelial growth factor. Cancer research. 2007; 67:10823-10830.
6. Kim J, Koyanagi T, Mochly-Rosen D. PKCdelta activation mediates angiogenesis via NADPH oxidase activity in PC-3 prostate cancer cells. The Prostate. 2011; 71:946-954.
7. Studeny M, Marini FC, Dembinski JL, Zompetta C, Cabreira-Hansen M, Bekele BN, Champlin RE, AndreeffM. Mesenchymal stem cells: potential precursors for tumor stroma and targeted-delivery vehicles for anticancer agents. Journal of the National Cancer Institute. 2004; 96:1593-1603.
8. Kucerova L, Altanerova V, Matuskova M, Tyciakova S, Altaner C. Adipose tissue-derived human mesenchymal stem cells mediated prodrug cancer gene therapy. Cancer research. 2007; 67:6304-6313.
9. Zhang T, Lee YW, Rui YF, Cheng TY, Jiang XH, Li G. Bone marrow-derived mesenchymal stem cells promote growth, angiogenesis of breast and prostate tumors. Stem cell research & therapy. 2013; 4:70.
10. Beckermann BM, Kallifatidis G, Groth A, Frommhold D, Apel A, Mattern J, Salnikov AV, Moldenhauer G, Wagner W, Diehlmann A, Saffrich R, Schubert M, Ho AD, Giese N, Buchler MW, Friess H, et al. VEGF expression by mesenchymal stem cells contributes to angiogenesis in pancreatic carcinoma. British journal of cancer. 2008; 99:622-631.
11. Orecchioni S, Gregato G, Martin-Padura I, Reggiani F, Braidotti P, Mancuso P, Calleri A, Quarna J, Marighetti P, Aldeni C, Pruneri G, Martella S, Manconi A, Petit JY, Rietjens M, Bertolini F. Complementary populations of human adipose CD34+ progenitor cells promote growth, angiogenesis, and metastasis of breast cancer. Cancer research. 2013; 73:5880-5891.
12. Keramidas M, de Fraipont F, Karageorgis A, Moisan A, Persoons V, Richard MJ, Coll JL, Rome C. The dual effect of mesenchymal stem cells on tumour growth, tumour angiogenesis. Stem cell research & therapy. 2013; 4:41.
13. Otsu K, Das S, Houser SD, Quadri SK, Bhattacharya S, Bhattacharya J. Concentration-dependent inhibition of angiogenesis by mesenchymal stem cells. Blood. 2009; 113:4197-4205.
14. Ho IA, Toh HC, Ng WH, Teo YL, Guo CM, Hui KM, Lam PY. Human bone marrow-derived mesenchymal stem cells suppress human glioma growth through inhibition of angiogenesis. Stem cells. 2013; 31:146-155.
15. Alcayaga-Miranda F, Varas-Godoy M, Khoury M. Harnessing the Angiogenic Potential of Stem Cell-Derived Exosomes for Vascular Regeneration. Stem cells international. 2016; 2016:3409169.
16. Akimoto K, Kimura K, Nagano M, Takano S, To'a Salazar G, Yamashita T, Ohneda O. Umbilical cord blood-derived mesenchymal stem cells inhibit, but adipose tissuederived mesenchymal stem cells promote, glioblastoma multiforme proliferation. Stem cells and development. 2013; 22:1370-1386.
17. Cousin B, Ravet E, Poglio S, De Toni F, Bertuzzi M, Lulka H, Touil I, Andre M, Grolleau JL, Peron JM, Chavoin JP, Bourin P, Penicaud L, Casteilla L, Buscail L, Cordelier P. Adult stromal cells derived from human adipose tissue provoke pancreatic cancer cell death both in vitro and in vivo. PloS one. 2009; 4:e6278.
18. Klopp AH, Gupta A, Spaeth E, AndreeffM, Marini F, 3rd. Concise review: Dissecting a discrepancy in the literature: do mesenchymal stem cells support or suppress tumor growth? Stem cells. 2011; 29:11-19.
19. Menge T, Gerber M, Wataha K, Reid W, Guha S, Cox CS, Jr., Dash P, Reitz MS, Jr., Khakoo AY, Pati S. Human mesenchymal stem cells inhibit endothelial proliferation and angiogenesis via cell-cell contact through modulation of the VE-Cadherin/beta-catenin signaling pathway. Stem cells and development. 2013; 22:148-157.
20. S ELA, Mager I, Breakefield XO, Wood MJ. Extracellular vesicles: biology and emerging therapeutic opportunities. Nature reviews Drug discovery. 2013; 12:347-357.
21. Costa-Silva B, Aiello NM, Ocean AJ, Singh S, Zhang H, Thakur BK, Becker A, Hoshino A, Mark MT, Molina H, Xiang J, Zhang T, Theilen TM, Garcia-Santos G, Williams C, Ararso Y, et al. Pancreatic cancer exosomes initiate premetastatic niche formation in the liver. Nature cell biology. 2015; 17:816-826.
22. Mulcahy LA, Pink RC, Carter DR. Routes, mechanisms of extracellular vesicle uptake. Journal of extracellular vesicles. 2014; 3.
23. Urbich C, Kuehbacher A, Dimmeler S. Role of microRNAs in vascular diseases, inflammation, and angiogenesis. Cardiovascular research. 2008; 79:581-588.
24. 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.
25. 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 letters. 2012; 315:28-37.
26. Baglio SR, Rooijers K, Koppers-Lalic D, Verweij FJ, Perez Lanzon M, Zini N, Naaijkens B, Perut F, Niessen HW, Baldini N, Pegtel DM. Human bone marrow-and adiposemesenchymal stem cells secrete exosomes enriched in distinctive miRNA and tRNA species. Stem cell research & therapy. 2015; 6:127.
27. Pepper MS. Manipulating angiogenesis. From basic science to the bedside. Arteriosclerosis, thrombosis, and vascular biology. 1997; 17:605-619.
28. Maas JW, Groothuis PG, Dunselman GA, de Goeij AF, Struyker Boudier HA, Evers JL. Endometrial angiogenesis throughout the human menstrual cycle. Human reproduction. 2001; 16:1557-1561.
29. Alcayaga-Miranda F, Cuenca J, Luz-Crawford P, Aguila-Diaz C, Fernandez A, Figueroa FE, Khoury M. Characterization of menstrual stem cells: angiogenic effect, migration, hematopoietic stem cell support in comparison with bone marrow mesenchymal stem cells. Stem cell research & therapy. 2015; 6:32.
30. Khoury M, Alcayaga-Miranda F, Illanes SE, Figueroa FE. The promising potential of menstrual stem cells for antenatal diagnosis, cell therapy. Frontiers in immunology. 2014; 5:205.
31. Luz-Crawford P, Torres MJ, Noel D, Fernandez A, Toupet K, Alcayaga-Miranda F, Tejedor G, Jorgensen C, Illanes SE, Figueroa FE, Djouad F, Khoury M. The immunosuppressive signature of menstrual blood mesenchymal stem cells entails opposite effects on experimental arthritis and graft versus host diseases. Stem cells. 2016; 34:456-469.
32. Alcayaga-Miranda F, Cuenca J, Martin A, Contreras L, Figueroa FE, Khoury M. Combination therapy of menstrual derived mesenchymal stem cells and antibiotics ameliorates survival in sepsis. Stem cell research & therapy. 2015; 6:199.
33. Thery C, Amigorena S, Raposo G, Clayton A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Current protocols in cell biology/editorial board, Juan S Bonifacino [et al]. 2006; Chapter 3:Unit 3 22.
34. Lopez-Verrilli MA, Caviedes A, Cabrera A, Sandoval S, Wyneken U, Khoury M. Mesenchymal stem cell-derived exosomes from different sources selectively promote neuritic outgrowth. Neuroscience. 2016; 320:129-139.
35. Gonzalez PL, Carvajal C, Cuenca J, Alcayaga-Miranda F, Figueroa FE, Bartolucci J, Salazar-Aravena L, Khoury M. Chorion Mesenchymal Stem Cells Show Superior Differentiation, Immunosuppressive, and Angiogenic Potentials in Comparison With Haploidentical Maternal Placental Cells. Stem cells translational medicine. 2015; 4:1109-1121.
36. Alcayaga-Miranda F, Cascallo M, Rojas JJ, Pastor J, Alemany R. Osteosarcoma cells as carriers to allow antitumor activity of canine oncolytic adenovirus in the presence of neutralizing antibodies. Cancer gene therapy. 2010; 17:792-802.
37. Meng X, Ichim TE, Zhong J, Rogers A, Yin Z, Jackson J, Wang H, Ge W, Bogin V, Chan KW, Thebaud B, Riordan NH. Endometrial regenerative cells: a novel stem cell population. Journal of translational medicine. 2007; 5:57.
38. Lopez-Verrilli MA, Picou F, Court FA. Schwann cellderived exosomes enhance axonal regeneration in the peripheral nervous system. Glia. 2013; 61:1795-1806.
39. Escrevente C, Keller S, Altevogt P, Costa J. Interaction and uptake of exosomes by ovarian cancer cells. BMC cancer. 2011; 11:108.
40. Svensson KJ, Christianson HC, Wittrup A, Bourseau-Guilmain E, Lindqvist E, Svensson LM, Morgelin M, Belting M. Exosome uptake depends on ERK1/2-heat shock protein 27 signaling and lipid Raft-mediated endocytosis negatively regulated by caveolin-1. The Journal of biological chemistry. 2013; 288:17713-17724.
41. Huang S, Pettaway CA, Uehara H, Bucana CD, Fidler IJ. Blockade of NF-kappaB activity in human prostate cancer cells is associated with suppression of angiogenesis, invasion, and metastasis. Oncogene. 2001; 20:4188-4197.
42. Kumar B, Koul S, Khandrika L, Meacham RB, Koul HK. Oxidative stress is inherent in prostate cancer cells and is required for aggressive phenotype. Cancer research. 2008; 68:1777-1785.
43. Deer EL, Gonzalez-Hernandez J, Coursen JD, Shea JE, Ngatia J, Scaife CL, Firpo MA, Mulvihill SJ. Phenotype and genotype of pancreatic cancer cell lines. Pancreas. 2010; 39:425-435.
44. Xu W, Liu LZ, Loizidou M, Ahmed M, Charles IG. The role of nitric oxide in cancer. Cell research. 2002; 12:311-320.
45. Fujioka S, Sclabas GM, Schmidt C, Frederick WA, Dong QG, Abbruzzese JL, Evans DB, Baker C, Chiao PJ. Function of nuclear factor kappaB in pancreatic cancer metastasis. Clin Cancer Res. 2003; 9:346-354.
46. Qiao L, Zhao TJ, Wang FZ, Shan CL, Ye LH, Zhang XD. NF-kappaB downregulation may be involved the depression of tumor cell proliferation mediated by human mesenchymal stem cells. Acta pharmacologica Sinica. 2008; 29:333-340.
47. Laurent A, Nicco C, Chereau C, Goulvestre C, Alexandre J, Alves A, Levy E, Goldwasser F, Panis Y, Soubrane O, Weill B, Batteux F. Controlling tumor growth by modulating endogenous production of reactive oxygen species. Cancer research. 2005; 65:948-956.
48. Wang Y, Huang X, Cang H, Gao F, Yamamoto T, Osaki T, Yi J. The endogenous reactive oxygen species promote NF-kappaB activation by targeting on activation of NF-kappaB-inducing kinase in oral squamous carcinoma cells. Free radical research. 2007; 41:963-971.
49. Kim YW, West XZ, Byzova TV. Inflammation and oxidative stress in angiogenesis and vascular disease. Journal of molecular medicine. 2013; 91:323-328.
50. Del Fattore A, Luciano R, Saracino R, Battafarano G, Rizzo C, Pascucci L, Alessandri G, Pessina A, Perrotta A, Fierabracci A, Muraca M. Differential effects of extracellular vesicles secreted by mesenchymal stem cells from different sources on glioblastoma cells. Expert opinion on biological therapy. 2015; 15:495-504.
51. Yu B, Zhang X, Li X. Exosomes derived from mesenchymal stem cells. International journal of molecular sciences. 2014; 15:4142-4157.