VEGF secreted by Mesenchymal stem cells mediates the differentiation of endothelial progenitor cells into endothelial cells via paracrine mechanisms

Molecular Medicine Reports

Volumn 17, Issue 1, 2018, Pages 1667-1675

  Ge, Quanhu ^a   Zhang, Hongwei ^a   Hou, Jixue ^a   Wan, Longfei ^a   Cheng, Wenzhe ^a   Wang, Xiaoyi ^a   Dong, Dan ^a   Chen, Congzhe ^a   Xia, Jie ^a   Guo, Jun ^a   Chen, Xueling ^a   Wu, Xiangwei ^a  

^a SHIHEZI UNIVERSITY   (China)

Author keywords

Differentiation; Endothelial cells; Endothelial progenitor cells; Mesenchymal stem cells; Vascular endothelial growth factor

Indexed keywords

VASCULOTROPIN; VON WILLEBRAND FACTOR; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE; VASCULOTROPIN A;

ANIMAL CELL; ARTICLE; CELL COMMUNICATION; CELL DIFFERENTIATION; COCULTURE; CONTROLLED STUDY; ENDOTHELIAL PROGENITOR CELL; ENDOTHELIUM CELL; GENE EXPRESSION; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PARACRINE SIGNALING; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN SECRETION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CELL CULTURE; MALE; MESENCHYMAL STROMA CELL; PHYSIOLOGY; SECRETION (PROCESS); SMOOTH MUSCLE CELL;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; COCULTURE TECHNIQUES; ENDOTHELIAL PROGENITOR CELLS; MALE; MESENCHYMAL STROMAL CELLS; MICE, INBRED C57BL; MYOCYTES, SMOOTH MUSCLE; PARACRINE COMMUNICATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 85034953369     PISSN: 17912997     EISSN: 17913004     Source Type: Journal    
DOI: 10.3892/mmr.2017.8059     Document Type: Article

References (43)

1. Lenti M, Cieri E, De Rango P, Pozzilli P, Coscarella C, Bertoglio C, Troiani R and Cao P: Endovascular treatment of long lesions of the superficial femoral artery: Results from a multicenter registry of a spiral, covered polytetrafluoroethylene stent. J Vasc Surg 45:32-39, 2007.
2. Vasa M, Fichtlscherer S, Aicher A, Adler K, Urbich C, Martin H, Zeiher AM and Dimmeler S: Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res 89: E1-E7, 2001.
3. Tateishi-Yuyama E, Matsubara H, Murohara T, Ikeda U, Shintani S, Masaki H, Amano K, Kishimoto Y, Yoshimoto K, Akashi H, et al: Therapeutic angiogenesis for patients with limb ischaemia by autologous transplantation of bone-marrow cells: A pilot study and a randomised controlled trial. Lancet 360:427-435, 2002.
4. Kim SW, Han H, Chae GT, Lee SH, Bo S, Yoon JH, Lee YS, Lee KS, Park HK and Kang KS: Successful stem cell therapy using umbilical cord blood-derived multipotent stem cells for Buerger's disease and ischemic limb disease animal model. Stem Cells 24:1620-1626, 2006.
5. Saigawa T, Kato K, Ozawa T, Toba K, Makiyama Y, Minagawa S, Hashimoto S, Furukawa T, Nakamura Y, Hanawa H, et al: Clinical application of bone marrow implantation in patients with arteriosclerosis obliterans, and the association between efficacy and the number of implanted bone marrow cells. Circ J 68:1189-1193, 2004.
6. Friedenstein AJ, Chailakhjan RK and Lalykina KS: The develop - ment of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet 3:393-403, 1970.
7. Bianco P, Robey PG and Simmons PJ: Mesenchymal stem cells: Revisiting history, concepts and assays. Cell Stem Cell 2:313-319, 2008.
8. Wu X, Pang L, Lei W, Lu W, Li J, Li Z, Frassica FJ, Chen X, Wan M and Cao X: Inhibition of Sca-1-positive skeletal stem cell recruitment by alendronate blunts the anabolic effects of parathyroid hormone on bone remodeling. Cell Stem Cell 7:571-580, 2010.
9. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G and Isner JM: Isolation of putative progenitor endothelial cells for angiogenesis. Science 275:964-967, 1997.
10. Ribatti D: The discovery of endothelial progenitor cells. An historical review. Leuk Res 31:439-444, 2007.
11. Cao X, Wu X, Frassica D, Yu B, Pang L, Xian L, Wan M, Lei W, Armour M, Tryggestad E, Wong J, Wen CY, Lu WW and Frassica FJ: Irradiation induces bone injury by damaging bone marrow microenvironment for stem cells. Proc Natl Acad Sci USA 108:1609-1614, 2011.
12. Geng YJ, Yang YJ, Casscells SW and Willerson JT: Vascular stem cells: A new concept in the pathogenesis of atherosclerosis and interventions for coronary heart disease. Future Cardiol 2:585-592, 2006.
13. Zhang H, Xian L, Lin Z, Yang C, Zhang M, Feng W, Peng X, Chen X and Wu X: Endothelial progenitor cells as a possible component of stem cell niche to promote self-renewal of mesenchymal stem cells. Mol Cell Biochem 397:235-243, 2014.
14. Xia J, Zhang H, Gao X, Guo J, Hou J, Wang X, Wang S, Yang T, Zhang X, Ge Q, et al: E-cadherin-mediated contact of endothelial progenitor cells with mesenchymal stem cells through β-catenin signaling. Cell Biol Int 40:407-418, 2016.
15. Zhang M, Zhang H, Feng W, Wang Y, Yin S, Chen X and Wu X: Endothelial progenitor cells promote osteogenic differentiation of marrow stromal cells in a paracrine manner. Zhonghua Yi Xue Za Zhi 95:1253-1257, 2015 (In Chinese).
16. Bost F, Caron L, Marchetti I, Dani C, Le Marchand-Brustel Y and Binétruy B: Retinoic acid activation of the ERK pathway is required for embryonic stem cell commitment into the adipocyte lineage. Biochem J 361:621-627, 2002.
17. Tashiro K, Kawabata K, Sakurai H, Kurachi S, Sakurai F, Yamanishi K and Mizuguchi H: Efficient adenovirus vector-mediated PPAR gamma gene transfer into mouse embryoid bodies promotes adipocyte differentiation. J Gene Med 10:498-507, 2008.
18. Shah NM, Groves AK and Anderson DJ: Alternative neural crest cell fates are instructively promoted by TGFbeta superfamily members. Cell 85:331-343, 1996.
19. Cepko CL, Austin CP, Yang X, Alexiades M and Ezzeddine D: Cell fate determination in the vertebrate retina. Proc Natl Acad Sci USA 93:589-595, 1996.
20. Morrison SJ, Shah NM and Anderson DJ: Regulatory mechanisms in stem cell biology. Cell 88:287-298, 1997.
21. Li H, Daculsi R, Grellier M, Bareille R, Bourget C, Remy M and Amedee J: The role of vascular actors in two dimensional dialogue of human bone marrow stromal cell and endothelial cell for inducing self-assembled network. PLoS One 6:e16767, 2011.
22. Mayer H, Bertram H, Lindenmaier W, Korff T, Weber H and Weich H: Vascular endothelial growth factor (VEGF-A) expression in human mesenchymal stem cells: Autocrine and paracrine role on osteoblastic and endothelial differentiation. J Cell Biochem 95:827-839, 2005.
23. Asahara T, Takahashi T, Masuda H, Kalka C, Chen D, Iwaguro H, Inai Y, Silver M and Isner JM: VEGF contributes to postnatal neovascularization by mobilizing bone marrow-derived endothelial progenitor cells. EMBO J 18:3964-3972, 1999.
24. Newman PJ, Berndt MC, Gorski J, White GC II, Lyman S, Paddock C and Muller WA: PECAM-1 (CD31) cloning and relation to adhesion molecules of the immunoglobulin gene superfamily. Science 247:1219-1222, 1990.
25. Lopes da Silva M and Cutler DF: von Willebrand factor multimerization and the polarity of secretory pathways in endothelial cells. Blood 128:277-285, 2016.
26. Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2 (Delta Delta C (T)) method. Methods 25:402-408, 2001.
27. Oswald J, Boxberger S, Jørgensen B, Feldmann S, Ehninger G, Bornhäuser M and Werner C: Mesenchymal stem cells can be differentiated into endothelial cells in vitro. Stem Cells 22:377-384, 2004.
28. Zaniboni A, Bernardini C, Bertocchi M, Zannoni A, Bianchi F, Avallone G, Mangano C, Sarli G, Calzà L, Bacci ML and Forni M: In vitro differentiation of porcine aortic vascular precursor cells to endothelial and vascular smooth muscle cells. Am J Physiol Cell Physiol 309: C320-C331, 2015.
29. Zachary I: VEGF signalling: Integration and multi-tasking in endothelial cell biology. Biochem Soc Trans 31:1171-1177, 2003.
30. Gupta K, Ramakrishnan S, Browne PV, Solovey A and Hebbel RP: A novel technique for culture of human dermal microvascular endothelial cells under either serum-free or serum-supplemented conditions: Isolation by panning and stimulation with vascular endothelial growth factor. Exp Cell Res 230:244-251, 1997.
31. Fong GH, Rossant J, Gertsenstein M and Breitman ML: Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 376:66-70, 1995.
32. Risau W: Mechanisms of angiogenesis. Nature 386:671-674, 1997.
33. Ziche M, Morbidelli L, Choudhuri R, Zhang HT, Donnini S, Granger HJ and Bicknell R: Nitric oxide synthase lies downstream from vascular endothelial growth factor-induced but not basic fibroblast growth factor-induced angiogenesis. J Clin Invest 99:2625-2634, 1997.
34. Jiang Y, Vaessen B, Lenvik T, Blackstad M, Reyes M and Verfaillie CM: Multipotent progenitor cells can be isolated from postnatal murine bone marrow, muscle, and brain. Exp Hematol 30:896-904, 2002.
35. Liu Z, Jiang Y, Hao H, Gupta K, Xu J, Chu L, McFalls E, Zweier J, Verfaillie C and Bache RJ: Endothelial nitric oxide synthase is dynamically expressed during bone marrow stem cell differentiation into endothelial cells. Am J Physiol Heart Circ Physiol 293: H1760-H1765, 2007.
36. Xu J, Liu X, Jiang Y, Chu L, Hao H, Liua Z, Verfaillie C, Zweier J, Gupta K and Liu Z: MAPK/ERK signalling mediates VEGF-induced bone marrow stem cell differentiation into endothelial cell. J Cell Mol Med 12:2395-2406, 2008.
37. Guo S, Cheng Y, Ma Y and Yang X: Endothelial progenitor cells derived from CD34+ cells form cooperative vascular networks. Cell Physiol Biochem 26:679-688, 2010.
38. Gehling UM, Ergün S, Schumacher U, Wagener C, Pantel K, Otte M, Schuch G, Schafhausen P, Mende T, Kilic N, et al: In vitro differentiation of endothelial cells from AC133-positive progenitor cells. Blood 95:3106-3112, 2000.
39. Quirici N, Soligo D, Caneva L, Servida F, Bossolasco P and Deliliers GL: Differentiation and expansion of endothelial cells from human bone marrow CD133 (+) cells. Br J Haematol 115:186-194, 2001.
40. Reyes M, Lund T, Lenvik T, Aguiar D, Koodie L and Verfaillie CM: Purification and ex vivo expansion of postnatal human marrow mesodermal progenitor cells. Blood 98:2615-2625, 2001.
41. Horwitz EM, Gordon PL, Koo WK, Marx JC, Neel MD, McNall RY, Muul L and Hofmann T: Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: Implications for cell therapy of bone. Proc Natl Acad Sci USA 99:8932-8937, 2002.
42. Glaser DE, Turner WS, Madfis N, Wong L, Zamora J, White N, Reyes S, Burns AB, Gopinathan A and McCloskey KE: Multifactorial Optimizations for Directing Endothelial Fate from Stem Cells. PLoS One 11:e0166663, 2016.
43. Kinnaird T, Stabile E, Burnett MS, Lee CW, Barr S, Fuchs S and Epstein SE: Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ Res 94:678-685, 2004.