Vascular smooth muscle cell apoptosis promotes transplant arteriosclerosis through inducing the production of SDF-1α

American Journal of Transplantation

Volumn 12, Issue 8, 2012, Pages 2029-2043

  Li, J ^a   Liu, S ^a   Li, W ^b   Hu, S ^a   Xiong, J ^a   Shu, X ^b   Hu, Q ^a   Zheng, Q ^a   Song, Z ^a  

^a Union Hospital   (China)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Apoptosis; chemokine; mesenchymal stem cells; smooth muscle cells; transplant arteriosclerosis

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; ENDOGLIN; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BCL XL; PROTEIN KINASE B; PROTEIN P53; RAPAMYCIN; STROMAL CELL DERIVED FACTOR 1ALPHA; THY 1 ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; AORTA GRAFT; APOPTOSIS; ARTERIOSCLEROSIS; ARTICLE; CELL CULTURE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; LENTIVIRINAE; MALE; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; TRANSPLANT ARTERIOSCLEROSIS; VASCULAR SMOOTH MUSCLE CELL;

ANIMALS; AORTA; APOPTOSIS; ARTERIOSCLEROSIS; BLOTTING, WESTERN; CHEMOKINE CXCL12; CULTURE MEDIA, CONDITIONED; IN SITU NICK-END LABELING; MALE; MUSCLE, SMOOTH, VASCULAR; POLYMERASE CHAIN REACTION; PROTEIN KINASES; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; TRANSPLANTATION;

EID: 84864473848     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/j.1600-6143.2012.04082.x     Document Type: Article

References (60)

1. Lechler RI, Sykes M, Thomson AW, Turka LA,. Organ transplantation-how much of the promise has been realized? Nat Med 2005; 11: 605-613.
2. Sayegh MH, Carpenter CB,. Transplantation 50 years later-progress, challenges, and promises. N Engl J Med 2004; 351: 2761-2766.
3. Tantravahi J, Womer KL, Kaplan B,. Why hasn't eliminating acute rejection improved graft survival? Annu Rev Med 2007; 58: 369-385.
4. Hillebrands JL, Rozing J,. Chronic transplant dysfunction and transplant arteriosclerosis: new insights into underlying mechanisms. Expert Rev Mol Med 2003; 5: 1-23.
5. Rahmani M, Cruz RP, Granville DJ, McManus BM,. Allograft vasculopathy versus atherosclerosis. Circ Res 2006; 99: 801-815.
6. Libby P, Pober JS,. Chronic rejection. Immunity 2001; 14: 387-397.
7. Ross R,. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 1993; 362: 801-809.
8. Vallabhaneni KC, Tkachuk S, Kiyan Y, et al,. Urokinase receptor mediates mobilization, migration, and differentiation of mesenchymal stem cells. Cardiovasc Res 2011; 90: 113-121.
9. Hillebrands JL, Klatter FA, van den Hurk BM, Popa ER, Nieuwenhuis P, Rozing J,. Origin of neointimal endothelium and alpha-actin-positive smooth muscle cells in transplant arteriosclerosis. J Clin Invest 2001; 107: 1411-1422.
10. Religa P, Bojakowski K, Maksymowicz M, et al,. Smooth-muscle progenitor cells of bone marrow origin contribute to the development of neointimal thickenings in rat aortic allografts and injured rat carotid arteries. Transplantation 2002; 74: 1310-1315.
11. Sata M, Saiura A, Kunisato A, et al,. Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis. Nat Med 2002; 8: 403-409.
12. Wang CH, Cherng WJ, Yang NI, et al,. Late-outgrowth endothelial cells attenuate intimal hyperplasia contributed by mesenchymal stem cells after vascular injury. Arterioscler Thromb Vasc Biol 2008; 28: 54-60.
13. Sakihama H, Masunaga T, Yamashita K, et al,. Stromal cell-derived factor-1 and CXCR4 interaction is critical for development of transplant arteriosclerosis. Circulation 2004; 110: 2924-2930.
14. Zernecke A, Schober A, Bot I, et al,. SDF-1alpha/CXCR4 axis is instrumental in neointimal hyperplasia and recruitment of smooth muscle progenitor cells. Circ Res 2005; 96: 784-791.
15. Cailhier JF, Laplante P, Hebert MJ,. Endothelial apoptosis and chronic transplant vasculopathy: recent results, novel mechanisms. Am J Transplant 2006; 6: 247-253.
16. Legare JF, Issekutz T, Lee TD, Hirsch G,. CD8+ T lymphocytes mediate destruction of the vascular media in a model of chronic rejection. Am J Pathol 2000; 157: 859-865.
17. Currie M, Zaki AM, Nejat S, Hirsch GM, Lee TD,. Immunologic targets in the etiology of allograft vasculopathy: endothelium versus media. Transpl Immunol 2008; 19: 120-126.
18. Nejat S, Zaki A, Hirsch GM, Lee TD,. CD8(+) T cells mediate aortic allograft vasculopathy under conditions of calcineurin immunosuppression: role of IFN-gamma and CTL mediators. Transpl Immunol 2008; 19: 103-111.
19. Tellides G, Tereb DA, Kirkiles-Smith NC, et al,. Interferon-gamma elicits arteriosclerosis in the absence of leukocytes. Nature 2000; 403: 207-211.
20. Bigaud M, Schraa EO, Andriambeloson E, et al,. Complete loss of functional smooth muscle cells precedes vascular remodeling in rat aorta allografts. Transplantation 1999; 68: 1701-1707.
21. Matsumoto Y, Hof A, Baumlin Y, Muller M, Prescott MF, Hof RP,. Dynamics of medial smooth muscle changes after carotid artery transplantation in transgenic mice expressing green fluorescent protein. Transplantation 2003; 76: 1569-1572.
22. Andriambeloson E, Pally C, Hengerer B, et al,. Transplantation-induced endothelial dysfunction as studied in rat aorta allografts. Transplantation 2001; 72: 1881-1889.
23. Solway J, Seltzer J, Samaha FF, et al,. Structure and expression of a smooth muscle cell-specific gene, SM22 alpha. J Biol Chem 1995; 270: 13460-13469.
24. Tiscornia G, Singer O, Verma IM,. Production and purification of lentiviral vectors. Nat Protoc 2006; 1: 241-245.
25. Sena-Esteves M, Tebbets JC, Steffens S, Crombleholme T, Flake AW,. Optimized large-scale production of high titer lentivirus vector pseudotypes. J Virol Methods 2004; 122: 131-139.
26. Ji J, Xu F, Li L, Chen R, Wang J, Hu WC,. Activation of adventitial fibroblasts in the early stage of the aortic transplant vasculopathy in rat. Transplantation 2010; 89: 945-953.
27. Mennander A, Tiisala S, Halttunen J, Yilmaz S, Paavonen T, Hayry P,. Chronic rejection in rat aortic allografts. An experimental model for transplant arteriosclerosis. Arterioscler Thromb 1991; 11: 671-680.
28. Langenickel TH, Olive M, Boehm M, San H, Crook MF, Nabel EG,. KIS protects against adverse vascular remodeling by opposing stathmin-mediated VSMC migration in mice. J Clin Invest 2008; 118: 3848-3859.
29. Xu M, Wani M, Dai YS, et al,. Differentiation of bone marrow stromal cells into the cardiac phenotype requires intercellular communication with myocytes. Circulation 2004; 110: 2658-2665.
30. Zhang F, Tsai S, Kato K, et al,. Transforming growth factor-beta promotes recruitment of bone marrow cells and bone marrow-derived mesenchymal stem cells through stimulation of MCP-1 production in vascular smooth muscle cells. J Biol Chem 2009; 284: 17564-17574.
31. Curnock AP, Logan MK, Ward SG,. Chemokine signalling: pivoting around multiple phosphoinositide 3-kinases. Immunology 2002; 105: 125-136.
32. Kukreja P, Abdel-Mageed AB, Mondal D, Liu K, Agrawal KC,. Up-regulation of CXCR4 expression in PC-3 cells by stromal-derived factor-1alpha (CXCL12) increases endothelial adhesion and transendothelial migration: role of MEK/ERK signaling pathway-dependent NF-kappaB activation. Cancer Res 2005; 65: 9891-9898.
33. Hay N, Sonenberg N,. Upstream and downstream of mTOR. Genes Dev 2004; 18: 1926-1945.
34. Liu L, Parent CA,. Review series: TOR kinase complexes and cell migration. J Cell Biol 2011; 194: 815-824.
35. Sata M, Maejima Y, Adachi F, et al,. A mouse model of vascular injury that induces rapid onset of medial cell apoptosis followed by reproducible neointimal hyperplasia. J Mol Cell Cardiol 2000; 32: 2097-2104.
36. Bennett MR, Evan GI, Schwartz SM,. Apoptosis of human vascular smooth muscle cells derived from normal vessels and coronary atherosclerotic plaques. J Clin Invest 1995; 95: 2266-2274.
37. Lopez-Candales A, Holmes DR, Liao S, Scott MJ, Wickline SA, Thompson RW,. Decreased vascular smooth muscle cell density in medial degeneration of human abdominal aortic aneurysms. Am J Pathol 1997; 150: 993-1007.
38. Mayr M, Xu Q,. Smooth muscle cell apoptosis in arteriosclerosis. Experimental Gerontol. 2001; 36: 969-987.
39. Geng YJ,. Molecular signal transduction in vascular cell apoptosis. Cell Res 2001; 11: 253-264.
40. Pollman MJ, Hall JL, Mann MJ, Zhang L, Gibbons GH,. Inhibition of neointimal cell bcl-x expression induces apoptosis and regression of vascular disease. Nat Med 1998; 4: 222-227.
41. Clarke MC, Figg N, Maguire JJ, et al,. Apoptosis of vascular smooth muscle cells induces features of plaque vulnerability in atherosclerosis. Nat Med 2006; 12: 1075-1080.
42. Clarke MC, Littlewood TD, Figg N, et al,. Chronic apoptosis of vascular smooth muscle cells accelerates atherosclerosis and promotes calcification and medial degeneration. Circ Res 2008; 102: 1529-1538.
43. Yu H, Clarke MC, Figg N, Littlewood TD, Bennett MR,. Smooth muscle cell apoptosis promotes vessel remodeling and repair via activation of cell migration, proliferation, and collagen synthesis. Arterioscler Thromb Vasc Biol 2011; 31: 2402-2409.
44. Beohar N, Flaherty JD, Davidson CJ, et al,. Antirestenotic effects of a locally delivered caspase inhibitor in a balloon injury model. Circulation 2004; 109: 108-113.
45. Wang CH, Verma S, Hsieh IC, et al,. Stem cell factor attenuates vascular smooth muscle apoptosis and increases intimal hyperplasia after vascular injury. Arterioscler Thromb Vasc Biol 2007; 27: 540-547.
46. Hegner B, Lange M, Kusch A, et al,. mTOR regulates vascular smooth muscle cell differentiation from human bone marrow-derived mesenchymal progenitors. Arterioscler Thromb Vasc Biol 2009; 29: 232-238.
47. Pittenger MF, Martin BJ,. Mesenchymal stem cells and their potential as cardiac therapeutics. Circ Res 2004; 95: 9-20.
48. Dominici M, Le Blanc K, Mueller I, et al,. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006; 8: 315-317.
49. Clarke MC, Talib S, Figg NL, Bennett MR,. Vascular smooth muscle cell apoptosis induces interleukin-1-directed inflammation: effects of hyperlipidemia-mediated inhibition of phagocytosis. Circ Res 2010; 106: 363-372.
50. Schober A, Knarren S, Lietz M, Lin EA, Weber C,. Crucial role of stromal cell-derived factor-1alpha in neointima formation after vascular injury in apolipoprotein E-deficient mice. Circulation 2003; 108: 2491-2497.
51. Bhakta S, Hong P, Koc O,. The surface adhesion molecule CXCR4 stimulates mesenchymal stem cell migration to stromal cell-derived factor-1 in vitro but does not decrease apoptosis under serum deprivation. Cardiovasc Revasc Med 2006; 7: 19-24.
52. Liu X, Duan B, Cheng Z, et al,. SDF-1/CXCR4 axis modulates bone marrow mesenchymal stem cell apoptosis, migration and cytokine secretion. Protein Cell 2011; 2: 845-854.
53. Vanhaesebroeck B, Guillermet-Guibert J, Graupera M, Bilanges B,. The emerging mechanisms of isoform-specific PI3K signalling. Nat Rev Mol Cell Biol 2010; 11: 329-341.
54. Fingar DC, Richardson CJ, Tee AR, Cheatham L, Tsou C, Blenis J,. mTOR controls cell cycle progression through its cell growth effectors S6K1 and 4E-BP1/eukaryotic translation initiation factor 4E. Mol Cell Biol 2004; 24: 200-216.
55. Murooka TT, Rahbar R, Platanias LC, Fish EN,. CCL5-mediated T-cell chemotaxis involves the initiation of mRNA translation through mTOR/4E-BP1. Blood 2008; 111: 4892-4901.
56. Muslin AJ,. MAPK signalling in cardiovascular health and disease: molecular mechanisms and therapeutic targets. Clin Sci (Lond) 2008; 115: 203-218.
57. Wang JF, Park IW, Groopman JE,. Stromal cell-derived factor-1alpha stimulates tyrosine phosphorylation of multiple focal adhesion proteins and induces migration of hematopoietic progenitor cells: roles of phosphoinositide-3 kinase and protein kinase C. Blood 2000; 95: 2505-2513.
58. Ge W, Jiang J, Baroja ML, et al,. Infusion of mesenchymal stem cells and rapamycin synergize to attenuate alloimmune responses and promote cardiac allograft tolerance. Am J Transplant 2009; 9: 1760-1772.
59. Roemeling-van Rhijn M, Weimar W, Hoogduijn MJ,. Mesenchymal stem cells: application for solid-organ transplantation. Curr Opin Organ Transplant 2012; 17: 55-62.
60. Uccelli A, Moretta L, Pistoia V,. Mesenchymal stem cells in health and disease. Nat Rev Immunol 2008; 8: 726-736.