Thrombospondin-1/CD36 pathway contributes to bone marrow-derived angiogenic cell dysfunction in type 1 diabetes via sonic hedgehog pathway suppression

American Journal of Physiology - Endocrinology and Metabolism

Volumn 305, Issue 12, 2013, Pages

  Wang, Jie Mei ^a,b,c   Isenberg, Jeffery S ^a   Billiar, Timothy R ^a   Chen, Alex F ^a,b,c  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c CENTRAL SOUTH UNIVERSITY   (China)

Author keywords

Bone marrow derived angiogenic cells; Sonic hedgehog; Thrombospondin 1; Type 1 diabetes

Indexed keywords

MATRIGEL; SONIC HEDGEHOG PROTEIN; THROMBOSPONDIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL ADHESION; CELL MIGRATION; CONTROLLED STUDY; DIABETIC PATIENT; INSULIN DEPENDENT DIABETES MELLITUS; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; WOUND; WOUND HEALING;

EID: 84890384778     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00516.2013     Document Type: Article

References (48)

1. Agouni A, Mostefai HA, Porro C, Carusio N, Favre J, Richard V, Henrion D, Martinez MC, Andriantsitohaina R. Sonic hedgehog carried by microparticles corrects endothelial injury through nitric oxide release. FASEB J 21: 2735-2741, 2007
2. Asai J, Takenaka H, Kusano KF, Ii M, Luedemann C, Curry C, Eaton E, Iwakura A, Tsutsumi Y, Hamada H, Kishimoto S, Thorne T, Kishore R, Losordo DW. Topical sonic hedgehog gene therapy accelerates wound healing in diabetes by enhancing endothelial progenitor cell-mediated microvascular remodeling. Circulation 113: 2413-2424, 2006
3. Barcelos LS, Duplaa C, Krankel N, Graiani G, Invernici G, Katare R, Siragusa M, Meloni M, Campesi I, Monica M, Simm A, Campagnolo P, Mangialardi G, Stevanato L, Alessandri G, Emanueli C, Madeddu P. Human CD133+ progenitor cells promote the healing of diabetic ischemic ulcers by paracrine stimulation of angiogenesis and activation of Wnt signaling. Circ Res 104: 1095-1102, 2009
4. Bayraktar M, Dundar S, Kirazli S, Teletar F. Platelet factor 4, betathromboglobulin and thrombospondin levels in type I diabetes mellitus patients. J Int Med Res 22: 90-94, 1994
5. Bhattacharyya S, Marinic TE, Krukovets I, Hoppe G, Stenina OI. Cell type-specific post-transcriptional regulation of production of the potent antiangiogenic and proatherogenic protein thrombospondin-1 by high glucose. J Biol Chem 283: 5699-5707, 2008
6. Bujold K, Rhainds D, Jossart C, Febbraio M, Marleau S, Ong H. CD36-mediated cholesterol efflux is associated with PPARgamma activation via a MAPK-dependent COX-2 pathway in macrophages. Cardiovasc Res 83: 457-464, 2009
7. Chinchilla P, Xiao L, Kazanietz MG, Riobo NA. Hedgehog proteins activate pro-angiogenic responses in endothelial cells through non-canonical signaling pathways. Cell Cycle 9: 570-579, 2010
8. Csanyi G, Yao M, Rodriguez AI, Al Ghouleh I, Sharifi-Sanjani M, Frazziano G, Huang X, Kelley EE, Isenberg JS, Pagano PJ. Thrombospondin- 1 regulates blood flow via CD47 receptor-mediated activation of NADPH oxidase 1. Arterioscler Thromb Vasc Biol 32: 2966-2973, 2012
9. Dawson DW, Pearce SF, Zhong R, Silverstein RL, Frazier WA, Bouck NP. CD36 mediates the In vitro inhibitory effects of thrombospondin-1 on endothelial cells. J Cell Biol 138: 707-717, 1997
10. Du YH, Guan YY, Alp NJ, Channon KM, Chen AF. Endotheliumspecific GTP cyclohydrolase I overexpression attenuates blood pressure progression in salt-sensitive low-renin hypertension. Circulation 117: 1045-1054, 2008
11. Febbraio M, Abumrad NA, Hajjar DP, Sharma K, Cheng W, Pearce SF, Silverstein RL. A null mutation in murine CD36 reveals an important role in fatty acid and lipoprotein metabolism. J Biol Chem 274: 19055-19062, 1999
12. Gonzalez-Quesada C, Cavalera M, Biernacka A, Kong P, Lee DW, Saxena A, Frunza O, Dobaczewski M, Shinde AV, Frangogiannis NG. Thrombospondin-1 Induction in the Diabetic Myocardium Stabilizes the Cardiac Matrix, While Promoting Vascular Rarefaction Through Angiopoietin- 2 Upregulation. Circ Res. In press.
13. Hamada H, Kim MK, Iwakura A, Ii M, Thorne T, Qin G, Asai J, Tsutsumi Y, Sekiguchi H, Silver M, Wecker A, Bord E, Zhu Y, Kishore R, Losordo DW. Estrogen receptors alpha and beta mediate contribution of bone marrow-derived endothelial progenitor cells to functional recovery after myocardial infarction. Circulation 114: 2261-2270, 2006
14. Huh HY, Pearce SF, Yesner LM, Schindler JL, Silverstein RL. Regulated expression of CD36 during monocyte-to-macrophage differentiation: potential role of CD36 in foam cell formation. Blood 87: 2020-2028, 1996
15. Ii M, Takenaka H, Asai J, Ibusuki K, Mizukami Y, Maruyama K, Yoon YS, Wecker A, Luedemann C, Eaton E, Silver M, Thorne T, Losordo DW. Endothelial progenitor thrombospondin-1 mediates diabetes- induced delay in reendothelialization following arterial injury. Circ Res 98: 697-704, 2006
16. Isenberg JS, Martin-Manso G, Maxhimer JB, Roberts DD. Regulation of nitric oxide signalling by thrombospondin 1: implications for antiangiogenic therapies. Nat Rev Cancer 9: 182-194, 2009
17. Isenberg JS, Maxhimer JB, Hyodo F, Pendrak ML, Ridnour LA, DeGraff WG, Tsokos M, Wink DA, Roberts DD. Thrombospondin-1 and CD47 limit cell and tissue survival of radiation injury. Am J Pathol 173: 1100-1112, 2008
18. Isenberg JS, Ridnour LA, Perruccio EM, Espey MG, Wink DA, Roberts DD. Thrombospondin-1 inhibits endothelial cell responses to nitric oxide in a cGMP-dependent manner. Proc Natl Acad Sci USA 102: 13141-13146, 2005
19. Isenberg JS, Romeo MJ, Maxhimer JB, Smedley J, Frazier WA, Roberts DD. Gene silencing of CD47 and antibody ligation of thrombospondin- 1 enhance ischemic tissue survival in a porcine model: implications for human disease. Ann Surg 247: 860-868, 2008
20. Isenberg JS, Shiva S, Gladwin M. Thrombospondin-1-CD47 blockade and exogenous nitrite enhance ischemic tissue survival, blood flow and angiogenesis via coupled NO-cGMP pathway activation. Nitric Oxide 21: 52-62, 2009
21. Jeffcoate WJ, Harding KG. Diabetic foot ulcers. Lancet 361: 1545-1551, 2003
22. Jimenez B, Volpert OV, Crawford SE, Febbraio M, Silverstein RL, Bouck N. Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat Med 6: 41-48, 2000
23. Kazerounian S, Duquette M, Reyes MA, Lawler JT, Song K, Perruzzi C, Primo L, Khosravi-Far R, Bussolino F, Rabinovitz I, Lawler J. Priming of the vascular endothelial growth factor signaling pathway by thrombospondin-1, CD36, and spleen tyrosine kinase. Blood 117: 4658-4666, 2009
24. Kazerounian S, Yee KO, Lawler J. Thrombospondins in cancer. Cell Mol Life Sci 65: 700-712, 2008
25. Kusano KF, Pola R, Murayama T, Curry C, Kawamoto A, Iwakura A, Shintani S, Ii M, Asai J, Tkebuchava T, Thorne T, Takenaka H, Aikawa R, Goukassian D, von Samson P, Hamada H, Yoon YS, Silver M, Eaton E, Ma H, Heyd L, Kearney M, Munger W, Porter JA, Kishore R, Losordo DW. Sonic hedgehog myocardial gene therapy: tissue repair through transient reconstitution of embryonic signaling. Nat Med 11: 1197-1204, 2005
26. Lawler J. Thrombospondin-1 as an endogenous inhibitor of angiogenesis and tumor growth. J Cell Mol Med 6: 1-12, 2002
27. Loomans CJ, de Koning EJ, Staal FJ, Rookmaaker MB, Verseyden C, de Boer HC, Verhaar MC, Braam B, Rabelink TJ, van Zonneveld AJ. Endothelial progenitor cell dysfunction: a novel concept in the pathogenesis of vascular complications of type 1 diabetes. Diabetes 53: 195-199, 2004
28. Luo JD, Hu TP, Wang L, Chen MS, Liu SM, Chen AF. Sonic hedgehog improves delayed wound healing via enhancing cutaneous nitric oxide function in diabetes. Am J Physiol Endocrinol Metab 297: E525-E531, 2009
29. Luo JD, Wang YY, Fu WL, Wu J, Chen AF. Gene therapy of endothelial nitric oxide synthase and manganese superoxide dismutase restores delayed wound healing in type 1 diabetic mice. Circulation 110: 2484-2493, 2004
30. Marrotte EJ, Chen DD, Hakim JS, Chen AF. Manganese superoxide dismutase expression in endothelial progenitor cells accelerates wound healing in diabetic mice. J Clin Invest 120: 4207-4219, 2010
31. McMahon AP, Ingham PW, Tabin CJ. Developmental roles and clinical significance of hedgehog signaling. Curr Top Dev Biol 53: 1-114, 2003
32. Oquendo P, Hundt E, Lawler J, Seed B. CD36 directly mediates cytoadherence of Plasmodium falciparum parasitized erythrocytes. Cell 58: 95-101, 1989
33. Primo L, Ferrandi C, Roca C, Marchio S, di Blasio L, Alessio M, Bussolino F. Identification of CD36 molecular features required for its in vitro angiostatic activity. FASEB J 19: 1713-1715, 2005
34. Reddy S, Andl T, Bagasra A, Lu MM, Epstein DJ, Morrisey EE, Millar SE. Characterization of Wnt gene expression in developing and postnatal hair follicles and identification of Wnt5a as a target of Sonic hedgehog in hair follicle morphogenesis. Mech Dev 107: 69-82, 2001
35. Renault MA, Roncalli J, Tongers J, Thorne T, Klyachko E, Misener S, Volpert OV, Mehta S, Burg A, Luedemann C, Qin G, Kishore R, Losordo DW. Sonic hedgehog induces angiogenesis via Rho kinasedependent signaling in endothelial cells. J Mol Cell Cardiol 49: 490-498, 2010
36. Roberts DD, Miller TW, Rogers NM, Yao M, Isenberg JS. The matricellular protein thrombospondin-1 globally regulates cardiovascular function and responses to stress via CD47. Matrix Biol 31: 162-169, 2012
37. Sato N, Leopold PL, Crystal RG. Induction of the hair growth phase in postnatal mice by localized transient expression of Sonic hedgehog. J Clin Invest 104: 855-864, 1999
38. Schroder K, Kohnen A, Aicher A, Liehn EA, Buchse T, Stein S, Weber C, Dimmeler S, Brandes RP. NADPH oxidase Nox2 is required for hypoxia-induced mobilization of endothelial progenitor cells. Circ Res 105: 537-544, 2009
39. Sheridan C. Genentech obtains proof of concept for hedgehog inhibition. Nat Biotechnol 27: 968-969, 2009
40. Silverstein RL, Febbraio M. CD36, a scavenger receptor involved in immunity, metabolism, angiogenesis, and behavior. Sci Signal 2: re3, 2009
41. Stenina OI, Krukovets I, Wang K, Zhou Z, Forudi F, Penn MS, Topol EJ, Plow EF. Increased expression of thrombospondin-1 in vessel wall of diabetic Zucker rat. Circulation 107: 3209-3215, 2003
42. Tepper OM, Galiano RD, Capla JM, Kalka C, Gagne PJ, Jacobowitz GR, Levine JP, Gurtner GC. Human endothelial progenitor cells from type II diabetics exhibit impaired proliferation, adhesion, and incorporation into vascular structures. Circulation 106: 2781-2786, 2002
43. Tie L, Li XJ, Wang X, Channon KM, Chen AF. Endothelium-specific GTP cyclohydrolase I overexpression accelerates refractory wound healing by suppressing oxidative stress in diabetes. Am J Physiol Endocrinol Metab 296: E1423-E1429, 2009
44. Wang XR, Zhang MW, Chen DD, Zhang Y, Chen AF. AMP-activated protein kinase rescues the angiogenic functions of endothelial progenitor cells via manganese superoxide dismutase induction in type 1 diabetes. Am J Physiol Endocrinol Metab 300: E1135-E1145, 2011
45. Xia YP, Dai RL, Li YN, Mao L, Xue YM, He QW, Huang M, Huang Y, Mei YW, Hu B. The protective effect of sonic hedgehog is mediated by the phosphoinositide [corrected] 3-kinase/AKT/Bcl-2 pathway in cultured rat astrocytes under oxidative stress. Neuroscience 209: 1-11, 2012
46. Xu MG, Wang JM, Chen L, Wang Y, Yang Z, Tao J. Berberineinduced upregulation of circulating endothelial progenitor cells is related to nitric oxide production in healthy subjects. Cardiology 112: 279-286, 2009
47. Yoo YA, Kang MH, Lee HJ, Kim BH, Park JK, Kim HK, Kim JS, Oh SC. Sonic hedgehog pathway promotes metastasis and lymphangiogenesis via activation of Akt, EMT, and MMP-9 pathway in gastric cancer. Cancer Res 71: 7061-7070, 2011
48. Zhao T, Li J, Chen AF. MicroRNA-34a induces endothelial progenitor cell senescence and impedes its angiogenesis via suppressing silent information regulator 1. Am J Physiol Endocrinol Metab 299: E110-E116, 2010.