Activated CD47 regulates multiple vascular and stress responses: Implications for acute kidney injury and its management

American Journal of Physiology - Renal Physiology

Volumn 303, Issue 8, 2012, Pages

  Rogers, Natasha M ^a,b   Yao, Mingyi ^a   Novelli, Enrico M ^a   Thomson, Angus W ^b   Roberts, David D ^c   Isenberg, Jeffrey S ^a  

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

^b UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

CD47; Ischemia reperfusion injury; Kidney injury; Nitric oxide; Reactive oxygen species; Thrombospondin 1; Transplant

Indexed keywords

CD47 ANTIGEN; CYCLIC AMP; CYCLIC GMP; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GUANYLATE CYCLASE; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY CD47; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; THROMBOSPONDIN 1; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ACUTE GLOMERULONEPHRITIS; ACUTE KIDNEY FAILURE; APOPTOSIS; ARTICLE; CELL DAMAGE; CELL HYPOXIA; CELL SURFACE; CELL SURVIVAL; DIABETIC NEPHROPATHY; HUMAN; KIDNEY FIBROSIS; KIDNEY INJURY; KIDNEY TUBULE EPITHELIUM; LIGAND BINDING; MEMBRANOPROLIFERATIVE GLOMERULONEPHRITIS; MESANGIUM CELL; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RENAL PROTECTION; REPERFUSION INJURY;

EID: 84867704506     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00359.2012     Document Type: Article

References (105)

1. Abbott KC, Hypolite IO, Agodoa LY. Sickle cell nephropathy at end-stage renal disease in the United States: patient characteristics and survival. Clin Nephrol 58: 9-15, 2002.
2. Agah A, Kyriakides TR, Lawler J, Bornstein P. The lack of throm-bospondin-1 (TSP1) dictates the course of wound healing in double-TSP1/TSP2-null mice. Am J Pathol 161: 831-839, 2002.
3. Arora S, Vaishya R, Dabla PK, Singh B. NAD(P)H oxidases in coronary artery disease. Adv Clin Chem 50: 65-86, 2010.
4. Barclay AN. Signal regulatory protein alpha (SIRPalpha)/CD47 interaction and function. Curr Opin Immunol 21: 47-52, 2009.
5. Bauer EM, Qin Y, Miller TW, Bandle RW, Csanyi G, Pagano PJ, Bauer PM, Schnermann J, Roberts DD, Isenberg JS. Thrombospon-din-1 supports blood pressure by limiting eNOS activation and endothe-lial-dependent vasorelaxation. Cardiovasc Res 88: 471-481, 2010.
6. Bauer PM, Bauer EM, Rogers NM, Yao M, Feijoo-Cuaresma M, Pilewski JM, Champion HC, Zuckerbraun BS, Calzada MJ, Isen-berg JS. Activated CD47 promotes pulmonary arterial hypertension through targeting caveolin-1. Cardiovasc Res 93: 682-693.
7. Bijuklic K, Sturn DH, Jennings P, Kountchev J, Pfaller W, Wieder-mann CJ, Patsch JR, Joannidis M. Mechanisms of neutrophil transmigration across renal proximal tubular HK-2 cells. Cell Physiol Biochem 17: 233-244, 2006.
8. Bohmova R, Viklicky O. Renal ischemia-reperfusion injury: an inescapable event affecting kidney transplantation outcome. Folia Microbiol (Praha) 46: 267-276, 2001.
9. Brown EJ, Frazier WA. Integrin-associated protein (CD47) and its ligands. Trends Cell Biol 11: 130-135, 2001.
10. Brown GC. Nitric oxide and mitochondria. Front Biosci 12: 1024-1033, 2007.
11. Campbell IG, Freemont PS, Foulkes W, Trowsdale J. An ovarian tumor marker with homology to vaccinia virus contains an IgV-like region and multiple transmembrane domains. Cancer Res 52: 5416- 5420, 1992.
12. Carlucci A, Lignitto L, Feliciello A. Control of mitochondria dynamics and oxidative metabolism by cAMP, AKAPs and the proteasome. Trends Cell Biol 18: 604-613, 2008.
13. Chandrasekaran S, Guo NH, Rodrigues RG, Kaiser J, Roberts DD. Pro-adhesive and chemotactic activities of thrombospondin-1 for breast carcinoma cells are mediated by alpha3beta1 integrin and regulated by insulin-like growth factor-1 and CD98. J Biol Chem 274: 11408-11416, 1999.
14. Chen H, Herndon ME, Lawler J. The cell biology of thrombospon-din-1. Matrix Biol 19: 597-614, 2000.
15. Chen H, Sottile J, Strickland DK, Mosher DF. Binding and degradation of thrombospondin-1 mediated through heparan sulphate proteogly-cans and low-density-lipoprotein receptor-related protein: localization of the functional activity to the trimeric N-terminal heparin-binding region of thrombospondin-1. Biochem J 318: 959-963, 1996.
16. Corless CL, Mendoza A, Collins T, Lawler J. Colocalization of thrombospondin and syndecan during murine development. Dev Dyn 193: 346-358, 1992.
17. Coultas L, Chawengsaksophak K, Rossant J. Endothelial cells and VEGF in vascular development. Nature 438: 937-945, 2005.
18. Cuzzocrea S, Riley DP, Caputi AP, Salvemini D. Antioxidant therapy: a new pharmacological approach in shock, inflammation, and ischemia/ reperfusion injury. Pharmacol Rev 53: 135-159, 2001.
19. Daniel C, Wiede J, Krutzsch HC, Ribeiro SM, Roberts DD, Murphy-Ullrich JE, Hugo C. Thrombospondin-1 is a major activator of TGF-beta in fibrotic renal disease in the rat in vivo. Kidney Int 65: 459-468, 2004.
20. Dawson DW, Pearce SF, Zhong R, Silverstein RL, Frazier WA, Bouck NP. CD36 mediates the In vitro inhibitory effects of thrombos-pondin-1 on endothelial cells. J Cell Biol 138: 707-717, 1997.
21. Denner L. Stroke and ischemia-reperfusion injury. IDrugs 4: 20-22, 2001.
22. Du C, Wang S, Diao H, Guan Q, Zhong R, Jevnikar AM. Increasing resistance of tubular epithelial cells to apoptosis by shRNA therapy ameliorates renal ischemia-reperfusion injury. Am J Transplant 6: 2256-2267, 2006.
23. Dubernard V, Arbeille BB, Lemesle MB, Legrand C. Evidence for an alpha-granular pool of the cytoskeletal protein alpha-actinin in human platelets that redistributes with the adhesive glycoprotein thrombospon-din-1 during the exocytotic process. Arterioscler Thromb Vasc Biol 17: 2293-2305, 1997.
24. Faubel S, Edelstein CL. Caspases as drug targets in ischemic organ injury. Curr Drug Targets Immune Endocr Metabol Disord 5: 269-287, 2005.
25. Felley-Bosco E, Bender F, Quest AF. Caveolin-1-mediated post-tran-scriptional regulation of inducible nitric oxide synthase in human colon carcinoma cells. Biol Res 35: 169-176, 2002.
26. Frazier EP, Isenberg JS, Shiva S, Zhao L, Schlesinger P, Dimitry J, Abu-Asab MS, Tsokos M, Roberts DD, Frazier WA. Age-dependent regulation of skeletal muscle mitochondria by the thrombospondin-1 receptor CD47. Matrix Biol 30: 154-161, 2011.
27. Fryckstedt J, Meister B, Aperia A. Control of electrolyte transport in the kidney through a dopamine- and cAMP-regulated phosphoprotein, DARPP-32. J Auton Pharmacol 12: 183-189, 1992.
28. Grigoryev DN, Liu M, Cheadle C, Barnes KC, Rabb H. Genomic profiling of kidney ischemia-reperfusion reveals expression of specific alloimmunity-associated genes: linking "immune" and "nonimmune" injury events. Transplant Proc 38: 3333-3336, 2006.
29. Grinyo JM. Role of ischemia-reperfusion injury in the development of chronic renal allograft damage. Transplant Proc 33: 3741-3742, 2001.
30. Guo YL, Liu DQ, Bian Z, Zhang CY, Zen K. Down-regulation of platelet surface CD47 expression in Escherichia coli O157:H7 infection-induced thrombocytopenia. PLoS One 4: e7131, 2009.
31. Hafdi Z, Lesavre P, Nejjari M, Halbwachs-Mecarelli L, Droz D, Noel LH. Distribution of alphavbeta3, alphavbeta5 integrins and the integrin associated protein-IAP (CD47) in human glomerular diseases. Cell Adhes Commun 7: 441-451, 2000.
32. Hohenstein B, Daniel C, Hausknecht B, Boehmer K, Riess R, Amann KU, Hugo CP. Correlation of enhanced thrombospondin-1 expression, TGF-beta signalling and proteinuria in human type-2 diabetic nephrop-athy. Nephrol Dial Transplant 23: 3880-3887, 2008.
33. Hohenstein B, Daniel C, Wittmann S, Hugo C. PDE-5 inhibition impedes TSP-1 expression, TGF-beta activation and matrix accumulation in experimental glomerulonephritis. Nephrol Dial Transplant 23: 3427-3436, 2008.
34. Hotchkiss H, Chu TT, Hancock WW, Schroppel B, Kretzler M, Schmid H, Liu Y, Dikman S, Akalin E. Differential expression of profibrotic and growth factors in chronic allograft nephropathy. Transplantation 81: 342-349, 2006.
35. Hugo C. The thrombospondin 1-TGF-beta axis in fibrotic renal disease. Nephrol Dial Transplant 18: 1241-1245, 2003.
36. Hugo CP, Pichler RP, Schulze-Lohoff E, Prols F, Adler S, Krutsch HC, Murphy-Ullrich JE, Couser WG, Roberts DD, Johnson RJ. Thrombospondin peptides are potent inhibitors of mesangial and glomer-ular endothelial cell proliferation in vitro and in vivo. Kidney Int 55: 2236-2249, 1999.
37. Ignarro LJ. Nitric oxide as a unique signaling molecule in the vascular system: a historical overview. J Physiol Pharmacol 53: 503-514, 2002.
38. Ignarro LJ, Wood KS, Wolin MS. Activation of purified soluble guanylate cyclase by protoporphyrin IX. Proc Natl Acad Sci USA 79: 2870-2873, 1982.
39. Iruela-Arispe ML, Liska DJ, Sage EH, Bornstein P. Differential expression of thrombospondin 1, 2, and 3 during murine development. Dev Dyn 197: 40-56, 1993.
40. Isenberg JS, Annis DS, Pendrak ML, Ptaszynska M, Frazier WA, Mosher DF, Roberts DD. Differential interactions of thrombospon-din-1, -2, and -4 with CD47 and effects on cGMP signaling and ischemic injury responses. J Biol Chem 284: 1116-1125, 2009.
41. Isenberg JS, Frazier WA, Roberts DD. Thrombospondin-1: a physiological regulator of nitric oxide signaling. Cell Mol Life Sci 65: 728-742, 2008.
42. Isenberg JS, Hyodo F, Matsumoto K, Romeo MJ, Abu-Asab M, Tsokos M, Kuppusamy P, Wink DA, Krishna MC, Roberts DD. Thrombospondin-1 limits ischemic tissue survival by inhibiting nitric oxide-mediated vascular smooth muscle relaxation. Blood 109: 1945-1952, 2007.
43. Isenberg JS, Martin-Manso G, Maxhimer JB, Roberts DD. Regulation of nitric oxide signalling by thrombospondin 1: implications for anti-angiogenic therapies. Nat Rev Cancer 9: 182-194, 2009.
44. 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.
45. Isenberg JS, Maxhimer JB, Powers P, Tsokos M, Frazier WA, Roberts DD. Treatment of liver ischemia-reperfusion injury by limiting thrombospondin-1/CD47 signaling. Surgery 144: 752-761, 2008.
46. Isenberg JS, Qin Y, Maxhimer JB, Sipes JM, Despres D, Schner-mann J, Frazier WA, Roberts DD. Thrombospondin-1 and CD47 regulate blood pressure and cardiac responses to vasoactive stress. Matrix Biol 28: 110-119, 2009.
47. Isenberg JS, Ridnour LA, Dimitry J, Frazier WA, Wink DA, Roberts DD. CD47 is necessary for inhibition of nitric oxide-stimulated vascular cell responses by thrombospondin-1. J Biol Chem 281: 26069-26080, 2006.
48. 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.
49. Isenberg JS, Roberts DD, Frazier WA. CD47: a new target in cardiovascular therapy. Arterioscler Thromb Vasc Biol 28: 615-621, 2008.
50. Isenberg JS, Romeo MJ, Abu-Asab M, Tsokos M, Oldenborg A, Pappan L, Wink DA, Frazier WA, Roberts DD. Increasing survival of ischemic tissue by targeting CD47. Circ Res 100: 712-720, 2007.
51. Isenberg JS, Romeo MJ, Yu C, Yu CK, Nghiem K, Monsale J, Rick ME, Wink DA, Frazier WA, Roberts DD. Thrombospondin-1 stimulates platelet aggregation by blocking the antithrombotic activity of nitric oxide/cGMP signaling. Blood 111: 613-623, 2008.
52. Iwazu Y, Muto S, Fujisawa G, Nakazawa E, Okada K, Ishibashi S, Kusano E. Spironolactone suppresses peritubular capillary loss and prevents deoxycorticosterone acetate/salt-induced tubulointerstitial fibro-sis. Hypertension 51: 749-754, 2008.
53. Jin G, Tsuji K, Xing C, Yang YG, Wang X, Lo EH. CD47 gene knockout protects against transient focal cerebral ischemia in mice. Exp Neurol 217: 165-170, 2009.
54. Kaur S, Martin-Manso G, Pendrak ML, Garfield SH, Isenberg JS, Roberts DD. Thrombospondin-1 inhibits VEGF receptor-2 signaling by disrupting its association with CD47. J Biol Chem 285: 38923-38932, 2010.
55. Klement GL, Yip TT, Cassiola F, Kikuchi L, Cervi D, Podust V, Italiano JE, Wheatley E, Abou-Slaybi A, Bender E, Almog N, Kieran MW, Folkman J. Platelets actively sequester angiogenesis regulators. Blood 113: 2835-2842, 2009.
56. Kobayashi S, Yamamoto T. The molecular biologic study of the expression of thrombospondin in vascular smooth muscle cells and mesangial cells. J Diabet Complications 5: 121-123, 1991.
57. Kosugi T, Heinig M, Nakayama T, Connor T, Yuzawa Y, Li Q, Hauswirth WW, Grant MB, Croker BP, Campbell-Thompson M, Zhang L, Atkinson MA, Segal MS, Nakagawa T. Lowering blood pressure blocks mesangiolysis and mesangial nodules, but not tubuloin-terstitial injury, in diabetic eNOS knockout mice. Am J Pathol 174: 1221-1229, 2009.
58. Krol R, Chudek J, Karkoszka H, Ziaja J, Kolonko A, Pawlicki J, Kajor M, Wiecek A, Cierpka L. Apoptosis of tubular epithelial cells in preimplantation biopsies of kidney grafts with immediate, slow and delayed function. Ann Transplant 16: 17-22.
59. Kroncke KD, Suschek CV, Kolb-Bachofen V. Implications of inducible nitric oxide synthase expression and enzyme activity. Antioxid Redox Signal 2: 585-605, 2000.
60. Kurihara H, Harita Y, Ichimura K, Hattori S, Sakai T. SIRP-a-CD47 system functions as an intercellular signal in the renal glomerulus. Am J Physiol Renal Physiol 299: F517-F527, 2010.
61. Lario S, Bescos M, Campos B, Mur C, Luque P, Alvarez R, Camp-istol JM. Thrombospondin-1 mRNA expression in experimental kidney transplantation with heart-beating and non-heart-beating donors. J Nephrol 20: 588-595, 2007.
62. Lu A, Miao M, Schoeb TR, Agarwal A, Murphy-Ullrich JE. Blockade of TSP1-dependent TGF-β activity reduces renal injury and proteinuria in a murine model of diabetic nephropathy. Am J Pathol 178: 2573-2586, 2011.
63. Lu X, Guo X, Wassall CD, Kemple MD, Unthank JL, Kassab GS. Reactive oxygen species cause endothelial dysfunction in chronic flow overload. J Appl Physiol 110: 520-527, 2011.
64. Manna PP, Dimitry J, Oldenborg PA, Frazier WA. CD47 augments Fas/CD95-mediated apoptosis. J Biol Chem 280: 29637-29644, 2005.
65. Manna PP, Frazier WA. CD47 mediates killing of breast tumor cells via Gi-dependent inhibition of protein kinase A. Cancer Res 64: 1026-1036, 2004.
66. Mateo V, Brown EJ, Biron G, Rubio M, Fischer A, Deist FL, Sarfati M. Mechanisms of CD47-induced caspase-independent cell death in normal and leukemic cells: link between phosphatidylserine exposure and cytoskeleton organization. Blood 100: 2882-2890, 2002.
67. Maxhimer JB, Shih HB, Isenberg JS, Miller TW, Roberts DD. Thrombospondin-1/CD47 blockade following ischemia-reperfusion injury is tissue protective. Plast Reconstr Surg 124: 1880-1889, 2009.
68. Maxhimer JB, Soto-Pantoja DR, Ridnour LA, Shih HB, Degraff WG, Tsokos M, Wink DA, Isenberg JS, Roberts DD. Radioprotection in normal tissue and delayed tumor growth by blockade of CD47 signaling. Sci Transl Med 1: 3ra7, 2009.
69. Mayhan WG, Arrick DM, Sharpe GM, Patel KP, Sun H. Inhibition of NAD(P)H oxidase alleviates impaired NOS-dependent responses of pial arterioles in type 1 diabetes mellitus. Microcirculation 13: 567-575, 2006.
70. McDonald LJ, Murad F. Nitric oxide and cGMP signaling. Adv Pharmacol 34: 263-275, 1995.
71. Miller TW, Isenberg JS, Roberts DD. Thrombospondin-1 is an inhibitor of pharmacological activation of soluble guanylate cyclase. Br J Pharmacol 159: 1542-1547, 2010.
72. Miller YE, Daniels GL, Jones C, Palmer DK. Identification of a cell-surface antigen produced by a gene on human chromosome 3 (cen-q22) and not expressed by Rhnull cells. Am J Hum Genet 41: 1061-1070, 1987.
73. Murphy-Ullrich JE, Poczatek M. Activation of latent TGF-beta by thrombospondin-1: mechanisms and physiology. Cytokine Growth Factor Rev 11: 59-69, 2000.
74. Narizhneva NV, Razorenova OV, Podrez EA, Chen J, Chan-drasekharan UM, DiCorleto PE, Plow EF, Topol EJ, Byzova TV. Thrombospondin-1 up-regulates expression of cell adhesion molecules and promotes monocyte binding to endothelium. FASEB J 19: 1158-1160, 2005.
75. Nishiyama Y, Tanaka T, Naitoh H, Mori C, Fukumoto M, Hiai H, Toyokuni S. Overexpression of integrin-associated protein (CD47) in rat kidney treated with a renal carcinogen, ferric nitrilotriacetate. Jpn J Cancer Res 88: 120-128, 1997.
76. Novelli EM, Kato GJ, Ragni MV, Zhang Y, Hildesheim ME, Nouraie M, Barge S, Meyer MP, Hassett AC, Gordeuk VR, Gladwin MT, Isenberg JS. Plasma thrombospondin-1 is increased during acute sickle cell vaso-occlusive events and associated with acute chest syndrome, hydroxyurea therapy, and lower hemolytic rates. Am J Hematol 87: 326-330, 2012.
77. Osada-Oka M, Ikeda T, Akiba S, Sato T. Hypoxia stimulates the autocrine regulation of migration of vascular smooth muscle cells via HIF-1alpha-dependent expression of thrombospondin-1. J Cell Biochem 104: 1918-1926, 2008.
78. Ostman A, Frijhoff J, Sandin A, Bohmer FD. Regulation of protein tyrosine phosphatases by reversible oxidation. J Biochem 150: 345-356, 2011.
79. Pallero MA, Elzie CA, Chen J, Mosher DF, Murphy-Ullrich JE. Thrombospondin 1 binding to calreticulin-LRP1 signals resistance to anoikis. FASEB J 22: 3968-3979, 2008.
80. Pascher A, Klupp J. Biologics in the treatment of transplant rejection and ischemia/reperfusion injury: new applications for TNFalpha inhibitors? BioDrugs 19: 211-231, 2005.
81. Payne JA, Reckelhoff JF, Khalil RA. Role of oxidative stress in age-related reduction of NO-cGMP-mediated vascular relaxation in SHR. Am J Physiol Regul Integr Comp Physiol 285: R542-R551, 2003.
82. Ramanathan S, Mazzalupo S, Boitano S, Montfort WR. Thrombos-pondin-1 and angiotensin II inhibit soluble guanylyl cyclase through an increase in intracellular calcium concentration. Biochemistry 50: 7787-7799, 2011.
83. Ridnour LA, Isenberg JS, Espey MG, Thomas DD, Roberts DD, Wink DA. Nitric oxide regulates angiogenesis through a functional switch involving thrombospondin-1. Proc Natl Acad Sci USA 102: 13147-13152, 2005.
84. Roberts DD. Regulation of tumor growth and metastasis by thrombos-pondin-1. FASEB J 10: 1183-1191, 1996.
85. 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.
86. Rogers NM, Thomson AW, Isenberg JS. Acitvated parenchymal CD47 is a proximate promoter of renal ischemia reperfusion injury. J Am Soc Nephrol [Epub before print].
87. Ryter SW, Kim HP, Hoetzel A, Park JW, Nakahira K, Wang X, Choi AM. Mechanisms of cell death in oxidative stress. Antioxid Redox Signal 9: 49-89, 2007.
88. Saumet A, Slimane MB, Lanotte M, Lawler J, Dubernard V. Type 3 repeat/C-terminal domain of thrombospondin-1 triggers caspase-inde-pendent cell death through CD47/alphavbeta3 in promyelocytic leukemia NB4 cells. Blood 106: 658-667, 2005.
89. Schneeberger H, Aydemir S, Illner WD, Land W. Nonspecific primary ischemia/reperfusion injury in combination with secondary specific acute rejection-mediated injury of human kidney allografts contributes mainly to development of chronic transplant failure. Transplant Proc 29: 948-949, 1997.
90. Shao D, Oka SI, Brady CD, Haendeler J, Eaton P, Sadoshima J. Redox modification of cell signaling in the cardiovascular system. J Mol Cell Cardiol 52: 550-558, 2012.
91. Shvetsov M, Ivanov AA, Kuznetsova AV, Popova OP, Rameeva AS. [Molecular factors of angiogenesis in renal tissue of patients with chronic glomerulonephritis: association with nephrosclerosis and anemia]. Ter Arkh 81: 14-19, 2009.
92. Suzuki K, Wang R, Kubota H, Shibuya H, Saegusa J, Sato T. Kinetics of biglycan, decorin and thrombospondin-1 in mercuric chloride-induced renal tubulointerstitial fibrosis. Exp Mol Pathol 79: 68-73, 2005.
93. Thakar CV, Zahedi K, Revelo MP, Wang Z, Burnham CE, Barone S, Bevans S, Lentsch AB, Rabb H, Soleimani M. Identification of thrombospondin 1 (TSP-1) as a novel mediator of cell injury in kidney ischemia. J Clin Invest 115: 3451-3459, 2005.
94. van Beek EM, Cochrane F, Barclay AN, van den Berg TK. Signal regulatory proteins in the immune system. J Immunol 175: 7781-7787, 2005.
95. Wang X, Yan L, Chen W, Xu L, Zhang X. The renal protective effects of cilostazol on suppressing pathogenic thrombospondin-1 and transforming growth factor-beta expression in streptozotocin-induced diabetic rats. J Int Med Res 37: 145-153, 2009.
96. Wani J, Carl M, Henger A, Nelson PJ, Rupprecht H. Nitric oxide modulates expression of extracellular matrix genes linked to fibrosis in kidney mesangial cells. Biol Chem 388: 497-506, 2007.
97. Xie XS, Li FY, Liu HC, Deng Y, Li Z, Fan JM. LSKL, a peptide antagonist of thrombospondin-1, attenuates renal interstitial fibrosis in rats with unilateral ureteral obstruction. Arch Pharm Res 33: 275-284, 2010.
98. Xing C, Lee S, Kim WJ, Jin G, Yang YG, Ji X, Wang X, Lo EH. Role of oxidative stress and caspase 3 in CD47-mediated neuronal cell death. J Neurochem 108: 430-436, 2009.
99. Yang YL, Chuang LY, Guh JY, Liu SF, Hung MY, Liao TN, Huang YL. Thrombospondin-1 mediates distal tubule hypertrophy induced by glycated albumin. Biochem J 379: 89-97, 2004.
100. Yao M, Roberts DD, Isenberg JS. Thrombospondin-1 inhibition of vascular smooth muscle cell responses occurs via modulation of both cAMP and cGMP. Pharmacol Res 63: 13-22, 2011.
101. Yellon DM, Hausenloy DJ. Myocardial reperfusion injury. N Engl J Med 357: 1121-1135, 2007.
102. Yung S, Lee CY, Zhang Q, Lau SK, Tsang RC, Chan TM. Elevated glucose induction of thrombospondin-1 up-regulates fibronectin synthesis in proximal renal tubular epithelial cells through TGF-beta1 dependent and TGF-beta1 independent pathways. Nephrol Dial Transplant 21: 1504-1513, 2006.
103. Zaccolo M. Spatial control of cAMP signalling in health and disease. Curr Opin Pharmacol 11: 649-655, 2011.
104. 2+-ATPase. Free Radic Biol Med 27: 810-821, 1999.
105. Zeng C, Villar VA, Yu P, Zhou L, Jose PA. Reactive oxygen species and dopamine receptor function in essential hypertension. Clin Exp Hypertens 31: 156-178, 2009.