Thrombospondin-1 activation of signal-regulatory protein-α stimulates reactive oxygen species production and promotes renal Ischemia reperfusion injury

Journal of the American Society of Nephrology

Volumn 25, Issue 6, 2014, Pages 1171-1186

  Yao, Mingyi ^a   Rogers, Natasha M ^a   Csányi, Gábor ^a   Rodriguez, Andres I ^a   Ross, Mark A ^a   St Croix, Claudette ^a   Knupp, Heather ^a   Novelli, Enrico M ^a   Thomson, Angus W ^a   Pagano, Patrick J ^a   Isenberg, Jeffrey S ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

CD47 ANTIGEN; CELL SURFACE RECEPTOR; PROTEIN P47; PROTEIN TYROSINE PHOSPHATASE SHP 1; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; SIGNAL REGULATORY PROTEIN ALPHA; SUPEROXIDE; THROMBOSPONDIN 1; UNCLASSIFIED DRUG; BASIC HELIX LOOP HELIX LEUCINE ZIPPER TRANSCRIPTION FACTOR; CD47 PROTEIN, HUMAN; CD47 PROTEIN, MOUSE; CD47 PROTEIN, RAT; DIFFERENTIATION ANTIGEN; IMMUNOGLOBULIN RECEPTOR; NITRIC OXIDE DONOR; NITROPRUSSIDE SODIUM; PTPNS1 PROTEIN, MOUSE; SIRPA PROTEIN, HUMAN; SIRPALPHA PROTEIN, RAT; SPZ1 PROTEIN, HUMAN; THROMBOSPONDIN 1, MOUSE; THROMBOSPONDIN 1, RAT; THROMBOSPONDIN-1, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; INFLAMMATORY CELL; KIDNEY BLOOD FLOW; KIDNEY ISCHEMIA; KIDNEY TUBULE CELL; MALE; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; REPERFUSION INJURY; SIGNAL TRANSDUCTION; UPREGULATION; VASCULAR RING; VASCULAR SMOOTH MUSCLE; VASODILATATION; ANIMAL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DRUG EFFECT; KIDNEY DISEASE; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; ANTIGENS, CD47; ANTIGENS, DIFFERENTIATION; BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; CELLS, CULTURED; HUMANS; KIDNEY DISEASES; MALE; MICE; MICE, INBRED C57BL; MUSCLE, SMOOTH, VASCULAR; NITRIC OXIDE DONORS; NITROPRUSSIDE; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; RECEPTORS, IMMUNOLOGIC; REPERFUSION INJURY; SIGNAL TRANSDUCTION; THROMBOSPONDIN 1;

EID: 84900996680     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2013040433     Document Type: Article

References (70)

1. Lawler J: Thrombospondin-1 as an endogenous inhibitor of angiogenesis and tumor growth. J CellMolMed 6: 1-12, 2002
2. Chen H, HerndonME, Lawler J: The cell biology of thrombospondin-1. Matrix Biol 19: 597-614, 2000
3. Rogers NM, Thomson AW, Isenberg JS: Activation of parenchymal CD47 promotes renal ischemia-reperfusion injury. J Am Soc Nephrol 23: 1538-1550, 2012
4. Riessen R, Kearney M, Lawler J, Isner JM: Immunolocalization of thrombospondin-1 in human atherosclerotic and restenotic arteries. Am Heart J 135: 357-364, 1998
5. Bauer EM, Qin Y, Miller TW, Bandle RW, Csanyi G, Pagano PJ, Bauer PM, Schnermann J, Roberts DD, Isenberg JS: Thrombospondin-1 supports blood pressure by limiting eNOS activation and endothelialdependent vasorelaxation. Cardiovasc Res 88: 471-481, 2010
6. Moura R, Tjwa M, Vandervoort P, Cludts K, Hoylaerts MF: Thrombospondin-1 activates medial smooth muscle cells and triggers neointima formation upon mouse carotid artery ligation. Arterioscler Thromb Vasc Biol 27: 2163-2169, 2007
7. Novelli EM, Kato GJ, Ragni MV, Zhang Y, Hildesheim ME, Nouraie M, Barge S,MeyerMP, Hassett AC,Gordeuk VR,GladwinMT, Isenberg JS: Plasma thrombospondin-1 is increased during acute sickle cell vasoocclusive events and associated with acute chest syndrome, hydroxyurea therapy, and lower hemolytic rates. Am J Hematol 87: 326-330, 2012
8. Kharitonenkov A,Chen Z, Sures I, WangH, Schilling J, Ullrich A: A family of proteins that inhibit signalling through tyrosine kinase receptors. Nature 386: 181-186, 1997
9. Stofega MR, Argetsinger LS, Wang H, Ullrich A, Carter-Su C: Negative regulation of growth hormone receptor/JAK2 signaling by signal regulatory protein alpha. J Biol Chem275: 28222-28229, 2000
10. Gresham HD, Dale BM, Potter JW, Chang PW, Vines CM, Lowell CA, Lagenaur CF, Willman CL: Negative regulation of phagocytosis in murine macrophages by the Src kinase family member, Fgr. J ExpMed 191: 515-528, 2000
11. Yamao T, Noguchi T, Takeuchi O, Nishiyama U, Morita H, Hagiwara T, AkahoriH, Kato T, Inagaki K,OkazawaH,Hayashi Y, Matozaki T, Takeda K, Akira S, Kasuga M: Negative regulation of platelet clearance and of the macrophage phagocytic response by the transmembrane glycoprotein SHPS-1. J Biol Chem 277: 39833-39839, 2002
12. Chirkov YY, Horowitz JD: Impaired tissue responsiveness to organic nitrates and nitric oxide: A new therapeutic frontier? Pharmacol Ther 116: 287-305, 2007
13. Wink DA, Cook JA, Pacelli R, Liebmann J, Krishna MC, Mitchell JB: Nitric oxide (NO) protects against cellular damage by reactive oxygen species. Toxicol Lett 82-83: 221-226, 1995
14. Isenberg JS, Hyodo F,Matsumoto K, RomeoMJ, 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
15. 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
16. 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
17. Isenberg JS, Annis DS, Pendrak ML, Ptaszynska M, FrazierWA, Mosher DF, Roberts DD: Differential interactions of thrombospondin-1,-2, and-4 with CD47 and effects on cGMP signaling and ischemic injury responses. J Biol Chem284: 1116-1125, 2009
18. Barclay AN: Signal regulatory protein alpha (SIRPalpha)/CD47 interaction and function. Curr Opin Immunol 21: 47-52, 2009
19. Palen DI, Belmadani S, Lucchesi PA, Matrougui K: Role of SHP-1, Kv.1.2, and cGMP in nitric oxide-induced ERK1/2 MAP kinase dephosphorylation in rat vascular smooth muscle cells. Cardiovasc Res 68: 268-277, 2005
20. Isenberg JS, FrazierWA, RobertsDD: Thrombospondin-1:Aphysiological regulator of nitric oxide signaling. Cell Mol Life Sci 65: 728-742, 2008
21. 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
22. 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 U S A 102: 13141-13146, 2005
23. Palmer RF, Lasseter KC: Drug therapy. Sodium nitroprusside. N Engl J Med 292: 294-297, 1975
24. Reves JG, Sheppard LC, Wallach R, Lell WA: Therapeutic uses of sodium nitroprusside and an automated method of administration. Int Anesthesiol Clin 16: 51-88, 1978
25. Maile LA, Badley-Clarke J, Clemmons DR: The association between integrin-associated protein and SHPS-1 regulates insulin-like growth factor-I receptor signaling in vascular smoothmuscle cells.Mol Biol Cell 14: 3519-3528, 2003
26. Oldenborg PA, Zheleznyak A, Fang YF, Lagenaur CF, Gresham HD, Lindberg FP: Role of CD47 as a marker of self on red blood cells. Science 288: 2051-2054, 2000
27. Maile LA, Clemmons DR: Integrin-associated protein binding domain of thrombospondin-1 enhances insulin-like growth factor-I receptor signaling in vascular smooth muscle cells. Circ Res 93: 925-931, 2003
28. Tulasne D, Judd BA, Johansen M, Asazuma N, Best D, Brown EJ, Kahn M, Koretzky GA,Watson SP: C-terminal peptide of thrombospondin-1 induces platelet aggregation through the Fc receptor gammachain-associated signaling pathway and by agglutination. Blood 98: 3346-3352, 2001
29. Heasman J: Morpholino oligos: Making sense of antisense? Dev Biol 243: 209-214, 2002
30. Isenberg JS, RomeoMJ, Abu-AsabM, TsokosM,Oldenborg A, Pappan L, Wink DA, Frazier WA, Roberts DD: Increasing survival of ischemic tissue by targeting CD47. Circ Res 100: 712-720, 2007
31. Vernon-Wilson EF, KeeWJ,Willis AC, Barclay AN, Simmons DL, Brown MH: CD47 is a ligand for rat macrophage membrane signal regulatory protein SIRP (OX41) and human SIRPalpha 1. Eur J Immunol 30: 2130-2137, 2000
32. CalzadaMJ, Zhou L, Sipes JM, Zhang J, Krutzsch HC, Iruela-Arispe ML, Annis DS, Mosher DF, Roberts DD: Alpha4beta1 integrin mediates selective endothelial cell responses to thrombospondins 1 and 2 in vitro and modulates angiogenesis in vivo. Circ Res 94: 462-470, 2004
33. 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
34. Hamilton CA, BrosnanMJ, Al-Benna S, Berg G, Dominiczak AF: NAD(P) H oxidase inhibition improves endothelial function in rat and human blood vessels. Hypertension 40: 755-762, 2002
35. Lassègue B, Griendling KK: NADPH oxidases: functions and pathologies in the vasculature. Arterioscler Thromb Vasc Biol 30: 653-661, 2010
36. Huang J, Kleinberg ME: Activation of the phagocyte NADPH oxidase protein p47(phox). Phosphorylation controls SH3 domain-dependent binding to p22(phox). J Biol Chem274: 19731-19737, 1999
37. Squadrito GL, Pryor WA: The formation of peroxynitrite in vivo from nitric oxide and superoxide. Chem Biol Interact 96: 203-206, 1995
38. Medina P, Segarra G, Martínez-León JB, Vila JM, Otero E, Lluch S: Relaxation and cGMP formation in response to sildenafil and sodium nitroprusside in saphenous veins from normotensive and hypertensive patients. Am J Hypertens 15: 798-802, 2002
39. Simonsen U, Christensen FH, Buus NH: The effect of tempol on endothelium-dependent vasodilatation and blood pressure. Pharmacol Ther 122: 109-124, 2009
40. Djamali A, Vidyasagar A, Yagci G, Huang LJ, Reese S: Mycophenolic acid may delay allograft fibrosis by inhibiting transforming growth factor-beta1-induced activation of Nox-2 through the nuclear factorkappaB pathway. Transplantation 90: 387-393, 2010
41. Xu Y, Yang S, Huang J, Ruan S, Zheng Z, Lin J: Tgf-b1 induces autophagy and promotes apoptosis in renal tubular epithelial cells. Int J Mol Med 29: 781-790, 2012
42. Khanna AK, Xu J, Baquet C, MehraMR: Adverse effects of nicotine and immunosuppression on proximal tubular epithelial cell viability, tissue repair and oxidative stress gene expression. J Heart Lung Transplant 28: 612-620, 2009
43. Simão S, Fraga S, Jose PA, Soares-da-Silva P: Oxidative stress plays a permissive role in alpha2-adrenoceptor-mediated events in immortalized SHR proximal tubular epithelial cells. Mol Cell Biochem 315: 31-39, 2008
44. 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
45. Guo N, Krutzsch HC, Inman JK, Roberts DD: Thrombospondin 1 and type I repeat peptides of thrombospondin 1 specifically induce apoptosis of endothelial cells. Cancer Res 57: 1735-1742, 1997
46. Halloran PF, Homik J, Goes N, Lui SL, Urmson J, Ramassar V, Cockfield SM: The "injury response": a concept linking nonspecific injury, acute rejection, and long-term transplant outcomes. Transplant Proc 29: 79-81, 1997
47. Gobé G,Willgoss D, Hogg N, Schoch E, Endre Z: Cell survival or death in renal tubular epithelium after ischemia-reperfusion injury. Kidney Int 56: 1299-1304, 1999
48. Ambrosio G, Zweier JL, Duilio C, Kuppusamy P, Santoro G, Elia PP, Tritto I, Cirillo P, Condorelli M, Chiariello M, et al: Evidence that mitochondrial respiration is a source of potentially toxic oxygen free radicals in intact rabbit hearts subjected to ischemia and reflow. J Biol Chem 268: 18532-18541, 1993
49. Li C, Jackson RM: Reactive species mechanisms of cellular hypoxiareoxygenation injury. Am J Physiol Cell Physiol 282: C227-C241, 2002
50. Chatterjee PK: Novel pharmacological approaches to the treatment of renal ischemia-reperfusion injury: A comprehensive review. Naunyn Schmiedebergs Arch Pharmacol 376: 1-43, 2007
51. Laurindo FR, Fernandes DC, Santos CX: Assessment of superoxide production and NADPH oxidase activity by HPLC analysis of dihydroethidium oxidation products. Methods Enzymol 441: 237-260, 2008
52. Liu J, Ormsby A, Oja-Tebbe N, Pagano PJ: Gene transfer of NAD(P)H oxidase inhibitor to the vascular adventitia attenuates medial smooth muscle hypertrophy. Circ Res 95: 587-594, 2004
53. Nediani C, Raimondi L, Borchi E, Cerbai E: Nitric oxide/reactive oxygen species generation and nitroso/redox imbalance in heart failure: From molecular mechanisms to therapeutic implications. Antioxid Redox Signal 14: 289-331, 2011
54. van Beek EM, Zarate JA, van Bruggen R, Schornagel K, Tool AT, Matozaki T, Kraal G, Roos D, van den Berg TK: SIRPa controls the activity of the phagocyte NADPH oxidase by restricting the expression of gp91(phox). Cell Rep 2: 748-755, 2012
55. JohansenML, Brown EJ: Dual regulation of SIRPalpha phosphorylation by integrins and CD47. J Biol Chem282: 24219-24230, 2007
56. Brown EJ, Frazier WA: Integrin-associated protein (CD47) and its ligands. Trends Cell Biol 11: 130-135, 2001
57. Maile LA, Allen LB, Hanzaker CF, Gollahon KA, Dunbar P, Clemmons DR: Glucose regulation of thrombospondin and its role in the modulation of smooth muscle cell proliferation. Exp Diabetes Res 2010: 2010
58. Csányi G, Yao M, Rodríguez 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
59. Sohn HY, Raff U, Hoffmann A, Gloe T, Heermeier K, Galle J, Pohl U: Differential role of angiotensin II receptor subtypes on endothelial superoxide formation. Br J Pharmacol 131: 667-672, 2000
60. Briones AM, Tabet F, Callera GE, Montezano AC, Yogi A, He Y, Quinn MT, Salaices M, Touyz RM: Differential regulation of Nox1, Nox2 and Nox4 in vascular smooth muscle cells from WKY and SHR. J Am Soc Hypertens 5: 137-153, 2011
61. Kawahara T, Ritsick D, Cheng G, Lambeth JD: Point mutations in the proline-rich region of p22phox are dominant inhibitors of Nox1-and Nox2-dependent reactive oxygen generation. J Biol Chem 280: 31859-31869, 2005
62. Isenberg JS, Wink DA, Roberts DD: Thrombospondin-1 antagonizes nitric oxide-stimulated vascular smooth muscle cell responses. Cardiovasc Res 71: 785-793, 2006
63. Baud L, Ardaillou R: Involvement of reactive oxygen species in kidney damage. Br Med Bull 49: 621-629, 1993
64. Padanilam BJ: Cell death induced by acute renal injury: A perspective on the contributions of apoptosis and necrosis. Am J Physiol Renal Physiol 284: F608-F627, 2003
65. Matozaki T, Murata Y, Okazawa H, Ohnishi H: Functions and molecular mechanisms of the CD47-SIRPalpha signalling pathway. Trends Cell Biol 19: 72-80, 2009
66. Wu H, Chen G, Wyburn KR, Yin J, Bertolino P, Eris JM, Alexander SI, Sharland AF, Chadban SJ: TLR4 activation mediates kidney ischemia/reperfusion injury. J Clin Invest 117: 2847-2859, 2007
67. Bauer PM, Bauer EM, Rogers NM, YaoM, Feijoo-CuaresmaM, Pilewski JM, Champion HC, Zuckerbraun BS, Calzada MJ, Isenberg JS: Activated CD47 promotes pulmonary arterial hypertension through targeting caveolin-1. Cardiovasc Res 93: 682-693, 2012
68. Touyz RM, Yao G, Schiffrin EL: c-Src induces phosphorylation and translocation of p47phox: Role in superoxide generation by angiotensin II in human vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 23: 981-987, 2003
69. Csányi G, Cifuentes-Pagano E, Al Ghouleh I, Ranayhossaini DJ, Egaña L, Lopes LR, Jackson HM, Kelley EE, Pagano PJ: Nox2 B-loop peptide, Nox2ds, specifically inhibits the NADPH oxidase Nox2. Free Radic Biol Med 51: 1116-1125, 2011
70. Cascino T, Csanyi G, Al Ghouleh I, Montezano AC, Touyz RM, Haurani MJ, Pagano PJ: Adventitia-derived hydrogen peroxide impairs relaxation of the rat carotid artery via smooth muscle cell p38 mitogenactivated protein kinase. Antioxid Redox Signal 15: 1507-1515, 2011