Loss of Rat Glomerular ATP Diphosphohydrolase Activity during Reperfusion Injury Is Associated with Oxidative Stress Reactions

Daniel Candinas; Nozomi Koyamada; Tsukasa Miyatake; Jonathan Siegel; Wayne W Hancock; Fritz H Bach; Simon C Robson

doi:10.1055/s-0038-1650664

Thrombosis and Haemostasis, Table of Contents

Thromb Haemost 1996; 76(05): 807-812
DOI: 10.1055/s-0038-1650664

Original article

Schattauer GmbH Stuttgart

Loss of Rat Glomerular ATP Diphosphohydrolase Activity during Reperfusion Injury Is Associated with Oxidative Stress Reactions

Daniel Candinas

¹The Sandoz Center for Immunobiology, Departments of Medicine, Surgery and Pathology, New England Deaconess Hospital, Harvard Medical School, Boston, Massachusetts, USA

,

Nozomi Koyamada

¹The Sandoz Center for Immunobiology, Departments of Medicine, Surgery and Pathology, New England Deaconess Hospital, Harvard Medical School, Boston, Massachusetts, USA

,

Tsukasa Miyatake

¹The Sandoz Center for Immunobiology, Departments of Medicine, Surgery and Pathology, New England Deaconess Hospital, Harvard Medical School, Boston, Massachusetts, USA

,

Jonathan Siegel

¹The Sandoz Center for Immunobiology, Departments of Medicine, Surgery and Pathology, New England Deaconess Hospital, Harvard Medical School, Boston, Massachusetts, USA

,

Wayne W Hancock

¹The Sandoz Center for Immunobiology, Departments of Medicine, Surgery and Pathology, New England Deaconess Hospital, Harvard Medical School, Boston, Massachusetts, USA

,

Fritz H Bach

¹The Sandoz Center for Immunobiology, Departments of Medicine, Surgery and Pathology, New England Deaconess Hospital, Harvard Medical School, Boston, Massachusetts, USA

,

Simon C Robson

¹The Sandoz Center for Immunobiology, Departments of Medicine, Surgery and Pathology, New England Deaconess Hospital, Harvard Medical School, Boston, Massachusetts, USA

› Author Affiliations

Abstract

PDF Download

Summary

Endothelial cell ATP diphosphohydrolases or ATPDases degrade extracellular inflammatory mediators ATP and ADP, thus inhibiting the formation of platelet thrombi, but the modulation of these ecto-enzymes during vascular injury remains largely undetermined. Renal glomerular ATPDase levels were determined in the rat following ische-mia-reperfusion or systemic complement activation, by direct biochemical methods and histochemistry. Ischemia followed by reperfusion times over 30 min were associated with loss of glomerular ATPDase activity. Cobra Venom Factor (CVF) inhibited ATPDase activity and potentiated the deleterious effects of reperfusion. Treatment with either soluble complement receptor type 1 (sCRl), an inhibitor of complement activation, or antioxidants prior to the ischemia-reperfusion was largely protective. Expression of rat glomerular ATPDase activity appears susceptible to the inflammatory injury associated with systemic complement activation and ischemia/reperfusion processes. Oxidative stress could, at least in part, result in the loss of ATPDase activity and thus thrombotic consequences of vascular injury.

PDF (426 kb)

References

References
1 Cotran RS, Pober JS. Endothelial activation and inflammation. Prog Immun 1989; 8: 747-792
2 Pober JS, Cotran RS. Cytokines and endothelial cell biology. Physiol Rev 1990; 70 (02) 427-451
3 Pober JS, Cotran RS. The role of endothelial cells in inflammation. Transplantation 1991; 50 (537) 537-544
4 Bach FH, Robson SC, Winkler H, Ferran C, Stuhlmeier KM, Wrighton CJ, Hancock WW. Barriers to xenotransplantation. Nature Med 1995; 1 (09) 869-873
5 Bach FH, Robson SC, Ferran C, Winkler H, Millan MT, Stuhlmeier KM, Vanhove B, Blakely ML, van der Werf WJ, Hofer E, de Martin R, Hancock WW. Endothelial cell activation and thromboregulation during xenograft rejection. (Review). Immunol Rev 1994; 141 (05) 5-30
6 Robson SC, Candinas D, Hancock WW, Wrighton C, Winkler H, Bach FH. Role of endothelial cells in transplantation. (Review). Int Arch Allerg Immunol 1995; 106 (04) 305-322
7 Bakker WW, Willink EJ, Donga J, Hulstaert CE, Hardonk MJ. Antithrombotic activity of glomerular adenosine diphosphatase in the glomerular basement membrane of the rat kidney. J Lab Clin Med 1987; 109 (02) 171-177
8 Marcus AJ, Safier LB. Thromboregulation: multicellular modulation of platelet reactivity in hemostasis and thrombosis. (Review). FASEB J 1993; 7 (06) 516-522
9 Luthje J. Origin, metabolism and function of extracellular adenine nucleotides in the blood (published erratum appears in Klin Wochenschr 1989 May 15; 67 (10): 558). (Review). Klin Wochensch 1989; 67 (06) 317-327
10 Bakker WW, Poelstra K, Barradas MA, Mikhailidis DP. Platelets and ectonucleotidases. Platelet 1994; 5: 121-129
11 Plesner L. Ecto-ATPases: identities and functions. Int Rev Cytol 1995; 158: 141-214
12 Yagi K, Shinbo M, Hashizume M, Shimba LS, Kurimura S, Miura Y. ATP diphosphohydrolase is responsible for ecto-ATPase and ecto-ADPase activities in bovine aortic endothelial and smooth muscle cells. Biochem Biophys Res Comm 1991; 180: 1200-1206
13 Zimmermann H. 5‘-nucleotidase: molecular structure and functional aspects. Biochem J 1992; 285: 345-365
14 Deussen A, Bading B, Kelm M, Schrader J. Formation and salvage of adenosine by macrovascular endothelial cells. Am J Physiol 1993; 264 (3 Pt 2) 692-700
15 Robson SC, Candinas D, Hancock WW, Siegel JB, Millan M, Bach FH. Mechanism of abnormal thromboregulation in xenograft rejection: loss of ecto-ADPase activity. Transplant Proc 1996; 28: 536
16 Shackleton CR, Ettinger SL, Scudamore CH, Toleikis PF, Keown PA. Effect of a 21-aminosteroid, U74006F, on lipid peroxidation and glomeru-lotubular function following experimental renal ischemia. J Surg Res 1994; 57: 433-437
17 Buerke M, Murohara T, Lefer AM. Cardioprotective effects of a Cl esterase inhibitor in myocardial ischemia and reperfusion. Circulation 1995; 91: 393-402
18 Albelda SM, Smith CW, Ward PA. Adhesion molecules and inflammatory injury. FASEB J 1994; 8: 504-512
19 Ward PA, Mulligan MS. New insights into mechanisms of oxyradical and neutrophil mediated lung injury. Klin Wochenschr 1991; 69: 1009-1111
20 Robson SC, Siegel JB, Lesnikoski BA, Kopp C, Candinas D, Ryan U, Bach FH. Aggregation of human platelets induced by porcine endothelial cells is dependent upon both activation of complement and thrombin generation. Xenotransplantation 1996; 3: 24-34
21 Candinas D, Bach FH, Hancock WW. Delayed xenograft rejection in complement depleted T cell deficient (nude) rat recipients of guinea pig xenografts. Transplant Proc 1996; 28: 678
22 Lesnikoski BA, Candinas D, Hancock WW, Otsu I, Siegel JB, Bach FH, Robson SC. Inhibition of platelet GPIIbllla prolongs survival of discordant xenografts. Transplant Proc 1996; 28: 703
23 Bakker WW, Poelstra K, Timmerman W, Hardonk MJ, Koiter TR, Schuil-ing GA. Experimental endotoxemia in pregnancy: in situ glomerular microthrombus formation associated with impaired glomerular adenosine diphosphatase activity. J Lab Clin Med 1989; 114 (05) 531-537
24 Poelstra K, Bailer JF, Hardonk MJ, Bakker WW. Intraglomerular thrombotic tendency and glomerular ADPase. Unilateral impairment of ADPase elicits a proaggregatory microenvironment in experimental glomerulonephritis. Lab Invest 1991; 64 (04) 520-526
25 LeBel D, Poirier GG, Phaneuf S, St-Jean P, Laliberte JF, Beaudoin AR. Characterization and purification of a calcium-sensitive ATP diphospho-hydrolase from pig pancreas. J Biol Chem 1980; 255 (03) 1227-1233
26 Cote YP, Picher M, St-Jean P, Beliveau R, Potier M, Beaudoin AR. Identification and localization of ATP-diphosphohydrolase (apyrase) in bovine aorta: relevance to vascular tone and platelet aggregation. Biochim. Biophys Acta 1991; 1078 (02) 187-191
27 Crutchley DJ, Eling TE, Anderson MW. ADPase activity of isolated perfused rat lung. Life Sciences 1978; 22 (16) 1413-1420
28 Poelstra K, Hardonk MJ, Koudstaal J, Bakker WW. Intraglomerular platelet aggregation and experimental glomerulonephritis. Kidney Int 1990; 37 (06) 1500-1508
29 Murphy HS, Shayman JA, Till GO, Mahrougui M, Owens CB, Ryan US, Ward PA. Superoxide responses of endothelial cells to C5a and TNF-alpha: divergent signal transduction pathways. Am J Physiol 1992; 263 (1 Pt 1) L51-L59
30 Cotran RS, Pober JS. Cytokine-endothelial interactions in inflammation, immunity, and vascular injury. J Am Soc Nephrol 1990; 1 (03) 225-235
31 Baker GL, Corry RJ, Autor AP. Oxygen free radical induced damage in kidneys subjected to ischemic acute renal failure in the rat. J Clin Invest 1985; 74: 628-634
32 Borg DC. Oxygen radicals and tissue damage. In: Tarr M, Samson F. eds Oxygen free radicals and tissue damage. Boston: Birkhauser: 1993: 12-53
33 Chessman KH. Protein oxidation and aging. Toxicol. Indust. Health 1993 9. 39-51
34 Magee JC, Platt JL, Oldham KT, Guice KS. Oxidant stress increases susceptibility of porcine endothelial cells to injury by xenoreactive antibody and complement. Transplant Proc 1994; 26 (03) 1170
35 Aalto TK, Raivio KO. Metabolism of extracellular adenine nucleotides by human endothelial cells exposed to reactive oxygen metabolites. Am J Physiol 1993; 264: C282-C286
36 Kozar RA, McKeone BJ, Pownall HJ. Free radical-induced alterations in endothelial cell function. J Surg Res 1994; 56 (01) 32-36
37 Ambrosio G, Oriente A, Napoli C, Palumbo G, Chiariello P, Marone G, Condorelli M, Chariello M, Triggiani M. Oxygen radicals inhibit human plasma acetylhydrolase, the enzyme that catabolizes platelet-activating factor. Clin Invest 1994; 93: 2408-2416
38 Brisseau GF, Dackiw AP, Cheung PY, Christie N, Rotstein OD. Posttran-scriptional regulation of macrophage tissue factor expression by antioxidants. Blood 1995; 85 (04) 1025-1035
39 Kalsi JK, Clay K, Rickard D, Hall ND. Suppressive effects of a novel antioxidant compound on human T-cell functions in vitro. Agents & Actions 1993; 39 (Special Issue): CI 10-12
40 Mulligan MS, Miyasaka M, Tamatani T, Jones ML, Ward PA. Requirements for L-selectin in neutrophil-mediated lung injury in rats. J Immunol 1994; 152 (832) 832-840
41 Baldwin WMI, Pruitt SK, Brauer RB, Daha MR, Sanfilippo F. Complement in organ transplantation. Transplantation 1995; 59: 797-808
42 Valenzuela MA, Kettlun AM, Sandoval S, Garcia L, Mancilla M, Neckel-mann G, Chayet L, Alvarez A, Cuevas F, Collados L, Espinosa V, Traver-socori A, Bravo I, Acevedo CG, Aranda E. Comparison of biochemical properties, regulation and function of ATP-diphosphohydrolase from human placenta and rat kidney. Braz J Med Biol Res 1996; 29: 589-597