Kidney Damage in Autoimmune Disease

  • Gerald C. Groggel
Part of the Contemporary Immunology book series (CONTIM)

Abstract

In 1641, Daniel Sennet noted the association of scarlatina and dropsy (1), but it was not until 40 years ago that Mellors first demonstrated in human kidney biopsies the deposition in the glomerulus of gamma globulins (2). Since that time, there has been a tremendous amount of work, both experimental and clinical, demonstrating that the kidney is an important site of injury in autoimmune disease. In systemic lupus erythematous, the prototypic autoimmune disorder, the kidney is the organ most commonly affected. By kidney biopsy, at least mild abnormalities are seen in all patients with lupus.

Keywords

Lipase Cysteine Serine Angiotensin Prostaglandin 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Sennet, D. (1641) De febribus libri IV: Accessit ad calcem, ejusdem de dysenteria tractatus: E. movossoma. cie accessit fasciculus medicamentorum contra pestum Venetiis (Venice): F. Baba, 178–190.Google Scholar
  2. 2.
    Mellors, R. C. and Ortega, L. G. (1956) Analytical pathology: II New observations on the pathogenesis of glomerulonephritis, lipoid nephrosis, periarteritis nodosa and secondary amyloidosis in man. Amer. J. Pathol. 32, 455–499.Google Scholar
  3. 3.
    Wilson, C. B. (1991) The renal response to immunologie injury, in The Kidney (Brenner, B. M. and Rector, F. C., eds.), 4th edn., Saunders, Philadelphia, PA, pp. 1062–1181.Google Scholar
  4. 4.
    Falk, R. J. and Jennette, J. C. (1991) Wegener’s granulomatosis, systemic vasculi-tis and anti-neutrophil cytoplasmic autoantibodies. Ann. Rev. Med. 42, 456–469.CrossRefGoogle Scholar
  5. 5.
    Couser, W. G. (1990) Mediation of immune glomerular injury. J. Amer. Soc. Neph. 1, 13–29.Google Scholar
  6. 6.
    Johnson, R. J. (1994) The glomerular response to injury: Progression or resolution? Kidney Int. 45, 1769–1782.PubMedCrossRefGoogle Scholar
  7. 7.
    Dixon, F. J. (1968) The pathogenesis of glomerulonephritis. Amer. J. Med. 44, 493–498.PubMedCrossRefGoogle Scholar
  8. 8.
    Couser, W. G. and Salant, D. J. (1980) Immune complex formation and glomerular injury. Kidney Int. 17, 1–13.PubMedCrossRefGoogle Scholar
  9. 9.
    Couser, W. G. (1985) Mechanisms of glomerular injury in immune-complex disease. Kidney Int. 28, 569–583.PubMedCrossRefGoogle Scholar
  10. 10.
    Salant, D. J., Adler, S., Darby, C., Capparell, N. J., Groggel, G. C., Feintzeig, I. D., et al. (1985) Influence of antigen distribution on the mediation of immunologic glomerular injury. Kidney Int. 27, 938–950.PubMedCrossRefGoogle Scholar
  11. 11.
    Couser, W. G., Stilmant, M. M., and Jermanovich, N. B. (1977) Complement-independent nephrotoxic nephritis in the guinea pig. Kidney Int. 11, 170–180.PubMedCrossRefGoogle Scholar
  12. 12.
    Couser, W. G., Darby, C., Salant, D. J. Adler, S., Stilmant, M. M., and Lowenstein, L. M. (1985) Anti-GBM antibody induced proteinuria in isolated perfused rat kidney. Amer. J. Physiol. 249, F241–F250.PubMedGoogle Scholar
  13. 13.
    Salant, D. J., Madaio, M. P., Adler, S., Stilmant, M. M., and Couser, W. G. (1981) Altered glomerular permeability induced by F(ab’)2 and Fab’ antibodies to rat renal tubular epithelial antigen. Kidney Int. 21, 36–43.CrossRefGoogle Scholar
  14. 14.
    Mendrick, D. L. and Rennke, H. G. (1988) Induction of proteinuria in the rat by a monoclonal antibody against SGP-115/107. Kidney Int. 33, 818–830.PubMedCrossRefGoogle Scholar
  15. 15.
    Orikasa, M., Matsui, K., Oite, T., and Shimizu, F. (1988) Massive proteinuria induced in rats by a single intravenous injection of a monoclonal antibody. J. Immunol. 141, 807–814.PubMedGoogle Scholar
  16. 16.
    Johnson, R., Yamabe, H., Chen, Y-P, Campbell, C., Gordon, K., Baker, P., et al. (1992) Glomerular epithelial cell secrete a glomerular basement membrane-degrading metalloproteinase. J. Amer. Soc. Nephrol. 2, 1388–1397.Google Scholar
  17. 17.
    Couser, W. G., Baker, P. J., and Adler, S. (1985) Complement and the direct mediation of immune glomerular injury: a new perspective. Kidney Int. 28, 879–890.PubMedCrossRefGoogle Scholar
  18. 18.
    Cybulsky, A. V., Quigg, R. J., and Salant, D. J. (1988) Role of the complement membrane attack complex in glomerular injury, in Immunopathology of Renal Disease (Brenner, B. M. and Stein, J., eds.), Churchill, Livingstone, New York, pp. 57–86.Google Scholar
  19. 19.
    Schreiber, R. D. and Muller-Eberhard, H. J. (1979) Complement and renal disease, in Immunologic Mechanisms of Renal Disease (Brenner, B. M. and Stein, J., eds.), Churchill, Livingstone, New York, pp. 67–105.Google Scholar
  20. 20.
    Cochrane, C. G., Unanue, E. R., and Dixon, F. J. (1965) A role of polymorphonuclear leukocytes and complement in nephrotoxic nephritis. J. Exp. Med. 122, 99–116.PubMedCrossRefGoogle Scholar
  21. 21.
    Henson, P. M. (1972) Pathologic mechanisms in neutrophil-mediated injury. Amer. J. Path. 68, 593–605.PubMedGoogle Scholar
  22. 22.
    Salant, D. J., Belok, S., Madaio, M. P., and Couser, W. G. (1980) A new role for complement in experimental membranous nephropathy in rats. J. Clin. Invest. 66, 1339–1350.PubMedCrossRefGoogle Scholar
  23. 23.
    Groggel, G. C., Adler, S., Rennke, H. G., Couser, W. G., and Salant, D. J. (1983) Role of the terminal complement pathway in experimental membranous nephropathy in the rabbit. J. Clin. Invest. 72, 1948–1957.PubMedCrossRefGoogle Scholar
  24. 24.
    Cybulsky, A. V., Rennke, H. G., Feintzeig, I. D., and Salant, D. J. (1986) Complement-induced glomerular epithelial cell injury. Role of the membrane attack complex in rat membranous nephropathy. J. Clin. Invest. 77, 1096–1107.PubMedCrossRefGoogle Scholar
  25. 25.
    Groggel, G. C., Salant, D. J., Darby, C., Renke, H. G., and Couser, W. G. (1985) Role of terminal complement pathway in the heterologous phase of antiglomerular basement membrane nephritis. Kidney Int. 27, 643–651.PubMedCrossRefGoogle Scholar
  26. 26.
    Falk, R. J., Dalmasso, A. P., Kim, Y., Tsai, C. H., Scheinman, J. I., Gerwurz, H., et al. (1983) Neoantigen of the polymerized ninth component of complement. Characterization of a monoclonal antibody and immunohistochemical localization in renal disease. J. Clin. Invest. 72, 560–573.PubMedCrossRefGoogle Scholar
  27. 27.
    Muller-Eberhard, H. J. (1988) Molecular organization and function of the complement system. Ann. Rev. Biochem. 57, 321–347.PubMedCrossRefGoogle Scholar
  28. 28.
    Quigg, R. J., Cybulsky, A.V., Jacobs, J. B., and Salant, D.J. (1988) Anti-Fx1A produces complement-dependent cytotoxicity of glomerular epithelial cells. Kidney Int. 34, 43–52.PubMedCrossRefGoogle Scholar
  29. 29.
    Cybulsky, A. V., Salant, D. J., Quigg, R. J., Badalamenti, J., and Bonventre, J. V. (1989) Complement C5b-9 complex activates phospholipases in glomerular epithelial cells. Amer. J. Physiol. 257, F826–F836.PubMedGoogle Scholar
  30. 30.
    Adler, S., Baker, P. J., Johnson, R. J., Ochi, R. F., Pritzl, P., and Couser, W. G. (1986) Complement membrane attack complex stimulates production of reactive oxygen metabolites by cultured rat mesangial cells. J. Clin. Invest. 77, 762–767.PubMedCrossRefGoogle Scholar
  31. 31.
    Torbohm, I., Schonermark, M., Wingen, A. M., Berger, B., Rother, K., and Hansch, G. M. (1990) C5b-8 and C5b-9 modulate the collagen release of human glomerular epithelial cells. Kidney Int. 37, 1098–1104.PubMedCrossRefGoogle Scholar
  32. 32.
    Groggel, G. C. and Terreros, D. A. (1990) Role of the terminal complement pathway in accelerated autologous anti-glomerular basement membrane nephritis. Amer. J. Pathol. 136, 533–540.Google Scholar
  33. 33.
    Hebert, L. A. and Cosio, F. G. (1987) The erythrocyte-immune complex-glomeru-lonephritis connection in man. Kidney Int. 31, 877–885.PubMedCrossRefGoogle Scholar
  34. 34.
    Schifferli, J. A., Ng, Y. C., and Peters, D. K. (1986) The role of complement and its receptor in the elimination of immune complexes. N. Engl. J. Med. 315, 488–495.PubMedCrossRefGoogle Scholar
  35. 35.
    Brady, H. R. (1994) Leukocyte adhesion molecules and kidney diseases. Kidney Int. 45, 1285–1300.PubMedCrossRefGoogle Scholar
  36. 36.
    Naisch, P. F., Thomson, N. M., Simpson, I. J., and Peters, D. K. (1975) The role of polymorphonuclear leukocytes in the autologous phase of nephrotoxic nephritis. Clin. Exp. Immunol. 22, 102–111.Google Scholar
  37. 37.
    Hooke, D. H., Gee, D. C., and Atkins, R. C. (1987) Leucocyte analysis using monoclonal antibodies in human glomerulonephritis. Kidney Int. 31, 964–972.PubMedCrossRefGoogle Scholar
  38. 38.
    Cook, H. T., Smith, J., and Cattell, V. (1987) Isolation and characterization of inflammatory leukocytes from glomeruli in an in situ model of glomerulonephritis in the rat. Amer. J. Pathol. 126, 126–136.Google Scholar
  39. 39.
    Tucker, B. J., Gushwa, L. C., and Wilson, C. B. (1985) Effect of leucocyte depletion on glomerular dynamics during active glomerular immune injury. Kidney Int. 28, 28–35.PubMedCrossRefGoogle Scholar
  40. 40.
    Adachi, T., Fukuta, M., Ito, Y., Hirano, K., Sugiura, M., and Sugiura, K. (1986) Effect of Superoxides dismutase on glomerular nephritis. Biochem Pharmacol 35, 341–345.PubMedCrossRefGoogle Scholar
  41. 41.
    Rehan, A., Johnson, K. J., Wiggins, R. C., Kunkel, R. G., and Ward, P. A. (1984) Evidences for the role of oxygen radicals in acute nephrotoxic nephritis. Lab. Invest. 51, 96–403.Google Scholar
  42. 42.
    Johnson, R. B. and Lehmeyer, J. E. (1976) Elaboration of toxic oxygen by-products by neutrophils in a model of immune complex disease. J. Clin. Invest. 57, 836–841.CrossRefGoogle Scholar
  43. 43.
    Baricos, W. H. and Shah, S. V. (1991) Proteolytic enzymes as mediators of glomerular injury. Kidney Int. 40, 161–173.PubMedCrossRefGoogle Scholar
  44. 44.
    Davies, M., Barrett, A. J., Travis, J., Sanders, E., and Coles, G. A. (1978) The degradation of human glomerular basement membrane with purified lysosomal proteinases: evidence for the pathogenic role of the polymorphonuclear leukocyte in glomerulonephritis. Clin. Sci. Mol. Med. 54, 233–240.PubMedGoogle Scholar
  45. 45.
    Harlan, J. M., Killen, P. D., Harker, L. A., and Striker, G. E. (1981) Neutrophil mediated endothelial injury in vitro mechanisms of cell detachment. J. Clin. Invest. 68, 1394–1403.PubMedCrossRefGoogle Scholar
  46. 46.
    Shah, S. V., Baricos, W. H., and Basci, A. (1987) Degradation of human glomerular basement membrane by stimulated neutrophils activation of a metalloproteinase by reactive oxygen metabolites. J. Clin. Invest. 79, 25–31.PubMedCrossRefGoogle Scholar
  47. 47.
    Lovett, D. H., Sterzel, B. R., Kashgarian, M., and Ryan, J. L. (1983) Neutral pro-teinase activity produced in vitro by cells of the glomerular mesangium. Kidney Int. 23, 342–349.PubMedCrossRefGoogle Scholar
  48. 48.
    Baricos, W. H., Cortez, S. L., Le, Q. C., Zhou, Y., Dicarlo, R. M., O’Connor, S. F., et al. (1990) Glomerular basement membrane degradation by endogenous cysteine proteinases in isolated rat glomeruli. Kidney Int. 38, 395–401.PubMedCrossRefGoogle Scholar
  49. 49.
    Johnson, R. J., Couser, W. G., Alpers, C. E., Vissers, M., Schulze, M., and Klebanoff, S. J. (1988) The human neutrophil serine proteinases elastase and cathe-psin G can mediate glomerular injury in vivo. J. Exp. Med. 168, 1169–1174.PubMedCrossRefGoogle Scholar
  50. 50.
    Davin, J. C., Davies, M., Foidart, J. M., Foidart, J. B., Dechenne, C. A., and Mahieu, P. R. (1987) Urinary excretion of neutral proteinases in nephrotic rats with a glomerular disease. Kidney Int. 31, 32–40.PubMedCrossRefGoogle Scholar
  51. 51.
    Schrijver, G., Schwalkwijk, J., Robben, J. C. M., Assmann, K. J. M., and Koene, R. A. P. (1989) Antiglomerular basement membrane nephritis in Beije mice. J. Exp. Med. 169, 1435–1448.PubMedCrossRefGoogle Scholar
  52. 52.
    Baricos, W. H., O’Connor, S. E., Cortez, S. L., Wu, L.-T., and Shah, S. V. (1988) The cysteine proteinase inhibitor, E-64, reduces proteinuria in an experimental model of glomerulonephritis. Biochem. Biophys. Res. Comm. 155, 1318–1323.PubMedCrossRefGoogle Scholar
  53. 53.
    Vassalli, J. D., Sappino, A.-P., and Belin, D. (1991) The plasminogen activator/ plasmin system. J. Clin. Invest. 88, 1067–1072.PubMedCrossRefGoogle Scholar
  54. 54.
    He, C. S., Wilhelm, S. M., Pentland, A. P., Marmer, B. L., Grant, G. A., Eisen, A. Z., et al. (1989) Tissue cooperation in a proteolytic cascade activating human interstitial collagenase. Proc. Natl. Acad. Sci. USA 86, 2632–2636.PubMedCrossRefGoogle Scholar
  55. 55.
    Lacave, R., Rondeau, E., Ochi, S., Delaure, F., Schleuning, W. D., and Sraer, J.-D. (1989) Characterization of a plasminogen activator and its inhibitor in human mesangial cells. Kidney Int. 35, 806–811.PubMedCrossRefGoogle Scholar
  56. 56.
    Nguyen, G., Li, X.-M., Peraldi, M.-N., Zacharias, U., Hagege, J., Rondeau, E., et al. (1994) Receptor binding and degradation of urokinase-type plasminogen activator by human mesangial cells. Kidney Int. 46, 208–215.PubMedCrossRefGoogle Scholar
  57. 57.
    Hagege, J., Peraldi, M. N., Rondeau, E., Adida, C., Delarue, F., Medcalf, R., et al. (1992) Plasminogen activator inhibitor-1 deposition in the extracellular matrix of cultured human mesangial cells. Amer. J. Pathol. 141, 117–128.Google Scholar
  58. 58.
    Rondeau, E., Ochi, S., Lacave, R., He, C.-J., Medcalf, R., Delrue, F., et al. (1989) Urokinase synthesis and binding by glomerular epithelial cells in culture. Kidney Int. 36, 593–600.PubMedCrossRefGoogle Scholar
  59. 59.
    Becquemont, L., Nguyen, G., Peraldi, M.-N., He, C.-J., Sraer, J.-D., and Rondeau, E. (1994) Expression of plasminogen/plasmin receptors on human glomerular epithelial cells. Amer. J. Physiol. 267, F303–F310.PubMedGoogle Scholar
  60. 60.
    Wong, A. P., Cortez, S. L., and Baricos, W. H. (1992) Role of plasmin and gelatinase in extracellular matrix degradation by cultured rat mesangial cells. Amer. J. Physiol. 263, F1112–F1118.PubMedGoogle Scholar
  61. 61.
    Tomooka, S., Border, W. A., Marshall, B. C., and Noble, N. A. (1992) Glomerular matrix accumulation is linked to inhibition of the plasmin protease system. Kidney Int. 42, 1462–1469.PubMedCrossRefGoogle Scholar
  62. 62.
    Feng, L., Tang, W. W., Wilson, C. B., and Loskutoff, D. J. (1993) Dysfunction of glomerular fibrinolysis in experimental antiglomerular basement membrane antibody glomerulonephritis. J. Amer. Soc. Nephrol. 3, 1753–1764.Google Scholar
  63. 63.
    Tange, W. W., Feng, L., Xia, Y., and Wilson, C. B. (1994) Extracellular matrix accumulation in immune-mediated tubulointerstitial injury. Kidney Int. 45, 1077–1084.CrossRefGoogle Scholar
  64. 64.
    Schreiner, G. F. (1991) The role of the macrophage in glomerular injury. Semin. Nephrol. 11, 268–275.PubMedGoogle Scholar
  65. 65.
    Schreiner, G. F., Cotran, R. S., Pardo, U., and Uhane, E. R. (1978) A mononuclear cell component in experimental immunological glomerulonephritis. J. Exp. Med. 147, 369–384.PubMedCrossRefGoogle Scholar
  66. 66.
    Holdsworth, S. R. and Tipping, P. G. (1987) Macrophage-induced glomerular fibrin deposition in experimental glomerulonephritis in the rabbit. J. Clin. Invest. 76, 1367–1374.CrossRefGoogle Scholar
  67. 67.
    Tipping, P. G. and Holdsworth, S. R. (1986) The participation of macrophages, glomerular procoagulant activity, and Factor VIII in glomerular fibrin deposition. Amer. J. Pathol. 124, 10–17.Google Scholar
  68. 68.
    Nathan, C. F. (1987) Secretory products of macrophages. J. Clin. Invest. 79, 319–326.PubMedCrossRefGoogle Scholar
  69. 69.
    Kreisberg, J. I., Wayne, D. B., and Karnovsky, M. D. (1979) Rapid and focal loss of negative charge associated with mononuclear cell infiltration early in nephro-toxic serum nephritis. Kidney Int. 16, 290–300.PubMedCrossRefGoogle Scholar
  70. 70.
    Bolton, W. K., Tucker, F. L., and Sturgill, C. (1984) New avian model of experimental glomerulonephritis consistent with mediation by cellular immunity. J. Clin. Invest. 73, 1263–1276.PubMedCrossRefGoogle Scholar
  71. 71.
    Johnson, R. J. (1991) Platelets in inflammatory glomerular injury. Semin. Nephrol. 11, 276–284.PubMedGoogle Scholar
  72. 72.
    Johnson, R. J., Alpers, C. E., Pritzl, P., Schulze, M., Baker, P., Pruchno, C., et al. (1988) Platelets mediate neutrophil-dependent immune complex nephritis in the rat. J. Clin. Invest. 82, 1225–1235.PubMedCrossRefGoogle Scholar
  73. 73.
    Johnson, R. J., Alpers, C. E., Pruchno, C., Schulze, M., Baker, P. J., Pritzl, P., et al. (1989) Mechanisms and kinetics for platelet and neutrophil localization in immune complex nephritis. Kidney Int. 36, 780–789.PubMedCrossRefGoogle Scholar
  74. 74.
    Johnson, R. J., Garcia, R. L., Pritzl, P., and Alpers, C. E. (1990) Platelets mediate glomerular cell proliferation in immune complex nephritis induced by anti-mesangial cell antibodies in the rat. Amer. J. Pathol. 136, 369–374.Google Scholar
  75. 75.
    Johnson, R. J., Pritzl, P., Iida, H., and Alpers, C. E. (1991) Platelet-complement interactions in mesangial proliferative nephritis in the rat. Amer. J. Pathol. 138, 313–321.Google Scholar
  76. 76.
    Iida, H., Seifert, R., Alpers, C. E., Gronwald, R. G. K., Phillips, P. E., Pritzl, P. G., et al. (1991) Platelet-derived growth factor (PDGF) and PDGF receptor are induced in mesangial proliferative nephritis in the rat. Proc. Natl. Acad. Sci. USA 88, 6560–6569.PubMedCrossRefGoogle Scholar
  77. 77.
    Abboud, H. E. (1991) Resident glomerular cells in glomerular injury: mesangial cells. Semin. Nephrol. 11, 304–310.PubMedGoogle Scholar
  78. 78.
    Mene, P., Simonson, M. S., and Dunn, M. J. (1989) Physiology of the mesangial cell. Physiol. Rev. 69, 1347–1424.PubMedGoogle Scholar
  79. 79.
    Schlondorff, D. (1987) The glomerular mesangial cell: an expanding role for a specialized pericyte. FASEB J. 1, 272–281.PubMedGoogle Scholar
  80. 80.
    Kreisberg, J. I., Venkatachalam, M., and Troyer, D. (1985) Contractile properties of cultured glomerular mesangial cells. Amer. J. Physiol. 249, F457–F463.PubMedGoogle Scholar
  81. 81.
    Sterzel, R. B. and Lovett, D. H. (1988) Interactions of inflammatory and glomerular cells in the response to glomerular injury, in Immunopathology of Renal Disease (Wilson, C. B., Brenner B. M., and Stein, J. H., eds.), Churchill, Livingstone, New York, pp. 137–173.Google Scholar
  82. 82.
    Groggel, G. C. and Hughes, M. L. (1995) Heparan sulfate stimulates extracellular matrix component synthesis by mesangial cells. Nephron. 71, 197–202.PubMedCrossRefGoogle Scholar
  83. 83.
    Striker, L. J., Peten, E. P., Elliot, S. J., Doi, T., and Striker, G. E. (1991) Biology of disease: mesangial cell turnover: effect of heparin and peptide growth factors. Lab. Invest. 64, 446–456.PubMedGoogle Scholar
  84. 84.
    Groggel, G. C., Marinedes, G. M., Hovingh, P., Hammond, E., and Linker, A. (1990) Inhibition of rat mesangial cell growth by heparan sulfate. Amer. J. Physiol. 258, F259–F265.PubMedGoogle Scholar
  85. 85.
    Groggel, G. C., Hovingh, P., Border, W. A., and Linker, A. (1987) Changes in glomerular heparan sulfate in puromycin aminonucleoside nephrosis. Amer. J. Path. 128, 521–527.PubMedGoogle Scholar
  86. 86.
    Groggel, G. C., Stevenson, J., Hovingh, P., Linker, A., and Border, W. A. (1988) Changes in heparan sulfate correlate with increased glomerular permeability. Kidney Int. 33, 517–523.PubMedCrossRefGoogle Scholar
  87. 87.
    Gesualdo, L., Pinzani, M., Floriano, J. J., Hassan, M. O., Nagy, N. U., Schena, F. P., et al. (1991) Platelet-derived growth factor expression in mesangial proliferative glomerulonephritis. Lab. Invest. 65, 160–167.PubMedGoogle Scholar
  88. 88.
    Lovett, D. H., Johnson, R. J., Marti, H. P., Martin, J., Davies, M., and Couser, W. G. (1992) Structural characterization of the mesangial cell type IV collagenase and enhanced expression in a model of mmune complex-mediated glomerulonephritis. Amer. J. Pathol. 141, 85–98.Google Scholar
  89. 89.
    Falk, R. J. and Jennette, J. C. (1988) Anti-neutrophil cytoplasmic autoantibodies with specificity for myeloperoxidase in patients with systemic vasculitis and idiopathic necrotizing and crescentic glomerulonephritis. N. Engl. J. Med. 318, 1651–1657.PubMedCrossRefGoogle Scholar
  90. 90.
    Falk, R. J., Terrell, R. S., Charles, L. A., and Jennette, J. C. (1990) Anti-neutrophil cytoplasmic autoantibodies induce neutrophils to degranulate and produce oxygen radicals in vitro. Proc. Natl. Acad. Sci. USA 87, 4115–4119.PubMedCrossRefGoogle Scholar
  91. 91.
    Ewert, B., Jennette, J. C., and Falk, R. (1992) Anti-myeloperoxidase antibodies stimulate neutrophils to damage human endothelial cells. Kidney Int. 41, 375–383.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1999

Authors and Affiliations

  • Gerald C. Groggel

There are no affiliations available

Personalised recommendations