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. 1992 Nov;90(2):312–318. doi: 10.1111/j.1365-2249.1992.tb07948.x

Passive immunization against tumour necrosis factor-alpha (TNF-alpha) and IL-1 beta protects from LPS enhancing glomerular injury in nephrotoxic nephritis in rats.

A M Karkar 1, Y Koshino 1, S J Cashman 1, A C Dash 1, J Bonnefoy 1, A Meager 1, A J Rees 1
PMCID: PMC1554602  PMID: 1385027

Abstract

Glomerular injury caused by injection of heterologous anti-glomerular basement membrane antibodies (anti-GBM Ab) is increased in rats pretreated with small doses of bacterial lipopolysaccharide (LPS). We have investigated the involvement of tumour necrosis factor-alpha (TNF-alpha), IL-1 alpha and IL-1 beta in this phenomenon by passive immunization against these cytokines. Anti-TNF-alpha or anti-IL-1 beta antibodies given 1.5 h before the induction of nephritis significantly decreased injury in this model, whether assessed by the magnitude of albuminuria, the prevalence of glomerular capillary thrombi or the intensity of glomerular neutrophil infiltrate. Albuminuria in anti-GBM Ab alone was 11 +/- 3, LPS/anti-GBM Ab 87 +/- 22, and anti-TNF-alpha antibodies/LPS/anti-GBM Ab 21 +/- 6 mg/24 h (mean +/- s.e.) P < 0.05. Passive immunization with antibodies to IL-1 beta had a similar effect (anti-GBM Ab, 0.6 +/- 0.1, LPS/anti-GBM Ab, 92 +/- 19, anti-IL-1 beta antibodies/LPS/anti-GBM Ab 39 +/- 8 mg/24 h, P < 0.05). The prevalence of glomerular capillary thrombi was also reduced significantly by these treatments; from 22 +/- 5% to 4 +/- 1% in the case of anti-TNF-alpha antibodies and 28 +/- 5% to 13 +/- 4% with anti-IL-1 beta antibodies. Similarly, the glomerular neutrophil infiltrate was also reduced by these treatments; from 42 +/- 3 to 25 +/- 1 in the case of anti-TNF-alpha and 47 +/- 2 to 30 +/- 1 with anti-IL-1 beta antibodies. In contrast, passive immunization against IL-1 alpha had no effect on either albumin excretion (4 +/- 3, 83 +/- 22 and 77 +/- 24 mg/24 h), glomerular capillary thrombi (2 +/- 1; 19 +/- 5 and 16 +/- 3) or glomerular neutrophil infiltrate (22 +/- 3; 47 +/- 5 and 48 +/- 5 from the three groups respectively). These results demonstrate that enhanced antibody mediated injury in the kidney is modulated by TNF-alpha and IL-1 beta but not by IL-1 alpha.

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Selected References

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  1. Baumann H., Onorato V., Gauldie J., Jahreis G. P. Distinct sets of acute phase plasma proteins are stimulated by separate human hepatocyte-stimulating factors and monokines in rat hepatoma cells. J Biol Chem. 1987 Jul 15;262(20):9756–9768. [PubMed] [Google Scholar]
  2. Beasley D., Dinarello C. A., Cannon J. G. Interleukin-1 induces natriuresis in conscious rats: role of renal prostaglandins. Kidney Int. 1988 Jun;33(6):1059–1065. doi: 10.1038/ki.1988.111. [DOI] [PubMed] [Google Scholar]
  3. Bergh A., Söder O. Interleukin-1 beta but not interleukin-1 alpha, induces acute inflammation-like changes in the testicular microcirculation of adult rats. J Reprod Immunol. 1990 Apr;17(2):155–165. doi: 10.1016/0165-0378(90)90033-3. [DOI] [PubMed] [Google Scholar]
  4. Beutler B., Milsark I. W., Cerami A. C. Passive immunization against cachectin/tumor necrosis factor protects mice from lethal effect of endotoxin. Science. 1985 Aug 30;229(4716):869–871. doi: 10.1126/science.3895437. [DOI] [PubMed] [Google Scholar]
  5. Boraschi D., Villa L., Volpini G., Bossù P., Censini S., Ghiara P., Scapigliat G., Nencioni L., Bartalini M., Matteucci G. Differential activity of interleukin 1 alpha and interleukin 1 beta in the stimulation of the immune response in vivo. Eur J Immunol. 1990 Feb;20(2):317–321. doi: 10.1002/eji.1830200213. [DOI] [PubMed] [Google Scholar]
  6. Cotran R. S., Pober J. S. Effects of cytokines on vascular endothelium: their role in vascular and immune injury. Kidney Int. 1989 Apr;35(4):969–975. doi: 10.1038/ki.1989.80. [DOI] [PubMed] [Google Scholar]
  7. De Young L. M., Spires D. A., Kheifets J., Terrell T. G. Biology and pharmacology of recombinant human interleukin-1 beta-induced rat ear inflammation. Agents Actions. 1987 Aug;21(3-4):325–327. doi: 10.1007/BF01966505. [DOI] [PubMed] [Google Scholar]
  8. Dinarello C. A., Cannon J. G., Wolff S. M., Bernheim H. A., Beutler B., Cerami A., Figari I. S., Palladino M. A., Jr, O'Connor J. V. Tumor necrosis factor (cachectin) is an endogenous pyrogen and induces production of interleukin 1. J Exp Med. 1986 Jun 1;163(6):1433–1450. doi: 10.1084/jem.163.6.1433. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dinarello C. A. Interleukin-1 and its biologically related cytokines. Adv Immunol. 1989;44:153–205. doi: 10.1016/s0065-2776(08)60642-2. [DOI] [PubMed] [Google Scholar]
  10. El Nahas A. M., Lechler R., Zoob S. N., Rees A. J. Progression to renal failure after nephrotoxic nephritis in rats studied by renal transplantation. Clin Sci (Lond) 1985 Jan;68(1):15–21. doi: 10.1042/cs0680015. [DOI] [PubMed] [Google Scholar]
  11. Fong Y., Tracey K. J., Moldawer L. L., Hesse D. G., Manogue K. B., Kenney J. S., Lee A. T., Kuo G. C., Allison A. C., Lowry S. F. Antibodies to cachectin/tumor necrosis factor reduce interleukin 1 beta and interleukin 6 appearance during lethal bacteremia. J Exp Med. 1989 Nov 1;170(5):1627–1633. doi: 10.1084/jem.170.5.1627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gauthier F., Mouray H. Rat alpha2 acute-phase macroglobulin. Isolation and physicochemical properties. Biochem J. 1976 Dec 1;159(3):661–665. doi: 10.1042/bj1590661. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Grau G. E., Fajardo L. F., Piguet P. F., Allet B., Lambert P. H., Vassalli P. Tumor necrosis factor (cachectin) as an essential mediator in murine cerebral malaria. Science. 1987 Sep 4;237(4819):1210–1212. doi: 10.1126/science.3306918. [DOI] [PubMed] [Google Scholar]
  14. Heim W. G. Relation between rat slow alpha-2-globulin and alpha-2-macroglobulin of other mammals. Nature. 1968 Mar 16;217(5133):1057–1059. doi: 10.1038/2171057a0. [DOI] [PubMed] [Google Scholar]
  15. Kopaniak M. M., Issekutz A. C., Movat H. Z. Kinetics of acute inflammation induced by E coli in rabbits. Quantitation of blood flow, enhanced vascular permeability, hemorrhage, and leukocyte accumulation. Am J Pathol. 1980 Feb;98(2):485–498. [PMC free article] [PubMed] [Google Scholar]
  16. Long N. C., Otterness I., Kunkel S. L., Vander A. J., Kluger M. J. Roles of interleukin 1 beta and tumor necrosis factor in lipopolysaccharide fever in rats. Am J Physiol. 1990 Oct;259(4 Pt 2):R724–R728. doi: 10.1152/ajpregu.1990.259.4.R724. [DOI] [PubMed] [Google Scholar]
  17. Mahadevan V., Malik S. T., Meager A., Fiers W., Lewis G. P., Hart I. R. Role of tumor necrosis factor in flavone acetic acid-induced tumor vasculature shutdown. Cancer Res. 1990 Sep 1;50(17):5537–5542. [PubMed] [Google Scholar]
  18. Miller T. J., Stone H. O. The rapid isolation of ribonuclease-free immunoglobulin G by protein A-sepharose affinity chromatography. J Immunol Methods. 1978;24(1-2):111–125. doi: 10.1016/0022-1759(78)90092-3. [DOI] [PubMed] [Google Scholar]
  19. Movat H. Z., Burrowes C. E., Cybulsky M. I., Dinarello C. A. Acute inflammation and a Shwartzman-like reaction induced by interleukin-1 and tumor necrosis factor. Synergistic action of the cytokines in the induction of inflammation and microvascular injury. Am J Pathol. 1987 Dec;129(3):463–476. [PMC free article] [PubMed] [Google Scholar]
  20. Movat H. Z., Cybulsky M. I., Colditz I. G., Chan M. K., Dinarello C. A. Acute inflammation in gram-negative infection: endotoxin, interleukin 1, tumor necrosis factor, and neutrophils. Fed Proc. 1987 Jan;46(1):97–104. [PubMed] [Google Scholar]
  21. Okusawa S., Gelfand J. A., Ikejima T., Connolly R. J., Dinarello C. A. Interleukin 1 induces a shock-like state in rabbits. Synergism with tumor necrosis factor and the effect of cyclooxygenase inhibition. J Clin Invest. 1988 Apr;81(4):1162–1172. doi: 10.1172/JCI113431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Piguet P. F., Grau G. E., Allet B., Vassalli P. Tumor necrosis factor/cachectin is an effector of skin and gut lesions of the acute phase of graft-vs.-host disease. J Exp Med. 1987 Nov 1;166(5):1280–1289. doi: 10.1084/jem.166.5.1280. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Pinching A. J., Rees A. J., Pussell B. A., Lockwood C. M., Mitchison R. S., Peters D. K. Relapses in Wegener's granulomatosis: the role of infection. Br Med J. 1980 Sep 27;281(6244):836–838. doi: 10.1136/bmj.281.6244.836. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Praga M., Gutierrez-Millet V., Navas J. J., Ruilope L. M., Morales J. M., Alcazar J. M., Bello I., Rodicio J. L. Acute worsening of renal function during episodes of macroscopic hematuria in IgA nephropathy. Kidney Int. 1985 Jul;28(1):69–74. doi: 10.1038/ki.1985.120. [DOI] [PubMed] [Google Scholar]
  25. Ramilo O., Sáez-Llorens X., Mertsola J., Jafari H., Olsen K. D., Hansen E. J., Yoshinaga M., Ohkawara S., Nariuchi H., McCracken G. H., Jr Tumor necrosis factor alpha/cachectin and interleukin 1 beta initiate meningeal inflammation. J Exp Med. 1990 Aug 1;172(2):497–507. doi: 10.1084/jem.172.2.497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Rees A. J., Lockwood C. M., Peters D. K. Enhanced allergic tissue injury in Goodpasture's syndrome by intercurrent bacterial infection. Br Med J. 1977 Sep 17;2(6089):723–726. doi: 10.1136/bmj.2.6089.723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Schirmer W. J., Schirmer J. M., Fry D. E. Recombinant human tumor necrosis factor produces hemodynamic changes characteristic of sepsis and endotoxemia. Arch Surg. 1989 Apr;124(4):445–448. doi: 10.1001/archsurg.1989.01410040055012. [DOI] [PubMed] [Google Scholar]
  28. Taverne J., Matthews N., Depledge P., Playfair J. H. Malarial parasites and tumour cells are killed by the same component of tumour necrosis serum. Clin Exp Immunol. 1984 Aug;57(2):293–300. [PMC free article] [PubMed] [Google Scholar]
  29. Tomosugi N. I., Cashman S. J., Hay H., Pusey C. D., Evans D. J., Shaw A., Rees A. J. Modulation of antibody-mediated glomerular injury in vivo by bacterial lipopolysaccharide, tumor necrosis factor, and IL-1. J Immunol. 1989 May 1;142(9):3083–3090. [PubMed] [Google Scholar]
  30. Tracey K. J., Beutler B., Lowry S. F., Merryweather J., Wolpe S., Milsark I. W., Hariri R. J., Fahey T. J., 3rd, Zentella A., Albert J. D. Shock and tissue injury induced by recombinant human cachectin. Science. 1986 Oct 24;234(4775):470–474. doi: 10.1126/science.3764421. [DOI] [PubMed] [Google Scholar]
  31. Tracey K. J., Fong Y., Hesse D. G., Manogue K. R., Lee A. T., Kuo G. C., Lowry S. F., Cerami A. Anti-cachectin/TNF monoclonal antibodies prevent septic shock during lethal bacteraemia. Nature. 1987 Dec 17;330(6149):662–664. doi: 10.1038/330662a0. [DOI] [PubMed] [Google Scholar]
  32. Uehara A., Gottschall P. E., Dahl R. R., Arimura A. Stimulation of ACTH release by human interleukin-1 beta, but not by interleukin-1 alpha, in conscious, freely-moving rats. Biochem Biophys Res Commun. 1987 Aug 14;146(3):1286–1290. doi: 10.1016/0006-291x(87)90788-1. [DOI] [PubMed] [Google Scholar]
  33. Ulich T. R., del Castillo J., Keys M., Granger G. A., Ni R. X. Kinetics and mechanisms of recombinant human interleukin 1 and tumor necrosis factor-alpha-induced changes in circulating numbers of neutrophils and lymphocytes. J Immunol. 1987 Nov 15;139(10):3406–3415. [PubMed] [Google Scholar]
  34. Vargas R., Thomson K. J., Wilson D., Cameron J. S., Turner D. R., Gill D., Chantler C., Ogg C. S. Mesangiocapillary glomerulonephritis with dense "deposits" in the basement membranes of the kidney. Clin Nephrol. 1976 Feb;5(2):73–82. [PubMed] [Google Scholar]
  35. Wankowicz Z., Megyeri P., Issekutz A. Synergy between tumour necrosis factor alpha and interleukin-1 in the induction of polymorphonuclear leukocyte migration during inflammation. J Leukoc Biol. 1988 Apr;43(4):349–356. doi: 10.1002/jlb.43.4.349. [DOI] [PubMed] [Google Scholar]
  36. Ward P. S., Fuller R. W., Ritter J. M., Cashman S. J., Rees A. J., Dollery C. T. Excretion of metabolites of prostacyclin and thromboxane by rats with nephrotoxic nephritis: effects of interleukin-1. Br J Pharmacol. 1991 Jul;103(3):1663–1668. doi: 10.1111/j.1476-5381.1991.tb09844.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. di Giovine F. S., Duff G. W. Interleukin 1: the first interleukin. Immunol Today. 1990 Jan;11(1):13–20. doi: 10.1016/0167-5699(90)90005-t. [DOI] [PubMed] [Google Scholar]

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