Summary
Inflammation, the reaction of vascularized tissue to local injury, not only limits the effects of injury; it may also be the underlying pathological process which initiates or sustains disease. In this paper, the evidence is reviewed for a role for nitric oxide (NO) as a chemical indicator of inflammation and inflammatory diseases.
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Albina, J. E., Abate, J. A. & Henry, W. L. (1991) Nitric oxide production is required for murine resident peritoneal macrophages to suppress mitogen-stimulated T cell proliferation. J. Immunol. 147, 144–8.
Bandaletova, T., Brouet, I., Bartsch, H., Sugimura, T., Esumi, H. & Ohshima, H. (1993) Immunohistochemical localization of an inducible form of nitric oxide synthase in various organs of rats treated with Propionibacterium acnes and lipopolysaccharide. APMIS 101, 330–6.
Belenky, S. N., Robbins, R. A., Rennard, S. I., Gossman, G. L., Nelson, K. J. & Rubinstein, I. (1993a) Inhibitors of nitric oxide synthase attenuate human neutrophil chemotaxis in vitro. J. Lab. Clin. Med 122, 388–94.
Belenky, S. N., Robbins, R. A. & Rubinstein, I. (1993b) Nitric oxide synthase inhibitors attenuate human monocyte chemotaxis in vitro. J. Leuko. Biol. 53, 498–503.
Boughton-Smith, N. K., Evans, S. M., Hawkey, C. J., Cole, A. T., Balsitis, M., Whittle, B. J. R. & Moncada, S. (1993) Nitric oxide synthase activity in ulcerative colitis and Crohn's disease. Lancet 342, 338–40.
Cattell, V. & Cook, H. T. (1993) Nitric oxide: role in the physiology and pathology of the glomerulus. Exp. Nephrol. 1, 265–80.
Cattell, V., Cook, T. & Moncada, S. (1990) Glomeruli synthesize nitrite in experimental nephrotoxic nephritis. Kid. Int. 38, 1056–60.
Charles, I. G., Palmer, R. M. J., Hickery, M. S., Bayliss, M. T., Chubb, A. P., Hall, V. S., Moss, D. W. & Moncada, S. (1993) Cloning, characterization and expression of a cDNA encoding an inducible nitric oxide synthase from the human chondrocyte. Proc. Natl Acad. Sci. USA 90, 11 419–23.
Cook, H. T., Ebrahim, H., Jansen, A. S., Foster, G. R., Largen, P. & Cattell, V. (1994a) Expression of the gene for inducible nitric oxide synthase in experimental glomerulonephritis in the rat. Clin. Exp. Immunol 97, 315–20.
Cook, H. T., Bune, A. J., Jansen, A. S., Taylor, G. M., Loi, R. K. & Cattell, V. (1994b) Cellular localisation of inducible nitric oxide synthase in experimental endotoxic shock in the rat. Clin. Sci. 87, 179–86.
DiRosa, M., Moncada, S. & Ialenti, A. (1993) Modulation of acute and chronic inflammation by endogenous nitric oxide. In Nitric Oxide: Brain and Immune System (edited by Moncada, S. et al.), pp. 231–6. London: Portland Press Proceedings.
Evans, T. G., Thai, L., Granger, D. L. & Hibbs, J. B. (1993) Effect of in vivo inhibition of nitric oxide production in murine leishmaniasis. J. Immunol. 151, 907–15.
Farrell, A. J., Blake, D. R., Palmer, R. M. & Moncada, S. (1992) Increased concentrations of nitrite in synovial fluid and serum samples suggest increased nitric oxide synthesis in rheumatic diseases. Ann. Rheum. Dis. 51, 1219–22.
Garside, P., Hutton, A. K., Severn, A., Liew, F. Y. & Mowat, A. M. (1992) Nitric oxide mediates intestinal pathology in graft-vs-host disease. Eur. J. Immunol. 22, 2141–5.
Geller, D. A., Lowenstein, C. J., Shapiro, R. A., Nussler, A. K., DiSilvio, M., Wang, S. C., Nakayama, D. K., Simmons, R. L., Snyder, S. H. & Billiar, T. R. (1993) Molecular cloning and expression of inducible nitric oxide synthase from human hepatocytes. Proc. Natl Acad. Sci. USA 90, 3491–5.
Green, S. J. & Nacy, C. A. (1993) Antimicrobial and immunopathologic effects of cytokine-induced nitric oxide synthesis. Curr. Opin. Inf. Dis. 6, 384–96.
Hamid, Q., Springall, D. R., Riveros-Moreno, V., Chanez, P., Howarth, P., Redington, A., Bousquet, J., Godard, P., Holgate, S. & Polak, J. M. (1993) Induction of nitric oxide synthase in asthma. Lancet 342, 1510–3.
Harbrecht, B. G., Billiar, T. R., Stadler, J., Demetris, A. J., Ochoa, J., Curran, R. D. & Simmons, R. L. (1992) Inhibition of nitric oxide synthesis during endotoxemia promotes intrahepatic thrombosis and an oxygen radical-mediated hepatic injury. J. Leukoc. Biol. 52, 390–4.
Hibbs, J. B., Westenfelder, C., Taintor, R., Vavrin, Z., Kablitz, C., Baranowski, R. L., Ward, J. H., Menlove, R. L., Mcmurry, M. P., Kushner, J. P. & Samlowski, W. E. (1992) Evidence for cytokine inducible nitric oxide synthesis from {spl-arginine in patients receiving interleukin-2 therapy}. Clin. Invest. 89, 867–77.
Hoffman, R. A., Langrehr, J. M., Billiar, T. R., Curran, R. D. & Simmons, R. L. (1990) Alloantigen-induced activation of rat splenocytes is regulated by the oxidative metabolism of {spl-arginine}. J. Immunol. 145, 2220–6.
Ialenti, A., Ianaro, A., Moncada, S. & DiRosa, M. (1992) Modulation of acute inflammation by endogenous nitric oxide. Eur. J. Pharm. 211, 177–82.
Ialenti, A., Moncada, S. & DiRosa, M. (1993) Modulation of adjuvant arthritis by endogenous nitric oxide. Br. J. Pharmacol. 110, 701–6.
Jansen, A., Cook, T., Taylor, G. M., Largen, P., Riveros-Moreno, V., Moncada, S. & Cattell, V. (1994) Induction of nitric oxide synthase in rat immune complex glomerulonephritis. Kidney Int. 45, 1215–9.
Kaplan, S. S., Billiar, T., Curran, R. D., Zdziarski, U. E., Simmons, R. L. & Basford, R. E. (1989) Blood 74, 1885–7.
Ketteler, M., Narita, I., Border, W. A. & Noble, N. A. (1993) Nitric oxide-inhibition prevents mesangial cell lysis in experimental glomerulonephritis. J. Am. Soc. Nephrol. 4, 610.
Kilbourn, R. G. & Griffith, O. W. (1992) Overproduction of nitric oxide in cytokine-mediated and septic shock. J. Natl Can. Inst. 84, 827–31.
Kilbourn, R. G., Jubran, A., GrossS. S., Griffith, O. W., Levi, R., Adams, J. & Lodato, R. F. (1990) Reversal of endotoxin mediated shock by NG-methyl-l-arginine, an inhibitor of nitric oxide synthesis. Biochem. Biophys. Res. Commun. 172, 1132–8.
Kirk, S. J., Regan, M. C. & Barbul, A. (1990) Cloned murine T lymphocytes synthesize a molecule with the biological characteristics of nitric oxide. Biochem. Biophys. Res. Comm. 173, 660–5.
Koprowski, H., Mu Zheng, Y., Heber-Katz, E., Fraser, N., Rorke, L., Fang Fu, Z., Hanlonc & Dietzschold, B. (1993) In vivo expression of inducible nitric oxide synthase in experimentally induced neurologic diseases. Proc. Natl Acad. Sci. USA 90, 3024–7.
Kubes, P., Suzuki, M. & Granger, D. N. (1991) Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc. Natl Acad. Sci. USA 88, 4651–5.
Langrehr, J. M., Hoffman, R. A., Lancaster, J. R. & Simmons, R. L. (1993) Nitric oxide — a new endogenous immunomodulator. Transplantation 55, 1205–12.
Mccartney-Francis, N., Allen, J. B., Mizel, D. E., Albina, J. E., Xie, Q-W., Nathan, C. F. & Wahl, S. M. (1993) Suppression of arthritis by an inhibitor of nitric oxide synthase. J. Exp. Med. 178, 749–54.
Macmicking, J. D., Willenborg, D. O., Weidemann, M. J., Rockett, K. A. & Cowden, W. B. (1992) Elevated secretion of reactive nitrogen and oxygen intermediates by inflammatory leukocytes in hyperacute experimental autoimmune encephalomyelitis: enhancement by the soluble products of encephalitogenic T cells. J. Exp. Med. 176, 303–7.
Mcnamara, D. B., Bedi, B., Aurora, H., Tena, L., Ignarro, L. J., Kadowitz, P. J. & Akers, D. L. (1993) l-arginine inhibits balloon catheter-induced intimal hyperplasia. Biochem. Biophys. Res. Comm. 193, 291–6.
Miller, M. J. S., Sadowska-Krowicka, H., Chotinaruemol, S., Kakkis, J. L. & ClarkD. A. (1993) Amelioration of chronic ileitis by nitric oxide synthase inhibition. J. Pharmacol. 264, 11–6.
Mills, C. D. (1991) Molecular basis of ‘suppressor’ macrophages; arginine metabolism via the nitric oxide synthetase pathway. J. Immunol. 146, 2719–23.
Mulligan, M. S., Hevel, J. M., Marletta, M. A. & Ward, P. A. (1991) Tissue injury caused by deposition of immune complexes is l-arginine dependent. Proc. Natl Acad. Sci. USA 88, 6338–42.
Mulligan, M. S., Warren, J. S., Smith, C. W., Anderson, D. C., Grace, C., Rudolph, A. R. & Ward, P. A. (1992) Lung injury after deposition of IgA immune complexes. J. Immunol. 148, 3086–92.
Nathan, C. (1992) Nitric oxide as a secretory product of mammalian cells. FASEB J. 6, 3051–64.
Nicholson, A. G., Haites, N. E., Mckay, N. G., Wilson, H. M., Macleod, A. M. & Benjamin, N. (1993) Induction of nitric oxide synthase in human mesangial cells. Biochem. Biophys. Res. Comm. 193, 1269–74.
Nussler, A. K., Renia, L., Pasquetto, V., Miltgen, F., Matile, H. & Mazier, D. (1993) In vivo induction of the nitric oxide pathway in hepatocytes after injection with irradiated malaria sporozoites, malaria blood parasites or adjuvants. Eur. J. Immunol. 23, 882–7.
Ohshima, H., Brouet, I. M., Bandaletova, T., Adachi, H., Oguchi, S., Lida, S., Kurashima, Y., Morishita, Y., Sugimura, T. & Esumi, H. (1992) Polyclonal antibody against an inducible form of nitric oxide synthase purified from the liver of rats treated with Propionibacterium acnes and lipopolysaccharide. Biochem. Biophys. Res. Commun. 187, 1291–7.
Petros, A., Bennett, D. & Vallance, P. (1991) Effect of nitric oxide synthase inhibitors on hypotension in patients with septic shock. Lancet 338, 1557–8.
Pipili-Synetos, E., Sakkoula, E. & Maragoudakis, M. E. (1993) Nitric oxide is involved in the regulation of angiogenesis. Br. J. Pharmacol. 108, 855–7.
Schultz, P. J. & Raij, L. (1992) Endogenously synthesized nitric oxide prevents endotoxin-induced glomerular thrombosis. J. Clin. Invest. 90, 1718–25.
Sherman, P. A., Laubach, V. E., Reep, B. R. & Wood, E. R. (1993) Purification and cDNA sequence of an inducible nitric oxide synthase from a human tumour cell line. Biochemistry 32, 11 600–5.
Shi, Y., Li, H., Shen, C., Wang, J., Qin, S., Liu, R. & Pan, J. (1993) Plasma nitric oxide levels in newborn infants with sepsis. J. Pediatr. 123, 435–8.
Stefani, M. M. A., Muller, I. & Louis, J. A. (1994) Leishmania major-specific CD8+ T cells are inducers and targets of nitric oxide produced by parasitized macrophages. Eur. J. Immunol. 24, 746–52.
Taylor-Robinson, A. W., Liew, F. Y., Severn, A., XuDamo, Mcsorley, S. J., Garside, P., Padron, J. & Phillips, R. S. (1994) Regulation of the immune response of nitric oxide differentially produced by T helper type 1 and T helper type 2 cells. Eur. J. Immunol. 24, 980–4.
Warren, J. B., Loi, R. K. & Coughlan, M. L. (1993) Involvement of nitric oxide synthase in the delayed vasodilator response to ultraviolet light irradiation of rat skin in vivo. Br. J. Pharm. 109, 802–6.
WrenS. M., Hoffman, R. A., Billiar, T. R., AbouEl Ezz, A., Hronakes, M. L. & Ildstad, S. T. (1992) T-cell mitogenic responses in fully xenogeneic chimeras (WF RAT → B10 mouse) are restored by blocking the l-arginine-dependent nitric oxide pathway. Trans. Proc. 24, 499–500.
Wright, C. E., Rees, D. D. & Moncada, S. (1992) Protective and pathological roles of nitric oxide in endotoxin shock. Cardiovasc. Res. 26, 48–57.
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Cattell, V., Jansen, A. Inducible nitric oxide synthase in inflammation. Histochem J 27, 777–784 (1995). https://doi.org/10.1007/BF00171758
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DOI: https://doi.org/10.1007/BF00171758