Inducible nitric oxide synthase in pulmonary alveolar macrophages from patients with tuberculosis

Journal of Experimental Medicine

Volumn 183, Issue 5, 1996, Pages 2293-2302

  Nicholson, Susan ^a   Bonecini Almeida, Maria Da Glória ^a   Lapa E Silva, Jose Roberto ^b   Nathan, Carl ^a   Xie, Qiao Wen ^a   Mumford, Richard ^d   Weidner, Jeffrey R ^d   Calaycay, Jimmy ^d   Geng, Jiayuan ^a   Boechat, Neio ^b   Linhares, Cristiane ^b   Rom, William ^c   Ho, John L ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d MERCK RESEARCH LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; NITRIC OXIDE SYNTHASE;

ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; HOST RESISTANCE; HUMAN; HUMAN CELL; LUNG ALVEOLUS MACROPHAGE; LUNG LAVAGE; LUNG TUBERCULOSIS; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES; BASE SEQUENCE; CELL LINE; CELLS, CULTURED; DIHYDROLIPOAMIDE DEHYDROGENASE; DNA PRIMERS; ENDOTHELIUM, VASCULAR; HUMANS; IMMUNOHISTOCHEMISTRY; ISOENZYMES; LUNG; MACROPHAGES, ALVEOLAR; MACROPHAGES, PERITONEAL; MICE; MICE, INBRED STRAINS; MOLECULAR SEQUENCE DATA; NITRIC OXIDE SYNTHASE; OLIGOPEPTIDES; PEPTIDE FRAGMENTS; POLYMERASE CHAIN REACTION; RABBITS; RECOMBINANT PROTEINS; REFERENCE VALUES; RNA, MESSENGER; TRANSCRIPTION, GENETIC; TUBERCULOSIS, PULMONARY;

EID: 15844380037     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.183.5.2293     Document Type: Article

References (59)

1. Raviglione, M.C., D.E. Snider, Jr., and A. Kochi. 1995. Global epidemiology of tuberculosis. Morbidity and mortality of a worldwide epidemic. JAMA (J. Am. Med. Assoc.). 273:220-226.
2. Nathan, C. 1995. Natural resistance and nitric oxide. Cell. 82:873-876.
3. Degroote, M.A., and F.C. Fang. 1995. NO inhibitions: antimicrobial properties of nitric oxide Clin. Infect. Dis. 21 (Sup. 2):S162-165.
4. MacMicking, J.D., C. Nathan, G. Hom, N. Chartrain, M. Trumbauer, K. Stevens, Q.-w. Xie, K. Sokol, D.S. Fletcher, N. Hutchinson, H. Chen, and J.S. Mudgett. 1995. Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase. Cell. 81:641-650.
5. Wei, X.Q., I.G. Charles, A. Smith, J. Ure, G.J. Feng, F.P. Huang, D. Xu, W. Muller, S. Moncada, and F.Y. Liew. 1995. Altered immune responses in mice lacking inducible nitric oxide synthase. Nature (Lond.). 375:408-411.
6. Flesch, I.E., and S.H. Kaufmann. 1991. Mechanisms involved in mycobacterial growth inhibition by gamma interferon-activated bone marrow macrophages: role of reactive nitrogen intermediates. Infect. Immun. 59:3213-3218.
7. Chan, J., J. Flynn, K.J. Triebold, D.K. Dalton, T.A. Stewart, and B.R. Bloom. 1993. An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J. Exp. Med. 178:2249-2254.
8. Chan, J., K. Tanaka, D. Carroll, J. Flynn, and B.R. Bloom. 1995. Effects of nitric oxide synthase inhibitors on murine infection with Mycobacterium tuberculosis. Infect. Immun. 63: 736-740.
9. Greenberg, S.S., J. Xie, J. Kolls, C. Mason, and P. Didier. 1995. Rapid induction of mRNA for nitric oxide synthase II in rat alveolar macrophages by intratracheal administration of Mycobacterium tuberculosis and Mycobacterium avium. Proc. Soc. Exp. Biol. Med. 209:46-53.
10. Cooper, A.M., D.K. Dalton, T.A. Stewart, J.P. Griffin, D.G. Russell, and I.M. Orme. 1993. Disseminated tuberculosis in interferon gamma gene-disrupted mice. J. Exp. Med 178: 2243-2247.
11. Kamijo, R., J. Le, D. Shapiro, E.A. Havell, S. Huang, M. Aguet, M. Bosland, and J. Vilcek. 1993. Mice that lack the interferon-gamma receptor have profoundly altered responses to infection with Bacillus Calmette-Guerin and subsequent challenge with lipopolysaccharide. J. Exp. Med. 178:1435-1440.
12. Kamijo, R., H. Harada, T. Matsuyama, M. Bosland, J. Gerecitano, D. Shapiro, J. Le, K.S. Im, T. Kimura, S. Green, T.W. Mak, T. Taniguchi ,and J. Vilcek. 1994. Requirement for transcription factor IRF-1 in NO synthase induction in macrophage. Science (Wash. DC). 263:1612-1615.
13. Denis, M. 1994. Human monocytes/macrophages: NO or no NO? J. Leuk. Biol. 55:682-684.
14. Schoedon, G., M. Schneemann, R. Walter, N. Blau, S. Hofer, and A. Schaffner. 1995. Nitric oxide and infection: another view. Clin. Infect. Dis. 21 (Suppl. 2):5152-5157.
15. Dugas, B., M.D. Mossalayi, C. Damais, and J.-P. Kolb. 1995. Nitric oxide production by human monocyte: evidence for a role of CD23. Immunol. Today. 16:574-580.
16. Denis, M. 1991. Tumor necrosis factor and granulocyte macrophage-colony stimulating factor stimulate human macrophages to restrict growth of virulent Mycobacterium avium and to kill a virulent M. avium. J. Leuk. Biol. 49:380-387.
17. Sherman, M.P., M.L. Loro, V.Z. Wong, and D.P. Tashkin. 1991. Cytokine- and Pneumocystis carinii-induced L-arginine oxidation by murine and human pulmonary alveolar macrophages. J. Protozool. 38:234-236.
18. Muñoz-Fernandez, M.A., M.A. Fernandez, and M. Fresno. 1992. Activation of human macrophages for the killing of intracellular Trypanosoma cruzi by TNF-alpha and IFN-gamma through a nitric oxide-dependent mechanism. Immunol. Lett. 33:35-40.
19. Hunt, N.C.A., and R.D. Goldin. 1992. Nitric oxide production by monocytes in alcoholic liver disease. J. Hepatol. 14: 146-150.
20. Martin, J.H.J., and S.W. Edwards. 1993. Changes in mechanisms of monocyte/macrophage-mediated cytotoxicity during culture. J. Immunol. 150:3478-3486.
21. Weinberg, J.B., M.A. Misukonis, E.R. Wood, G.L. Smith, P.L. Shami, S.N. Mason, and D.L. Granger. 1993. Human mononuclear phagocyte nitric oxide synthase (NOS): evidence for induction of NOS mRNA and protein without detectable capacity for nitric oxide production. Blood. 82:186a. (Abstr.)
22. Pietraforte, D., E. Tritarelli, U. Testa, and M. Minetti. 1994. gp120 HIV envelope glycoprotein increases the production of nitric oxide in human monocyte-derived macrophages. J. Leuk. Biol. 55:175-182.
23. Zembala, M., M. Siedlar, J. Marcinkiewicz, and J. Pryjma. 1994. Human monocytes are stimulated for nitric oxide release in vitro by some tumor cells but not by cytokines and lipopolysaccharide. Eur. J. Immunol. 24:435-439.
24. De Maria, R., M.G. Cifone, R. Trotta, M.R. Rippo, C. Festucia, A. Santoni, and R. Testi. 1994. Triggering of human monocyte activation through CD69, a member of the natural killer cell gene complex family of signal transducing receptors. J. Exp. Med. 180:1999-2004.
25. Reiling, N., A.J. Ulmer, M. Duchrow, M. Ernst, H.-D. Flad, and S. Hauschildt. 1994. Nitric oxide synthase: mRNA expression of different isoforms in human monocytes/macrophages. Eur. J. Immunol. 24:1941-1944.
26. Kroncke, K.D., K. Fehsel, L. Alsdorff, and V. Kolb-Bachofen. 1994. Expression of inducible NO-synthase in human monocytes. Immunobiol. 191:267-268.
27. Peterson, P.K., S. Hu, W.R. Anderson, and C.C. Chao. 1994. Nitric oxide production and neurotoxicity mediated by activated microglia from human versus mouse brain. J. Inf. Dis. 170:457-460.
28. Mautino, G., N. Paul-Eugene, P. Chanez, A.M. Vignola, J.P. Kolb, J. Bousquet, and B. Dugas. 1994. Heterogeneous spontaneous and interleukin-4-induced nitric oxide production by human monocytes. J. Leuk. Biol. 56:15-20.
29. Perez-Mediavilla, L.A., M.J. Lopez-Zabalza, M. Calonge, L. Montuenga, N. Lopez-Moratalla, and E. Santiago. 1995. Inducible nitric oxide synthase in human lymphomononuclear cells activated by synthetic peptides derived from extracellular matrix proteins. FEBS Lett. 357:121-124.
30. Bukrinsky, M.I., H.D.L.M. Nottet, N. Schmidtmayerove, L. Dubrovsky, M.E. Mullins, S.A. Lipton, and H.E. Gendelman. 1994. Regulation of nitric oxide synthase activity in human immunodeficiency virus type 1 (HIV-1)-infected monocytes: implications for HIV-associated neurological disease. J. Exp. Med. 181:735-745.
31. Dumarey, C.H., V. Labrousse, N. Rastogi, B.B. Vargaftig, and M. Bachelet. 1994. Selective Mycobacterium avium-induced production of nitric oxide by human monocyte-derived macrophages. J. Leuk. Biol. 56:36-40.
32. Vouldoukis, I., V. Riveros-Moreno, B. Dugas, F. Ouaaz, P. Bécherel, P. Debré, S. Moncada, and M.D. Mossalayi. 1995. The killing of Leishmania major by human macrophages is mediated by nitric oxide induced after ligation of the FcεRII/ CD23 surface antigen. Proc. Natl. Acad. Sci. USA. 92:7804-7808.
33. Cameron, M.L., D.L. Granger, J.B. Weinberg, W.J. Kozumbo, and H.S. Koren. 1990. Human alveolar and peritoneal macrophages mediate fungistasis independently of L-arginine oxidation to nitrite or nitrate. Am. Rev. Respir. Dis. 142:1313-1319.
34. Padgett, E.L., and S.B. Pruett. 1992. Evaluation of nitrite production by human monocyte-derived macrophages. Biochem. Biophys. Res. Commun. 186:775-781.
35. Murray, H.W., and R.F. Teitelbaum. 1992. L-arginine-dependent reactive nitrogen intermediates and the antimicrobial effect of activated human mononuclear phagocytes. J. Inf. Dis. 165:513-517.
36. Schneemann, M., G. Schoedon, S. Hofer, N. Blau, L. Guerrero, and A. Schaffner. 1993. Nitric oxide synthase is not a constituent of the antimicrobial armature of human mononuclear phagocytes. J. Infect. Dis. 167:1358-1363.
37. Sakai, N., and S. Milstien. 1993. Availability of tetrahydrobiopterin is not a factor in the inability to detect nitric oxide production by human macrophages. Biochem. Biophys. Res. Commun. 193:378-383.
38. Albina, J.E. 1995. On the expression of nitric oxide synthase by human macrophages. Why no NO? J. Leuk. Biol. 58:643-649.
39. Miller, D.K., J.M. Ayala, L.A. Egger, S.M. Raju, T.T. Yamin, G.J. Ding, E.P. Gaffney, A.D. Howard, O.C. Palyha, A.M. Rolando et al. 1993. Purification and characterization of active human interleukin-1 beta-converting enzyme from THP.1 monocytic cells. J. Biol. Chem. 268:18062-18069.
40. Xie, Q.-w., H. Cho, J. Calaycay, R.A. Mumford, K.M. Swiderek, T.D. Lee, A. Ding, T. Troso, and C. Nathan. 1992. Cloning and characterization of inducible nitric oxide synthase from mouse macrophages. Science (Wash. DC). 256: 225-228.
41. Xie, Q.-w., H. Cho, Y. Kashiwabara, M. Baum, J.R. Weidner, K. Elliston, R. Mumford, and C. Nathan. 1994. Carboxyl terminus of inducible nitric oxide synthase: contribution to NADPH binding and enzymatic activity. J. Biol. Chem. 269:28500-28505.
42. Geller, D.A., C.J. Lowenstein, R.A. Shapiro, A.K. Nussler, M. DiSivio, S.C. Wang, D.K. Nakayama, R.L. Simmons, S.H. Snyder, and T.R. Billiar. 1993. Molecular cloning and expression of inducible nitric oxide synthase from human hepatocytes. Proc. Natl. Acad. Sci. USA. 90:3491-3495.
43. Marsden, P.A., K.T. Schappert, H.S. Chen, M. Flowers, C.L. Sundell, J.N. Wilcox, S. Lamas, and T. Michel. 1992. Molecular cloning and characterization of human endothelial nitric oxide synthase. FEBS Lett. 307:287-293
44. Chartrain, N.A., D.A. Geller, P.P. Koty, N.F. Sitrin, A.K. Nussler, E.P. Hoffman, T.R. Billiar, N.I. Hutchinson, and J.S. Mudgett. 1994. Molecular cloning, structure, and chromosomal localization of the human inducible nitric oxide synthase gene. J. Biol. Chem. 269:6765-6772.
45. Flesch, I.E., J.H. Hess, and S.H. Kaufmann. 1994. NADPH diaphorase staining suggests a transient and localized contribution of nitric oxide to host defence against an intracellular pathogen in situ. Int. Immunol. 6:1751-1757.
46. Stenger, S., H. Thuring, M. Rollinghoff, and C. Bogdan. 1994. Tissue expression of inducible nitric oxide synthase is closely associated with resistance to Leishmania major. J. Exp. Med. 180:783-793.
47. Klebanoff, S.J., and R.A. Clark. 1978. The Neutrophil: Function and Clinical Disorders. North-Holland Publishing Co., Amsterdam. 308-316.
48. 2 release by alveolar macrophages from sarcoid patients and by alveolar macrophages from normals after exposure to recombinant interferons α, β, γ, and 1,25-dihydroxyvitamin D3. J. Clin. Invest. 80:381-386.
49. Amin, A.R., P.E. Di Cesare, P. Vyas, M. Attur, E. Tzeng, T.R. Billiar, S.A. Stuchin, and S.B. Abramson. 1995. The expression and regulation of nitric oxide synthase in human osteoarthritis-affected chondrocytes: evidence for up-regulated neuronal nitric oxide synthase. J. Exp. Med. 182:2097-2102.
50. Nathan, C., and Q.-w. Xie, 1994. Minireview: regulation of biosynthesis of nitric oxide. J. Biol. Chem. 269:13725-13728.
51. Guo, F.H., H.R. De Raeve, T.W. Rice, D.J. Stuehr, B.J.M. Thunnissen, and S.C. Erzurum, 1995. Continuous nitric oxide synthesis by inducible nitric oxide synthase in normal human airway epithelium in vivo. Proc. Natl. Acad. Sci. USA. 92:7809-7813.
52. Vodovotz, Y., N.S. Kwon, M. Pospichil, J. Manning, J. Paik, and C. Nathan. 1994. Inactivation of nitric oxide synthase following prolonged incubation of mouse macrophages with interferon-gamma and bacterial lipopolysaccharide. J. Immunol. 152:4110-4118.
53. Asana, K., C.B. Chee, B. Gaston, C.M. Lilly, C. Gerard, J.M. Drazen, and J.S. Stamler. 1994. Constitutive and inducible nitric oxide synthase gene expression, regulation and activity in human lung epithelial cells. Proc. Natl. Acad. Sci. USA. 91:10089-10093.
54. Karupiah, G., Q.-W. Xie, R.M.L. Buller, C. Nathan, C. Duarte, and J. MacMicking. 1993. Inhibition of viral replication by interteron-γ-induced nitric oxide synthase. Science (Wash. DC). 261:1445-1448.
55. Doi, T., M. Ando, T. Akaike, M. Suga, K. Sato, and H. Maeda. 1993. Resistance to nitric oxide in Mycobacterium avium complex and its implications in pathogenesis. Infect. Immun. 61:1980-1989.
56. Hoffman, R.A, J.M. Langrehr, T.R. Billiar, R.D. Curran, and R.L. Simmons. 1990. Alloantigen-induced activation of rat splenocytes is regulated by the oxidative metabolism of L-arginine. J. Immunol. 145:2220-2226.
57. Heiss, L.N., J.R. Lancaster, Jr., J.A. Corbett, and W.E. Goldman. 1994. Epithelial autotoxicity of nitric oxide: role in the respiratory cytopathology of pertussis. Proc. Natl. Acad. Sci. USA. 91:267-270.
58. Royall, J.A., N.W. Kooy, and J.S. Beckman. 1995. Nitric oxide-related oxidants in acute lung injury. New Horiz. 3: 113-122.
59. Stamler, J.S., E. Loh, M.A. Roddy, K.E. Currie, and M.A. Creager. 1994. Nitric oxide regulates basal systemic and pulmonary vascular resistance in healthy humans. Circulation. 89: 2035-2040.