Essential role of induced nitric oxide in the initiation of the inflammatory response after hemorrhagic shock

Journal of Experimental Medicine

Volumn 187, Issue 6, 1998, Pages 917-928

  Hierholzer, Christian ^a   Harbrecht, Brian ^a   Menezes, John M ^a   Kane, John ^a   MacMicking, John ^e,f   Nathan, Carl F ^e   Peitzman, Andrew B ^a   Billiar, Timothy R ^a   Tweardy, David J ^b,c,d  

^a UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PITTSBURGH   (United States)

^d UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

^e WEILL CORNELL MEDICAL COLLEGE   (United States)

^f ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GRANULOCYTE COLONY STIMULATING FACTOR; INTERLEUKIN 6; N6 (IMINOETHYL)LYSINE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE INHIBITOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HEMORRHAGIC SHOCK; INFLAMMATION; LIVER INJURY; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; RESUSCITATION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ANIMALS; DNA-BINDING PROTEINS; GRANULOCYTE COLONY-STIMULATING FACTOR; INFLAMMATION; INTERLEUKIN-6; LUNG; MALE; MICE; MICE, KNOCKOUT; NF-KAPPA B; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; RATS; RATS, SPRAGUE-DAWLEY; SHOCK, HEMORRHAGIC; STAT3 TRANSCRIPTION FACTOR; TRANS-ACTIVATORS;

EID: 0032536875     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.187.6.917     Document Type: Article

References (38)

1. Chaudry, I.H., W. Ertel, and A. Ayala. 1993. Alterations in inflammatory cytokine production following hemorrhage and resuscitation. In Shock, Sepsis, and Organ Failure, Third Wiggers Bernard Conference. G. Schlag, H. Redl, and D.L. Traber, editors. Springer Verlag, Berlin. 73-127.
2. Cotran, R.S., V. Kumar, and S.L. Robbins, editors. 1989. Robbins Pathologic Basis of Disease. 4th ed. W.B. Saunders Company, Philadelphia. 39-71.
3. Le Tulzo, Y., R. Shenkar, D. Kaneko, P. Moine, G. Fantuzzi, C.A. Dinarello, and E. Abraham. 1997. Hemorrhage increases cytokine expression in lung mononuclear cells in mice: involvement of catecholamines in nuclear factor-κB regulation and cytokine expression. J. Clin. Invest. 99:1516-1524.
4. Deitch, E.A., J. Morrison, R. Berg, and R.D. Specian. 1990. Effect of hemorrhagic shock on bacterial translocation, intestinal morphology, and intestinal permeability in conventional and antibiotic-decontaminated rats. Crit. Care Med. 18:529-536.
5. Peitzman, A.B., A.O. Udekwu, J. Ochoa, and S. Smith. 1991. Bacterial translocation in trauma patients. J. Trauma. 31:1083-1087.
6. Lander, H.M. 1997. An essential role for free radicals and derived species in signal transduction. FASEB J. 11:118-124.
7. Kelly, E., N.S. Shah, N.N. Morgan, S.C. Watkins, A.B. Peitzman, and T.R. Billiar. 1997. Physiologic and molecular characterization of the role of nitric oxide in hemorrhagic shock: evidence that type II nitric oxide synthase does not regulate vascular decompensation. Shock. 7:157-163.
8. Thiemermann, C., C. Szabo, J.A. Mitchell, and J.R. Vane. 1993. Vascular hyporeactivity to vasoconstrictor agents and hemodynamic decompensation in hemorrhagic shock is mediated by nitric oxide. Proc. Nat. Acad. Sci. USA. 90:267-271.
9. Szabo, C. 1996. The pathophysiological role of peroxynitrite in shock, inflammation, and ischemia-reperfusion injury. Shock. 6:79-88.
10. Moore, W.M., R.K. Webber, G.M. Jerome, F.S. Tjoeng, T.P. Misko, and M.G. Currie. 1994. L-N6-(1-iminoethyl)lysine: a selective inhibitor of inducible nitric oxide synthase. J. Med. Chem. 37:3886-3888.
11. MacMicking, J.D., C. Nathan, G. Hom, N. Chartrain, D.S. Fletcher, M. Trumbauer, K. Stevens, Q.W. Xie, K. Sokol, N. Hutchinson, et al. 1995. Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase. Cell. 81:641-650. (See published erratum 81: 1170.)
12. Hierholzer, C., E. Kelly, K. Tsukada, E. Loeffert, S. Watkins, T. Billiar, and D. Tweardy. 1997. Hemorrhagic shock induces granulocyte colony-stimulating factor (G-CSF) expression in bronchial epithelium. Am. J. Physiol. 273:L1058-L1064.
13. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenolchloroform extraction. Anal. Biochem. 162:156-159.
14. Hierholzer, C., E. Kelly, T.R. Billiar, and D.J. Tweardy. 1997. Granulocyte colony-stimulating factor (G-CSF) production in hemorrhagic shock requires both the ischemic and resuscitation phase. Arch. Orth. Trauma Surg. 116:173-176.
15. Northemann, W., T.A. Braciak, M. Hattori, F. Lee, and G.H. Fey. 1989. Structure of the rat interleukin 6 gene and its expression in macrophage-derived cells. J. Biol. Chem. 264:16072-16082.
16. Adachi, H., S. Iida, S. Oguchi, H. Ohshima, H. Suzuki, K. Nagasaki, H. Kawasaki, T. Sugimura, and H. Esumi. 1993. Molecular cloning of a cDNA encoding an inducible calmodulin-dependent nitric-oxide synthase from rat liver and its expression in COS 1 cells. Eur. J. Biochem. 217:37-43.
17. Kawasaki, E.S. 1990. Amplification of RNA. In PCR Protocols: A Guide to Methods and Applications. M.A. Innis, D.H. Gelfang, J.J. Sninsky, and T.J. White, editors. Academic Press, New York. 22-27.
18. Hierholzer, C., J. Kalff, Y. Kim, T. Billiar, and D. Tweardy. 1997. G-CSF and IL-6 are produced in the lung in hemorrhagic shock where they contribute to the recruitment and activation of neutrophils. In 4th International Congress on The Immune Consequences of Trauma, Shock, and Sepsis. Mechanisms and Therapeutic Approaches. E. Faist, editor. Monduzzi, Bologna. 595-598.
19. de Vera, M.E., D.A. Geller, and T.R. Billiar. 1995. Hepatic inducible nitric oxide synthase: regulation and function. Biochem. Soc. Trans. 23:1008-1013.
20. Wagner, B.J., T.E. Hayes, C.J. Hoban, and B.H. Cochran. 1990. The SIF binding element confers sis/PDGF inducibility onto the c-fos promoter. EMBO (Eur. Mol. Biol. Organ.) J. 9:4477-4484.
21. Chakraborty, A., S.M. White, T.S. Schaefer, E.D. Ball, K.F. Dyer, and D.J. Tweardy. 1996. Granulocyte colony-stimulating factor activation of Stat3-alpha and Stat3-beta in immature normal and leukemic human myeloid cells. Blood. 88: 2442-2449.
22. Romano, M., M. Sironi, C. Toniatti, N. Polentarutti, P. Fruscella, P. Ghezzi, R. Faggioni, W. Luini, V. van Hinsbergh, S. Sozzani, et al. 1997. Role of IL-6 and its soluble receptor in induction of chemokines and leukocyte recruitment. Immunity. 6:315-325.
23. Dunn, S.M., L.S. Coles, R.K. Lang, S. Gerondakis, M.A. Vadas, and M.F. Shannon. 1994. Requirement for nuclear factor (NF)-kappa B p65 and NF-interleukin-6 binding elements in the tumor necrosis factor response region of the granulocyte colony-stimulating factor promoter. Blood. 83: 2469-2479.
24. Taniguchi, T. 1995. Cytokine signaling through nonreceptor protein tyrosine kinases. Science. 268:251-255.
25. Hierholzer, C., J. Kalff, T. Billiar, and D. Tweardy. 1998. Activation of STAT proteins in the lung of rats following resuscitation from hemorrhagic shock. Arch. Orth. Trauma Surg. In press.
26. Sadowski, H.B., K. Shuai, J.E. Darnell, Jr., and M.Z. Gilman. 1993. A common nuclear signal transduction pathway activated by growth factor and cytokine receptors. Science. 261: 1739-1744.
27. Akira, S., Y. Nishio, M. Inoue, X.J. Wang, S. Wei, T. Matsusaka, K. Yoshida, T. Sudo, M. Naruto, and T. Kishimoto. 1994. Molecular cloning of APRF, a novel IFN-stimulated gene factor 3 p91-related transcription factor involved in the gp130-mediated signaling pathway. Cell. 77:63-71.
28. Tweardy, D.J., T.M. Wright, S.F. Ziegler, H. Baumann, A. Chakraborty, S.M. White, K.F. Dyer, and K.A. Rubin. 1995. Granulocyte colony-stimulating factor rapidly activates a distinct STAT-like protein in normal myeloid cells. Blood. 86:4409-4416.
29. Szabo, C., and C. Thiemermann. 1994. Invited opinion: role of nitric oxide in hemorrhagic, traumatic, and anaphylactic shock and thermal injury. Shock. 2:145-155.
30. Cressman, D.E., L.E. Greenbaum, R.A. Deangelis, G. Ciliberto, E.E. Furth, V. Poli, and R. Taub. 1996. Liver failure and defective hepatocyte regeneration in interleukin-6-deficient mice. Science. 274:1379-1383.
31. Diefenbach, A., H. Schindler, N. Donhauser, E. Lorenz, T. Laskay, J. MacMicking, M. Röllinghoff, I. Gresser, and C. Bogdan. 1998. Type 1 interferon (IFN-α/β) and type 2 nitric oxide synthase regulate the innate immune response to a protozoan parasite. Immunity. 8:77-87.
32. Nathan, C. 1992. Nitric oxide as a secretory product of mammalian cells. FASEB J. 6:3051-3064.
33. Lander, H.M., D.P. Hajjar, B.L. Hempstead, U.A. Mirza, B.T. Chait, S. Campbell, and L.A. Quilliam. 1997. A molecular redox switch on p21(ras). Structural basis for the nitric oxide-p21(ras) interaction. J. Biol. Chem. 272:4323-4326.
34. Lander, H.M., A.J. Milbank, J.M. Tauras, D.P. Hajjar, B.L. Hempstead, G.D. Schwartz, R.T. Kraemer, U.A. Mirza, B.T. Chait, S.C. Burk, and L.A. Quilliam. 1996. Redox regulation of cell signalling. Nature. 381:380-381.
35. Lander, H.M., A.T. Jacovina, R.J. Davis, and J.M. Tauras. 1996. Differential activation of mitogen-activated protein kinases by nitric oxide-related species. J. Biol. Chem. 271: 19705-19709.
36. Abraham, E., S. Bursten, R. Shenkar, J. Allbee, R. Tuder, P. Woodson, D.M. Guidot, G. Rice, J.W. Singer, and J.E. Repine. 1995. Phosphatidic acid signaling mediates lung cytokine expression and lung inflammatory injury after hemorrhage in mice. J. Exp. Med. 181:569-575.
37. Harbrecht, B.G., B. Wu, S.C. Watkins, H.P. Marshall, Jr., A.B. Peitzman, and T.R. Billiar. 1995. Inhibition of nitric oxide synthase during hemorrhagic shock increases hepatic injury. Shock. 4:332-337.
38. Ou, J., T.M. Carlos, S.C. Watkins, J.E. Saavedra, L.K. Keefer, Y.M. Kim, B.G. Harbrecht, and T.R. Billiar. 1997. Differential effects of nonselective nitric oxide synthase (NOS) and selective inducible NOS inhibition on hepatic necrosis, apoptosis, ICAM-1 expression, and PMN accumulation during endotoxemia. NO: Biol. Chem. 1:404-416.