Differential effects of nonselective nitric oxide synthase (NOS) and selective inducible NOS inhibition on hepatic necrosis, apoptosis, ICAM-1 expression, and neutrophil accumulation during endotoxemia

Nitric Oxide - Biology and Chemistry

Volumn 1, Issue 5, 1997, Pages 404-416

  Ou, Junhai ^a   Carlos, Timothy M ^b   Watkins, Simon C ^b   Saavedra, Joseph E ^c   Keefer, Larry K ^c   Kim, Young Myeong ^a,b   Harbrecht, Brian G ^a   Billiar, Timothy R ^a  

^a UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

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

^c SAIC FREDERICK INC   (United States)

Author keywords

Adhesion molecule; Apoptosis; Liver; Necrosis; Neutrophil; Nitric oxide; NOS inhibitors

Indexed keywords

ALANINE AMINOTRANSFERASE; AMINOGUANIDINE; ASPARTATE AMINOTRANSFERASE; DNA FRAGMENT; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; INTERCELLULAR ADHESION MOLECULE 1; LIVER ENZYME; MONOCLONAL ANTIBODY; N(G) (1 IMINOETHYL)LYSINE; N(G) METHYLARGININE; N(G) NITROARGININE METHYL ESTER; NITRATE; NITRIC OXIDE; NITRIC OXIDE DONOR; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE INHIBITOR; NITRITE; SODIUM CHLORIDE; UNCLASSIFIED DRUG; VINBLASTINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; ENDOTOXEMIA; ENZYME INHIBITION; LIVER NECROSIS; MALE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALIA; ESCHERICHIA COLI;

EID: 0031431194     PISSN: 10898603     EISSN: None     Source Type: Journal    
DOI: 10.1006/niox.1997.0136     Document Type: Article

References (60)

1. Hirata K., Kaneko A., Ogawa K., Hayasaka H., Onoe E. Effect of endotoxin on rat liver. Lab. Invest. 43:1980;165-171.
2. Nolan J. P. The role of endotoxin in liver injury. Gastroenterology. 69:1975;1346-1356.
3. Hartung T., Wendel A. Endotoxin-inducible cytotoxicity in liver cell cultures. I. Biochem. Pharmacol. 42:1991;1129-1135.
4. Billiar T. R., Curran R. D., West M. A., Hofmann K., Simmons R. L. Kupffer cell cytotoxicity to hepatocytes in coculture requiresL. Arch. Surg. 124:1989;1416-1421.
5. Leist M., Gantner F., Jilg S., Wendel A. Activation of the 55 kDa TNF receptor is necessary and sufficient for TNF-induced liver failure, hepatocyte apoptosis, and nitrite release. J. Immunol. 154:1995;1307-1316.
6. Bautista A. P., Meszaros K., Bojta J., Spitzer J. J. Superoxide anion generation in the liver during the early stage of endotoxemia in rats. J. Leukocyte Biol. 48:1990;123-128.
7. Redmond H. P., Wang J. H., Bouchier-Hayes D. Taurine attenuates nitric oxide- and reactive oxygen intermediate-dependent hepatocyte injury. Arch. Surg. 131:1996;1280-1288.
8. Ma T. T., Ischiropoulos H., Brass C. A. Endotoxin-stimulated nitric oxide production increases injury and reduces rat liver chemiluminescence during reperfusion. Gastroenterology. 108:1995;463-469.
9. GL. J. Leukocyte Biol. 48:1990;565-569.
10. Harbrecht B. G., Billiar T. R., Stadler J., Demetris A. J., Ochoa J., Curran R. D., Simmons R. L. Inhibition of nitric oxide synthesis during endotoxemia promotes intrahepatic thrombosis and an oxygen radical-mediated hepatic injury. J. Leukocyte Biol. 52:1992;390-394.
11. Harbrecht B. G., Stadler J., Demetris A. J., Simmons R. L., Billiar T. R. Nitric oxide and prostacyclin interact to prevent hepatic damage during murine endotoxemia. Am. J. Physiol. 266:1994;G1004-G1010.
12. Kim Y. M., Bergonia H., Lancaster J. R. Jr. Nitrogen oxide-induced autoprotection in isolated rat hepatocytes. FEBS Lett. 374:1995;228-232.
13. Bohlinger I., Leist M., Barsig J., Uhlig S., Tiegs G., Wendel A. Interleukin-1 and nitric oxide protect against tumor necrosis factor α-induced liver injury through distinct pathways. Hepatology. 22:1995;1829-1837.
14. Kim Y. M., de Vera M. E., Watkins S. C., Billiar T. R. Nitric oxide protects cultured rat hepatocytes from TNFα-induced apoptosis by inducing heat shock protein 70 expression. J. Biol. Chem. 272:1997;1402-1411.
15. Billiar T. R. The delicate balance of nitric oxide and superoxide in liver pathology. Gastroenterology. 108:1995;603-605.
16. Moncada S., Palmer R. M., Higgs E. A. Nitric oxide: Physiology, pathophysiology, and pharmacology. Pharmacol. Rev. 43:1991;109-142.
17. Morris S. M. Jr., Billiar T. R. New insights into the regulation of inducible nitric oxide synthesis. Am. J. Physiol. 266:1994;E829-E839.
18. Billiar T. R., Curran R. D., Stuehr D. J., Stadler J., Simmons R. L., Murray S. A. Inducible cytosolic enzyme activity for the production of nitrogen oxides fromL. Biochem. Biophys. Res. Commun. 168:1990;1034-1040.
19. Curran R. D., Billiar T. R., Stuehr D. J., Hofmann K., Simmons R. L. Hepatocytes produce nitrogen oxides fromL. J. Exp. Med. 170:1989;1769-1774.
20. Geller D. A., Nussler A. K., Di Silvio M., Lowenstein C. J., Shapiro R. A., Wang S. C., Simmons R. L., Billiar T. R. Cytokines, endotoxin, and glucocorticoids regulate the expression of inducible nitric oxide synthase in hepatocytes. Proc. Natl. Acad. Sci. USA. 90:1993;522-526.
21. Billiar T. R., Curran R. D., Stuehr D. J., West M. A., Bentz B. G., Simmons R. L. AnLin vitro. J. Exp. Med. 169:1989;1467-1472.
22. Helyar L., Bundschuh D. S., Laskin J. D., Laskin D. L. Induction of hepatic Ito cell nitric oxide production after acute endotoxemia. Hepatology. 20:1994;1509-1515.
23. Spitzer J. A. Cytokine stimulation of nitric oxide formation and differential regulation in hepatocytes and nonparenchymal cells of endotoxemic rats. Hepatology. 19:1994;217-228.
24. Feder L. S., Laskin D. L. Regulation of hepatic endothelial cell and macrophage proliferation and nitric oxide production by GM-CSF, M-CSF, and IL-1β following acute endotoxemia. J. Leukocyte Biol. 55:1994;507-513.
25. Harbrecht B. G., Billiar T. R., Stadler J., Demetris A. J., Ochoa J. B., Curran R. D., Simmons R. L. Nitric oxide synthesis serves to reduce hepatic damage during acute murine endotoxemia. Crit. Care Med. 20:1992;1568-1574.
26. Szabo C., Southan G. J., Thiermermann C. Beneficial effects and improved survival in rodent models of septic shock withS. Proc. Natl. Acad. Sci. USA. 91:1994;12472-12476.
27. Misko T. P., Moore W. M., Kasten T. P., Nickols G. A., Corbett J. A., Tilton R. G., McDaniel M. L., Williamson J. R., Currie M. G. Selective inhibition of the inducible nitric oxide synthase by aminoguanidine. Eur. J. Pharmacol. 233:1993;119-125.
28. 6. J. Med. Chem. 37:1994;3886-3888.
29. Connor J. R., Manning P. T., Settle S. L., Moore W. M., Jerome G. M., Webber R. K., Tjoeng F. S., Currie M. G. Suppression of adjuvant-induced arthritis by selective inhibition of inducible nitric oxide synthase. Eur. J. Pharmacol. 273:1995;15-24.
30. Sekiya S., Gotoh S., Yamashita T., Watanabe T., Saitoh S., Sendo F. Selective depletion of rat neutrophils by in vivo administration of a monoclonal antibody. J. Leukocyte Biol. 46:1989;96-102.
31. Saavedra J. E., Billiar T. R., Williams D. L., Kim Y.-M., Watkins S. C., Keefer L. K. Targeting nitric oxide (NO) delivery in vivo. Design of a liver-selective NO donor prodrug that blocks tumor necrosis factor-α-induced apoptosis and toxicity in the liver. J. Med. Chem. 40:1997;1947-1954.
32. Hsu S. M., Raine L., Fanger H. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: A comparison of ABC and unlabeled antibody (PAP) procedure. J. Histochem. Cytochem. 29:1981;577-580.
33. Kudo C., Yamashita T., Araki A., Terashita M., Watanabe T., Atsumi M., Tumura M., Sendo F. Modulation of in vivo immune response by selective depletion of neutrophils using a monoclonal antibody, RP-3. I. Inhibition by RP-3 treatment of the priming and effector phases of delayed type hypersensitivity to sheep red blood cells in rats. J. Immunol. 150:1993;3728-3738.
34. Wyllie A. H. Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature. 284:1980;555-556.
35. Hughes F. M., Gorospe W. C. Biochemical identification of apoptosis (programmed cell death) in granulosa cells: Evidence for a potential mechanism underlying follicular atresia. Endocrinology. 129:1991;2415-2422.
36. 15. Anal. Biochem. 126:1982;131-138.
37. Geller D. A., Di Silvio M., Nussler A. K., Wang S. C., Shapiro R. A., Simmons R. L., Billiar T. R. Nitric oxide synthase expression is induced in hepatocytesin vivo. J. Surg. Res. 55:1993;427-432.
38. Nishida J., McCuskey R. S., McDonnell D., Fox E. S. Protective role of NO in hepatic microcirculatory dysfunction during endotoxemia. Am. J. Physiol. 267:1994;G1135-G1141.
39. Wang Y., Mathews W. R., Guido D., Farhood A., Jaeschke H. Inhibition of nitric oxide synthesis aggravates reperfusion injury after hepatic ischemia and endotoxemia. Shock. 4:1995;282-288.
40. Jaeschke H., Essani N. A., Fisher M. A., Vonderfecht S. L., Farhood A., Smith C. W. Release of soluble intercellular adhesion molecule I into bile and serum in murine endotoxin shock. Hepatology. 23:1996;530-536.
41. Tosa Y., Kollias N., Lee W. P., May J. W. Reduction of ischemia-reperfusion injury by monoclonal antibody to intercellular adhesion molecule-1. Transplant. Proc. 28:1996;1210-1211.
42. Albina J. E., Cui S., Mateo R. B., Reichner J. S. Nitric oxide-mediated apoptosis in murine peritoneal macrophages. J. Immunol. 150:1993;5080-5085.
43. Fehsel K., Kroncke K. D., Meyer K. L., Huber H., Wahn V., Kolb-Bachofen V. Nitric oxide induces apoptosis in mouse thymocytes. J. Immunol. 155:1995;2858-2865.
44. Dawson V. L., Kizushi V. M., Huang P. L., Snyder S. H., Dawson T. M. Resistance to neurotoxicity in cortical cultures from neuronal nitric oxide synthase-deficient mice. J. Neurosci. 16:1996;2479-2487.
45. Mannick J. B., Asano K., Izumi K., Kieff E., Stamler J. S. Nitric oxide produced by human B lymphocytes inhibits apoptosis and Epstein-Barr virus reactivation. Cell. 79:1994;1137-1146.
46. Chun S. Y., Eisenhauer K. M., Kubo M., Hsueh A. J. Interleukin-1 beta suppresses apoptosis in rat ovarian follicles by increasing nitric oxide production. Endocrinology. 136:1995;3120-3127.
47. Genaro A. M., Hortelano S., Alvarez A., Martinez C., Bosca L. Splenic B lymphocyte programmed cell death is prevented by nitric oxide release through mechanisms involving sustained Bcl-2 levels. J. Clin. Invest. 95:1995;1884-1890.
48. Wang G.-S., Liu G.-T. Role of nitric oxide in immunological liver damage in mice. Biochem. Pharmacol. 49:1995;1277-1281.
49. Ruetten H., Thiemermann C. Prevention of the expression of inducible nitric oxide synthase by aminoguanidine or aminoethyl-isothiourea in macrophages and in the rat. Biochem. Biophys. Res. Commun. 225:1996;525-530.
50. Harbrecht B. G., Billiar T. R., Curran R. D., Stadler J., Simmons R. L. Hepatocyte injury by activated neutrophils in vitro is mediated by proteases. Ann. Surg. 218:1993;120-128.
51. Pastor C. M., Billiar T. R. Nitric oxide causes hyporeactivity to phenylephrine in isolated perfused livers from endotoxin-treated rats. Am. J. Physiol. 268:1995;G177-G182.
52. Kubes P., Suzuki M., Granger D. N. Nitric oxide: An endogenous modulator of leukocyte adhesion. Proc. Natl. Acad. Sci. USA. 88:1991;4651-4655.
53. Davenpeck K. L., Gauthier T. W., Lefer A. M. Inhibition of endothelial-derived nitric oxide promotes P-selectin expression and actions in the rat microcirculation. Gastroenterology. 107:1994;1050-1058.
54. Kubes P., Kanwar S., Niu X.-F., Gaboury J. P. Nitric oxide synthesis inhibition induces leukocyte adhesion via superoxide and mast cells. FASEB J. 7:1993;1293-1299.
55. Niu X. F., Smith C. W., Kubes P. Intracellular oxidative stress induced by nitric oxide synthesis inhibition increases endothelial cell adhesion to neutrophils. Circ. Res. 74:1994;1133-1140.
56. Gauthier T. W., Davenpeck K. L., Lefer A. M. Nitric oxide attenuates leukocyte-endothelial interaction via P-selection in splanchnic ischemia-reperfusion. Am. J. Physiol. 267:1994;G562-G568.
57. Lefer D. J., Scalia R., Campbell B., Nossuli T., Hayward R., Salamon M., Grayson J., Lefer A. M. Peroxynitrite inhibits leukocyte-endothelial cell interactions and protects against ischemia-reperfusion injury in rats. J. Clin. Invest. 99:1997;684-691.
58. Y-M. Kim, R. V. Talanian, T. R. Billiar, Nitric oxide prevents apoptosis by preventing increases in caspase-3-like activity via two distinct mechanisms, J. Biol. Chem.
59. Lingnau W., McGuire R., Dehring D. J., Traber L. D., Linares H. A., Nelson S. H., Kilbourn R. G., Traber D. L. Changes in regional hemodynamics after nitric oxide inhibition during ovine bacteremia. Am. J. Physiol. 270:1996;R207-R216.
60. Kilbourn R. G. Nitric oxide: Moving towards the clinic. Mol. Med. Today. 2:1996;324.