Enhancement of allyl alcohol hepatotoxicity by endotoxin requires extrahepatic factors

Toxicological Sciences

Volumn 69, Issue 2, 2002, Pages 470-481

  Kinser, Shawn ^a   Copple, Bryan L ^a   Roth, Robert A ^a   Ganey, Patricia E ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Coagulation; Heparin; Inflammation; Lipopolysaccharide; Liver; Perfusion; Potentiation; Thrombin

Indexed keywords

ALANINE AMINOTRANSFERASE; ALLYL ALCOHOL; ENDOTOXIN; FIBRINOGEN; HEPARIN; LIPOPOLYSACCHARIDE; THROMBIN; WARFARIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD CLOTTING; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME RELEASE; FIBRINOGEN BLOOD LEVEL; ISOLATED LIVER; KUPFFER CELL; LIVER CELL; LIVER INJURY; LIVER PERFUSION; LIVER TOXICITY; MALE; NONHUMAN; RAT;

ANIMALS; ANTICOAGULANTS; BLOOD COAGULATION; CELL SEPARATION; CHEMOKINES; CHEMOKINES, CXC; CHEMOTACTIC FACTORS; COCULTURE TECHNIQUES; CYCLOOXYGENASE 2; ENDOTOXINS; FIBRINOGEN; HEPARIN; HEPATITIS, TOXIC; HEPATOCYTES; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; ISOENZYMES; KUPFFER CELLS; LIPOPOLYSACCHARIDES; LIVER FUNCTION TESTS; MALE; NEUTROPHIL INFILTRATION; PERFUSION; PROPANOLS; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; THROMBIN;

ANIMALIA; BACTERIA (MICROORGANISMS);

EID: 0036772790     PISSN: 10966080     EISSN: None     Source Type: Journal    
DOI: 10.1093/toxsci/69.2.470     Document Type: Article

References (64)

1. Aasen, A. O., Dale, J., Ohlsson, D., and Gallimore, M. (1978). Effects of slow intravenous administration of endotoxin on blood cells and coagulation in dogs. Eur. Surg. Res. 10, 194-205.
2. Adachi, Y., Bradford, B. U., Gao, W., Bojes, H. K., and Thurman, R. G. (1994). Inactivation of Kupffer cells prevents early alcohol-induced liver injury. Hepatology 20, 453-460.
3. Altin, J. G., and Bygrave, F. L. (1988). Prostaglandin F2 alpha and the thromboxane A2 analogue ONO-11113 stimulate Ca2+ fluxes and other physiological responses in rat liver. Further evidence that prostanoids may be involved in the action of arachidonic acid and platelet-activating factor. Biochem. J. 249, 677-685.
4. Badger, D. A., Sauer, J. M., Hoglen, N. C., Jolley, C. S., and Sipes, I. G. (1996). The role of inflammatory cells and cytochrome P450 in the potentiation of CCl4-induced liver injury by a single dose of retinol. Toxicol. Appl. Pharmacol. 141, 507-519.
5. Barton, C. C., Barton, E. X., Ganey, P. E., Kunkel, S. L., and Roth, R. A. (2001). Bacterial lipopolysaccharide enhances aflatoxin B1 hepatotoxicity in rats by a mechanism that depends on tumor necrosis factor-α. Hepatology 33, 66-73.
6. Bautista, A. P., and Spitzer, J. J. (1999). Role of Kupffer cells in the ethanol-induced oxidative stress in the liver. Front. Biosci. 4, D589-D595.
7. Beltran, A. E., Concepcion, F., Manzanares, D., Garrido, G., Glaria, L. A., and Rojas, A. (1999). Heparin and low molecular weight heparin decrease nitric oxide production by human polymorphonuclear cells. Arch. Med. Res. 30, 116-119.
8. 2 production in vitro. J. Leukoc. Biol. 47, 305-311.
9. Chomczynski, P. (1993). A reagent for the single-step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples. BioTechniques 15, 532-537.
10. Chomczynski, P., and Mackey, K. (1995). Short technical reports. Modification of the TRI reagent procedure for isolation of RNA from polysaccharide- and proteoglycan-rich sources. BioTechniques 19, 942-945.
11. Copple, B. L., Moulin, F., Ganey, P. E., and Roth, R. A. (2000). Endotoxin-induced liver injury requires activation of protease-activated receptor-1. FASEB J. 14, A290, (Abstract).
12. Darien, B. J., Fareed, J., Centgraf, K. S., Hart, A. P., MacWilliams, P. S., Clayton, M. K., Wolf, H., and Kruse-Elliott, K. T. (1998). Low molecular weight heparin prevents the pulmonary hemodynamic and pathomorphologic effects of endotoxin in a porcine acute lung injury model. Shock 9, 274-281.
13. Downing, L. J., Strieter, R. M., Kadell, A. M., Wilke, C. A., Greenfield, L. J., and Wakefield, T. W. (1998). Low-dose low-molecular-weight heparin is anti-inflammatory during venous thrombosis. J. Vasc. Surg. 28, 948-854.
14. Formal, S. B., Noyes, H. E., and Schneider, H. (1960). Experimental Shigella infections. III. Sensitivity of normal, starved and carbon tetrachloride treated guinea pigs to endotoxin. Proc. Soc. Exp. Biol. Med. 103, 415-418.
15. Fujita, S., Aril, S., Monden, K., Adachi, Y., Funaki, N., Higashitsuji, H., Furutani, M., Mise, M., Ishiguro, S., Kitao, T., et al. (1995). Participation of hepatic macrophages and plasma factors in endotoxin-induced liver injury. J. Surg. Res. 59, 263-270.
16. Ganey, P. E., Barton, Y. W., Kinser, S., Sneed, R.A., Barton, C. C., and Roth, R. A. (2001). Involvement of cyclooxygenase-2 in the potentiation of allyl alcohol-induced liver injury by bacterial lipopolysaccharide. Toxicol. Appl. Pharmacol. 174, 113-121.
17. Ganey, P. E., Keller, B., Lichtman, S. N., Lemasters, J. J., and Thurman, R. G. (1991). A new method to monitor Kupffer cell phagocytosis continuously in perfused rat liver. Hepatology 13, 567-574.
18. Ganey, P. E., and Schultze, A. E. (1995). Depletion of neutrophils and modulation of Kupffer cell function in allyl alcohol-induced hepatotoxicity. Toxicology 99, 99-106.
19. Hammes, S. R., Shapiro, M. J., and Coughlin, S. R. (1999). Shutoff and agonist-triggered internalization of protease-activated receptor 1 can be separated by mutation of putative phosphorylation sites in the cytoplasmic tail. Biochemistry 38, 9308-9316.
20. Hewett, J. A., Jean, P. A., Kunkel, S. L., and Roth, R. A. (1993). Relationship between tumor necrosis factor-alpha and neutrophils in endotoxin-induced liver injury. Am. J. Physiol. 265, G1011-1015.
21. Hewett, J. A., and Roth, R. A. (1993). Hepatic and extrahepatic pathobiology of bacterial lipopolysaccharides. Pharmacol. Rev. 45, 382-411.
22. Hewett, J. A., and Roth, R. A. (1995). The coagulation system, but not circulating fibrinogen, contributes to liver injury in rats exposed to lipopolysaccharide from gram-negative bacteria. J. Pharmacol. Exp. Ther. 272, 53-62.
23. Hewett, J. A., Schultze, A. E., VanCise, S., and Roth, R. A. (1992). Neutrophil depletion protects against liver injury from bacterial endotoxin. Lab. Invest. 66, 347-361.
24. Hisama, N., Yamaguchi, Y., Ishiko, T., Miyanari, N., Ichiguchi, O., Goto, M., Mori, K., Watanabe, K., Kawamura, K., Tsurufuji, S., and Ogawa, M. (1996). Kupffer cell production of cytokine-induced neutrophil chemoattractant following ischemia/reperfusion injury in rats. Hepatology 24, 1193-1198.
25. Hoglen, N. C., Younis, H. S., Hartley, D, P., Gunawardhana, L., Lantz, R. C., and Sipes, I. G. (1998). 1,2-Dichlorobenzene-induced lipid peroxidation in male Fischer 344 rats is Kupffer cell dependent. Toxicol. Sci. 46, 376-385.
26. Iimuro, Y., Yamamoto, M., Kohno, H., Itakura, J., Fujii, H., and Matsumoto, Y. (1994). Blockade of liver macrophages by gadolinium chloride reduces lethality in endotoxemic rats-analysis of mechanisms of lethality in endotoxemia. J. Leukoc. Biol. 55, 723-728.
27. Ikejima, K., Enomoto, N., Seabra, V., Ikejima, A., Brenner, D. A., and Thurman, R. G. (1999). Pronase destroys the lipopolysaccharide receptor CD14 on Kupffer cells. Am. J. Physiol. 276, G591-G598.
28. Ishii, K., Hein, L., Kobilka, B., and Coughlin, S. R. (1993). Kinetics of thrombin receptor cleavage on intact cells. Relation to signaling. J. Biol. Chem. 268, 9780-9786.
29. Ishiyama, H., Ogino, K., and Hobara, T. (1995). Role of Kupffer cells in rat liver injury induced by diethyldithiocarbamate. Eur. J. Pharmacol. 292, 135-141.
30. Kausalya, S., Malla, N., Ganguly, N. K., and Mahajan, R. C. (1993). Leishmania donovani: In vitro evidence of hepatocyte damage by Kupffer cells and immigrant macrophages in a murine model. Exp. Parasitol. 77, 326-333.
31. Knook, D. L., and Sleyster, E. C. (1977). Preparation and characterization of Kupffer cells from rat and mouse liver. In Kupffer Cells and Other Liver Sinusoidal Cells. (E. Wisse and D. L. Knock, Eds.), pp. 273-288. Elsevier/ North-Holland Biomedical, Amsterdam.
32. Lichtman, S. N., Wang, J., Zhang, C., and Lemasters, J. J. (1996). Endocytosis and Ca2+ are required for endotoxin-stimulated TNF-α release by rat Kupffer cells. Am. J. Physiol. 271, G920-G928.
33. 14C-arachidonate incorporation in response to endotoxin in vitro. Prostaglandins 39, 497-514.
34. Margaretten, W., McKay, D. G., and Phillips, L. L. (1967). The effect of heparin on endotoxin shock in the rat. Am. J. Pathol. 51, 61-68.
35. Michael, S. L., Pumford, N. R., Mayeux, P. R., Niesman, M. R., and Hinson, J. A. (1999). Pretreatment of mice with macrophage inactivators decreases acetaminophen hepatotoxicity and the formation of reactive oxygen and nitrogen species. Hepatology 30, 186-195.
36. Morgan, E. T. (2001). Regulation of cytochrome P450 by inflammatory mediators: Why and how? Drug Metab. Dispos. 29, 207-212.
37. Moulin, F., Copple, B. L., Ganey, P. E., and Roth, R. A. (2001). Hepatic and extrahepatic factors critical for liver injury during lipopolysaccharide exposure. Am. J. Physiol. Gastrointest. Liver Physiol. 281, G1423-1431.
38. Moulin, F., Pearson, J. M., Schultze, A. E., Scott, M. A., Schwartz, K. A., Davis, J. M., Ganey, P. E., and Roth, R. A. (1996). Thrombin is a distal mediator of lipopolysaccharide-induced liver injury in the rat. J. Surg. Res. 65, 149-158.
39. Ohno, Y., Ormstad, K., Ross, D., and Orrenius, S. (1985). Mechanism of allyl alcohol toxicity and protective effects of low-molecular-weight thiols studied with isolated rat hepatocytes. Toxicol. Appl. Pharmacol. 78, 169-179.
40. Pang, J. M., Zaleski, J., and Kauffman, F. C. (1997). Toxicity of allyl alcohol in primary cultures of freshly isolated and cryopreserved hepatocytes maintained on hydrated collagen gels. Toxicol. Appl. Pharmacol. 142, 87-94.
41. Patel, J. M., Wood, J. C., and Leibman, K. C. (1980). The biotransformation of allyl alcohol and acrolein in rat liver and lung preparations. Drug Metab. Dispos. 8, 305-308.
42. Pearson, J. M., Schultze, A. E., Jean, P. A., and Roth, R. A. (1995). Platelet participation in liver injury from gram-negative bacterial lipopolysaccharide in the rat. Shock 4, 178-186.
43. Pearson, J. M., Schultze, A. E., Schwartz, K. A., Scott, M. A., Davis, J. M., and Roth, R. A. (1996). The thrombin inhibitor, hirudin, attenuates lipopolysaccharide-induced liver injury in the rat. J. Pharmacol. Exp. Ther. 278, 378-383.
44. Pereira, F. E., Motta, L., and Cardoso, A. A. (1997). Kupffer cell activation with BCG. Corynebacterium parvum or zymosan protects against acute liver injury induced by carbon tetrachloride in rats. Arq. Gastroenterol. 34, 157-162.
45. Pernerstorfer, T., Hollenstein, U., Hansen, J., Knechtelsdorfer, M., Stohlawetz, P., Graninger, W., Eichler, H. G., Speiser, W., and Jilma, B. (1999). Heparin blunts endotoxin-induced coagulation activation. Circulation 100, 2485-2490.
46. Prager, R. L., Dunn, E. L., Kirsh, M. M., and Penner, J. A. (1979). Endotoxin-induced intravascular coagulation (DIC) and its therapy. Adv. Shock Res. 2, 277-287.
47. Reid, W. D. (1972). Mechanism of allyl alcohol-induced hepatic necrosis. Experientia 28, 1058-1061.
48. Riesenberg, K., Schlaeffer, F., Katz, A., and Levy, R. (1995). Inhibition of superoxide production in human neutrophils by combinations of heparin and thrombolytic agents. Br. Heart J. 73, 14-19.
49. Roth, R. A., Harkema, J. R., Pestka, J. P., and Ganey, P. E. (1997). Is exposure to bacterial endotoxin a determinant of susceptibility to intoxication from xenobiotic agents? Toxicol. Appl. Pharmacol. 147, 300-311.
50. Rovai, L. E., Herschman, H. R., and Smith, J. B. (1998). The murine neutrophil-chemoattractant chemokines LIX, KC, and MIP-2 have distinct induction kinetics, tissue distributions, and tissue-specific sensitivities to glucocorticoid regulation in endotoxemia. J. Leukoc. Biol. 64, 494-502.
51. Ruetten, H., and Thiemermann, C. (1997). Effects of tyrphostins and genistein on the circulatory failure and organ dysfunction caused by endotoxin in the rat: A possible role for protein tyrosine kinase. Br. J. Pharmacol. 122, 59-70.
52. Sarphie, T. G., D'Souza, N. B., and Deaciuc, I. V. (1996). Kupffer cell inactivation prevents lipopolysaccharide-induced structural changes in the rat liver sinusoid: An electron-microscopic study. Hepatology 23, 788-796.
53. Seglen, P. O. (1973). Preparation of rat liver cells. 3. Enzymatic requirements for tissue dispersion. Exp. Cell Res. 82, 391-398.
54. Serafini-Cessi, F. (1972). Conversion of allyl alcohol into acrolein by rat liver. Biochem. J. 128, 1103-1107.
55. Shibayama, Y. (1987). Sinusoidal circulatory disturbance by microthrombosis as a cause of endotoxin-induced hepatic injury. J. Pathol. 151, 315-321.
56. Shin, C. S., Han, J. U., Kim, J. L., Schenarts, P. J., Traber, L. D., Hawkins, H., and Traber, D. L. (1997). Heparin attenuated neutrophil infiltration but did not affect renal injury induced by ischemia reperfusion. Yonsei Med. J. 38, 133-141.
57. Sladek, N. E. (1971). Metabolism of cyclophosphamide by rat hepatic microsomes. Cancer Res. 31, 901-908.
58. Sneed, R. A., Grimes, S. D., Schultze, A. E., Brown, A. P., and Ganey, P. E. (1997). Bacterial endotoxin enhances the hepatotoxicity of allyl alcohol. Toxicol. Appl. Pharmacol. 144, 77-87.
59. Stachlewitz, R. F., Seabra, V., Bradford, B., Bradham, C. A., Rusyn, I., Germolec, D., and Thurman, R. G. (1999). Glycine and uridine prevent D-galactosamine hepatotoxicity in the rat: Role of Kupffer cells. Hepatology 29, 737-745.
60. Thurman, R. G. (1998). II. Alcoholic liver injury involves activation of Kupffer cells by endotoxin. Am. J. Physiol. 275, G605-G611.
61. Wueweera, J. B., Gandolfi, A. J., Badger, D. A., Sipes, I. G., and Brendel, K. (1996). Vitamin A potentiation of vinylidene chloride hepatotoxicity in rats and precision-cut rat liver slices. Fundam. Appl. Toxicol. 34, 73-83.
62. Yamaguchi, K., Majima, M., Katori, M., Kakita, A., and Sugimoto, K. (2000). Preferential consumption of coagulation factors I, V, and VIII in rat endotoxemia. Shock 14, 535-543.
63. Yee, S. B., Kinser, S., Hill, D. A., Barton, C. C., Hotchkiss, J. A., Harkema, J. R., Ganey, P. E., and Roth, R. A. (2000). Synergistic hepatotoxicity from coexposure to bacterial endotoxin and the pyrrolizidine alkaloid monocrotaline. Toxicol. Appl. Pharmacol. 166, 173-185.
64. Zhang, P., Xie, M., Zagorski, J., and Spitzer, J. A. (1995). Attenuation of hepatic neutrophil sequestration by anti-CINC antibody in endotoxic rats. Shock 4, 262-268.