Role of galectin-3 in acetaminophen-induced hepatotoxicity and inflammatory mediator production

Toxicological Sciences

Volumn 127, Issue 2, 2012, Pages 609-619

  Dragomir, Ana Cristina ^a   Sun, Richard ^a   Mishin, Vladimir ^a   Hall, LeRoy B ^b   Laskin, Jeffrey D ^c   Laskin, Debra L ^a  

^a RUTGERS UNIVERSITY   (United States)

^b JANSSEN RESEARCH AND DEVELOPMENT   (Belgium)

^c RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

Acetaminophen; Galectin 3; Inflammation; Liver; Macrophages; TNFR1

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; CD98 ANTIGEN; CXCL3 CHEMOKINE; CYTOCHROME P450 2E1; GALECTIN 3; GELATINASE B; GLUTATHIONE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MESSENGER RNA; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; PARACETAMOL; TUMOR NECROSIS FACTOR RECEPTOR 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOSE RESPONSE; DRUG INDUCED DISEASE; ENZYME ACTIVITY; GENE EXPRESSION; HEPATITIS; IMMUNOHISTOCHEMISTRY; LIVER MICROSOME; LIVER NECROSIS; LIVER TOXICITY; MALE; MONONUCLEAR CELL; MOUSE; NONHUMAN; OXIDATIVE STRESS; RECEPTOR UPREGULATION; WILD TYPE;

MUS;

EID: 84861473786     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfs117     Document Type: Article

References (61)

1. Ahmad, N., Chen, L. C., Gordon, M. A., Laskin, J. D., and Laskin, D. L. (2002). Regulation of cyclooxygenase-2 by nitric oxide in activated hepatic macrophages during acute endotoxemia. J. Leukoc. Biol. 71, 1005-1011.
2. Bernardes, E. S., Silva, N. M., Ruas, L. P., Mineo, J. R., Loyola, A. M., Hsu, D. K., Liu, F. T., Chammas, R., and Roque-Barreira, M. C. (2006). Toxoplasma gondii infection reveals a novel regulatory role for galectin-3 in the interface of innate and adaptive immunity. Am. J. Pathol. 168, 1910-1920.
3. Borkham-Kamphorst, E., Drews, F., and Weiskirchen, R. (2011). Induction of lipocalin-2 expression in acute and chronic experimental liver injury moderated by pro-inflammatory cytokines interleukin-1β through nuclear factor-kappaB activation. Liver Int. 31, 656-665.
4. Bourdi, M., Eiras, D. P., Holt, M. P., Webster, M. R., Reilly, T. P., Welch, K. D., and Pohl, L. R. (2007). Role of IL-6 in an IL-10 and IL-4 double knockout mouse model uniquely susceptible to acetaminopheninduced liver injury. Chem. Res. Toxicol. 20, 208-216.
5. Chang, T. K. H., Crespi, C. L., and Waxman, D. J. (1998). Spectrophotometric analysis of human CYP2E1-catalyzed p-nitrophenol hydroxylation. In Methods in Molecular Biology. Cytochrome P450 Protocols (I. R. Phillips and E. A. Shephard, Eds.), Vol. 107, pp. 147-152. Humana Press, Inc., Totowa, NJ.
6. Chiu, H., Gardner, C. R., Dambach, D. M., Brittingham, J. A., Durham, S. K., Laskin, J. D., and Laskin, D. L. (2003a). Role of p55 tumor necrosis factor receptor 1 in acetaminophen-induced antioxidant defense. Am. J. Physiol. Gastrointest. Liver Physiol. 285, G959-G966.
7. Chiu, H., Gardner, C. R., Dambach, D. M., Durham, S. K., Brittingham, J. A., Laskin, J. D., and Laskin, D. L. (2003b). Role of tumor necrosis factor receptor 1 (p55) in hepatocyte proliferation during acetaminophen-induced toxicity in mice. Toxicol. Appl. Pharmacol. 193, 218-227.
8. Clarke, C. N., Kuboki, S., Tevar, A., Lentsch, A. B., and Edwards, M. (2009). CXC chemokines play a critical role in liver injury, recovery, and regeneration. Am. J. Surg. 198, 415-419.
9. Cook, J. A. (2005). Eicosanoids. Crit. Care Med. 33, S488-S491.
10. Dahlin, D. C., Miwa, G. T., Lu, A. Y., and Nelson, S. D. (1984). N-acetyl-pbenzoquinone imine: A cytochrome P-450-mediated oxidation product of acetaminophen. Proc. Natl. Acad. Sci. U.S.A. 81, 1327-1331.
11. Dambach, D. M., Durham, S. K., Laskin, J. D., and Laskin, D. L. (2006). Distinct roles of NF-κB p50 in the regulation of acetaminophen-induced inflammatory mediator production and hepatotoxicity. Toxicol. Appl. Pharmacol. 211, 157-165.
12. Dong, S., and Hughes, R. C. (1997). Macrophage surface glycoproteins binding to galectin-3 (Mac-2-antigen). Glycoconj. J. 14, 267-274.
13. Doverhag, C., Hedtjarn, M., Poirier, F., Mallard, C., Hagberg, H., Karlsson, A., and Savman, K. (2010). Galectin-3 contributes to neonatal hypoxic-ischemic brain injury. Neurobiol. Dis. 38, 36-46.
14. Dragomir, A. C., Laskin, J. D., and Laskin, D. L. (2011). Macrophage activation by factors released from acetaminophen-injured hepatocytes: Potential role of HMGB1. Toxicol. Appl. Pharmacol. 253, 170-177.
15. Fernandes Bertocchi, A. P., Campanhole, G., Wang, P. H., Goncalves, G. M., Damiao, M. J., Cenedeze, M. A., Beraldo, F. C., de Paula Antunes Teixeira, V., Dos Reis, M. A., Mazzali, M., et al. (2008). A role for galectin-3 in renal tissue damage triggered by ischemia and reperfusion injury. Transpl. Int. 21, 999-1007.
16. Forsman, H., Islander, U., Andreasson, E., Andersson, A., Onnheim, K., Karlstrom, A., Savman, K., Magnusson, M., Brown, K. L., and Karlsson, A. (2011). Galectin 3 aggravates joint inflammation and destruction in antigeninduced arthritis. Arthritis Rheum. 63, 445-454.
17. Gardner, C. R., Gray, J. P., Joseph, L. B., Cervelli, J., Bremer, N., Kim, Y., Mishin, V., Laskin, J. D., and Laskin, D. L. (2010). Potential role of caveolin-1 in acetaminophen-induced hepatotoxicity. Toxicol. Appl. Pharmacol. 245, 36-46.
18. Gardner, C. R., Laskin, J. D., Dambach, D. M., Chiu, H., Durham, S. K., Zhou, P., Bruno, M., Gerecke, D. R., Gordon, M. K., and Laskin, D. L. (2003). Exaggerated hepatotoxicity of acetaminophen in mice lacking tumor necrosis factor receptor-1. Potential role of inflammatory mediators. Toxicol. Appl. Pharmacol. 192, 119-130.
19. Gardner, C. R., Laskin, J. D., Dambach, D. M., Sacco, M., Durham, S. K., Bruno, M. K., Cohen, S. D., Gordon, M. K., Gerecke, D. R., Zhou, P., et al. (2002). Reduced hepatotoxicity of acetaminophen in mice lacking inducible nitric oxide synthase: Potential role of tumor necrosis factor-a and interleukin-10. Toxicol. Appl. Pharmacol. 184, 27-36.
20. Henderson, N. C., Mackinnon, A. C., Farnworth, S. L., Poirier, F., Russo, F. P., Iredale, J. P., Haslett, C., Simpson, K. J., and Sethi, T. (2006). Galectin-3 regulates myofibroblast activation and hepatic fibrosis. Proc. Natl. Acad. Sci. U.S.A. 103, 5060-5065.
21. Henderson, N. C., and Sethi, T. (2009). The regulation of inflammation by galectin-3. Immunol. Rev. 230, 160-171.
22. Hogaboam, C. M., Simpson, K. J., Chensue, S. W., Steinhauser, M. L., Lukacs, N. W., Gauldie, J., Strieter, R. M., and Kunkel, S. L. (1999). Macrophage inflammatory protein-2 gene therapy attenuates adenovirus- and acetaminophen-mediated hepatic injury. Gene Ther. 6, 573-584.
23. Hsu, D. K., Yang, R. Y., Pan, Z., Yu, L., Salomon, D. R., Fung-Leung, W. P., and Liu, F. T. (2000). Targeted disruption of the galectin-3 gene results in attenuated peritoneal inflammatory responses. Am. J. Pathol. 156, 1073-1083.
24. Iacobini, C., Menini, S., Ricci, C., Fantauzzi, C. B., Scipioni, A., Salvi, L., Cordone, S., Delucchi, F., Serino, M., Federici, M., et al. (2011). Galectin-3 ablation protects mice from diet-induced NASH: A major scavenging role for galectin-3 in liver. J. Hepatol. 54, 975-983.
25. Imaeda, A. B., Watanabe, A., Sohail, M. A., Mahmood, S., Mohamadnejad, M., Sutterwala, F. S., Flavell, R. A., and Mehal, W. Z. (2009). Acetaminopheninduced hepatotoxicity in mice is dependent on Tlr9 and the Nalp3 inflammasome. J. Clin. Investig. 119, 305-314.
26. Ishida, Y., Kondo, T., Tsuneyama, K., Lu, P., Takayasu, T., and Mukaida, N. (2004). The pathogenic roles of tumor necrosis factor receptor p55 in acetaminophen-induced liver injury in mice. J. Leukoc. Biol. 75, 59-67.
27. Ito, Y., Abril, E. R., Bethea, N. W., and McCuskey, R. S. (2005). Inhibition of matrix metalloproteinases minimizes hepatic microvascular injury in response to acetaminophen in mice. Toxicol. Sci. 83, 190-196.
28. Janelle-Montcalm, A., Boileau, C., Poirier, F., Pelletier, J. P., Guevremont, M., Duval, N., Martel-Pelletier, J., and Reboul, P. (2007). Extracellular localization of galectin-3 has a deleterious role in joint tissues. Arthritis Res. Ther. 9, R20.
29. Jeon, S. B., Yoon, H. J., Chang, C. Y., Koh, H. S., Jeon, S. H., and Park, E. J. (2010). Galectin-3 exerts cytokine-like regulatory actions through the JAKSTAT pathway. J. Immunol. 185, 7037-7046.
30. Jollow, D. J., Mitchell, J. R., Potter, W. Z., Davis, D. C., Gillette, J. R., and Brodie, B. B. (1973). Acetaminophen-induced hepatic necrosis. II. Role of covalent binding in vivo. J. Pharmacol. Exp. Ther. 187, 195-202.
31. Laskin, D. L. (2009). Macrophages and inflammatory mediators in chemical toxicity: A battle of forces. Chem. Res. Toxicol. 22, 1376-1385.
32. Laskin, D. L., Gardner, C. R., Price, V. F., and Jollow, D. J. (1995). Modulation of macrophage functioning abrogates the acute hepatotoxicity of acetaminophen. Hepatology 21, 1045-1050.
33. Laskin, J. D., Heck, D. E., and Laskin, D. L. (2010). Nitric oxide pathways in toxic responses. In General and Applied Toxicology, Chapter 17, pp. 425-438, 3rd ed. (B. Ballantyne, T. Marrs, T. Syversen, Eds.) Wiley-Blackwell, Oxford, U.K.
34. Laskin, D. L., and Pilaro, A. M. (1986). Potential role of activated macrophages in acetaminophen hepatotoxicity. I. Isolation and characterization of activated macrophages from rat liver. Toxicol. Appl. Pharmacol. 86, 204-215.
35. Laskin, D. L., Pilaro, A. M., and Ji, S. (1986). Potential role of activated macrophages in acetaminophen hepatotoxicity. II. Mechanism of macrophage accumulation and activation. Toxicol. Appl. Pharmacol. 86, 216-226.
36. Laskin, D. L., Sunil, V. R., Gardner, C. R., and Laskin, J. D. (2011). Macrophages and tissue injury: Agents of defense or destruction? Annu. Rev. Pharmacol. Toxicol. 51, 267-288.
37. Lee, S. S., Buters, J. T., Pineau, T., Fernandez-Salguero, P., and Gonzalez, F. J. (1996). Role of CYP2E1 in the hepatotoxicity of acetaminophen. J. Biol. Chem. 271, 12063-12067.
38. Lee, W. M., Squires, R. H., Jr, Nyberg, S. L., Doo, E., and Hoofnagle, J. H. (2008). Acute liver failure: Summary of a workshop. Hepatology 47, 1401-1415.
39. Liu, F. T., Hsu, D. K., Zuberi, R. I., Kuwabara, I., Chi, E. Y., Henderson, W. R., Jr (1995). Expression and function of galectin-3, a b-galactoside-binding lectin, in human monocytes and macrophages. Am. J. Pathol. 147, 1016-1028.
40. Liu, Z. X., Govindarajan, S., and Kaplowitz, N. (2004). Innate immune system plays a critical role in determining the progression and severity of acetaminophen hepatotoxicity. Gastroenterology 127, 1760-1774.
41. Martin-Murphy, B. V., Holt, M. P., and Ju, C. (2010). The role of damage associated molecular pattern molecules in acetaminophen-induced liver injury in mice. Toxicol. Lett. 192, 387-394.
42. Mensah-Brown, E. P., Al Rabesi, Z., Shahin, A., Al Shamsi, M., Arsenijevic, N., Hsu, D. K., Liu, F. T., and Lukic, M. L. (2009). Targeted disruption of the galectin-3 gene results in decreased susceptibility to multiple low dose streptozotocin-induced diabetes in mice. Clin. Immunol. 130, 83-88.
43. Mitchell, J. R., Jollow, D. J., Potter, W. Z., Gillette, J. R., and Brodie, B. B. (1973). Acetaminophen-induced hepatic necrosis. IV. Protective role of glutathione. J. Pharmacol. Exp. Ther. 187, 211-217.
44. Naito, M., Hasegawa, G., Ebe, Y., Yamamoto, T., et al. (2004). Differentiation and function of Kupffer cells. Med. Electron Microsc. 37, 16-28.
45. Nguyen, H. T., Dalmasso, G., Torkvist, L., Halfvarson, J., Yan, Y., Laroui, H., Shmerling, D., Tallone, T., D'Amato, M., Sitaraman, S. V., et al. (2011). CD98 expression modulates intestinal homeostasis, inflammation, and colitis-associated cancer in mice. J. Clin. Invest. 121, 1733-1747.
46. Nishi, Y., Sano, H., Kawashima, T., Okada, T., Kuroda, T., Kikkawa, K., Kawashima, S., Tanabe, M., Goto, T., Matsuzawa, Y., et al. (2007). Role of galectin-3 in human pulmonary fibrosis. Allergol. Int. 56, 57-65.
47. Norling, L. V., Perretti, M., and Cooper, D. (2009). Endogenous galectins and the control of the host inflammatory response. J. Endocrinol. 201, 169-184.
48. Papaspyridonos, M., McNeill, E., de Bono, J. P., Smith, A., Burnand, K. G., Channon, K. M., and Greaves, D. R. (2008). Galectin-3 is an amplifier of inflammation in atherosclerotic plaque progression through macrophage activation and monocyte chemoattraction. Arterioscler. Throm. Vasc. Biol. 28, 433-440.
49. Potter, W. Z., Davis, D. C., Mitchell, J. R., Jollow, D. J., Gillette, J. R., and Brodie, B. B. (1973). Acetaminophen-induced hepatic necrosis. 3. Cytochrome P-450-mediated covalent binding in vitro. J. Pharmacol. Exp. Ther. 187, 203-210.
50. Reilly, T. P., Brady, J. N., Marchick, M. R., Bourdi, M., George, J. W., Radonovich, M. F., Pise-Masison, C. A., and Pohl, L. R. (2001). A protective role for cyclooxygenase-2 in drug-induced liver injury in mice. Chem. Res. Toxicol. 14, 1620-1628.
51. Roudkenar, M. H., Kuwahara, Y., Baba, T., Roushandeh, A. M., Ebishima, S., Abe, S., Ohkubo, Y., and Fukumoto, M. (2007). Oxidative stress induced lipocalin 2 gene expression: Addressing its expression under the harmful conditions. J. Radiat. Res. (Tokyo) 48, 39-44.
52. Schutyser, E., Struyf, S., and Van Damme, J. (2003). The CC chemokine CCL20 and its receptor CCR6. Cytokine Growth Factor Rev. 14, 409-426.
53. Shen, J., Pavone, A., Mikulec, C., Hensley, S. C., Traner, A., Chang, T. K., Person, M. D., and Fischer, S. M. (2007). Protein expression profiles in the epidermis of cyclooxygenase-2 transgenic mice by 2-dimensional gel electrophoresis and mass spectrometry. J. Proteome Res. 6, 273-286.
54. Stables, M. J., and Gilroy, D. W. (2011). Old and new generation lipid mediators in acute inflammation and resolution. Prog. Lipid Res. 50, 35-51.
55. Sugita, S., Kohno, T., Yamamoto, K., Imaizumi, Y., Nakajima, H., Ishimaru, T., and Matsuyama, T. (2002). Induction of macrophageinflammatory protein-3α gene expression by TNF-dependent NF-κB activation. J. Immunol. 168, 5621-5628.
56. Sunil, V. R., Patel, K. J., Nilsen-Hamilton, M., Heck, D. E., Laskin, J. D., and Laskin, D. L. (2007). Acute endotoxemia is associated with upregulation of lipocalin 24p3/Lcn2 in lung and liver. Exp. Mol. Pathol. 83, 177-187.
57. Utans-Schneitz, U., Lorez, H., Klinkert, W. E., da Silva, J., and Lesslauer, W. (1998). A novel rat CC chemokine, identified by targeted differential display, is upregulated in brain inflammation. J. Neuroimmunol. 92, 179-190.
58. Volarevic, V., Milovanovic, M., Ljujic, B., Pejnovic, N., Arsenijevic, N., Nilsson, U., Leffler, H., and Lukic, M. L. (Forthcoming). Galectin-3 deficiency prevents concanavalin A-induced hepatitis in mice. Hepatology.
59. Weber, M., Sporrer, D., Weigert, J., Wanninger, J., Neumeier, M., Wurm, S., Stogbauer, F., Kopp, A., Bala, M., Schaffler, A., et al. (2009). Adiponectin downregulates galectin-3 whose cellular form is elevated whereas its soluble form is reduced in type 2 diabetic monocytes. FEBS Lett. 583, 3718-3724.
60. Williams, C. D., Farhood, A., and Jaeschke, H. (2010). Role of caspase-1 and interleukin-1b in acetaminophen-induced hepatic inflammation and liver injury. Toxicol. Appl. Pharmacol. 247, 169-178.
61. Zuberi, R. I., Hsu, D. K., Kalayci, O., Chen, H. Y., Sheldon, H. K., Yu, L., Apgar, J. R., Kawakami, T., Lilly, C. M., and Liu, F. T. (2004). Critical role for galectin-3 in airway inflammation and bronchial hyperresponsiveness in a murine model of asthma. Am. J. Pathol. 165, 2045-2053.