High Mobility Group Box-1 (HMGB1) participates in the pathogenesis of Alcoholic Liver Disease (ALD)

Journal of Biological Chemistry

Volumn 289, Issue 33, 2014, Pages 22672-22691

  Ge, Xiaodong ^a   Antoine, Daniel J ^b   Lu, Yongke ^a   Arriazu, Elena ^a   Leung, Tung Ming ^a,c   Klepper, Arielle L ^a   Branch, Andrea D ^a   Fiel, Maria Isabel ^a   Nieto, Natalia ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c SUNY DOWNSTATE MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BODY FLUIDS; CELL CULTURE; ETHANOL; PHOSPHORYLATION; SULFUR COMPOUNDS;

AMP-ACTIVATED PROTEIN KINASE; EXPERIMENTAL EVIDENCE; HIGH-MOBILITY GROUPS; NUCLEAR LOCALIZATION SIGNAL; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR; PHOSPHORYLATION SITES; POST-TRANSLATIONAL MODIFICATIONS; PRIMARY CELL CULTURES;

MAMMALS;

ADENOSINE PHOSPHATE ACTIVATED PROTEIN KINASE ALPHA; CARNITINE PALMITOYLTRANSFERASE I; HIGH MOBILITY GROUP B1 PROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LOW DENSITY LIPOPROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; UNCLASSIFIED DRUG; VERY LOW DENSITY LIPOPROTEIN; ANTIOXIDANT; HMGB1 PROTEIN, HUMAN; HMGB1 PROTEIN, MOUSE; OXIDIZING AGENT;

ACETYLATION; ALCOHOL LIVER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; LIVER CELL; LIVER TOXICITY; MALE; MOUSE; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN SECRETION; UPREGULATION; ANIMAL; CELL CULTURE; FEMALE; GENETICS; HUMAN; KNOCKOUT MOUSE; LIVER; MORTALITY; PATHOLOGY; PHOSPHORYLATION; PRIMARY CELL CULTURE; SECRETION (PROCESS);

ACETYLATION; ANIMALS; ANTIOXIDANTS; CELLS, CULTURED; FEMALE; HEPATOCYTES; HMGB1 PROTEIN; HUMANS; LIPOPROTEINS, LDL; LIPOPROTEINS, VLDL; LIVER; LIVER DISEASES, ALCOHOLIC; MALE; MICE; MICE, KNOCKOUT; OXIDANTS; PHOSPHORYLATION; PRIMARY CELL CULTURE; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84905979754     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.552141     Document Type: Article

References (57)

1. Bonaldi, T., Talamo, F., Scaffidi, P., Ferrera, D., Porto, A., Bachi, A., Rubartelli, A., Agresti, A., and Bianchi, M. E. (2003) Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion. EMBO J. 22, 5551-5560
2. Taira, J., Kida, Y., Kuwano, K., and Higashimoto, Y. (2013) Protein phosphatase 2A dephosphorylates phosphoserines in nucleocytoplasmic shuttling and secretion of high mobility group box 1. J. Biochem. 154, 299-308
3. Carneiro, V. C., de Moraes Maciel, R., de Abreu da Silva, I. C., da Costa, R. F., Paiva, C. N., Bozza, M. T., and Fantappié, M. R. (2009) The extracellular release of Schistosoma mansoni HMGB1nuclear protein is mediated by acetylation. Biochem. Biophys. Res. Commun. 390, 1245-1249
4. Liu, S., Stolz, D. B., Sappington, P. L., Macias, C. A., Killeen, M. E., Tenhunen, J. J., Delude, R. L., and Fink, M. P. (2006) HMGB1 is secreted by immunostimulated enterocytes and contributes to cytomix-induced hyperpermeability of Caco-2 monolayers. Am. J. Physiol. Cell Physiol. 290, C990-C999
5. Soop, A., Hållström, L., Frostell, C., Wallén, H., Mobarrez, F., and Pisetsky, D. S. (2013) Effect of lipopolysaccharide administration on the number, phenotype and content of nuclear molecules in blood microparticles of normal human subjects. Scand. J. Immunol. 78, 205-213
6. Li, W., Li, J., Sama, A. E., and Wang, H. (2013) Carbenoxolone blocks endotoxin-induced protein kinase R (PKR) activation and high mobility group box 1 (HMGB1) release. Mol. Med. 19, 203-211
7. Lu, B., Wang, H., Andersson, U., and Tracey, K. J. (2013) Regulation of HMGB1 release by inflammasomes. Protein Cell 4, 163-167
8. Lu, B., Nakamura, T., Inouye, K., Li, J., Tang, Y., Lundbäck, P., Valdes-Ferrer, S. I., Olofsson, P. S., Kalb, T., Roth, J., Zou, Y., Erlandsson-Harris, H., Yang, H., Ting, J. P., Wang, H., Andersson, U., Antoine, D. J., Chavan, S. S., Hotamisligil, G. S., and Tracey, K. J. (2012) Novel role of PKR in inflammasome activation and HMGB1 release. Nature 488, 670-674
9. Lamkanfi, M., Sarkar, A., Vande Walle, L., Vitari, A. C., Amer, A. O., Wewers, M. D., Tracey, K. J., Kanneganti, T. D., and Dixit, V. M. (2010) Inflammasome-dependent release of the alarmin HMGB1 in endotoxemia. J. Immunol. 185, 4385-4392
10. Willingham, S. B., Allen, I. C., Bergstralh, D. T., Brickey, W. J., Huang, M. T., Taxman, D. J., Duncan, J. A., and Ting, J. P. (2009) NLRP3 (NALP3, Cryopyrin) facilitates in vivo caspase-1 activation, necrosis, and HMGB1 release via inflammasome-dependent and -independent pathways. J. Immunol. 183, 2008-2015
11. Bianchi, M. E., and Manfredi, A. A. (2007) High-mobility group box 1 (HMGB1) protein at the crossroads between innate and adaptive immunity. Immunol. Rev 220, 35-46
12. Yu, M., Wang, H., Ding, A., Golenbock, D. T., Latz, E., Czura, C. J., Fenton, M. J., Tracey, K. J., and Yang, H. (2006) HMGB1 signals through toll-like receptor (TLR) 4 and TLR2. Shock 26, 174-179
13. Tian, J., Avalos, A. M., Mao, S. Y., Chen, B., Senthil, K., Wu, H., Parroche, P., Drabic, S., Golenbock, D., Sirois, C., Hua, J., An, L. L., Audoly, L., La Rosa, G., Bierhaus, A., Naworth, P., Marshak-Rothstein, A., Crow, M. K., Fitzgerald, K. A., Latz, E., Kiener, P. A., and Coyle, A. J. (2007) Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat. Immunol. 8, 487-496
14. Chen, G. Y., Tang, J., Zheng, P., and Liu, Y. (2009) CD24 and Siglec-10 selectively repress tissue damage-induced immune responses. Science 323, 1722-1725
15. Li, J., Kokkola, R., Tabibzadeh, S., Yang, R., Ochani, M., Qiang, X., Harris, H. E., Czura, C. J., Wang, H., Ulloa, L., Wang, H., Warren, H. S., Moldawer, L. L., Fink, M. P., Andersson, U., Tracey, K. J., and Yang, H. (2003) Structural basis for the proinflammatory cytokine activity of high mobility group box 1. Mol. Med. 9, 37-45
16. Bonaldi, T., Längst, G., Strohner, R., Becker, P. B., and Bianchi, M. E. (2002) The DNA chaperone HMGB1 facilitates ACF/CHRAC-dependent nucleosome sliding. EMBO J. 21, 6865-6873
17. Lu, W., Peterson, R., Dasgupta, A., and Scovell, W. M. (2000) Influence of HMG-1 and adenovirus oncoprotein E1A on early stages of transcriptional preinitiation complex assembly. J. Biol. Chem. 275, 35006-35012
18. Ueda, T., Chou, H., Kawase, T., Shirakawa, H., and Yoshida, M. (2004) Acidic C-tail of HMGB1 is required for its target binding to nucleosome linker DNA and transcription stimulation. Biochemistry 43, 9901-9908
19. Krynetski, E. Y., Krynetskaia, N. F., Bianchi, M. E., and Evans, W. E. (2003) A nuclear protein complex containing high mobility group proteins B1 and B2, heat shock cognate protein 70, ERp60, and glyceraldehyde-3- phosphate dehydrogenase is involved in the cytotoxic response to DNA modified by incorporation of anticancer nucleoside analogues. Cancer Res. 63, 100-106
20. Bustin, M. (1999) Regulation of DNA-dependent activities by the functional motifs of the high-mobility-group chromosomal proteins. Mol. Cell. Biol. 19, 5237-5246
21. Travers, A. A. (2003) Priming the nucleosome: a role for HMGB proteins? EMBO Rep. 4, 131-136
22. Prasad, R., Liu, Y., Deterding, L. J., Poltoratsky, V. P., Kedar, P. S., Horton, J. K., Kanno, S., Asagoshi, K., Hou, E. W., Khodyreva, S. N., Lavrik, O. I., Tomer, K. B., Yasui, A., and Wilson, S. H. (2007) HMGB1 is a cofactor in mammalian base excision repair. Mol. Cell 27, 829-841
23. Bianchi, M. E., Beltrame, M., and Paonessa, G. (1989) Specific recognition of cruciform DNA by nuclear protein HMG1. Science 243, 1056-1059
24. Qi, M. L., Tagawa, K., Enokido, Y., Yoshimura, N., Wada, Y., Watase, K., Ishiura, S., Kanazawa, I., Botas, J., Saitoe, M., Wanker, E. E., and Okazawa, H. (2007) Proteome analysis of soluble nuclear proteins reveals that HMGB1/2 suppress genotoxic stress in polyglutamine diseases. Nat. Cell Biol. 9, 402-414
25. Agresti, A., and Bianchi, M. E. (2003) HMGB proteins and gene expression. Curr. Opin. Genet. Dev. 13, 170-178
26. Scaffidi, P., Misteli, T., and Bianchi, M. E. (2002) Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418, 191-195
27. Wang, H., Bloom, O., Zhang, M., Vishnubhakat, J. M., Ombrellino, M., Che, J., Frazier, A., Yang, H., Ivanova, S., Borovikova, L., Manogue, K. R., Faist, E., Abraham, E., Andersson, J., Andersson, U., Molina, P. E., Abumrad, N. N., Sama, A., and Tracey, K. J. (1999) HMG-1 as a late mediator of endotoxin lethality in mice. Science 285, 248-251
28. Antoine, D. J., Williams, D. P., Kipar, A., Laverty, H., and Park, B. K. (2010) Diet restriction inhibits apoptosis and HMGB1 oxidation and promotes inflammatory cell recruitment during acetaminophen hepatotoxicity. Mol. Med. 16, 479-490
29. Schierbeck, H., Lundbäck, P., Palmblad, K., Klevenvall, L., Erlandsson- Harris, H., Andersson, U., and Ottosson, L. (2011) Monoclonal anti- HMGB1 (high mobility group box chromosomal protein 1) antibody protection in two experimental arthritis models. Mol. Med. 17, 1039-1044
30. Evankovich, J., Cho, S. W., Zhang, R., Cardinal, J., Dhupar, R., Zhang, L., Klune, J. R., Zlotnicki, J., Billiar, T., and Tsung, A. (2010) High mobility group box 1 release from hepatocytes during ischemia and reperfusion injury is mediated by decreased histone deacetylase activity. J. Biol. Chem. 285, 39888-39897
31. Dhupar, R., Klune, J. R., Evankovich, J., Cardinal, J., Zhang, M., Ross, M., Murase, N., Geller, D. A., Billiar, T. R., and Tsung, A. (2011) Interferon regulatory factor 1 mediates acetylation and release of high mobility group box 1 from hepatocytes during murine liver ischemia-reperfusion injury. Shock 35, 293-301
32. Oh, Y. J., Youn, J. H., Ji, Y., Lee, S. E., Lim, K. J., Choi, J. E., and Shin, J. S. (2009) HMGB1 is phosphorylated by classical protein kinase C and is secreted by a calcium-dependent mechanism. J. Immunol. 182, 5800-5809
33. Sterner, R., Vidali, G., and Allfrey, V. G. (1979) Studies of acetylation and deacetylation in high mobility group proteins. Identification of the sites of acetylation in HMG-1. J. Biol. Chem. 254, 11577-11583
34. Stemmer, C., Schwander, A., Bauw, G., Fojan, P., and Grasser, K. D. (2002) Protein kinase CK2 differentially phosphorylates maize chromosomal high mobility group B (HMGB) proteins modulating their stability and DNA interactions. J. Biol. Chem. 277, 1092-1098
35. Krohn, N. M., Yanagisawa, S., and Grasser, K. D. (2002) Specificity of the stimulatory interaction between chromosomal HMGB proteins and the transcription factor Dof2 and its negative regulation by protein kinase CK2-mediated phosphorylation. J. Biol. Chem. 277, 32438-32444
36. Einck, L., and Bustin, M. (1985) The intracellular distribution and function of the high mobility group chromosomal proteins. Exp. Cell Res. 156, 295-310
37. Ge, X., Leung, T. M., Arriazu, E., Lu, Y., Urtasun, R., Christensen, B., Fiel, M. I., Mochida, S., Sørensen, E. S., and Nieto, N. (2014) Osteopontin binding to lipopolysaccharide lowers tumor necrosis factor-α and prevents early alcohol-induced liver injury in mice. Hepatology 59, 1600-1616
38. Cubero, F. J., and Nieto, N. (2012) Arachidonic acid stimulates TNFα production in Kupffer cells via a reactive oxygen species-pERK1/2-Egr1-dependent mechanism. Am. J. Physiol. Gastrointest. Liver Physiol. 303, G228-G239
39. Leung, T. M., Lu, Y., Yan, W., Morón-Concepción, J. A., Ward, S. C., Ge, X., Conde de la Rosa, L., and Nieto, N. (2012) Argininosuccinate synthase conditions the response to acute and chronic ethanol-induced liver injury in mice. Hepatology 55, 1596-1609
40. Hübscher, S. G. (2006) Histological assessment of non-alcoholic fatty liver disease. Histopathology 49, 450-465
41. Huang, H., Nace, G. W., McDonald, K. A., Tai, S., Klune, J. R., Rosborough, B. R., Ding, Q., Loughran, P., Zhu, X., Beer-Stolz, D., Chang, E. B., Billiar, T., and Tsung, A. (2014) Hepatocyte-specific high-mobility group box 1 deletion worsens the injury in liver ischemia/reperfusion: a role for intracellular high-mobility group box 1 in cellular protection. Hepatology 59, 1984-1997
42. Lieber, C. S., and DeCarli, L. M. (1982) The feeding of alcohol in liquid diets: two decades of applications and 1982 update. Alcohol. Clin. Exp. Res. 6, 523-531
43. Antoine, D. J., Williams, D. P., Kipar, A., Jenkins, R. E., Regan, S. L., Sathish, J. G., Kitteringham, N. R., and Park, B. K. (2009) High-mobility group box-1 protein and keratin-18, circulating serum proteins informative of acetaminophen-induced necrosis and apoptosis in vivo. Toxicol. Sci. 112, 521-531
44. Antoine, D. J., Jenkins, R. E., Dear, J. W., Williams, D. P., McGill, M. R., Sharpe, M. R., Craig, D. G., Simpson, K. J., Jaeschke, H., and Park, B. K. (2012) Molecular forms of HMGB1 and keratin-18 as mechanistic biomarkers for mode of cell death and prognosis during clinical acetaminophen hepatotoxicity. J. Hepatol. 56, 1070-1079
45. Nyström, S., Antoine, D. J., Lundbäck, P., Lock, J. G., Nita, A. F., Högstrand, K., Grandien, A., Erlandsson-Harris, H., Andersson, U., and Applequist, S. E. (2013) TLR activation regulates damage-associated molecular pattern isoforms released during pyroptosis. EMBO J. 32, 86-99
46. Yang, H., Lundbäck, P., Ottosson, L., Erlandsson-Harris, H., Venereau, E., Bianchi, M. E., Al-Abed, Y., Andersson, U., Tracey, K. J., and Antoine, D. J. (2012) Redox modification of cysteine residues regulates the cytokine activity of high mobility group box-1 (HMGB1). Mol. Med. 18, 250-259
47. Bertola, A., Mathews, S., Ki, S. H., Wang, H., and Gao, B. (2013) Mouse model of chronic and binge ethanol feeding (the NIAAA model). Nat. Protoc. 8, 627-637
48. Antoine, D. J., Harris, H. E., Andersson, U., Tracey, K. J., and Bianchi, M. E. (2014) A systematic nomenclature for the redox states of high mobility group box (HMGB) proteins. Mol. Med. 20, 135-137
49. Lazaro, R. G., Ueno, A., Do, R., Zhu, N. L., Wu, R., Xu, J., French, S. W., Machida, K., and Tsukamoto, H. (2013) Mouse model of alcoholic hepatitis: no role of Osteopontin. Hepatology 58, suppl., 834A (Abstr. 1289)
50. Lu, B., Antoine, D. J., Kwan, K., Lundbäck, P., Wähämaa, H., Schierbeck, H., Robinson, M., Van Zoelen, M. A., Yang, H., Li, J., Erlandsson-Harris, H., Chavan, S. S., Wang, H., Andersson, U., and Tracey, K. J. (2014) JAK/STAT1 signaling promotes HMGB1 hyperacetylation and nuclear translocation. Proc. Natl. Acad. Sci. U.S.A. 111, 3068-3073
51. Venereau, E., Casalgrandi, M., Schiraldi, M., Antoine, D. J., Cattaneo, A., De Marchis, F., Liu, J., Antonelli, A., Preti, A., Raeli, L., Shams, S. S., Yang, H., Varani, L., Andersson, U., Tracey, K. J., Bachi, A., Uguccioni, M., and Bianchi, M. E. (2012) Mutually exclusive redox forms of HMGB1 promote cell recruitment or proinflammatory cytokine release. J. Exp. Med. 209, 1519-1528
52. Cokol, M., Nair, R., and Rost, B. (2000) Finding nuclear localization signals. EMBO Rep. 1, 411-415
53. Hoppe, G., Talcott, K. E., Bhattacharya, S. K., Crabb, J. W., and Sears, J. E. (2006) Molecular basis for the redox control of nuclear transport of the structural chromatin protein Hmgb1. Exp. Cell Res. 312, 3526-3538
54. Youn, J. H., and Shin, J. S. (2006) Nucleocytoplasmic shuttling of HMGB1 is regulated by phosphorylation that redirects it toward secretion. J. Immunol. 177, 7889-7897
55. Xiao, D. M., Pak, J. H., Wang, X., Sato, T., Huang, F. L., Chen, H. C., and Huang, K. P. (2000) Phosphorylation of HMG-I by protein kinase C attenuates its binding affinity to the promoter regions of protein kinase Cγ and neurogranin/RC3 genes. J. Neurochem. 74, 392-399
56. Kang, H. J., Lee, H., Choi, H. J., Youn, J. H., Shin, J. S., Ahn, Y. H., Yoo, J. S., Paik, Y. K., and Kim, H. (2009) Non-histone nuclear factor HMGB1 is phosphorylated and secreted in colon cancers. Lab. Invest. 89, 948-959
57. Lee, H., Park, M., Shin, N., Kim, G., Kim, Y. G., Shin, J. S., and Kim, H. (2012) High mobility group box-1 is phosphorylated by protein kinase Cζ and secreted in colon cancer cells. Biochem. Biophys. Res. Commun. 424, 321-326