Keratin 8 phosphorylation regulates its transamidation and hepatocyte Mallory-Denk body formation

FASEB Journal

Volumn 26, Issue 6, 2012, Pages 2318-2326

  Kwan, Raymond ^a   Hanada, Shinichiro ^b   Harada, Masaru ^c   Strnad, Pavel ^d   Li, Daniel H ^e   Omary, M Bishr ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b KURUME UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c UNIVERSITY OF OCCUPATIONAL AND ENVIRONMENTAL HEALTH   (Japan)

^d UNIVERSITY OF ULM   (Germany)

^e AnaSpec   (United States)

Author keywords

Intermediate filaments; Steatohepatitis; Transglutaminase 2

Indexed keywords

CYTOKERATIN 8; PHOSPHOPROTEIN PHOSPHATASE INHIBITOR; SYNTHETIC PEPTIDE;

AMIDATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL INCLUSION; INTERMEDIATE FILAMENT; LIVER CELL; MALE; MALLORY BODY; MALLORY DENK BODY; MOUSE; MYOPATHY; NEUROPATHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SITE DIRECTED MUTAGENESIS; TRANSAMIDATION;

AMINO ACID SEQUENCE; ANIMALS; GLUTAMINE; GTP-BINDING PROTEINS; HEPATOCYTES; INTERMEDIATE FILAMENTS; KERATIN-8; LIVER DISEASES; MALLORY BODIES; MICE; MICE, TRANSGENIC; PHOSPHORYLATION; TRANSGLUTAMINASES;

MUS MUSCULUS;

EID: 84861790466     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-198580     Document Type: Article

References (58)

1. Zatloukal, K., French, S. W., Stumptner, C., Strnad, P., Harada, M., Toivola, D. M., Cadrin, M., and Omary, M. B. (2007) From Mallory to Mallory-Denk bodies: what, how and why? Exp. Cell Res. 313, 2033-2049 (Pubitemid 46842981)
2. Omary, M. B., Ku, N. O., Strnad, P., and Hanada, S. (2009) Toward unraveling the complexity of simple epithelial keratins in human disease. J. Clin. Invest. 119, 1794-1805
3. Matteoni, C. A., Younossi, Z. M., Gramlich, T., Boparai, N., Liu, Y. C., and McCullough, A. J. (1999) Nonalcoholic fatty liver disease: a spectrum of clinical and pathological severity. Gastroenterology 116, 1413-1419 (Pubitemid 29258890)
4. Cortez-Pinto, H., Baptista, A., Camilo, M. E., and De Moura, M. C. (2003) Nonalcoholic steatohepatitis - a long-term follow-up study: comparison with alcoholic hepatitis in ambulatory and hospitalized patients. Dig. Dis. Sci. 48, 1909-1913 (Pubitemid 37419951)
5. Rakoski, M. O., Brown, M. B., Fontana, R. J., Bonkovsky, H. L., Brunt, E. M., Goodman, Z. D., Lok, A. S., and Omary, M. B. (2011) Mallory-Denk bodies are associated with outcomes and histological features in patients with chronic hepatitis C. Clin. Gastroenterol. Hepatol. 9, 902-909
6. Strnad, P., Zatloukal, K., Stumptner, C., Kulaksiz, H., and Denk, H. (2008) Mallory-Denk-bodies: lessons from keratin-containing hepatic inclusion bodies. Biochim Biophys Acta 1782, 764-774
7. Denk, H., Gschnait, F., and Wolff, K. (1975) Hepatocellar hyalin (Mallory bodies) in long-term griseofulvin-treated mice: a new experimental model for the study of hyalin formation. Lab. Invest. 32, 773-776
8. Yokoo, H., Harwood, T. R., Racker, D., and Arak, S. (1982) Experimental production of Mallory bodies in mice by diet containing 3,5-diethoxycarbonyl-1, 4-dihydrocollidine. Gastroenterology 83, 109-113 (Pubitemid 12123697)
9. Magin, T. M., Schroder, R., Leitgeb, S., Wanninger, F., Zatloukal, K., Grund, C., and Melton, D. W. (1998) Lessons from keratin 18 knockout mice: formation of novel keratin filaments, secondary loss of keratin 7 and accumulation of liver-specific keratin 8-positive aggregates. J. Cell Biol. 140, 1441-1451 (Pubitemid 28152992)
10. Zatloukal, K., Stumptner, C., Lehner, M., Denk, H., Baribault, H., Eshkind, L. G., and Franke, W. W. (2000) Cytokeratin 8 protects from hepatotoxicity, and its ratio to cytokeratin 18 determines the ability of hepatocytes to form Mallory bodies. Am. J. Pathol. 156, 1263-1274 (Pubitemid 30660005)
11. Harada, M., Strnad, P., Resurreccion, E. Z., Ku, N. O., and Omary, M. B. (2007) Keratin 18 overexpression but not phosphorylation or filament organization blocks mouse Mallory body formation. Hepatology 45, 88-96 (Pubitemid 46144368)
12. Nakamichi, I., Toivola, D. M., Strnad, P., Michie, S. A., Oshima, R. G., Baribault, H., and Omary, M. B. (2005) Keratin 8 overexpression promotes mouse Mallory body formation. J. Cell Biol. 171, 931-937 (Pubitemid 41815825)
13. Mahajan, V., Klingstedt, T., Simon, R., Nilsson, K. P., Thueringer, A., Kashofer, K., Haybaeck, J., Denk, H., Abuja, P. M., and Zatloukal, K. (2011) Cross beta-sheet conformation of keratin 8 is a specific feature of Mallory-Denk bodies compared to other hepatocyte inclusions. Gastroenterology 141, 1080-1090
14. Bonar, L., Cohen, A. S., and Skinner, M. M. (1969) Characterization of the amyloid fibril as a cross-beta protein. Proc. Soc. Exp. Biol. Med. 131, 1373-1375
15. Glenner, G. G., Eanes, E. D., Bladen, H. A., Linke, R. P., and Termine, J. D. (1974) Beta-pleated sheet fibrils. A comparison of native amyloid with synthetic protein fibrils. J. Histochem. Cytochem. 22, 1141-1158
16. Sunde, M., and Blake, C. C. (1998) From the globular to the fibrous state: protein structure and structural conversion in amyloid formation. Q. Rev. Biophys. 31, 1-39 (Pubitemid 28379176)
17. Cadrin, M., Marceau, N., and French, S. W. (1992) Cytokeratin of apparent high molecular weight in livers from griseofulvinfed mice. J. Hepatol. 14, 226-231
18. Zatloukal, K., Denk, H., Lackinger, E., and Rainer, I. (1989) Hepatocellular cytokeratins as substrates of transglutaminases. Lab. Invest. 61, 603-608 (Pubitemid 20027687)
19. Zatloukal, K., Fesus, L., Denk, H., Tarcsa, E., Spurej, G., and Bock, G. (1992) High amount of epsilon-(gamma-glutamyl)lysine cross-links in Mallory bodies. Lab. Invest. 66, 774-777
20. Denk, H., Bernklau, G., and Krepler, R. (1984) Effect of griseofulvin treatment and neoplastic transformation on transglutaminase activity in mouse liver. Liver 4, 208-213 (Pubitemid 14088674)
21. Riley, N. E., Li, J., Worrall, S., Rothnagel, J. A., Swagell, C., van Leeuwen, F. W., and French, S. W. (2002) The Mallory body as an aggresome: in vitro studies. Exp. Mol. Pathol. 72, 17-23 (Pubitemid 34948278)
22. Tazawa, J., Irie, T., and French, S. W. (1983) Mallory body formation runs parallel to gamma-glutamyl transferase induction in hepatocytes of griseofulvin-fed mice. Hepatology 3, 989-1001 (Pubitemid 14247641)
23. Jeitner, T. M., Bogdanov, M. B., Matson, W. R., Daikhin, Y., Yudkoff, M., Folk, J. E., Steinman, L., Browne, S. E., Beal, M. F., Blass, J. P., and Cooper, A. J. (2001) N(ε)-(γ-L-glutamyl)-L-lysine (GGEL) is increased in cerebrospinal fluid of patients with Huntington's disease. J. Neurochem. 79, 1109-1112 (Pubitemid 33117092)
24. Zainelli, G. M., Ross, C. A., Troncoso, J. C., and Muma, N. A. (2003) Transglutaminase cross-links in intranuclear inclusions in Huntington disease. J. Neuropathol. Exp. Neurol. 62, 14-24 (Pubitemid 36068889)
25. Nemes, Z., Petrovski, G., Aerts, M., Sergeant, K., Devreese, B., and Fesus, L. (2009) Transglutaminase-mediated intramolecular cross-linking of membrane-bound alpha-synuclein promotes amyloid formation in Lewy bodies. J. Biol. Chem. 284, 27252-27264
26. Schmid, A. W., Chiappe, D., Pignat, V., Grimminger, V., Hang, I., Moniatte, M., and Lashuel, H. A. (2009) Dissecting the mechanisms of tissue transglutaminase-induced cross-linking of alpha-synuclein: implications for the pathogenesis of Parkinson disease. J. Biol. Chem. 284, 13128-13142
27. Strnad, P., Harada, M., Siegel, M., Terkeltaub, R. A., Graham, R. M., Khosla, C., and Omary, M. B. (2007) Transglutaminase 2 regulates mallory body inclusion formation and injury-associated liver enlargement. Gastroenterology 132, 1515-1526 (Pubitemid 46627586)
28. Strnad, P., Siegel, M., Toivola, D. M., Choi, K., Kosek, J. C., Khosla, C., and Omary, M. B. (2006) Pharmacologic transglutaminase inhibition attenuates drug-primed liver hypertrophy but not Mallory body formation. FEBS Lett. 580, 2351-2357
29. Stumptner, C., Omary, M. B., Fickert, P., Denk, H., and Zatloukal, K. (2000) Hepatocyte cytokeratins are hyperphosphorylated at multiple sites in human alcoholic hepatitis and in a mallory body mouse model. Am. J. Pathol. 156, 77-90 (Pubitemid 30644441)
30. Ku, N. O., and Omary, M. B. (2006) A disease- and phosphorylation-related nonmechanical function for keratin 8. J. Cell Biol. 174, 115-125
31. Ku, N. O., Toivola, D. M., Zhou, Q., Tao, G. Z., Zhong, B., and Omary, M. B. (2004) Studying simple epithelial keratins in cells and tissues. Methods Cell Biol. 78, 489-517
32. Scheuer, P. J. (1991) Classification of chronic viral hepatitis: a need for reassessment. J. Hepatol. 13, 372-374
33. Omary, M. B., Ku, N. O., Tao, G. Z., Toivola, D. M., and Liao, J. (2006) "Heads and tails" of intermediate filament phosphorylation: multiple sites and functional insights. Trends Biochem. Sci. 31, 383-394 (Pubitemid 44038919)
34. Sugimura, Y., Hosono, M., Wada, F., Yoshimura, T., Maki, M., and Hitomi, K. (2006) Screening for the preferred substrate sequence of transglutaminase using a phage-displayed peptide library: identification of peptide substrates for TGASE 2 and Factor XIIIA. J. Biol. Chem. 281, 17699-17706 (Pubitemid 44035568)
35. Cadrin, M., French, S. W., and Wong, P. T. (1991) Alteration in molecular structure of cytoskeleton proteins in griseofulvin-treated mouse liver: a pressure tuning infrared spectroscopy study. Exp. Mol. Pathol. 55, 170-179
36. Harada, M., Hanada, S., Toivola, D. M., Ghori, N., and Omary, M. B. (2008) Autophagy activation by rapamycin eliminates mouse Mallory-Denk bodies and blocks their proteasome inhibitor-mediated formation. Hepatology 47, 2026-2035 (Pubitemid 351945569)
37. Kachi, K., Wong, P. T., and French, S. W. (1993) Molecular structural changes in Mallory body proteins in human and mouse livers: an infrared spectroscopy study. Exp. Mol. Pathol. 59, 197-210 (Pubitemid 24126642)
38. Strnad, P., Tao, G. Z., So, P., Lau, K., Schilling, J., Wei, Y., Liao, J., and Omary, M. B. (2008) "Toxic memory" via chaperone modification is a potential mechanism for rapid Mallory-Denk body reinduction. Hepatology 48, 931-942
39. Hanada, S., Snider, N. T., Brunt, E. M., Hollenberg, P. F., and Omary, M. B. (2010) Gender dimorphic formation of mouse Mallory-Denk bodies and the role of xenobiotic metabolism and oxidative stress. Gastroenterology 138, 1607-1617
40. Shin, D. M., Jeon, J. H., Kim, C. W., Cho, S. Y., Kwon, J. C., Lee, H. J., Choi, K. H., Park, S. C., and Kim, I. G. (2004) Cell type-specific activation of intracellular transglutaminase 2 by oxidative stress or ultraviolet irradiation: implications of transglutaminase 2 in age-related cataractogenesis. J. Biol. Chem. 279, 15032-15039
41. Lesort, M., Tucholski, J., Zhang, J., and Johnson, G. V. (2000) Impaired mitochondrial function results in increased tissue transglutaminase activity in situ. J. Neurochem. 75, 1951-1961
42. Shin, D. M., Jeon, J. H., Kim, C. W., Cho, S. Y., Lee, H. J., Jang, G. Y., Jeong, E. M., Lee, D. S., Kang, J. H., Melino, G., Park, S. C., and Kim, I. G. (2008) TGFβ mediates activation of transglutaminase 2 in response to oxidative stress that leads to protein aggregation. FASEB J. 22, 2498-2507 (Pubitemid 351948667)
43. Honkanen, R. E., and Golden, T. (2002) Regulators of serine/threonine protein phosphatases at the dawn of a clinical era? Curr. Med. Chem. 9, 2055-2075 (Pubitemid 35256504)
44. Haystead, T. A., Sim, A. T., Carling, D., Honnor, R. C., Tsukitani, Y., Cohen, P., and Hardie, D. G. (1989) Effects of the tumour promoter okadaic acid on intracellular protein phosphorylation and metabolism. Nature 337, 78-81 (Pubitemid 19022553)
45. Pinkas, D. M., Strop, P., Brunger, A. T., and Khosla, C. (2007) Transglutaminase 2 undergoes a large conformational change upon activation. PLoS Biol. 5, e327
46. Siegel, M., Strnad, P., Watts, R. E., Choi, K., Jabri, B., Omary, M. B., and Khosla, C. (2008) Extracellular transglutaminase 2 is catalytically inactive, but is transiently activated upon tissue injury. PLoS One 3, e1861
47. Stamnaes, J., Pinkas, D. M., Fleckenstein, B., Khosla, C., and Sollid, L. M. (2010) Redox regulation of transglutaminase 2 activity. J. Biol. Chem. 285, 25402-25409
48. Toivola, D. M., Strnad, P., Habtezion, A., and Omary, M. B. (2010) Intermediate filaments take the heat as stress proteins. Trends Cell Biol. 20, 79-91
49. Tao, G. Z., Nakamichi, I., Ku, N. O., Wang, J., Frolkis, M., Gong, X., Zhu, W., Pytela, R., and Omary, M. B. (2006) Bispecific and human disease-related anti-keratin rabbit monoclonal antibodies. Exp. Cell Res. 312, 411-422 (Pubitemid 41804106)
50. Ku, N. O., Azhar, S., and Omary, M. B. (2002) Keratin 8 phosphorylation by p38 kinase regulates cellular keratin filament reorganization: modulation by a keratin 1-like disease causing mutation. J. Biol. Chem. 277, 10775-10782 (Pubitemid 34952830)
51. He, T., Stepulak, A., Holmstrom, T. H., Omary, M. B., and Eriksson, J. E. (2002) The intermediate filament protein keratin 8 is a novel cytoplasmic substrate for c-Jun N-terminal kinase. J. Biol. Chem. 277, 10767-10774 (Pubitemid 34952829)
52. Snider, N. T., Weerasinghe, S. V., Iniguez-Lluhi, J. A., Herrmann, H., and Omary, M. B. (2011) Keratin hypersumoylation alters filament dynamics and is a marker for human liver disease and keratin mutation. J. Biol. Chem. 286, 2273-2284
53. Toivola, D. M., Zhou, Q., English, L. S., and Omary, M. B. (2002) Type II keratins are phosphorylated on a unique motif during stress and mitosis in tissues and cultured cells. Mol. Biol. Cell 13, 1857-1870 (Pubitemid 34651477)
54. de Lima, V. M., Oliveira, C. P., Alves, V. A., Chammas, M. C., Oliveira, E. P., Stefano, J. T., de Mello, E. S., Cerri, G. G., Carrilho, F. J., and Caldwell, S. H. (2008) A rodent model of NASH with cirrhosis, oval cell proliferation and hepatocellular carcinoma. J. Hepatol. 49, 1055-1061
55. Tatsukawa, H., Fukaya, Y., Frampton, G., Martinez-Fuentes, A., Suzuki, K., Kuo, T. F., Nagatsuma, K., Shimokado, K., Okuno, M., Wu, J., Iismaa, S., Matsuura, T., Tsukamoto, H., Zern, M. A., Graham, R. M., and Kojima, S. (2009) Role of transglutaminase 2 in liver injury via cross-linking and silencing of transcription factor Sp1. Gastroenterology 136, 1783-1795, e1710
56. Goebel, H. H. (2003) Congenital myopathies at their molecular dawning. Muscle Nerve 27, 527-548
57. Liem, R. K., and Messing, A. (2009) Dysfunctions of neuronal and glial intermediate filaments in disease. J. Clin. Invest. 119, 1814-1824
58. Armstrong, R. A., and Cairns, N. J. (2006) Topography of alpha-internexin-positive neuronal aggregates in 10 patients with neuronal intermediate filament inclusion disease. Eur. J. Neurol. 13, 528-532 (Pubitemid 43823370)