Mutation of caspase-digestion sites in keratin 18 interferes with filament reorganization, and predisposes to hepatocyte necrosis and loss of membrane integrity

Journal of Cell Science

Volumn 127, Issue 7, 2014, Pages 1464-1475

  Weerasinghe, Sujith V W ^a   Ku, Nam On ^b   Altshuler, Peter J ^a   Kwan, Raymond ^a   Omary, M Bishr ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b Yonsei University   (South Korea)

Author keywords

Apoptosis; Intermediate filament; Necrosis

Indexed keywords

CYCLOHEXIMIDE; CYTOKERATIN 18; FAS ANTIGEN; KERATIN; CASPASE; KRT18 PROTEIN, HUMAN;

ARTICLE; CELL DEATH; LIVER CELL; LIVER INJURY; LIVER NECROSIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; ANIMAL; APOPTOSIS; FEMALE; GENETICS; HUMAN; INTERMEDIATE FILAMENT; MALE; METABOLISM; MOUSE; MUTATION; NECROSIS; PATHOLOGY; PHOSPHORYLATION; TRANSGENIC MOUSE;

ANIMALS; APOPTOSIS; CASPASES; FEMALE; HEPATOCYTES; HUMANS; INTERMEDIATE FILAMENTS; KERATIN-18; MALE; MICE; MICE, TRANSGENIC; MUTATION; NECROSIS; PHOSPHORYLATION;

EID: 84897417177     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.138479     Document Type: Article

References (38)

1. Brockmann, K., Meins, M., Taubert, A., Trappe, R., Grond, M. and Hanefeld, F.(2003). A novel GFAP mutation and disseminated white matter lesions: adult Alexander disease? Eur. Neurol. 50, 100-105.
2. Butin-Israeli, V., Adam, S. A., Goldman, A. E. and Goldman, R. D. (2012). Nuclear lamin functions and disease. Trends Genet. 28, 464-471.
3. Byun, Y., Chen, F., Chang, R., Trivedi, M., Green, K. J. and Cryns, V. L. (2001).Caspase cleavage of vimentin disrupts intermediate filaments and promotes apoptosis. Cell Death Differ. 8, 443-450.
4. Caulín, C., Salvesen, G. S. and Oshima, R. G. (1997). Caspase cleavage of keratin 18 and reorganization of intermediate filaments during epithelial cell apoptosis. J. Cell Biol. 138, 1379-1394.
5. Chen, F., Chang, R., Trivedi, M., Capetanaki, Y. and Cryns, V. L. (2003).Caspase proteolysis of desmin produces a dominant-negative inhibitor of intermediate filaments and promotes apoptosis. J. Biol. Chem. 278, 6848-6853.
6. Coulombe, P. A. and Omary, M. B. (2002). 'Hard' and 'soft' principles defining the structure, function and regulation of keratin intermediate filaments. Curr. Opin.Cell Biol. 14, 110-122.
7. Coulombe, P. A., Kerns, M. L. and Fuchs, E. (2009). Epidermolysis bullosa simplex: a paradigm for disorders of tissue fragility. J. Clin. Invest. 119, 1784-1793.
8. Fuchs, E. and Weber, K. (1994). Intermediate filaments: structure, dynamics, function, and disease. Annu. Rev. Biochem. 63, 345-382.
9. Gehringer, M. M. (2004). Microcystin-LR and okadaic acid-induced cellular effects: a dualistic response. FEBS Lett. 557, 1-8.
10. Gilbert, S., Loranger, A., Daigle, N. and Marceau, N. (2001). Simple epithelium keratins 8 and 18 provide resistance to Fas-mediated apoptosis. The protection occurs through a receptor-targeting modulation. J. Cell Biol. 154, 763-774.
11. He, T., Stepulak, A., Holmström, 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.
12. Herrmann, H., Bär, H., Kreplak, L., Strelkov, S. V. and Aebi, U. (2007).Intermediate filaments: from cell architecture to nanomechanics. Nat. Rev. Mol.Cell Biol. 8, 562-573.
13. Kim, S. and Coulombe, P. A. (2007). Intermediate filament scaffolds fulfill mechanical, organizational, and signaling functions in the cytoplasm. Genes Dev. 21, 1581-1597.
14. Ku, N.-O., Zhou, X., Toivola, D. M. and Omary, M. B. (1999). The cytoskeleton of digestive epithelia in health and disease. Am. J. Physiol. 227, G1108-37.
15. Ku, N.-O. and Omary, M. B. (2001). Effect of mutation and phosphorylation of type I keratins on their caspase-mediated degradation. J. Biol. Chem. 276, 26792- 26798.
16. Ku, N.-O. and Omary, M. B. (2006). A disease- and phosphorylation-related nonmechanical function for keratin 8. J. Cell Biol. 174, 115-125.
17. Ku, N.-O., Michie, S., Oshima, R. G. and Omary, M. B. (1995). Chronic hepatitis, hepatocyte fragility, and increased soluble phosphoglycokeratins in transgenic mice expressing a keratin 18 conserved arginine mutant. J. Cell Biol. 131, 1303- 1314.
18. Ku, N.-O., Michie, S. A., Soetikno, R. M., Resurreccion, E. Z., Broome, R. L., Oshima, R. G. and Omary, M. B. (1996). Susceptibility to hepatotoxicity in transgenic mice that express a dominant-negative human keratin 18 mutant.J. Clin. Invest. 98, 1034-1046.
19. Ku, N.-O., Liao, J. and Omary, M. B. (1997). Apoptosis generates stable fragments of human type I keratins. J. Biol. Chem. 272, 33197-33203.
20. 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.
21. Ku, N.-O., Soetikno, R. M. and Omary, M. B. (2003). Keratin mutation in transgenic mice predisposes to Fas but not TNF-induced apoptosis and massive liver injury. Hepatology 37, 1006-1014.
22. 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.
23. Lanktree, M., Cao, H., Rabkin, S. W., Hanna, A. and Hegele, R. A. (2007). Novel LMNA mutations seen in patients with familial partial lipodystrophy subtype 2 (FPLD2; MIM 151660). Clin. Genet. 71, 183-186.
24. Leers, M. P., Kölgen, W., Björklund, V., Bergman, T., Tribbick, G., Persson, B., Björklund, P., Ramaekers, F. C., Björklund, B., Nap, M. et al. (1999).Immunocytochemical detection and mapping of a cytokeratin 18 neo-epitope exposed during early apoptosis. J. Pathol. 187, 567-572.
25. Loranger, A., Duclos, S., Grenier, A., Price, J., Wilson-Heiner, M., Baribault, H.and Marceau, N. (1997). Simple epithelium keratins are required for maintenance of hepatocyte integrity. Am. J. Pathol. 151, 1673-1683.
26. MacFarlane, M., Merrison, W., Dinsdale, D. and Cohen, G. M. (2000). Active caspases and cleaved cytokeratins are sequestered into cytoplasmic inclusions in TRAIL-induced apoptosis. J. Cell Biol. 148, 1239-1254.
27. Marceau, N., Loranger, A., Gilbert, S., Daigle, N. and Champetier, S. (2001).Keratin-mediated resistance to stress and apoptosis in simple epithelial cells in relation to health and disease. Biochem. Cell Biol. 79, 543-555.
28. Marceau, N., Schutte, B., Gilbert, S., Loranger, A., Henfling, M. E., Broers, J. L., Mathew, J. and Ramaekers, F. C. (2007). Dual roles of intermediate filaments in apoptosis. Exp. Cell Res. 313, 2265-2281.
29. 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.
30. Panagopoulou, P., Davos, C. H., Milner, D. J., Varela, E., Cameron, J., Mann, D. L.and Capetanaki, Y. (2008). Desmin mediates TNF-α-induced aggregate formation and intercalated disk reorganization in heart failure. J. Cell Biol. 181, 761-775.
31. Rao, L., Perez, D. and White, E. (1996). Lamin proteolysis facilitates nuclear events during apoptosis. J. Cell Biol. 135, 1441-1455.
32. Schutte, B., Henfling, M., Kölgen, W., Bouman, M., Meex, S., Leers, M. P., Nap, M., Björklund, V., Björklund, P., Björklund, B. et al. (2004). Keratin 8/18 breakdown and reorganization during apoptosis. Exp. Cell Res. 297, 11-26.
33. Schweizer, J., Bowden, P. E., Coulombe, P. A., Langbein, L., Lane, E. B., Magin, T. M., Maltais, L., Omary, M. B., Parry, D. A., Rogers, M. A. et al. (2006). New consensus nomenclature for mammalian keratins. J. Cell Biol. 174, 169-174.
34. Snider, N. T. and Omary, M. B. (2014). Post-translational modifications of intermediate filament proteins: mechanisms and functions. Nat. Rev. Mol. Cell Biol. 15, 163-77.
35. Snider, N. T., Weerasinghe, S. V., Singla, A., Leonard, J. M., Hanada, S., Andrews, P. C., Lok, A. S. and Omary, M. B. (2011). Energy determinants GAPDH and NDPK act as genetic modifiers for hepatocyte inclusion formation.J. Cell Biol. 195, 217-229.
36. Štros, M. (2010). HMGB proteins: interactions with DNA and chromatin. Biochim.Biophys. Acta 1799, 101-113.
37. Toivola, D. M., Omary, M. B., Ku, N.-O., Peltola, O., Baribault, H. and Eriksson, J. E. (1998). Protein phosphatase inhibition in normal and keratin 8/18 assemblyincompetent mouse strains supports a functional role of keratin intermediate filaments in preserving hepatocyte integrity. Hepatology 28, 116-128.
38. Weerasinghe, S. V., Moons, D. S., Altshuler, P. J., Shah, Y. M. and Omary, M. B. (2011). Fibrinogen-γ proteolysis and solubility dynamics during apoptotic mouse liver injury: heparin prevents and treats liver damage. Hepatology 53, 1323-1332.