Energy determinants GAPDH and NDPK act as genetic modifiers for hepatocyte inclusion formation

Journal of Cell Biology

Volumn 195, Issue 2, 2011, Pages 217-229

  Snider, Natasha T ^a   Weerasinghe, Sujith V W ^a   Singla, Amika ^a   Leonard, Jessica M ^a   Hanada, Shinichiro ^b   Andrews, Philip C ^a   Lok, Anna S ^a   Omary, M Bishr ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b KURUME UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 DIHYDRO 2,4,6 TRIMETHYL 3,5 PYRIDINEDICARBOXYLIC ACID DIETHYL ESTER; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE (NADP); NUCLEOSIDE DIPHOSPHATE KINASE; REACTIVE OXYGEN METABOLITE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; C3H MOUSE; C57BL 10 MOUSE; CELL INCLUSION; CELL MIGRATION; CELL STRAIN; CONTROLLED STUDY; DNA MODIFICATION; DOWN REGULATION; ENZYME ACTIVITY; HUMAN; HUMAN TISSUE; LIVER CELL; LIVER DISEASE; LIVER INJURY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; HEPATOCYTES; HUMANS; INCLUSION BODIES; LIVER DISEASES; MICE; MICE, INBRED STRAINS; NUCLEOSIDE-DIPHOSPHATE KINASE; OXIDATIVE STRESS; PYRIDINES; REACTIVE OXYGEN SPECIES;

MURINAE; MUS;

EID: 80155138553     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201102142     Document Type: Article

References (57)

1. Aithal, G.P., J.A. Thomas, P.V. Kaye, A. Lawson, S.D. Ryder, I. Spendlove, A.S. Austin, J.G. Freeman, L. Morgan, and J. Webber. 2008. Randomized, placebo-controlled trial of pioglitazone in nondiabetic subjects with nonalcoholic steatohepatitis. Gastroenterology. 135:1176-1184. http://dx.doi.org/10.1053/j.gastro.2008.06.047
2. Anstee, Q.M., A.K. Daly, and C.P. Day. 2011. Genetics of alcoholic and nonalcoholic fatty liver disease. Semin. Liver Dis. 31:128-146. http://dx.doi.org/10.1055/s-0031-1276643
3. Arnaud-Dabernat, S., K. Masse, M. Smani, E. Peuchant, M. Landry, P.M. Bourbon, R. Le Floch, J.Y. Daniel, and M. Larou. 2004. Nm23-M2/NDP kinase B induces endogenous c-myc and nm23-M1/NDP kinase A overexpression in BAF3 cells. Both NDP kinases protect the cells from oxidative stress-induced death. Exp. Cell Res. 301:293-304. http://dx.doi.org/10.1016/j.yexcr.2004.07.026
4. Askanas, V., W.K. Engel, and A. Nogalska. 2009. Inclusion body myositis: A degenerative muscle disease associated with intra-muscle fiber multiprotein aggregates, proteasome inhibition, endoplasmic reticulum stress and decreased lysosomal degradation. Brain Pathol. 19:493-506. http://dx.doi.org/10.1111/j.1750-3639.2009.00290.x
5. Beck, J.A., S. Lloyd, M. Hafezparast, M. Lennon-Pierce, J.T. Eppig, M.F. Festing, and E.M. Fisher. 2000. Genealogies of mouse inbred strains. Nat. Genet. 24:23-25. http://dx.doi.org/10.1038/71641
6. Berg, J.M., J.L. Tymoczko, and L. Stryer. 2002. Biochemistry. W.H. Freeman, New York. 1050 pp.
7. Boissan, M., S. Dabernat, E. Peuchant, U. Schlattner, I. Lascu, and M.L. Lacombe. 2009. The mammalian Nm23/NDPK family: From metastasis control to cilia movement. Mol. Cell. Biochem. 329:51-62. http://dx.doi.org/10.1007/s11010-009-0120-7
8. Braun, S., C. Mauch, P. Boukamp, and S. Werner. 2007. Novel roles of NM23 proteins in skin homeostasis, repair and disease. Oncogene. 26:532-542. http://dx.doi.org/10.1038/sj.onc.1209822
9. Cederbaum, A.I., Y. Lu, and D. Wu. 2009. Role of oxidative stress in alcoholinduced liver injury. Arch. Toxicol. 83:519-548. http://dx.doi.org/10.1007/s00204-009-0432-0
10. Chowdhury, I., Y. Mo, L. Gao, A. Kazi, A.B. Fisher, and S.I. Feinstein. 2009. Oxidant stress stimulates expression of the human peroxiredoxin 6 gene by a transcriptional mechanism involving an antioxidant response element. Free Radic. Biol. Med. 46:146-153. http://dx.doi.org/10.1016/j.freeradbiomed.2008.09.027
11. Colell, A., J.E. Ricci, S. Tait, S. Milasta, U. Maurer, L. Bouchier-Hayes, P. Fitzgerald, A. Guio-Carrion, N.J. Waterhouse, C.W. Li, et al. 2007. GAPDH and autophagy preserve survival after apoptotic cytochrome c release in the absence of caspase activation. Cell. 129:983-997. http://dx.doi.org/10.1016/j.cell.2007.03.045
12. Cortez-Pinto, H., A. Baptista, M.E. Camilo, and M.C. De Moura. 2003. Nonalcoholic steatohepatitis-a long-term follow-up study: comparison with alcoholic hepatitis in ambulatory and hospitalized patients. Dig. Dis. Sci. 48:1909-1913. http://dx.doi.org/10.1023/A:1026152415917
13. Ebert, B., M. Kisiela, P. Malátková, Y. El-Hawari, and E. Maser. 2010. Regulation of human carbonyl reductase 3 (CBR3; SDR21C2) expression by Nrf2 in cultured cancer cells. Biochemistry. 49:8499-8511. http://dx.doi.org/10.1021/bi100814d
14. Eruslanov, E., and S. Kusmartsev. 2010. Identification of ROS using oxidized DCFDA and flow-cytometry. Methods Mol. Biol. 594:57-72. http://dx.doi.org/10.1007/978-1-60761-411-1_4
15. Fleming, K.A., and J.O. McGee. 1984. Alcohol induced liver disease. J. Clin. Pathol. 37:721-733. http://dx.doi.org/10.1136/jcp.37.7.721
16. Gerber, M.A., W. Orr, H. Denk, F. Schaffner, and H. Popper. 1973. Hepatocellular hyalin in cholestasis and cirrhosis: Its diagnostic significance. Gastroenterology. 64:89-98.
17. Goldfarb, L.G., and M.C. Dalakas. 2009. Tragedy in a heartbeat: malfunctioning desmin causes skeletal and cardiac muscle disease. J. Clin. Invest. 119:1806-1813. http://dx.doi.org/10.1172/JCI38027
18. Gramlich, T., D.E. Kleiner, A.J. McCullough, C.A. Matteoni, N. Boparai, and Z.M. Younossi. 2004. Pathologic features associated with fibrosis in nonalcoholic fatty liver disease. Hum. Pathol. 35:196-199. http://dx.doi.org/10.1016/j.humpath.2003.09.018
19. Gruber, C.W., M. Cemazar, B. Heras, J.L. Martin, and D.J. Craik. 2006. Protein disulfide isomerase: The structure of oxidative folding. Trends Biochem. Sci. 31:455-464. http://dx.doi.org/10.1016/j.tibs.2006.06.001
20. Hanada, S., P. Strnad, E.M. Brunt, and M.B. Omary. 2008. The genetic background modulates susceptibility to mouse liver Mallory-Denk body formation and liver injury. Hepatology. 48:943-952. http://dx.doi.org/10.1002/hep.22436
21. Hanada, S., N.T. Snider, E.M. Brunt, P.F. Hollenberg, and M.B. Omary. 2010. Gender dimorphic formation of mouse Mallory-Denk bodies and the role of xenobiotic metabolism and oxidative stress. Gastroenterology. 138:1607-1617. http://dx.doi.org/10.1053/j.gastro.2009.12.055
22. Hara, M.R., N. Agrawal, S.F. Kim, M.B. Cascio, M. Fujimuro, Y. Ozeki, M. Takahashi, J.H. Cheah, S.K. Tankou, L.D. Hester, et al. 2005. S-nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding. Nat. Cell Biol. 7:665-674. http://dx.doi.org/10.1038/ncb1268
23. Harada, M., S. Hanada, D.M. Toivola, N. Ghori, and M.B. Omary. 2008. Autophagy activation by rapamycin eliminates mouse Mallory-Denk bodies and blocks their proteasome inhibitor-mediated formation. Hepatology. 47:2026-2035. http://dx.doi.org/10.1002/hep.22294
24. Jeong, J.Y., Y. Wang, and A.J. Sytkowski. 2009. Human selenium binding protein-1 (hSP56) interacts with VDU1 in a selenium-dependent manner. Biochem. Biophys. Res. Commun. 379:583-588. http://dx.doi.org/10.1016/j.bbrc.2008.12.110
25. Klaassen, C.D., and S.A. Reisman. 2010. Nrf2 the rescue: Effects of the antioxidative/electrophilic response on the liver. Toxicol. Appl. Pharmacol. 244:57-65. http://dx.doi.org/10.1016/j.taap.2010.01.013
26. Kornberg, M.D., N. Sen, M.R. Hara, K.R. Juluri, J.V. Nguyen, A.M. Snowman, L. Law, L.D. Hester, and S.H. Snyder. 2010. GAPDH mediates nitrosylation of nuclear proteins. Nat. Cell Biol. 12:1094-1100. http://dx.doi.org/10.1038/ncb2114
27. Ku, N.O., J.K. Lim, S.M. Krams, C.O. Esquivel, E.B. Keeffe, T.L. Wright, D.A. Parry, and M.B. Omary. 2005. Keratins as susceptibility genes for end-stage liver disease. Gastroenterology. 129:885-893. http://dx.doi.org/10.1053/j.gastro.2005.06.065
28. Lanfear, J., J. Fleming, M. Walker, and P. Harrison. 1993. Different patterns of regulation of the genes encoding the closely related 56 kDa selenium-and acetaminophen-binding proteins in normal tissues and during carcinogenesis. Carcinogenesis. 14:335-340. http://dx.doi.org/10.1093/carcin/14.3.335
29. Lee, E., J. Jeong, S.E. Kim, E.J. Song, S.W. Kang, and K.J. Lee. 2009. Multiple functions of Nm23-H1 are regulated by oxido-reduction system. PLoS ONE. 4:e7949. http://dx.doi.org/10.1371/journal.pone.0007949
30. Liem, R.K., and A. Messing. 2009. Dysfunctions of neuronal and glial intermediate filaments in disease. J. Clin. Invest. 119:1814-1824. http://dx.doi.org/10.1172/JCI38003
31. Marouga, R., S. David, and E. Hawkins. 2005. The development of the DIGE system: 2D fluorescence difference gel analysis technology. Anal. Bioanal. Chem. 382:669-678. http://dx.doi.org/10.1007/s00216-005-3126-3
32. Mohanty, S.R., T.N. Troy, D. Huo, B.L. O'Brien, D.M. Jensen, and J. Hart. 2009. Influence of ethnicity on histological differences in non-alcoholic fatty liver disease. J. Hepatol. 50:797-804. http://dx.doi.org/10.1016/j.jhep.2008.11.017
33. Muchowski, P.J., and J.L. Wacker. 2005. Modulation of neurodegeneration by molecular chaperones. Nat. Rev. Neurosci. 6:11-22. http://dx.doi.org/10.1038/nrn1587
34. Nakajima, H., W. Amano, A. Fujita, A. Fukuhara, Y.T. Azuma, F. Hata, T. Inui, and T. Takeuchi. 2007. The active site cysteine of the proapoptotic protein glyceraldehyde-3-phosphate dehydrogenase is essential in oxidative stress-induced aggregation and cell death. J. Biol. Chem. 282:26562-26574. http://dx.doi.org/10.1074/jbc.M704199200
35. Nakajima, H., W. Amano, T. Kubo, A. Fukuhara, H. Ihara, Y.T. Azuma, H. Tajima, T. Inui, A. Sawa, and T. Takeuchi. 2009. Glyceraldehyde-3-phosphate dehydrogenase aggregate formation participates in oxidative stress-induced cell death. J. Biol. Chem. 284:34331-34341. http://dx.doi.org/10.1074/jbc.M109.027698
36. Nguyen, G.C., and P.J. Thuluvath. 2008. Racial disparity in liver disease: Biological, cultural, or socioeconomic factors. Hepatology. 47:1058-1066. http://dx.doi.org/10.1002/hep.22223
37. Ou, X.M., C.A. Stockmeier, H.Y. Meltzer, J.C. Overholser, G.J. Jurjus, L. Dieter, K. Chen, D. Lu, C. Johnson, M.B. Youdim, et al. 2010. A novel role for glyceraldehyde-3-phosphate dehydrogenase and monoamine oxidase B cascade in ethanol-induced cellular damage. Biol. Psychiatry. 67:855-863. http://dx.doi.org/10.1016/j.biopsych.2009.10.032
38. Porat, A., Y. Sagiv, and Z. Elazar. 2000. A 56-kDa selenium-binding protein participates in intra-Golgi protein transport. J. Biol. Chem. 275:14457-14465. http://dx.doi.org/10.1074/jbc.275.19.14457
39. Postel, E.H., S.J. Berberich, S.J. Flint, and C.A. Ferrone. 1993. Human c-myc transcription factor PuF identified as nm23-H2 nucleoside diphosphate kinase, a candidate suppressor of tumor metastasis. Science. 261:478-480. http://dx.doi.org/10.1126/science.8392752
40. Promrat, K., G. Lutchman, G.I. Uwaifo, R.J. Freedman, A. Soza, T. Heller, E. Doo, M. Ghany, A. Premkumar, Y. Park, et al. 2004. A pilot study of pioglitazone treatment for nonalcoholic steatohepatitis. Hepatology. 39:188-196. http://dx.doi.org/10.1002/hep.20012
41. Räisänen, S.R., P. Lehenkari, M. Tasanen, P. Rahkila, P.L. Härkönen, and H.K. Väänänen. 1999. Carbonic anhydrase III protects cells from hydrogen peroxide-induced apoptosis. FASEB J. 13:513-522.
42. Rakoski, M.O., M.B. Brown, R.J. Fontana, H.L. Bonkovsky, E.M. Brunt, Z.D. Goodman, A.S. Lok, and M.B. Omary; HALT-C Trial Group. 2011. Mallory-Denk bodies are associated with outcomes and histologic features in patients with chronic hepatitis C. Clin. Gastroenterol. Hepatol. 9:902-909. http://dx.doi.org/10.1016/j.cgh.2011.07.006
43. Sanyal, A.J., N. Chalasani, K.V. Kowdley, A. McCullough, A.M. Diehl, N.M. Bass, B.A. Neuschwander-Tetri, J.E. Lavine, J. Tonascia, A. Unalp, et al; NASH CRN. 2010. Pioglitazone, vitamin E, or placebo for nonalcoholic steatohepatitis. N. Engl. J. Med. 362:1675-1685. http://dx.doi.org/10.1056/NEJMoa0907929
44. Sen, N., M.R. Hara, M.D. Kornberg, M.B. Cascio, B.I. Bae, N. Shahani, B. Thomas, T.M. Dawson, V.L. Dawson, S.H. Snyder, and A. Sawa. 2008. Nitric oxide-induced nuclear GAPDH activates p300/CBP and mediates apoptosis. Nat. Cell Biol. 10:866-873. http://dx.doi.org/10.1038/ncb1747
45. Sen, N., M.R. Hara, A.S. Ahmad, M.B. Cascio, A. Kamiya, J.T. Ehmsen, N. Agrawal, L. Hester, S. Doré, S.H. Snyder, and A. Sawa. 2009. GOSPEL: A neuroprotective protein that binds to GAPDH upon S-nitrosylation. Neuron. 63:81-91. http://dx.doi.org/10.1016/j.neuron.2009.05.0
46. Smith, D.M., N. Benaroudj, and A. Goldberg. 2006. Proteasomes and their associated ATPases: A destructive combination. J. Struct. Biol. 156:72-83. http://dx.doi.org/10.1016/j.jsb.2006.04.012
47. Snider, N.T., S.V. Weerasinghe, J.A. Iñiguez-Lluhí, H. Herrmann, and M.B. Omary. 2011. Keratin hypersumoylation alters filament dynamics and is a marker for human liver disease and keratin mutation. J. Biol. Chem. 286:2273-2284. http://dx.doi.org/10.1074/jbc.M110.171314
48. Steeg, P.S., and D. Theodorescu. 2008. Metastasis: A therapeutic target for cancer. Nat. Clin. Pract. Oncol. 5:206-219. http://dx.doi.org/10.1038/ncponc1066
49. Su, T., and D.J. Waxman. 2004. Impact of dimethyl sulfoxide on expression of nuclear receptors and drug-inducible cytochromes P450 in primary rat hepatocytes. Arch. Biochem. Biophys. 424:226-234. http://dx.doi.org/10.1016/j.abb.2004.02.008
50. Tristan, C., N. Shahani, T.W. Sedlak, and A. Sawa. 2011. The diverse functions of GAPDH: Views from different subcellular compartments. Cell. Signal. 23:317-323. http://dx.doi.org/10.1016/j.cellsig.2010.08.003
51. Whalen, R., and T.D. Boyer. 1998. Human glutathione S-transferases. Semin. Liver Dis. 18:345-358. http://dx.doi.org/10.1055/s-2007-1007169
52. Wong, C.M., A.K. Cheema, L. Zhang, and Y.J. Suzuki. 2008. Protein carbonylation as a novel mechanism in redox signaling. Circ. Res. 102:310-318. http://dx.doi.org/10.1161/CIRCRESAHA.107.159814
53. Wong, C.M., L. Marcocci, L. Liu, and Y.J. Suzuki. 2010. Cell signaling by protein carbonylation and decarbonylation. Antioxid. Redox Signal. 12:393-404. http://dx.doi.org/10.1089/ars.2009.2805
54. Wood, Z.A., L.B. Poole, and P.A. Karplus. 2003. Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science. 300:650-653. http://dx.doi.org/10.1126/science.1080405
55. Wu, Y., S.I. Feinstein, Y. Manevich, I. Chowdhury, J.H. Pak, A. Kazi, C. Dodia, D.W. Speicher, and A.B. Fisher. 2009. Mitogen-activated protein kinasemediated phosphorylation of peroxiredoxin 6 regulates its phospholipase A(2) activity. Biochem. J. 419:669-679. http://dx.doi.org/10.1042/BJ20082061
56. Yokoo, H., T.R. Harwood, D. Racker, and S. Arak. 1982. Experimental production of Mallory bodies in mice by diet containing 3,5-diethoxycarbonyl-1, 4-dihydrocollidine. Gastroenterology. 83:109-113.
57. Zatloukal, K., S.W. French, C. Stumptner, P. Strnad, M. Harada, D.M. Toivola, M. Cadrin, and M.B. Omary. 2007. From Mallory to Mallory-Denk bodies: What, how and why? Exp. Cell Res. 313:2033-2049. http://dx.doi.org/10.1016/j.yexcr.2007.04.024