Vacuolar-type H+-ATPase V1A subunit is a molecular partner of Wolfram syndrome 1 (WFS1) protein, which regulates its expression and stability

Human Molecular Genetics

Volumn 22, Issue 2, 2013, Pages 203-217

  Gharanei, Seley ^a   Zatyka, Malgorzata ^a   Astuti, Dewi ^a   Fenton, Janine ^a   Sik, Attila ^a,b   Nagy, Zsuzsanna ^a   Barrett, Timothy G ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROGEN POTASSIUM ADENOSINE TRIPHOSPHATASE; MEMBRANE PROTEIN; PEPTIDES AND PROTEINS; PROTON PUMP; UNCLASSIFIED DRUG; WFS1 PROTEIN;

ADENOVIRUS; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL CYCLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; EMBRYO; ENDOPLASMIC RETICULUM STRESS; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; NEUROBLASTOMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN STABILITY; WILD TYPE;

APOPTOSIS; CARRIER PROTEINS; CELL CYCLE; CELL LINE; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION REGULATION; HEAT-SHOCK PROTEINS; HUMANS; MEMBRANE PROTEINS; NEURONS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STABILITY; PROTEIN SUBUNITS; PROTEIN TRANSPORT; PROTON PUMPS; SECRETORY VESICLES; SODIUM-POTASSIUM-EXCHANGING ATPASE; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 84871584318     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds400     Document Type: Article

References (33)

1. Prusiner, S.B. (2001) Neurodegenerative diseases and prions. N. Eng. J. Med., 344, 1516-1526.
2. Barrett, T.G., Bundey, S.E. and Macleod, A.F. (1995) Neurodegeneration and diabetes-UK nationwide study of Wolfram (Didmoad) syndrome. Lancet, 346, 1458-1463.
3. Genis, D., Davalos, A., Molins, A. and Ferrer, I. (1997) Wolfram syndrome: a neuropathological study. Acta Neuropathol., 93, 426-429.
4. Inoue, Y., Tanizawa, J., Wasson, J. and Behn, P. (1998) A gene encoding a transmembrane protein is mutated in patients with diabetes mellitus and optic atrophy (Wolfram syndrome). Nat. Genet., 20, 143-148.
5. Strom, T.M., Hortnagel, K., Hofmann, S., Gekeler, F., Scharfe, C., Rabl, W., Gerbitz, K.D. and Meitinger, T. (1998) Diabetes insipidus, diabetes mellitus, optic atrophy and deafness (DIDMOAD) caused by mutations in a novel gene (Wolframin) coding for a predicted transmembrane protein. Hum. Mol. Genet., 7, 2021-2028.
6. Takeda, K., Inoue, H., Tanizawa, Y., Matsuzaki, Y., Oba, J., Watanabe, Y., Shinoda, K. and Oka, Y. (2001)WFS1 (Wolfram syndrome 1) gene product: predominant subcellular localization to endoplasmic reticulum in cultured cells and neuronal expression in rat brain. Hum. Mol. Genet., 10, 477-484.
7. Fonseca, S.G., Fukuma, M., Lipson, K.L., Nguyen, L.X., Allen, J.R., Oka, Y. and Urano, F. (2005) WFS1 is a novel component of the unfolded protein response and maintains homeostasis of the endoplasmic reticulum in pancreatic beta-cells. J. Biol. Chem., 280, 39609-39615.
8. Riggs, A.C., Bernal-Mizrachi, E., Ohsugi, M., Wasson, J., Fatrai, S., Welling, C., Murray, J., Schmidt, R.E., Herrera, P.L. and Permutt, M.A. (2005) Mice conditionally lacking the Wolfram gene in pancreatic islet beta cells exhibit diabetes as a result of enhanced endoplasmic reticulum stress and apoptosis. Diabetologia, 48, 2313-2321.
9. Yamada, T., Ishihara, H., Tamura, A., Takahashi, R., Yamaguchi, S., Takei, D., Tokita, A., Satake, C., Tashiro, F., Katagiri, H. et al. (2006) WFS1-deficiency increases endoplasmic reticulum stress, impairs cell cycle progression and triggers the apoptotic pathway specifically in pancreatic beta-cells. Hum. Mol. Genet., 15, 1600-1609.
10. Philbrook, C., Fritz, E. and Weiher, H. (2005) Expressional and functional studies of Wolframin, the gene function deficient in Wolfram syndrome, in mice and patient cells. Exp. Gerontol., 40, 671-678.
11. Luuk, H., Koks, S., Plaas, M., Hannibal, J., Rehfeld, J.F. and Vasar, E. (2008) Distribution of Wfs1 protein in the central nervous system of the mouse and its relation to clinical symptoms of the Wolfram syndrome. J. Comp. Neurol., 509, 642-660.
12. Swift, R.G., Sadler, D.B. and Swift, M. (1990) Psychiatric findings in Wolfram syndrome homozygotes. Lancet, 336, 667-669.
13. Kõks, S., Planken, A., Luuk, H. and Vasar, E. (2002) Cat odour exposure increases the expression of Wolframin gene in the amygdaloid area of rat. Neurosci. Lett., 322, 116-120.
14. Luuk, H., Plaas, M., Raud, S., Innos, J., Sutt, S., Lasner, H., Abramov, U., Kurrikoff, K., Koks, S. and Vasar, E. (2009) Wfs1-deficient mice display impaired behavioural adaptation in stressful environment. Behav. Brain Res., 198, 334-345.
15. Fonseca, S.G., Ishigaki, S., Oslowski, C.M., Lu, S., Lipson, K.L., Ghosh, R., Hayashi, E., Ishihara, H., Oka, Y., Permutt, M.A. et al. (2010) Wolfram syndrome 1 gene negatively regulates ER stress signaling in rodent and human cells. J. Clin. Invest., 120, 744-755.
16. Zatyka, M., Ricketts, C., Xavier, G.D., Minton, J., Fenton, S., Hofmann-Thiel, S., Rutter, G.A. and Barrett, T.G. (2008) Sodium-potassium ATPase beta 1 subunit is a molecular partner of Wolframin, an endoplasmic reticulum protein involved in ER stress. Hum. Mol. Genet., 17, 190-200.
17. Hatanaka, M., Tanabe, K., Yanai, A., Ohta, Y., Kondo, M., Akiyama, M., Shinoda, K., Oka, Y. and Tanizawa, Y. (2011) Wolfram syndrome 1 gene (WFS1) product localizes to secretory granules and determines granule acidification in pancreatic b-cells. Hum. Mol. Genet., 20, 1274-1284.
18. Payne, W.P.B.a.S.L. (2005). High-content screening in oncology using fluorescence microplate cytometry. Nat. Methods, 2, i-ii.
19. Short, B. (2010) The acid test of v-ATPase function. J. Cell Biol., 189, 773.
20. Futai, M., Oka, T., Sun-Wada, G., Moriyama, Y., Kanazawa, H. and Wada, Y. (2000) Luminal acidification of diverse organelles by V-ATPase in animal cells. J. Exp. Biol., 203, 107-116.
21. Ishihara, H., Takeda, S., Tamura, A., Takahashi, R., Yamaguchi, S., Takei, D., Yamada, T., Inoue, H., Soga, H., Katagiri, H. et al. (2004) Disruption of the WFS1 gene in mice causes progressive beta-cell loss and impaired stimulus-secretion coupling in insulin secretion. Hum. Mol. Genet., 13, 1159-1170.
22. Fu, H.Y., Minamino, T., Tsukamoto, O., Sawada, T., Asai, M., Kato, H., Asano, Y., Fujita, M., Takashima, S., Hori, M. et al. (2008) Overexpression of endoplasmic reticulum-resident chaperone attenuates cardiomyocyte deathinduced by proteosome inhibition. Cardiovasc. Res., 79, 600-610.
23. Tabares, L. and Betz, B. (2010) Multiple functions of the vesicular proton pump in nerve terminals. Neuron, 68, 1020-1022.
24. Beyenbach, K.W. and Wieczorek, H. (2006) The V-type H+ ATPase: molecular structure and function, physiological roles and regulation. J. Exp. Biol., 209, 577-589.
25. Wieczorek, H., Beyenbach, K.W., Huss, M. and Vitavska, O. (2009) Vacuolar-type proton pumps in insect epithelia. J. Exp. Biol., 212, 1611-1619.
26. Thévenod, F., Friedmann, J.M., Katsen, A.D. and Hauser, I.A. (2000) Up-regulation of multidrug resistance P-glycoprotein via nuclear factor-kB activation protects kidney proximal tubule cells from cadmiumand reactive oxygen species-induced apoptosis. J. Biol. Chem., 275, 1887-1896.
27. Hinton, A., Sennoune, S.R., Bond, S., Fang, M., Reuveni, M., Sahagian, G.G., Jay, D., Martinez-Zaguilan, R. and Forgac, M. (2009) Function of a subunit isoforms of the V-ATPase in pH homeostasis and in vitro invasion of MDA-MB231 human breast cancer cells. J. Biol. Chem., 284, 16400-16408.
28. Sun-Wada, G.-H., Toyomura, T., Murata, Y., Yamamoto, A., Futai, M. and Wada, Y. (2006) The a3 isoform of V-ATPase regulates insulin secretion from pancreatic b-cells. J. Cell Sci., 119, 4531-4540.
29. Forgac, M. (2007) Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat. Rev. Mol. Cell Biol., 8, 917-929.
30. Tabas, I. and Ron, D. (2011) Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat. Cell Biol., 13, 184-190.
31. Mihailidou, C., Papazian, I., Papavassiliou, A.G. and Kiaris, H. (2010) CHOP-dependent regulation of p21/waf1 during ER stress. Cell. Physiol. Biochem., 25, 761-766.
32. Lee, H.O., Davidson, J.M. and Duronio, R.J. (2009) Endoreplication: polyploidy with purpose. Genes Dev., 23, 2461-2477.
33. Fu, Y., Li, J. and Lee, A.S. (2007) GRP78/BiP inhibits endoplasmic reticulum BIK and protects human breast cancer cells against estrogen starvation-induced apoptosis. Cancer Research, 67, 3734-3740.