ALS-linked P56S-VAPB mutation impairs the formation of multinuclear myotube in C2C12 cells

International Journal of Molecular Sciences

Volumn 16, Issue 8, 2015, Pages 18628-18641

  Tokutake, Yukako ^a   Yamada, Keita ^a   Ohata, Masaki ^a   Obayashi, Yoshihito ^a   Tsuchiya, Megumi ^a   Yonekura, Shinichi ^a  

^a SHINSHU UNIVERSITY   (Japan)

Author keywords

Amyotrophic lateral sclerosis; Differentiation; Satellite cells; Unfolded protein response; Vesicle associated membrane protein associated protein B

Indexed keywords

MESSENGER RNA; SYNAPTOBREVIN; DNA BINDING PROTEIN; ERN2 PROTEIN, MOUSE; MEMBRANE PROTEIN; PROTEIN SERINE THREONINE KINASE; REGULATORY FACTOR X TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR; VAPB PROTEIN, MOUSE; X BOX BINDING PROTEIN 1; XBP1 PROTEIN, MOUSE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GENE MUTATION; GENETIC TRANSFECTION; HUMAN; IMMUNOCYTOCHEMISTRY; MOUSE; MYOTUBE; NONHUMAN; PROTEIN AGGREGATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UNFOLDED PROTEIN RESPONSE; ANIMAL; CELL LINE; CELL NUCLEUS; GENETICS; METABOLISM; MYOBLAST; PATHOLOGY; POINT MUTATION; PROTEINOSIS; SIGNAL TRANSDUCTION; SKELETAL MUSCLE CELL;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; CELL LINE; CELL NUCLEUS; DNA-BINDING PROTEINS; MEMBRANE PROTEINS; MICE; MUSCLE FIBERS, SKELETAL; MYOBLASTS; POINT MUTATION; PROTEIN AGGREGATION, PATHOLOGICAL; PROTEIN-SERINE-THREONINE KINASES; REGULATORY FACTOR X TRANSCRIPTION FACTORS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; UNFOLDED PROTEIN RESPONSE; X-BOX BINDING PROTEIN 1;

EID: 84939250775     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms160818628     Document Type: Article

References (34)

1. Brooks, B.R., Sanjak, M., Beiden, D., Juhasz-Poscine, K., Waclawik, A. Natural history of amyotrophic lateral sclerosis-Impairment, disability, handicap. In Amyotrophic Lateral Sclerosis, Brown, R.H., Jr., Meininger, V., Swash, M., Eds., Martin Dunitz: London, UK, 2000, pp. 31-58.
2. Bruijn, L.I., Miller, T.M., Cleveland, D.W. Unraveling the mechanisms involved in motor neuron degeneration in ALS. Annu. Rev. Neurosci. 2004, 27, 723-749.
3. Boillee, S., Velde, C.V., Cleveland, D.W. ALS: A disease of motor neurons and their nonneuronal neighbors. Neuron 2006, 52, 39-59.
4. Nagai, M., Re, D.B., Nagata, T., Chalazonitis, A., Jessell, T.M., Wichterle, H., Przedborski, S. Astrocytes expressing ALS-linked mutated sodl release factors selectively toxic to motor neurons. Nat. Neurosci. 2007, 10, 615-622.
5. Dobrowolny, G., Aucello, M., Rizzuto, E., Beccafico, S., Mammucari, C., Boncompagni, S., Belia, S., Wannenes, F., Nicoletti, C., Del Prete, Z., et al. Skeletal muscle is a primary target of SOD1G93A-mediated toxicity. CellMetab. 2008, 8, 425-436.
6. Ehrhardt, J., Morgan, J. Regenerative capacity of skeletal muscle. Curr. Opin. Neurol. 2005, 18, 548-553.
7. Seale, P., Sabourin, L.A., Girgis-Gabardo, A., Mansouri, A., Gruss, P., Rudnicki, M.A. Pax7 is required for the specification of myogenic satellite cells. Cell 2000, 102, 777-786.
8. Cooper, R.N., Tajbakhsh, S., Mouly, V., Cossu, G., Buckingham, M., Butler-Browne, G.S. In vivo satellite cell activation via Myf5 and MyoD in regenerating mouse skeletal muscle. J. Cell Sci. 1999, 112, 2895-2901.
9. Smith, C.K., Janney, M.J., Allen, R.E. Temporal expression of myogenic regulatory genes during activation, proliferation, and differentiation of rat skeletal muscle satellite cells. J. Cell. Physiol. 1994, 159, 379-385.
10. Seale, P., Rudnicki, M.A. A new look at the origin, function, and "stem-cell" status of muscle satellite cells. Dev. Biol. 2000, 218, 115-124.
11. Pradat, P.F., Barani, A., Wanschitz, J., Dubourg, O., Lombes, A., Bigot, A., Mouly, V., Bruneteau, G., Salachas, F., Lenglet, T., et al. Abnormalities of satellite cells function in amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. 2011, 12, 264-271.
12. Nishimura, A.L., Mitne-Neto, M., Silva, H.C., Richieri-Costa, A., Middleton, S., Cascio, D., Kok, F., Oliveira, J.R., Gillingwater, T., Webb, J., et al. A mutation in the vesicle-trafficking protein VAPB causes late-onset spinal muscular atrophy and amyotrophic lateral sclerosis. Am. J. Hum. Genet. 2004, 75, 822-831.
13. Kanekura, K., Nishimoto, I., Aiso, S., Matsuoka, M. Characterization of amyotrophic lateral sclerosis-linked P56S mutation of vesicle-associated membrane protein-associated protein B (VAPB/ALS8). J. Biol. Chem. 2006, 281, 30223-30233.
14. Teuling, E., Ahmed, S., Haasdijk, E., Demmers, J., Steinmetz, M.O., Akhmanova, A., Jaarsma, D., Hoogenraad, C.C. Motor neuron disease-associated mutant vesicle-associated membrane protein-associated protein (VAP) B recruits wild-type VAPs into endoplasmic reticulum-derived tubular aggregates. J. Neurosci. 2007, 27, 9801-9815.
15. Fasana, E., Fossati, M., Ruggiano, A., Brambillasca, S., Hoogenraad, C.C., Navone, F., Francolini, M., Borgese, N. A VAPB mutant linked to amyotrophic lateral sclerosis generates a novel form of organized smooth endoplasmic reticulum. FASEB J. 2010, 24, 1419-1430.
16. Gkogkas, C., Middleton, S., Kremer, A.M., Wardrope, C., Hannah, M., Gillingwater, T.H., Skehel, P. VAPB interacts with and modulates the activity of ATF6. Hum. Mol. Genet. 2008, 17, 1517-1526.
17. Suzuki, H., Kanekura, K., Levine, T.P., Kohno, K., Olkkonen, V.M., Aiso, S., Matsuoka, M. Als-linked P56S-VAPB, an aggregated loss-of-function mutant of VAPB, predisposes motor neurons to ER stress-related death by inducing aggregation of co-expressed wild-type VAPB. J. Neurochem. 2009, 108, 973-985.
18. Kanekura, K., Suzuki, H., Aiso, S., Matsuoka, M. ER stress and unfolded protein response in amyotrophic lateral sclerosis. Mol. Neurobiol. 2009, 39, 81-89.
19. Saxena, S., Cabuy, E., Caroni, P. A role for motoneuron subtype-selective ER stress in disease manifestations of FALS mice. Nat. Neurosci. 2009, 12, 627-636.
20. Banachewicz, W., Suplat, D., Krzeminski, P., Pomorski, P., Baranska, J. P2 nucleotide receptors on C2C12 satellite cells. Purinergic Signal. 2005, 1, 249-257.
21. Yaffe, D., Saxel, O. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 1977, 270, 725-727.
22. Tokutake, Y., Gushima, K., Miyazaki, H., Shimosato, T., Yonekura, S. ALS-associated P56S-VAPB mutation restrains 3T3-L1 preadipocyte differentiation. Biochem. Biophys. Res. Commun. 2015, 460, 831-837.
23. Folker, E.S., Baylies, M.K. Nuclear positioning in muscle development and disease. Front. Physiol. 2013, 4, 363, doi:10.3389/fphys.2013.00363.
24. Hall, Z.W., Ralston, E. Nuclear domains in muscle cells. Cell 1989, 59, 771-772.
25. Calfon, M., Zeng, H., Urano, F., Till, J.H., Hubbard, S.R., Harding, H.P., Clark, S.G., Ron, D. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 2002, 415, 92-96.
26. Yoshida, H., Matsui, T., Hosokawa, N., Kaufman, R.J., Nagata, K., Mori, K. A time-dependent phase shift in the mammalian unfolded protein response. Dev. Cell 2003, 4, 265-271.
27. Reimold, A.M., Iwakoshi, N.N., Manis, J., Vallabhajosyula, P., Szomolanyi-Tsuda, E., Gravallese, E.M., Friend, D., Grusby, M.J., Alt, F., Glimcher, L.H. Plasma cell differentiation requires the transcription factor XBP-1. Nature 2001, 412, 300-307.
28. Sha, H., He, Y., Chen, H., Wang, C., Zenno, A., Shi, H., Yang, X., Zhang, X., Qi, L. The IRE1a-XBP1 pathway of the unfolded protein response is required for adipogenesis. CellMetab. 2009, 9, 556-564.
29. Tohmonda, T., Miyauchi, Y., Ghosh, R., Yoda, M., Uchikawa, S., Takito, J., Morioka, H., Nakamura, M., Iwawaki, T., Chiba, K., et al. The IRE1a-XBP1 pathway is essential for osteoblast differentiation through promoting transcription of osterix. EMBO Rep. 2011, 12, 451-457.
30. Anagnostou, G., Akbar, M.T., Paul, P., Angelinetta, C., Steiner, T.J., de Belleroche, J. Vesicle associated membrane protein B (VAPB) is decreased in ALS spinal cord. Neurobiol. Aging 2010, 31, 969-985.
31. Moustaqim-Barrette, A., Lin, Y.Q., Pradhan, S., Neely, G.G., Bellen, H.J., Tsuda, H. The amyotrophic lateral sclerosis 8 protein, VAP, is required for ER protein quality control. Hum. Mol. Genet. 2014, 23, 1975-1989.
32. Prell, T., Lautenschlager, J., Witte, O.W., Carri, M.T., Grosskreutz, J. The unfolded protein response in models of human mutant G93A amyotrophic lateral sclerosis. Eur. J. Neurosci. 2012, 35, 652-660.
33. Garijo, N., Manzano, R., Osta, R., Perez, M.A. Stochastic cellular automata model of cell migration, proliferation and differentiation: Validation with in vitro cultures of muscle satellite cells. J. Theor. Biol. 2012, 314, 1-9.
34. Iwawaki, T., Akai, R., Kohno, K., Miura, M. A transgenic mouse model for monitoring endoplasmic reticulum stress. Nat. Med. 2004, 10, 98-102.