The brain expressed x-linked gene 1 (Bex1) regulates myoblast fusion

Developmental Biology

Volumn 409, Issue 1, 2016, Pages 16-25

  Jiang, Chunhui ^a   Wang, Jing Hua ^a   Yue, Feng ^a   Kuang, Shihuan ^a,b  

^a PURDUE UNIVERSITY   (United States)

^b Purdue University   (United States)

Author keywords

Myoblasts; Myogenesis; Regeneration; Skeletal muscle

Indexed keywords

MYOGENIN; TRANSCRIPTION FACTOR PAX7; BEX1 PROTEIN, MOUSE; NERVE PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN EXPRESSED X LINKED GENE 1; CELL DIFFERENTIATION; CELL FUSION; CELL MATURATION; CELL NUCLEUS; CELL PROLIFERATION; CONTROLLED STUDY; CYTOPLASM; DOWN REGULATION; GENE; GENE EXPRESSION; GENE TRANSLOCATION; IN VIVO STUDY; MOUSE; MUSCLE DEVELOPMENT; MUSCLE INJURY; MUSCLE REGENERATION; MUSCLE STEM CELL; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SATELLITE CELL; SKELETAL MUSCLE; SPATIOTEMPORAL ANALYSIS; STEM CELL; ANIMAL; CYTOLOGY; EMBRYO DEVELOPMENT; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; KNOCKOUT MOUSE; METABOLISM; REGENERATION; SKELETAL MUSCLE CELL;

ANIMALS; CELL DIFFERENTIATION; CELL FUSION; CELL PROLIFERATION; EMBRYONIC DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE, KNOCKOUT; MUSCLE DEVELOPMENT; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; MYOBLASTS; NERVE TISSUE PROTEINS; REGENERATION; STEM CELLS;

EID: 84948798412     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2015.11.007     Document Type: Article

References (41)

1. Alvarez E., Zhou W., Witta S.E., Freed C.R. Characterization of the Bex gene family in humans, mice, and rats. Gene 2005, 357:18-28.
2. Baylies M.K., Bate M., Ruiz Gomez M. Myogenesis: a view from Drosophila. Cell 1998, 93:921-927.
3. Behrens M., Margolis J.W., Margolis F.L. Identification of members of the Bex gene family as olfactory marker protein (OMP) binding partners. J. Neurochem. 2003, 86:1289-1296.
4. Biressi S., Molinaro M., Cossu G. Cellular heterogeneity during vertebrate skeletal muscle development. Dev. Biol. 2007, 308:281-293.
5. Cheng T.C., Hanley T.A., Mudd J., Merlie J.P., Olson E.N. Mapping of myogenin transcription during embryogenesis using transgenes linked to the myogenin control region. J. Cell Biol. 1992, 119:1649-1656.
6. Doberstein S.K., Fetter R.D., Mehta A.Y., Goodman C.S. Genetic analysis of myoblast fusion: blown fuse is required for progression beyond the prefusion complex. J. Cell Biol. 1997, 136:1249-1261.
7. Duan R., Jin P., Luo F., Zhang G., Anderson N., Chen E.H. Group I PAKs function downstream of Rac to promote podosome invasion during myoblast fusion in vivo. J. Cell Biol. 2012, 199:169-185.
8. Ernfors P., Hallbook F., Ebendal T., Shooter E.M., Radeke M.J., Misko T.P., Persson H. Developmental and regional expression of beta-nerve growth factor receptor mRNA in the chick and rat. Neuron 1988, 1:983-996.
9. Fernandez E.M., Diaz-Ceso M.D., Vilar M. Brain expressed and X-linked (Bex) proteins are intrinsically disordered proteins (IDPs) and form new signaling hubs. Plos One 2015, 10:e0117206.
10. Foltz G., Ryu G.Y., Yoon J.G., Nelson T., Fahey J., Frakes A., Lee H., Field L., Zander K., Sibenaller Z., Ryken T.C., Vibhakar R., Hood L., Madan A. Genome-wide analysis of epigenetic silencing identifies BEX1 and BEX2 as candidate tumor suppressor genes in malignant glioma. Cancer Res. 2006, 66:6665-6674.
11. Geisbrecht E.R., Haralalka S., Swanson S.K., Florens L., Washburn M.P., Abmayr S.M. Drosophila ELMO/CED-12 interacts with Myoblast city to direct myoblast fusion and ommatidial organization. Dev. Biol. 2008, 314:137-149.
12. Goetsch S.C., Hawke T.J., Gallardo T.D., Richardson J.A., Garry D.J. Transcriptional profiling and regulation of the extracellular matrix during muscle regeneration. Physiol. Genom. 2003, 14:261-271.
13. Hamoud N., Tran V., Croteau L.P., Kania A., Cote J.F. G-protein coupled receptor BAI3 promotes myoblast fusion in vertebrates. Proc. Natl. Acad. Sci. USA 2014, 111:3745-3750.
14. He T.C., Zhou S., da Costa L.T., Yu J., Kinzler K.W., Vogelstein B. A simplified system for generating recombinant adenoviruses. Proc. Natl. Acad. Sci. USA 1998, 95:2509-2514.
15. Hochreiter-Hufford A.E., Lee C.S., Kinchen J.M., Sokolowski J.D., Arandjelovic S., Call J.A., Klibanov A.L., Yan Z., Mandell J.W., Ravichandran K.S. Phosphatidylserine receptor BAI1 and apoptotic cells as new promoters of myoblast fusion. Nature 2013, 497:263-267.
16. Horsley V., Pavlath G.K. Forming a multinucleated cell: molecules that regulate myoblast fusion. Cells Tissues Organs 2004, 176:67-78.
17. Karakoula K., Jacques T.S., Phipps K.P., Harkness W., Thompson D., Harding B.N., Darling J.L., Warr T.J. Epigenetic genome-wide analysis identifies BEX1 as a candidate tumour suppressor gene in paediatric intracranial ependymoma. Cancer Lett. 2014, 346:34-44.
18. Khazaei M.R., Halfter H., Karimzadeh F., Koo J.H., Margolis F.L., Young P. Bex1 is involved in the regeneration of axons after injury. J. Neurochem. 2010, 115:910-920.
19. Koo J.H. Bex1 Participates in muscle regeneration by regulating myogenic satellite cell differentiation. Lab. Anim. Res. 2010, 26:145-151.
20. Koo J.H., Saraswati M., Margolis F.L. Immunolocalization of Bex protein in the mouse brain and olfactory system. J. Comp. Neurol. 2005, 487:1-14.
21. Koo J.H., Smiley M.A., Lovering R.M., Margolis F.L. Bex1 knock out mice show altered skeletal muscle regeneration. Biochem. Biophys. Res. Commun. 2007, 363:405-410.
22. Laurin M., Fradet N., Blangy A., Hall A., Vuori K., Cote J.F. The atypical Rac activator Dock180 (Dock1) regulates myoblast fusion in vivo. Proc. Natl. Acad. Sci. USA 2008, 105:15446-15451.
23. Lee C.H., Wong T.S., Chan J.Y., Lu S.C., Lin P., Cheng A.J., Chen Y.J., Chang J.S., Hsiao S.H., Leu Y.W., Li C.I., Hsiao J.R., Chang J.Y. Epigenetic regulation of the X-linked tumour suppressors BEX1 and LDOC1 in oral squamous cell carcinoma. J. Pathol. 2013, 230:298-309.
24. Lomen-Hoerth C., Shooter E.M. Widespread neurotrophin receptor expression in the immune system and other nonneuronal rat tissues. J. Neurochem. 1995, 64:1780-1789.
25. Millay D.P., O'Rourke J.R., Sutherland L.B., Bezprozvannaya S., Shelton J.M., Bassel-Duby R., Olson E.N. Myomaker is a membrane activator of myoblast fusion and muscle formation. Nature 2013, 499:301-305.
26. Mukai J., Hachiya T., Shoji-Hoshino S., Kimura M.T., Nadano D., Suvanto P., Hanaoka T., Li Y., Irie S., Greene L.A., Sato T.A. NADE, a p75NTR-associated cell death executor, is involved in signal transduction mediated by the common neurotrophin receptor p75NTR. J. Biol. Chem. 2000, 275:17566-17570.
27. Raivich G., Zimmermann A., Sutter A. The spatial and temporal pattern of beta NGF receptor expression in the developing chick embryo. EMBO J. 1985, 4:637-644.
28. Raivich G., Zimmermann A., Sutter A. Nerve growth factor (NGF) receptor expression in chicken cranial development. J. Comp. Neurol. 1987, 256:229-245.
29. Relaix F., Rocancourt D., Mansouri A., Buckingham M. A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 2005, 435:948-953.
30. Robertson T.A., Grounds M.D., Mitchell C.A., Papadimitriou J.M. Fusion between myogenic cells in vivo: an ultrastructural study in regenerating murine skeletal muscle. J. Struct. Biol. 1990, 105:170-182.
31. Rushton E., Drysdale R., Abmayr S.M., Michelson A.M., Bate M. Mutations in a novel gene, myoblast city, provide evidence in support of the founder cell hypothesis for Drosophila muscle development. Development 1995, 121:1979-1988.
32. Sambasivan R., Yao R., Kissenpfennig A., Van Wittenberghe L., Paldi A., Gayraud-Morel B., Guenou H., Malissen B., Tajbakhsh S., Galy A. Pax7-expressing satellite cells are indispensable for adult skeletal muscle regeneration. Development 2011, 138:3647-3656.
33. Schecterson L.C., Bothwell M. Novel roles for neurotrophins are suggested by BDNF and NT-3 mRNA expression in developing neurons. Neuron 1992, 9:449-463.
34. Schmalbruch H., Lewis D.M. Dynamics of nuclei of muscle fibers and connective tissue cells in normal and denervated rat muscles. Muscle Nerve 2000, 23:617-626.
35. Sweitzer T.D., Hanover J.A. Calmodulin activates nuclear protein import: a link between signal transduction and nuclear transport. Proc. Natl. Acad. Sci. USA 1996, 93:14574-14579.
36. Turk R., Sterrenburg E., de Meijer E.J., van Ommen G.J., den Dunnen J.T., t Hoen P.A. Muscle regeneration in dystrophin-deficient mdx mice studied by gene expression profiling. BMC Genom. 2005, 6:98.
37. Venuti J.M., Morris J.H., Vivian J.L., Olson E.N., Klein W.H. Myogenin is required for late but not early aspects of myogenesis during mouse development. J. Cell Biol. 1995, 128:563-576.
38. Vilar M., Murillo-Carretero M., Mira H., Magnusson K., Besset V., Ibanez C.F. Bex1, a novel interactor of the p75 neurotrophin receptor, links neurotrophin signaling to the cell cycle. EMBO J. 2006, 25:1219-1230.
39. von Maltzahn J., Jones A.E., Parks R.J., Rudnicki M.A. Pax7 is critical for the normal function of satellite cells in adult skeletal muscle. Proc. Natl. Acad. Sci. USA 2013, 110:16474-16479.
40. Yamamoto M., Sobue G., Yamamoto K., Terao S., Mitsuma T. Expression of mRNAs for neurotrophic factors (NGF, BDNF, NT-3, and GDNF) and their receptors (p75NGFR, trkA, trkB, and trkC) in the adult human peripheral nervous system and nonneural tissues. Neurochem. Res. 1996, 21:929-938.
41. Yan Z., Choi S., Liu X., Zhang M., Schageman J.J., Lee S.Y., Hart R., Lin L., Thurmond F.A., Williams R.S. Highly coordinated gene regulation in mouse skeletal muscle regeneration. J. Biol. Chem. 2003, 278:8826-8836.