Extracellular annexins and dynamin are important for sequential steps in myoblast fusion

Journal of Cell Biology

Volumn 200, Issue 1, 2013, Pages 109-123

  Leikina, Evgenia ^a   Melikov, Kamran ^a   Sanyal, Sarmistha ^a   Verma, Santosh K ^a   Eun, Bokkee ^a   Gebert, Claudia ^a   Pfeifer, Karl ^a   Lizunov, Vladimir A ^a   Kozlov, Michael M ^b   Chernomordik, Leonid V ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ANNEXIN; DYNAMIN; LIPID; LIPOCORTIN 1; LIPOCORTIN 5; LYSOPHOSPHATIDYLCHOLINE;

ANIMAL CELL; ARTICLE; CELL FUSION; CELL MEMBRANE; CELL METABOLISM; MOUSE; MUSCLE DEVELOPMENT; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

ANIMALS; ANNEXIN A1; ANNEXIN A5; CELL FUSION; CELL LINE; CELL MEMBRANE; DYNAMINS; MICE; MICE, KNOCKOUT; MUSCLE DEVELOPMENT; MYOBLASTS; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE;

MURINAE;

EID: 84872079429     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201207012     Document Type: Article

References (69)

1. Abmayr, S.M., and G.K. Pavlath. 2012. Myoblast fusion: lessons from flies and mice. Development. 139:641-656. http://dx.doi.org/10.1242/dev.068353
2. Arcuri, C., I. Giambanco, R. Bianchi, and R. Donato. 2002. Annexin V, annexin VI, S100A1 and S100B in developing and adult avian skeletal muscles. Neuroscience. 109:371-388. http://dx.doi.org/10.1016/S0306-4522(01)00330-X
3. Bach, A.S., S. Enjalbert, F. Comunale, S. Bodin, N. Vitale, S. Charrasse, and C. Gauthier-Rouvière. 2010. ADP-ribosylation factor 6 regulates mammalian myoblast fusion through phospholipase D1 and phosphatidylinositol 4,5-bisphosphate signaling pathways. Mol. Biol. Cell. 21:2412-2424. http://dx.doi.org/10.1091/mbc.E09-12-1063
4. Belluoccio, D., I. Grskovic, A. Niehoff, U. Schlötzer-Schrehardt, S. Rosenbaum, J. Etich, C. Frie, F. Pausch, S.E. Moss, E. Pöschl, et al. 2010. Deficiency of annexins A5 and A6 induces complex changes in the transcriptome of growth plate cartilage but does not inhibit the induction of mineralization. J. Bone Miner. Res. 25:141-153. http://dx.doi.org/10.1359/jbmr.090710
5. Bitoun, M., S. Maugenre, P.Y. Jeannet, E. Lacène, X. Ferrer, P. Laforêt, J.J. Martin, J. Laporte, H. Lochmüller, A.H. Beggs, et al. 2005. Mutations in dynamin 2 cause dominant centronuclear myopathy. Nat. Genet. 37:1207-1209. http://dx.doi.org/10.1038/ng1657
6. Bitto, E., and W. Cho. 1999. Structural determinant of the vesicle aggregation activity of annexin I. Biochemistry. 38:14094-14100. http://dx.doi.org/10.1021/bi990457p
7. Bizzarro, V., B. Fontanella, S. Franceschelli, M. Pirozzi, H. Christian, L. Parente, and A. Petrella. 2010. Role of Annexin A1 in mouse myoblast cell differentiation. J. Cell. Physiol. 224:757-765. http://dx.doi.org/10.1002/jcp.22178
8. Blau, H.M., C.P. Chiu, and C. Webster. 1983. Cytoplasmic activation of human nuclear genes in stable heterocaryons. Cell. 32:1171-1180. http://dx.doi.org/10.1016/0092-8674(83)90300-8
9. Blume, K.E., S. Soeroes, M. Waibel, H. Keppeler, S. Wesselborg, M. Herrmann, K. Schulze-Osthoff, and K. Lauber. 2009. Cell surface externalization of annexin A1 as a failsafe mechanism preventing inflammatory responses during secondary necrosis. J. Immunol. 183:8138-8147. http://dx.doi.org/10.4049/jimmunol.0902250
10. Bois, P.R., and G.C. Grosveld. 2003. FKHR (FOXO1a) is required for myotube fusion of primary mouse myoblasts. EMBO J. 22:1147-1157. http://dx.doi.org/10.1093/emboj/cdg116
11. Boucrot, E., S. Saffarian, R. Massol, T. Kirchhausen, and M. Ehrlich. 2006. Role of lipids and actin in the formation of clathrin-coated pits. Exp. Cell Res. 312:4036-4048. http://dx.doi.org/10.1016/j.yexcr.2006.09.025
12. Bouter, A., C. Gounou, R. Bérat, S. Tan, B. Gallois, T. Granier, B.L. d'Estaintot, E. Pöschl, B. Brachvogel, and A.R. Brisson. 2011. Annexin-A5 assembled into two-dimensional arrays promotes cell membrane repair. Nat. Commun. 2:270. http://dx.doi.org/10.1038/ncomms1270
13. Brachvogel, B., J. Dikschas, H. Moch, H. Welzel, K. von der Mark, C. Hofmann, and E. Pöschl. 2003. Annexin A5 is not essential for skeletal development. Mol. Cell. Biol. 23:2907-2913. http://dx.doi.org/10.1128/MCB.23.8.2907-2913.2003
14. Casadei, L., L. Vallorani, A.M. Gioacchini, M. Guescini, S. Burattini, A. D'Emilio, L. Biagiotti, E. Falcieri, and V. Stocchi. 2009. Proteomicsbased investigation in C2C12 myoblast differentiation. Eur. J. Histochem. 53:261-268.
15. Chen, E.H., E. Grote, W. Mohler, and A. Vignery. 2007. Cell-cell fusion. FEBS Lett. 581:2181-2193. http://dx.doi.org/10.1016/j.febslet.2007.03.033
16. Chernomordik, L.V., and M.M. Kozlov. 2005. Membrane hemifusion: crossing a chasm in two leaps. Cell. 123:375-382. http://dx.doi.org/10.1016/j.cell.2005.10.015
17. Clemen, C.S., A. Hofmann, C. Zamparelli, and A.A. Noegel. 1999. Expression and localisation of annexin VII (synexin) isoforms in differentiating myoblasts. J. Muscle Res. Cell Motil. 20:669-679. http://dx.doi.org/10.1023/A:1005524623337
18. Cunningham, C.C., R. Vegners, R. Bucki, M. Funaki, N. Korde, J.H. Hartwig, T.P. Stossel, and P.A. Janmey. 2001. Cell permeant polyphosphoinositidebinding peptides that block cell motility and actin assembly. J. Biol. Chem. 276:43390-43399. http://dx.doi.org/10.1074/jbc.M105289200
19. Doherty, K.R., A. Cave, D.B. Davis, A.J. Delmonte, A. Posey, J.U. Earley, M. Hadhazy, and E.M. McNally. 2005. Normal myoblast fusion requires myoferlin. Development. 132:5565-5575. http://dx.doi.org/10.1242/dev.02155
20. Doherty, J.T., K.C. Lenhart, M.V. Cameron, C.P. Mack, F.L. Conlon, and J.M. Taylor. 2011. Skeletal muscle differentiation and fusion are regulated by the BAR-containing Rho-GTPase-activating protein (Rho-GAP), GRAF1. J. Biol. Chem. 286:25903-25921. http://dx.doi.org/10.1074/jbc .M111.243030
21. Draeger, A., K. Monastyrskaya, and E.B. Babiychuk. 2011. Plasma membrane repair and cellular damage control: the annexin survival kit. Biochem. Pharmacol. 81:703-712. http://dx.doi.org/10.1016/j.bcp.2010.12.027
22. Duan, R. 2008. Molecular mechanisms governing skeletal muscle myoblast fusion. PhD thesis. Indiana University, Bloomington, IN. 114 pp.
23. Edelstein, A., N. Amodaj, K. Hoover, R. Vale, and N. Stuurman. 2010. Computer control of microscopes using microManager. Curr. Protoc. Mol. Biol. Chapter 14:Unit14.20.
24. Elegbede, A.I., D.K. Srivastava, and A. Hinderliter. 2006. Purification of recombinant annexins without the use of phospholipids. Protein Expr. Purif. 50:157-162. http://dx.doi.org/10.1016/j.pep.2006.05.003
25. Fan, X., S. Krahling, D. Smith, P. Williamson, and R.A. Schlegel. 2004. Macrophage surface expression of annexins I and II in the phagocytosis of apoptotic lymphocytes. Mol. Biol. Cell. 15:2863-2872. http://dx.doi.org/10.1091/mbc.E03-09-0670
26. Francis, J.W., K.J. Balazovich, J.E. Smolen, D.I. Margolis, and L.A. Boxer. 1992. Human neutrophil annexin I promotes granule aggregation and modulates Ca(2+)-dependent membrane fusion. J. Clin. Invest. 90:537- 544. http://dx.doi.org/10.1172/JCI115892
27. Gauster, M., and B. Huppertz. 2008. Fusion of cytothrophoblast with syncytiotrophoblast in the human placenta: factors involved in syncytialization. Journal für Reproduktionsmedizin und Endokrinologie. 5:76-82.
28. Gerke, V., and S.E. Moss. 2002. Annexins: from structure to function. Physiol. Rev. 82:331-371.
29. Gerke, V., C.E. Creutz, and S.E. Moss. 2005. Annexins: linking Ca2+ signalling to membrane dynamics. Nat. Rev. Mol. Cell Biol. 6:449-461. http://dx.doi.org/10.1038/nrm1661
30. Gonnet, F., B. Bouazza, G.A. Millot, S. Ziaei, L. Garcia, G.S. Butler-Browne, V. Mouly, J. Tortajada, O. Danos, and F. Svinartchouk. 2008. Proteome analysis of differentiating human myoblasts by dialysis-assisted twodimensional gel electrophoresis (DAGE). Proteomics. 8:264-278. http://dx.doi.org/10.1002/pmic.200700261
31. Gruenbaum-Cohen, Y., I. Harel, K.B. Umansky, E. Tzahor, S.B. Snapper, B.Z. Shilo, and E.D. Schejter. 2012. The actin regulator N-WASp is required for muscle-cell fusion in mice. Proc. Natl. Acad. Sci. USA. 109:11211- 11216. http://dx.doi.org/10.1073/pnas.1116065109
32. Hannon, R., J.D. Croxtall, S.J. Getting, F. Roviezzo, S. Yona, M.J. Paul-Clark, F.N. Gavins, M. Perretti, J.F. Morris, J.C. Buckingham, and R.J. Flower. 2003. Aberrant inflammation and resistance to glucocorticoids in annexin 1-/- mouse. FASEB J. 17:253-255.
33. Hnia, K., I. Vaccari, A. Bolino, and J. Laporte. 2012. Myotubularin phosphoinositide phosphatases: cellular functions and disease pathophysiology. Trends Mol. Med. 18:317-327. http://dx.doi.org/10.1016/j.molmed.2012.04.004
34. Hoekstra, D., R. Buist-Arkema, K. Klappe, and C.P. Reutelingsperger. 1993. Interaction of annexins with membranes: the N-terminus as a governing parameter as revealed with a chimeric annexin. Biochemistry. 32:14194- 14202. http://dx.doi.org/10.1021/bi00214a019
35. Jeong, J., and I.M. Conboy. 2011. Phosphatidylserine directly and positively regulates fusion of myoblasts into myotubes. Biochem. Biophys. Res. Commun. 414:9-13. http://dx.doi.org/10.1016/j.bbrc.2011.08.128
36. Jin, C.H., C. Miyaura, H. Tanaka, J. Takito, E. Abe, and T. Suda. 1990. Fusion of mouse alveolar macrophages induced by 1 alpha,25-dihydroxyvitamin D3 involves extracellular, but not intracellular, calcium. J. Cell. Physiol. 142:434-439. http://dx.doi.org/10.1002/jcp.1041420229
37. Kaspar, P., and M. Dvorák. 2008. Involvement of phosphatidylserine externalization in the down-regulation of c-myb expression in differentiating C2C12 cells. Differentiation. 76:245-252. http://dx.doi.org/10.1111/j.1432-0436.2007.00222.x
38. Kim, S., K. Shilagardi, S. Zhang, S.N. Hong, K.L. Sens, J. Bo, G.A. Gonzalez, and E.H. Chen. 2007. A critical function for the actin cytoskeleton in targeted exocytosis of prefusion vesicles during myoblast fusion. Dev. Cell. 12:571-586. http://dx.doi.org/10.1016/j.devcel.2007.02.019
39. Kislinger, T., A.O. Gramolini, Y. Pan, K. Rahman, D.H. MacLennan, and A. Emili. 2005. Proteome dynamics during C2C12 myoblast differentiation. Mol. Cell. Proteomics. 4:887-901. http://dx.doi.org/10.1074/mcp.M400182-MCP200
40. Kubista, H., S. Sacre, and S.E. Moss. 2000. Annexins and membrane fusion. Subcell. Biochem. 34:73-131. http://dx.doi.org/10.1007/0-306-46824-7_3
41. Logue, S.E., M. Elgendy, and S.J. Martin. 2009. Expression, purification and use of recombinant annexin V for the detection of apoptotic cells. Nat. Protoc. 4:1383-1395. http://dx.doi.org/10.1038/nprot.2009.143
42. Macia, E., M. Ehrlich, R. Massol, E. Boucrot, C. Brunner, and T. Kirchhausen. 2006. Dynasore, a cell-permeable inhibitor of dynamin. Dev. Cell. 10:839-850. http://dx.doi.org/10.1016/j.devcel.2006.04.002
43. Makarov, A.A., L.I. Kovalev, M.A. Kovaleva, I.Iu. Toropygin, and S.S. Shishkin. 2009. A study of protein profile changes in differentiating human myoblasts. [In Russian.] Ontogenez. 40:112-119.
44. McNeil, A.K., U. Rescher, V. Gerke, and P.L. McNeil. 2006. Requirement for annexin A1 in plasma membrane repair. J. Biol. Chem. 281:35202-35207. http://dx.doi.org/10.1074/jbc.M606406200
45. Moss, S.E., and R.O. Morgan. 2004. The annexins. Genome Biol. 5:219. http://dx.doi.org/10.1186/gb-2004-5-4-219
46. Mukai, A., T. Kurisaki, S.B. Sato, T. Kobayashi, G. Kondoh, and N. Hashimoto. 2009. Dynamic clustering and dispersion of lipid rafts contribute to fusion competence of myogenic cells. Exp. Cell Res. 315:3052-3063. http://dx.doi.org/10.1016/j.yexcr.2009.07.010
47. Nowak, S.J., P.C. Nahirney, A.K. Hadjantonakis, and M.K. Baylies. 2009. Nap1-mediated actin remodeling is essential for mammalian myoblast fusion. J. Cell Sci. 122:3282-3293. http://dx.doi.org/10.1242/jcs.047597
48. Onel, S.F., and R. Renkawitz-Pohl. 2009. FuRMAS: triggering myoblast fusion in Drosophila. Dev. Dyn. 238:1513-1525. http://dx.doi.org/10.1002/dvdy.21961
49. Quan, A., A.B. McGeachie, D.J. Keating, E.M. van Dam, J. Rusak, N. Chau, C.S. Malladi, C. Chen, A. McCluskey, M.A. Cousin, and P.J. Robinson. 2007. Myristyl trimethyl ammonium bromide and octadecyl trimethyl ammonium bromide are surface-active small molecule dynamin inhibitors that block endocytosis mediated by dynamin I or dynamin II. Mol. Pharmacol. 72:1425-1439. http://dx.doi.org/10.1124/mol.107.034207
50. Rao, L.V., J.F. Tait, and A.D. Hoang. 1992. Binding of annexin V to a human ovarian carcinoma cell line (OC-2008). Contrasting effects on cell surface factor VIIa/tissue factor activity and prothrombinase activity. Thromb. Res. 67:517-531. http://dx.doi.org/10.1016/0049-3848(92)90013-Z
51. Reporter, M., and D. Raveed. 1973. Plasma membranes: isolation from naturally fused and lysolecithin-treated muscle cells. Science. 181:863-865. http://dx.doi.org/10.1126/science.181.4102.863
52. Richard, J.P., E. Leikina, R. Langen, W.M. Henne, M. Popova, T. Balla, H.T. McMahon, M.M. Kozlov, and L.V. Chernomordik. 2011. Intracellular curvature-generating proteins in cell-to-cell fusion. Biochem. J. 440:185- 193. http://dx.doi.org/10.1042/BJ20111243
53. Rochlin, K., S. Yu, S. Roy, and M.K. Baylies. 2010. Myoblast fusion: when it takes more to make one. Dev. Biol. 341:66-83. http://dx.doi.org/10.1016/j.ydbio.2009.10.024
54. Salsman, J., D. Top, C. Barry, and R. Duncan. 2008. A virus-encoded cellcell fusion machine dependent on surrogate adhesins. PLoS Pathog. 4:e1000016. http://dx.doi.org/10.1371/journal.ppat.1000016
55. Sapir, A., O. Avinoam, B. Podbilewicz, and L.V. Chernomordik. 2008. Viral and developmental cell fusion mechanisms: conservation and divergence. Dev. Cell. 14:11-21. http://dx.doi.org/10.1016/j.devcel.2007.12.008
56. Schwoebel, E.D., T.H. Ho, and M.S. Moore. 2002. The mechanism of inhibition of Ran-dependent nuclear transport by cellular ATP depletion. J. Cell Biol. 157:963-974. http://dx.doi.org/10.1083/jcb.200111077
57. Sens, K.L., S. Zhang, P. Jin, R. Duan, G. Zhang, F. Luo, L. Parachini, and E.H. Chen. 2010. An invasive podosome-like structure promotes fusion pore formation during myoblast fusion. J. Cell Biol. 191:1013-1027. http://dx.doi.org/10.1083/jcb.201006006
58. Sessions, A., and A.F. Horwitz. 1983. Differentiation-related differences in the plasma membrane phospholipid asymmetry of myogenic and fibrogenic cells. Biochim. Biophys. Acta. 728:103-111. http://dx.doi.org/10.1016/0005-2736(83)90442-X
59. Shainberg, A., G. Yagil, and D. Yaffe. 1969. Control of myogenesis in vitro by Ca 2 + concentration in nutritional medium. Exp. Cell Res. 58:163-167. http://dx.doi.org/10.1016/0014-4827(69)90127-X
60. Spiro, A.J., G.M. Shy, and N.K. Gonatas. 1966. Myotubular myopathy. Persistence of fetal muscle in an adolescent boy. Arch. Neurol. 14:1-14. http://dx.doi.org/10.1001/archneur.1966.00470070005001
61. Tannu, N.S., V.K. Rao, R.M. Chaudhary, F. Giorgianni, A.E. Saeed, Y. Gao, and R. Raghow. 2004. Comparative proteomes of the proliferating C(2)C(12) myoblasts and fully differentiated myotubes reveal the complexity of the skeletal muscle differentiation program. Mol. Cell. Proteomics. 3:1065- 1082. http://dx.doi.org/10.1074/mcp.M400020-MCP200
62. van den Eijnde, S.M., M.J. van den Hoff, C.P. Reutelingsperger, W.L. van Heerde, M.E. Henfling, C. Vermeij-Keers, B. Schutte, M. Borgers, and F.C. Ramaekers. 2001. Transient expression of phosphatidylserine at cell-cell contact areas is required for myotube formation. J. Cell Sci. 114:3631-3642.
63. van Genderen, H.O., H. Kenis, L. Hofstra, J. Narula, and C.P. Reutelingsperger. 2008. Extracellular annexin A5: functions of phosphatidylserine-binding and two-dimensional crystallization. Biochim. Biophys. Acta. 1783:953- 963. http://dx.doi.org/10.1016/j.bbamcr.2008.01.030
64. Wakelam, M.J. 1983. Inositol phospholipid metabolism and myoblast fusion. Biochem. J. 214:77-82.
65. Wakelam, M.J. 1985. The fusion of myoblasts. Biochem. J. 228:1-12.
66. Wang, L.M., W.H. Li, Y.C. Xu, Q. Wei, H. Zhao, and X.F. Jiang. 2011. Annexin 1-derived peptide Ac2-26 inhibits eosinophil recruitment in vivo via decreasing prostaglandin D2. Int. Arch. Allergy Immunol. 154:137-148. http://dx.doi.org/10.1159/000320228
67. White, I.J., L.M. Bailey, M.R. Aghakhani, S.E. Moss, and C.E. Futter. 2006. EGF stimulates annexin 1-dependent inward vesiculation in a multivesicular endosome subpopulation. EMBO J. 25:1-12. http://dx.doi.org/10.1038/sj.emboj.7600759
68. Yanagimachi, R. 1978. Calcium requirement for sperm-egg fusion in mammals. Biol. Reprod. 19:949-958. http://dx.doi.org/10.1095/biolreprod19.5.949
69. Yin, C., Q. Long, T. Lei, X. Chen, H. Long, B. Feng, Y. Peng, Y. Wu, and Z. Yang. 2009. Lipid accumulation mediated by adiponectin in C2C12 myogenesis. BMB Rep. 42:667-672. http://dx.doi.org/10.5483/BMBRep.2009.42.10.667