A conserved role for calpains during myoblast fusion

Genesis

Volumn 53, Issue 7, 2015, Pages 417-430

  Buffolo, Marcio ^a   Batista Possidonio, Ana Claudia ^a   Mermelstein, Claudia ^a   Araujo, Helena ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Calpain; Chick; Drosophila; Muscle; Myoblast fusion

Indexed keywords

CALPAIN; CALPAIN A; CALPASTATIN; I KAPPA B ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL FUSION; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; GALLUS GALLUS; GENETIC TRANSFECTION; IN VITRO STUDY; IN VIVO STUDY; MUSCLE CELL; MUSCLE DEVELOPMENT; MUSCLE FUNCTION; MUSCLE LENGTH; MYOBLAST; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; ANIMAL; BIOLOGICAL MODEL; CELL COMMUNICATION; CELL CULTURE; CHICK EMBRYO; CHICKEN; CYTOLOGY; METABOLISM; PHYSIOLOGY; SKELETAL MUSCLE;

DROSOPHILA MELANOGASTER; MAMMALIA;

ANIMALS; CALPAIN; CELL COMMUNICATION; CELLS, CULTURED; CHICK EMBRYO; CHICKENS; DROSOPHILA MELANOGASTER; MODELS, BIOLOGICAL; MUSCLE DEVELOPMENT; MUSCLE, SKELETAL; MYOBLASTS;

EID: 84937686224     PISSN: 1526954X     EISSN: 1526968X     Source Type: Journal    
DOI: 10.1002/dvg.22870     Document Type: Article

References (72)

1. Abmayr SM, Pavlath GK. 2012. Myoblast fusion: Lessons from flies and mice. Development 139:641-656.
2. Artero RD, Castanon I, Baylies MK. 2001. The immunoglobulin-like protein Hibris functions as a dose-dependent regulator of myoblast fusion and is differentially controlled by Ras and Notch signaling. Development 128:4251-4264.
3. Baghdiguian S, Martin M, Richard I, Pons F, Astier C, Bourg N, Hay RT, Chemaly R, Halaby G, Loiselet J, Anderson LV, Lopez de Munain A, Fardeau M, Mangeat P, Beckmann JS, Lefranc G. 1999. Calpain 3 deficiency is associated with myonuclear apoptosis and profound perturbation of the IkappaB alpha/NF-kappaB pathway in limb-girdle muscular dystrophy type 2A. Nat Med 5:503-511.
4. Bakkar N, Guttridge DC. 2010. NF-kappaB signaling: A tale of two pathways in skeletal myogenesis. Physiol Rev 90:495-511.
5. Balcerzak D, Poussard S, Brustis JJ, Elamrani N, Soriano M, Cottin P, Ducastaing A. 1995. An antisense oligodeoxyribonucleotide to m-calpain mRNA inhibits myoblast fusion. J Cell Sci 108:2077-2082.
6. Barnoy S, Glaser T, Kosower NS. 1998. The calpain-calpastatin system and protein degradation in fusing myoblasts. Biochim Biophys Acta 1402:52-60.
7. Barnoy S, Maki M, Kosower NS. 2005. Overexpression of calpastatin inhibits L8 myoblast fusion. Biochem Biophys Res Commun 332:697-701.
8. Bate M. 1990. The embryonic development of larval muscles in Drosophila. Development 110:791-804.
9. Beckett K, Baylies MK. 2007. 3D analysis of founder cell and fusion competent myoblast arrangements outlines a new model of myoblast fusion. Dev Biol 309:113-125.
10. Beramendi A, Peron S, Megighian A, Reggiani C, Cantera R. 2005. The inhibitor kappaB-ortholog Cactus is necessary for normal neuromuscular function in Drosophila melanogaster. Neuroscience 134:397-406.
11. Berger S, Schafer G, Kesper DA, Holz A, Eriksson T, Palmer RH, Beck L, Klambt C, Renkawitz-Pohl R, Onel SF. 2008. WASP and SCAR have distinct roles in activating the Arp2/3 complex during myoblast fusion. J. Cell Sci 121:1303-1313.
12. Bolatto C, Chifflet S, Megighian A, Cantera R. 2003. Synaptic activity modifies the levels of Dorsal and Cactus at the neuromuscular junction of Drosophila. J Neurobiol 54:525-536.
13. Bour BA, Chakravarti M, West JM, Abmayr SM. 2000. Drosophila SNS, a member of the immunoglobulin superfamily that is essential for myoblast fusion. Genes Dev 14:1498-1511.
14. Bour BA, O'Brien MA, Lockwood WL, Goldstein ES, Bodmer R, Taghert PH, Abmayr SM, Nguyen HT. 1995. Drosophila MEF2, a transcription factor that is essential for myogenesis. Genes Dev 9:730-741.
15. Cantera R, Kozlova T, Barillas-Mury C, Kafatos FC. 1999. Muscle structure and innervation are affected by loss of Dorsal in the fruit fly, Drosophila melanogaster. Mol Cell Neurosci 13:131-141.
16. Chiannilkulchai N, Pasturaud P, Richard I, Auffray C, Beckmann JS. 1995. A primary expression map of the chromosome 15q15 region containing the recessive form of limb-girdle muscular dystrophy (LGMD2A) gene. Hum Mol Genet 4:717-725.
17. Cohen N, Kudryashova E, Kramerova I, Anderson LV, Beckmann JS, Bushby K, Spencer MJ. 2006. Identification of putative in vivo substrates of calpain 3 by comparative proteomics of overexpressing transgenic and nontransgenic mice. Proteomics 6:6075-6084.
18. Damm C, Wolk A, Buttgereit D, Loher K, Wagner E, Lilly B, Olson EN, Hasenpusch-Theil K, Renkawitz-Pohl R. 1998. Independent regulatory elements in the upstream region of the Drosophila 3 tubulin gene (Tub60D) guide expression in the dorsal vessel and the somatic muscles. Dev Biol 199:138-149.
19. Dedieu S, Poussard S, Mazères G, Grise F, Dargelos E, Cottin P, Brustis JJ. 2004. Myoblast migration is regulated by calpain through its involvement in cell attachment and cytoskeletal organization. Exp Cell Res 292:187-200.
20. Dourdin N, Balcerzak D, Brustis JJ, Poussard S, Cottin P, Ducastaing A. 1999. Potential m-calpain substrates during myoblast fusion. Exp Cell Res 246:433-442.
21. Dourdin N, Brustis JJ, Balcerzak B, Elamrani N, Poussard S, Cottin P, Ducastaing A. 1997. Myoblast fusion requires fibronectin degradation by exteriorized m-calpain. Exp Cell Res 235:385-394.
22. Duan R, Jin P, Luo F, Zhang G, Anderson N, Chen EH. 2012. Group I PAKs function downstream of Rac to promote podosome invasion during myoblast fusion in vivo. J Cell Biol 199:169-185.
23. Dworak HA, Charles MA, Pellerano LB, Sink H. 2001. Characterization of Drosophila hibris, a gene related to human nephrin. Development 128:4265-4276.
24. 2+-dependent protease Calpain A regulates Cactus/I kappaB levels during Drosophila development in response to maternal Dpp signals. Mech Dev 126:737-751.
25. Fontenele M, Lim B, Oliveira D, Buffolo M, Perlman DH, Schupbach T, Araujo H. 2013. Calpain A modulates Toll responses by limited Cactus/IκB proteolysis. Mol Biol Cell 24:2966-2980.
26. Friedrich P, Bozóky Z. 2005. Digestive versus regulatory proteases: On calpain action in vivo. Biol Chem 386:609-612.
27. Garnham CP, Hanna RA, Chou JS, Low KE, Gourlay K, Campbell RL, Beckmann JS, Davies PL. 2009. Limb-girdle muscular dystrophy type 2A can result from accelerated autoproteolytic inactivation of calpain 3. Biochemistry 48:3457-3467.
28. Gildor B, Massarwa R, Shilo BZ, Schejter ED. 2009. The SCAR and WASp nucleation-promoting factors act sequentially to mediate Drosophila myoblast fusion. EMBO Rep 10:1043-1050.
29. Gruenbaum-Cohen Y, Harel I, Umansky KB, Tzahor E, Snapper SB, Shilo BZ, Schejter ED. 2012. The actin regulator N-WASp is required for muscle-cell fusion in mice. Proc Natl Acad Sci USA 109:11211-11216.
30. Halfon MS, Hashimoto C, Keshishian H. 1995. The Drosophila toll gene functions zygotically and is necessary for proper motoneuron and muscle development. Dev Biol 169:151-167.
31. Halfon MS, Keshishian H. 1998. The Toll pathway is required in the epidermis for muscle development in the Drosophila embryo. Dev Biol 99:164-174.
32. Han Y, Weinman S, Boldogh I, Walker RK, Brasier AR. 1999. Tumor necrosis factor-alpha-inducible IkappaBalpha proteolysis mediated by cytosolic m-calpain. A mechanism parallel to the ubiquitin-proteasome pathway for nuclear factor-kappab activation. J Biol Chem 274:787-794.
33. Holtzer H, Dilullo C, Costa ML, Lu M, Choi J, Mermelstein CS, Schultheiss T, Holtzer S. 1991. Striated myoblasts and multinucleated myotubes induced in non-muscle cells by MyoD are similar to normal in vivo and in vitro counterparts. In: Ozawa E, Masaki T, Nabeshima Y, editors. Frontiers in muscle research. Amsterdam: Elsevier. pp 187-207.
34. Honda M, Masui F, Kanzawa N, Tsuchiya T, Toyo-oka T. 2008. Specific knockdown of m-calpain blocks myogenesis with cDNA deduced from the corresponding RNAi. Am J Physiol Cell Physiol 294:C957-C965.
35. Jékely G, Friedrich P. 1999a. Characterization of two recombinant Drosophila calpains. CALPA and a novel homolog, CALPB. J Biol Chem 274:23893-23900.
36. Jékely G, Friedrich P. 1999b. The evolution of the calpain family as reflected in paralogous chromosome regions. J Mol Evol 49:272-281.
37. Jin P, Duan R, Luo F, Zhang G, Hong SN, Chen EH. 2011. Competition between Blown fuse and WASP for WIP binding regulates the dynamics of WASP-dependent actin polymerization in vivo. Dev Cell 20:623-638.
38. Joffroy S, Dourdin N, Delage JP, Cottin P, Koenig J, Brustis JJ. 2000. M-calpain levels increase during fusion of myoblasts in the mutant muscular dysgenesis (mdg) mouse. Int J Dev Biol 44:421-428.
39. Kaipa BR, Shao H, Schafer G, Trinkewitz T, Groth V, Liu J, Beck L, Bogdan S, Abmayr SM, Onel SF. 2013. Dock mediates Scar-and WASp-dependent actin polymerization through interaction with cell adhesion molecules in founder cells and fusion-competent. J Cell Sci 126:360-372.
40. Kim JH, Jin P, Duan R, Chen EH. 2015. Mechanisms of myoblast fusion during muscle development. Curr Opin Genet Dev 32:162-170.
41. Kramerova I, Kudryashova E, Tidball JG, Spencer MJ. 2004. Null mutation of calpain 3 (p94) in mice causes abnormal sarcomere formation in vivo and in vitro. Hum Mol Genet 13:1373-1388.
42. Kwak KB, Kambayashi J, Kang MS, Ha DB, Chung CH. 1993. Cell-penetrating inhibitors of calpain block both membrane fusion and filamin cleavage in chick embryonic myoblasts. FEBS Lett 323:151-154.
43. Landemaine A, Rescan PY, Gabillard JC. 2014. Myomaker mediates fusion of fast myocytes in zebrafish embryos. Biochem Biophys Res Commun 451:480-484.
44. Lilly B, Zhao B, Ranganayakulu G, Paterson BM, Schulz RA, Olson EN. 1995. Requirement of MADS domain transcription factor D-MEF2 for muscle formation in Drosophila. Science 267:688-693.
45. Macqueen DJ, Wilcox AH. 2014. Characterization of the definitive classical calpain family of vertebrates using phylogenetic, evolutionary and expression analyses. Open Biol 4:130219.
46. Mermelstein C, dos S, Costa ML, Chagas Filho C, Moura Neto V. 1996. Intermediate filament proteins in TPA-treated skeletal muscle cells in culture. J Muscle Res Cell Motil 17:199-206.
47. Mermelstein CS, Portilho DM, Mendes FA, Costa ML, Abreu JG. 2007. Wnt/beta-catenin pathway activation and myogenic differentiation are induced by cholesterol depletion. Differentiation 75:184-192.
48. Millay DP, Sutherland LB, Bassel-Duby R, Olson EN. 2014. Myomaker is essential for muscle regeneration. Genes Dev 28:1641-1646.
49. Moussian B, Roth S. 2005. Dorsoventral axis formation in the Drosophila embryo-Shaping and transducing a morphogen gradient. Curr Biol 15:R887-R899.
50. Mukherjee P, Gildor B, Shilo BZ, VijayRaghavan K, Schejter ED. 2011. The actin nucleator WASp is required for myoblast fusion during adult Drosophila myogenesis. Development 138:2347-2357.
51. Ono Y, Sorimachi H. 2012. Calpains: An elaborate proteolytic system. Biochim Biophys Acta 1824:224-236.
52. Portilho DM, Soares CP, Morrot A, Thiago LS, Butler-Browne G, Savino W, Costa ML, Mermelstein C. 2012. Cholesterol depletion by methyl-β-cyclodextrin enhances cell proliferation and increases the number of desmin-positive cells in myoblast cultures. Eur J Pharmacol 694:1-12.
53. Powell GT, Wright GJ. 2011. Jamb and jamc are essential for vertebrate myocyte fusion. PLoS Biol 9:e1001216.
54. Richard I, Broux O, Allamand V, Fougerousse F, Chiannilkulchai N, Bourg N, Brenguier L, Devaud C, Pasturaud P, Roudaut C, Hillaire D, Passos-Bueno M, Zatz M, JTischfield J, Fardeau M, Jackson J, Cohen D, Beckmann D. 1995. Mutations in the proteolytic enzyme calpain 3 cause limb-girdle muscular dystrophy type 2A. Cell 81:27-40.
55. Richard I, Roudaut C, Marchand S, Baghdiguian S, Herasse M, Stockholm D, Ono Y, Suel L, Bourg N, Sorimachi H, Lefranc G, Fardeau M, Sébille A, Beckmann JS. 2000. Loss of calpain 3 proteolytic activity leads to muscular dystrophy and to apoptosis-associated IkappaBalpha/nuclear factor kappaB pathway perturbation in mice. J Cell Biol 151:1583-1590.
56. Richardson BE, Beckett K, Nowak SJ, Baylies MK. 2007. SCAR/WAVE and Arp2/3 are crucial for cytoskeletal remodeling at the site of myoblast fusion. Development 134:4357-4367.
57. Ruiz-Gómez M, Coutts N, Price A, Taylor MV, Bate M. 2000. Drosophila dumbfounded: A myoblast attractant essential for fusion. Cell 102:189-198.
58. Schnorrer F, Schönbauer C, Langer CC, Dietzl G, Novatchkova M, Schernhuber K, Fellner M, Azaryan A, Radolf M, Stark A, Keleman K, Dickson BJ. 2010. Systematic genetic analysis of muscle morphogenesis and function in Drosophila. Nature 464:287-291.
59. Shen J, Channavajhala P, Seldin DC, Sonenshein GE. 2001. Phosphorylation by the protein kinase CK2 promotes calpain-mediated degradation of IkappaBalpha. J Immunol 167:4919-4925.
60. Shelton C, Kocherlakota KS, Zhuang S, Abmayr SM. 2009. The immunoglobulin superfamily member Hbs functions redundantly with Sns in interactions between founder and fusion-competent myoblasts. Development 136:1159-1168.
61. Shilagardi K, Li S, Luo F, Marikar F, Duan R, Jin P, Kim JH, Murnen K, Chen EH. 2013. Actin-propelled invasive membrane protrusions promote fusogenic protein engagement during cell-cell fusion. Science 340:359-363.
62. Shumway SD, Maki M, Miyamoto S. 1999. The PEST domain of IkappaBalpha is necessary and sufficient for in vitro degradation by mu-calpain. J Biol Chem 274:30874-30881.
63. Sohn RL, Huang P, Kawahara G, Mitchell M, Guyon J, Kalluri R, Kunkel LM, Gussoni E. 2009. A role for nephrin, a renal protein, in vertebrate skeletal muscle cell fusion. Proc Natl Acad Sci USA 106:9274-9279.
64. Sorimachi H, Hata S, Ono Y. 2011. Calpain chronicle-An enzyme family under multidisciplinary characterization. Proc Jpn Acad Ser B Phys Biol Sci 87:287-327.
65. Sorimachi H, Imajoh-Ohmi S, Emori Y, Kawasaki H, Ohno S, Minami Y, Suzuki K. 1989. Molecular cloning of a novel mammalian calcium-dependent protease distinct from both m- and mu-types. Specific expression of the mRNA in skeletal muscle. J Biol Chem 264:20106-20111.
66. Srinivas BP, Woo J, Leong WY, Roy S. 2007. A conserved molecular pathway mediates myoblast fusion in insects and vertebrates. Nat Genet 39:781-786.
67. Strünkelnberg M, Bonengel B, Moda LM, Hertenstein A, de Couet HG, Ramos RG, Fischbach KF. 2001. rst and its paralogue kirre act redundantly during embryonic muscle development in Drosophila. Development 128:4229-4239.
68. Suzuki K, Bose P, Leong-Quong RY, Fujita DJ, Riabowol K. 2010. REAP: A two minute cell fractionation method. BMC Res Notes 3:294.
69. Temm-Grove CJ, Wert D, Thompson VF, Allen RE, Goll DE. 1999. Microinjection of calpastatin inhibits fusion in myoblasts. Exp Cell Res 247:293-303.
70. Theopold U, Pintér M, Daffre S, Tryselius Y, Friedrich P, Nässel DR, Hultmark D. 1995. CalpA, a Drosophila calpain homolog specifically expressed in a small set of nerve, midgut, and blood cells. Mol Cell Biol 15:824-834.
71. Wigler M, Pellicer A, Silverstein S, Axel R. 1978. Biochemical transfer of single-copy eucaryotic genes using total cellular DNA as donor. Cell 14:725-731.
72. Xu C, Tabebordbar M, Iovino S, Ciarlo C, Liu J, Castiglioni A, Price E, Liu M, Barton ER, Kahn CR, Wagers AJ, Zon LI. 2013. A zebrafish embryo culture system defines factors that promote vertebrate myogenesis across species. Cell 155:909-921.