Myoblast proliferation and syncytial fusion both depend on connexin43 function in transfected skeletal muscle primary cultures

Experimental Cell Research

Volumn 313, Issue 6, 2007, Pages 1135-1148

  Gorbe, Aniko ^a   Krenacs, Tibor ^b   Cook, Jeremy E ^c   Becker, David L ^c  

^a UNIVERSITY OF SZEGED   (Hungary)

^b SEMMELWEIS UNIVERSITY   (Hungary)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Cell cycle regulation; Connexin43; Differentiation; Gap junctions; Myoblast proliferation; Skeletal muscle development; Syncytial fusion

Indexed keywords

CONNEXIN 43; FLUORESCEIN ISOTHIOCYANATE DEXTRAN; GREEN FLUORESCENT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MEMBRANE; CELL NUCLEUS; CELL PROLIFERATION; CONTROLLED STUDY; CYTOPLASM; GAP JUNCTION; GENETIC TRANSFECTION; MUSCLE DEVELOPMENT; MYOBLAST; MYOTUBE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; REACTOR CASCADE; SKELETAL MUSCLE; STAINING; SYNCYTIUM; WILD TYPE;

RATTUS;

EID: 33947212046     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2007.01.012     Document Type: Article

References (51)

1. Tajbakhsh S. Stem cells to tissue: molecular, cellular and anatomical heterogeneity in skeletal muscle. Curr. Opin. Genet. Dev. 13 (2003) 413-422
2. Hawke T.J., and Garry D.J. Myogenic satellite cells: physiology to molecular biology. J. Appl. Physiol. 91 (2001) 534-551
3. Cossu G., and Biressi S. Satellite cells, myoblasts and other occasional myogenic progenitors: possible origin, phenotypic features and role in muscle regeneration. Semin. Cell Dev. Biol. 16 (2005) 623-631
4. Kablar B., Krastel K., Tajbakhsh S., and Rudnicki M.A. Myf5 and MyoD activation define independent myogenic compartments during embryonic development. Dev. Biol. 258 (2003) 307-318
5. Mendler L., Zador E., Dux L., and Wuytack F. mRNA levels of myogenic regulatory factors in rat slow and fast muscles regenerating from notexin-induced necrosis. Neuromuscular Disord. 8 (1998) 533-541
6. Ross J.J., Duxson M.J., and Harris A.J. Formation of primary and secondary myotubes in rat lumbrical muscles. Development 100 (1987) 383-394
7. Ontell M., Hughes D., and Bourke D. Morphometric analysis of the developing mouse soleus muscle. Am. J. Anat. 181 (1988) 279-288
8. Rash J.E., and Fambrough D. Ultrastructural and electrophysiological correlates of cell coupling and cytoplasmic fusion during myogenesis in vitro. Dev. Biol. 30 (1973) 166-186
9. Goodenough D.A., and Paul D.L. Beyond the gap: functions of unpaired connexon channels. Nat. Rev. Mol. Cell Biol. 4 (2003) 285-294
10. Bruzzone R., White T.W., and Paul D.L. Connections with connexins: the molecular basis of direct intercellular signalling. Eur. J. Biochem. 238 (1996) 1-27
11. Söhl G., and Willecke K. An update on connexin genes and their nomenclature in mouse and man. Cell Commun. Adhes. 10 (2003) 173-180
12. Loewenstein W.R., and Rose B. The cell-cell channel in the control of growth. Semin. Cell Biol. 3 (1992) 59-79
13. Kamei J., Toyofuku T., and Hori M. Negative regulation of p21 by beta-catenin/TCF signaling: a novel mechanism by which cell adhesion molecules regulate cell proliferation. Biochem. Biophys. Res. Comm. 312 (2003) 380-387
14. Cheng A., Tang H., Cai J., Zhu M., Zhang X., Rao M., and Mattson M.P. Gap junctional communication is required to maintain mouse cortical neural progenitor cells in a proliferative state. Dev. Biol. 272 (2004) 203-216
15. Becker D.L., and Mobbs P. Connexin alpha1 and cell proliferation in the developing chick retina. Exp. Neurol. 156 (1999) 326-332
16. Dermietzel R., Hwang T.K., and Spray D.S. The gap junction family: structure, function and chemistry. Anat. Embryol. (Berl.) 182 (1990) 517-528
17. Araya R., Eckardt D., Maxeiner S., Krüger O., Theis M., Willecke K., and Sáez J.C. Expression of connexins during differentiation and regeneration of skeletal muscle: functional relevance of connexin43. J. Cell Sci. 118 (2005) 27-37
18. Gorbe A., Becker D.L., Dux L., Stelkovics E., Krenacs L., Bagdi E., and Krenacs T. Transient upregulation of connexin43 gap junctions and synchronized cell cycle control precede myoblast fusion in regenerating skeletal muscle in vivo. Histochem. Cell Biol. 123 (2005) 573-583
19. Kalderon N., Epstein M.L., and Gilula N.B. Cell-to-cell communication and myogenesis. J. Cell Biol. 75 (1977) 788-806
20. Schmalbruch H. Skeletal muscle fibers of newborn rats are coupled by gap junctions. Dev. Biol. 91 (1982) 485-490
21. Duxson M.J., and Usson Y. Cellular insertion of primary and secondary myotubes in embryonic rat muscles. Development 107 (1989) 243-251
22. Maltzahn J., Euwens C., Willecke K., and Söhl G. The novel mouse connexin39 gene is expressed in developing striated muscle fibers. J. Cell Sci. 117 (2004) 5381-5392
23. Dahl E., Winterhager E., Traub O., and Willecke K. Expression of gap junction genes, connexin40 and connexin43, during fetal mouse development. Anat. Embryol. (Berl.) 191 (1995) 267-278
24. Gorbe A., Becker D.L., Dux L., Krenacs L., and Krenacs T. In differentiating prefusion myoblasts connexin43 gap junction coupling is upregulated before myoblast alignment then reduced in post-mitotic cells. Histochem. Cell Biol. 125 (2006) 705-716
25. Balogh S., Naus C.C., and Merrifield P.A. Expression of gap junctions in cultured rat L6 cells during myogenesis. Dev. Biol. 155 (1993) 351-360
26. Mège R.M., Goudou D., Giaume C., Nicolet M., and Rieger F. Is intercellular communication via gap junctions required for myoblast fusion?. Cell Adhes. Commun. 2 (1994) 329-343
27. Proulx A., Merrifield P.A., and Naus C.C. Blocking gap junctional intercellular communication in myoblasts inhibits myogenin and MRF4 expression. Dev. Genet. 20 (1997) 133-144
28. Constantin B., Cronier L., and Raymond G. Transient involvement of gap junctional communication before fusion of newborn rat myoblasts. C. R. Acad. Sci. III 320 (1997) 35-40
29. Becker D.L., Ciantar D., Catsicas M., Pearson R., and Mobbs P. Use of pIRES vectors to express eGFP and connexin constructs in studies of the role of gap junctional communication in the early development of the chick retina and brain. Cell Commun. Adhes. 8 (2001) 355-359
30. Wright C.S., Becker D.L., Lin S.J., Warner A.E., and Hardy K. Stage-specific and differential expression of gap junctions in the mouse ovary: connexin-specific roles in follicular regulation. Reproduction 121 (2001) 77-88
31. Becker D.L., Evans W.H., Green C.R., and Warner A.E. Functional analysis of amino acid sequences in connexin 43 involved in intercellular communication through gap junctions. J. Cell Sci. 108 (1995) 1455-1467
32. Olwin B.B., Arthur K., Hannon K., Hein P., McFall A., Riley B., Szebenyi G., Zhou Z., Zuber M.E., Rapraeger A.C., et al. Role of FGFs in skeletal muscle and limb development. Mol. Reprod. Dev. 39 (1994) 90-101
33. Hill C.S., Duran S., Lin Z., Weber K., and Holtzer H. Titin and myosin, but not desmin, are linked during myofibrillogenesis in postmitotic mononucleated myoblasts. J. Cell Biol. 103 (1986) 2185-2196
34. Pearson R., Lüneborg N., Becker D.L., and Mobbs P. Gap junctions modulate interkinetic nuclear migration in retinal progenitor cells. J. Neurosci. 25 (2005) 10803-10814
35. Lo C.W., and Gilula N.B. Gap junctional communication in the post-implantation mouse embryo. Cell 18 (1979) 399-409
36. Azzam E.I., de Toledo S.M., and Little J.B. Direct evidence for the participation of gap junction-mediated intercellular communication in the transmission of damage signals from alpha-particle irradiated to nonirradiated cells. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 473-478
37. kip1 after forced connexin expression in lung and liver carcinoma cells. J. Cell. Biochem. 79 (2000) 347-354
38. Zhang Y.-W., Morita I., Ikeda M., Ma K.-W., and Murota S. Connexin43 suppresses proliferation of osteosarcoma U2OS cells through post-transcriptional regulation of p27. Oncogene 20 (2001) 4138-4149
39. Nadarajah B., Makarenkova H., Becker D.L., Evans W.H., and Parnavelas J.G. Basic FGF increases communication between cells of the developing neocortex. J. Neurosci. 18 (1998) 7881-7890
40. de Alvaro C., Martinez N., Rojas J.M., and Lorenzo M. Sprouty-2 overexpression in C2C12 cells confers myogenic differentiation properties in the presence of FGF2. Mol. Biol. Cell 16 (2005) 4454-4461
41. Bukauskas F.F., Kempf C., and Weingart R. Cytoplasmic bridges and gap junctions in an insect cell line (Aedes albopictus). Exp. Physiol. 77 (1992) 903-911
42. 2+ signalling and gap junction coupling within and between pigment epithelium and neural retina in the developing chick. Eur. J. Neurosci. 19 (2004) 2435-2445
43. Scherberich A., Campos-Toimil M., Rondé P., Takeda K., and Beretz A. Migration of human vascular smooth muscle cells involves serum-dependent repeated cytosolic calcium transients. J. Cell Sci. 113 (2000) 653-662
44. Pfleiderer P.J., Lu K.K., Crow M.T., Keller R.S., and Singer H.A. Modulation of vascular smooth muscle cell migration by calcium/calmodulin-dependent protein kinase II-delta2. Am. J. Physiol. Cell Physiol. 286 (2004) C1238-C1245
45. Dedieu S., Poussard S., Mazères G., Grise F., Dargelos E., Cottin P., and Brustis J.-J. Myoblast migration is regulated by calpain through its involvement in cell attachment and cytoskeletal organization. Exp. Cell Res. 292 (2004) 187-200
46. Mazères G., Leloup L., Daury L., Cottin P., and Brustis J.-J. Myoblast attachment and spreading are regulated by different patterns by ubiquitous calpains. Cell Motil. Cytoskeleton 63 (2006) 193-207
47. Wang Y., Shibasaki F., and Mizuno K. Calcium signal-induced cofilin dephosphorylation is mediated by Slingshot via calcineurin. J. Biol. Chem. 280 (2005) 12683-12689
48. Araya R., Riquelme M.A., Brandan E., and Sáez J.C. The formation of skeletal muscle myotubes requires functional membrane receptors activated by extracellular ATP. Brain Res. Rev. 47 (2004) 147-188
49. 2+ concentration in nutritional medium. Exp. Cell Res. 58 (1969) 163-167
50. 2+ signals to human myoblast differentiation and fusion. Development 133 (2006) 3107-3144
51. + channels. News Physiol. Sci. 17 (2002) 22-26