Functional interaction between TRPC1 channel and connexin-43 protein: A novel pathway underlying S1P action on skeletal myogenesis

Cellular and Molecular Life Sciences

Volumn 67, Issue 24, 2010, Pages 4269-4285

  Meacci, Elisabetta ^a,b   Bini, Francesca ^a,b   Sassoli, Chiara ^a,b   Martinesi, Maria ^a   Squecco, Roberta ^a,b   Chellini, Flaminia ^a   Zecchi Orlandini, Sandra ^a,b   Francini, Fabio ^a,b   Formigli, Lucia ^a,b  

^a UNIVERSITY OF FLORENCE   (Italy)

^b Interuniversity Institute of Myology   (Italy)

Author keywords

Bioactive lipids; Calpain; Gap junctions; Myogenesis; Stretch activated channels

Indexed keywords

CALPAIN 1; CONNEXIN 43; PROTEIN KINASE C ALPHA; SMALL INTERFERING RNA; SPHINGOSINE 1 PHOSPHATE; TRANSIENT RECEPTOR POTENTIAL CHANNEL 1;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; GENE EXPRESSION; GENE FUNCTION; GENE LOCATION; GENE SILENCING; GENE TARGETING; MOUSE; MUSCLE DEVELOPMENT; MYOBLAST; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; UPREGULATION;

ANIMALS; CALPAIN; CELL DIFFERENTIATION; CELL LINE; CONNEXIN 43; LYSOPHOSPHOLIPIDS; MICE; MUSCLE DEVELOPMENT; MUSCLE, SKELETAL; MYOBLASTS, SKELETAL; PATCH-CLAMP TECHNIQUES; PROTEIN KINASE C-ALPHA; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SPHINGOSINE; TRPC CATION CHANNELS;

EID: 78651304694     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-010-0442-3     Document Type: Article

References (60)

1. Kim RH, Takabe K, Milstien S, Spiegel S (2009) Export and functions of sphingosine-1-phosphate. Biochim Biophys Acta 179:692-696
2. Nagata Y, Kobayashi H, Umeda M, Ohta N, Kawashima S, Zammit PS, Matsuda R (2006) Sphingomyelin levels in the plasma membrane correlate with the activation state of muscle satellite cells. J Histochem Cytochem 54:375-384
3. Nagata Y, Partridge TA, Matsuda R, Zammit PS (2006) Entry of muscle satellite cells into the cell cycle requires sphingolipid signaling. J Cell Biol 174:245-253
4. Formigli L, Sassoli C, Squecco R, Bini F, Martinesi M, Chellini F, Luciani G, Sbrana F, Zecchi-Orlandini S, Francini F, Meacci E (2009) Regulation of transient receptor potential canonical channel 1 (TRPC1) by sphingosine 1-phosphate in C2C12 myoblasts and its relevance for a role of mechanotransduction in skeletal muscle differentiation. J Cell Sci 122:1322-1333
5. Meacci E, Nuti F, Donati C, Concetti F, Farnararo M, Bruni P (2008) Sphingosine kinase activity is required for myogenic differentiation of C2C12 myoblasts. J Cell Physiol 214:210-220
6. Squecco R, Sassoli C, Nuti F, Nosi D, Chellini F, Zecchi-Orlandini S, Francini F, Formigli L, Meacci E (2006) Sphingosine 1-phosphate induces myoblast differentiation through Cx43 protein expression: role for a gap junction-dependent and -independent function. Mol Biol Cell 17:4896-4910
7. Zanin M, Germinario E, Dalla Libera L, Sandonà D, Sabbadini RA, Betto R, Danieli-Betto D (2008) Trophic action of sphingosine 1-phosphate in denervated rat soleus muscle. Am J Physiol Cell Physiol 294: C36-C46
8. 2+ transients and cytoskeletal rearrangement in C2C12 myoblastic cells. Am J Physiol Cell Physiol 282: C1361-C1373
9. Meacci E, Cencetti F, Formigli L, Squecco R, Donati C, Tiribilli B, Quercioli F, Zecchi Orlandini S, Francini F, Bruni P (2002) Sphingosine 1-phosphate evokes calcium signals in C2C12 myoblasts via Edg3 and Edg5 receptors. Biochem J 362:349-357
10. Abramowitz J, Birnbaumer L (2009) Physiology and pathophysiology of canonical transient receptor potential channels. FASEB J 23:297-328
11. Formigli L, Meacci E, Sassoli C, Squecco R, Nosi D, Chellini F, Naro F, Francini F, Zecchi-Orlandini S (2007) Actin cytoskeleton/stretch-activated ion channels interaction regulates myogenic differentiation of skeletal myoblasts. J Cell Physiol 211:296-306
12. Formigli L, Meacci E, Sassoli C, Chellini F, Quercioli F, Tiribilli B, Squecco R, Bruni P, Francini F, Zecchi-Orlandini S (2005) Sphingosine 1-phosphate induces cytoskeletal reorganization in C2C12 myoblasts: physiological relevance for stress fibres in the modulation of ion current through stretch-activated channels. J Cell Sci 118:1161-1171
13. Sbrana F, Sassoli C, Meacci E, Nosi D, Squecco R, Paternostro F, Tiribilli B, Zecchi-Orlandini S, Francini F, Formigli L (2008) Role for stress fiber contraction in surface tension development and stretch-activated channel regulation in C2C12 myoblasts. Am J Physiol Cell Physiol 295: C160-C172
14. Su Z, Zhou X, Loukin SH, Haynes WJ, SaimiY Kung C (2009) The use of yeast to understand TRP-channel mechanosensitivity. Pflugers Arch 458:861-867
15. Staaf S, Maxvall I, Lind U, Husmark J, Mattsson J, Ernfors P, Pierrou S (2009) Down regulation of TRPC1 by shRNA reduces mechanosensitivity in mouse dorsal root ganglion neurons in vitro. Neurosci Lett 457:3-7
16. Sharif-Naeini R, Dedman A, Folgering JH, Duprat F, Patel A, Nilius B, Honoré E (2008) TRP channels and mechanosensory transduction: insights into the arterial myogenic response. Pflugers Arch 456:529-540
17. Folgering JH, Sharif-Naeini R, Dedman A, Patel A, Delmas P, Honoré E (2008) Molecular basis of the mammalian pressuresensitive ion channels: focus on vascular mechanotransduction. Prog Biophys Mol Biol 97:180-195
18. Zanou N, Shapovalov G, Louis M, Tajeddine N, Gallo C, Van Schoor M, Anguish I, Cao ML, Schakman O, Dietrich A, Lebacq J, Ruegg U, Roulet E, Birnbaumer L, Gailly P (2010) Role of TRPC1 channel in skeletal muscle function. Am J Physiol Cell Physiol 298: C149-C162
19. Ambudkar IS, Ong HL, Liu X, Bandyopadhyay BC, Cheng KT (2007) TRPC1: the link between functionally distinct storeoperated calcium channels. Cell Calcium 42:213-223
20. Rodríguez-Sinovas A, Cabestrero A, López D, Torre I, Morente M, Abellán A, Miró E, Ruiz-Meana M, García-Dorado D (2009) The modulatory effects of connexin 43 on cell death/survival beyond cell coupling. Prog Biophys Mol Biol 94:219-232
21. Söhl G, Willecke K (2004) Gap junctions and the connexin protein family. Cardiovasc Res 62:228-232
22. Solan JL, Lampe PD (2009) Connexin 43 phosphorylation: structural changes and biological effects. Biochem J 15:261-272
23. Araya R, Eckardt D, Maxeiner S, Kruger O, Theis M, Willecke K, Saez JC (2005) Expression of connexins during differentiation and regeneration of skeletal muscle: functional relevance of connexin 43. J Cell Sci 118:27-37
24. Dobrowolski R, Willecke K (2009) Connexin-caused genetic diseases and corresponding mouse models. Antioxid Redox Signal 11:283-295
25. Cruciani V, Mikalsen SO (2006) The vertebrate connexin family. Cell Mol Life Sci 63:1125-1140
26. Butkevich E, Hulsmann S, Wenzel D, Shiraro T, Duden R, Majoul I (2004) Drebrin is a novel connexin-43 binding partner that links gap junctions to the submembrane cytoskeleton. Curr Biol 14:650-658
27. Joshi-Mukherjee R, Coombs W, Burrer C, Alvarez de Mora I, Delmar M, Taffet S (2007) Evidence for the presence of a free C-terminal fragment of Cx43 in cultured cells. Cell Commun Adhes 14:75-84
28. Hervé JC, Plaisance I, Loncarek J, Duthe F, Sarrouilhe D (2004) Is the junctional uncoupling elicited in rat ventricular myocytes by some dephosphorylation treatments due to changes in the phosphorylation status of Cx43? Eur Biophys J 33:201-210
29. Laird DW (2005) Connexin phosphorylation as a regulatory event linked to gap junction internalization and degradation. Biochim Biophys Acta 1711:172-182
30. Grossi A, Karlsson AH, Lawson MA (2008) Mechanical stimulation of C2C12 cells increases m-calpain expression, focal adhesion plaque protein degradation. Cell Biol Int 32:615-622
31. 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
32. Kramerova I, Kudryashova E, Wu B, Spencer MJ (2006) Regulation of the M-cadherin-beta-catenin complex by calpain 3 during terminal stages of myogenic differentiation. Mol Cell Biol 26:8437-8447
33. Liang YC, Yeh JY, Forsberg NE, Ou BR (2006) Involvement of μ- and m-calpains and protein kinase C isoforms in L8 myoblast differentiation. Int J Biochem Cell Biol 38:662-670
34. Ducret T, Vandebrouck C, Cao ML, Lebacq J, Gailly P (2006) Functional role of store-operated and stretch-activated channels in murine adult skeletal muscle fibers. J Physiol 575:913-924
35. Raynaud F, Carnac G, Marcilhac A, Benyamin Y (2004) m-Calpain implication in cell cycle during muscle precursor cell activation. Exp Cell Res 298:48-57
36. Meacci E, Donati C, Cencetti F, Romiti E, Bruni P (2000) Permissive role of protein kinase C alpha but not protein kinase C delta in sphingosine 1-phosphate-induced Rho A activation in C2C12 myoblasts. FEBS Lett 482:97-101
37. Meacci E, Concetti F, Donati C, Nuti F, Farnararo M, Kohno T, Igarashi Y, Bruni P (2003) Down-regulation of EDG5/S1P2 during myogenic differentiation results in the specific uncoupling of sphingosine 1-phosphate signalling to phospholipase D. Biochim Biophys Acta 1633:133-142
38. Meacci E, Donati C, Cencetti F, Oka T, Komuro I, Farnararo M, Bruni P (2001) Dual regulation of sphingosine 1-phosphateinduced phospholipase D activity through RhoA and protein kinase C-alpha in C2C12 myoblasts. Cell Signal 13:593-598
39. Sasaki T, Kikuchi T, Yumoto N, Yoshimura N, Murachi T (1984) Comparative specificity and kinetic studies on porcine calpain I and calpain II with naturally occurring peptides and synthetic fluorogenic substrates. J Biol Chem 259:12489-12494
40. Lampe PD, Cooper CD, King TJ, Burt JM (2006) Analysis of Connexin43 phosphorylated at S325, S328 and S330 in normoxic and ischemic heart. J Cell Sci 119:3435-3442
41. Louis M, Zanou N, Van Schoor M, Gailly P (2008) TRPC1 regulates skeletal myoblast migration and differentiation. J Cell Sci 121:3951-3959
42. Williams AB, Decourten-Myers GM, Fischer JE, Luo G, Sun X, Hasselgren PO (1999) Sepsis stimulates release of myofilaments in skeletal muscle by a calcium-dependent mechanism. FASEB J 13:1435-1443
43. Buday L, Downward J (2007) Roles of cortactin in tumor pathogenesis. Biochim Biophys Acta 1775:263-273
44. Sirnes S, Kjenseth A, Leithe E, Rivedal E (2009) Interplay between PKC and the MAP kinase pathway in Connexin43 phosphorylation and inhibition of gap junction intercellular communication. Biochem Biophys Res Commun 382:41-45
45. Sosinsky GE, Solan JL, Gaietta GM, Ngan L, Lee GJ, Mackey MR, Lampe PD (2007) The C-terminus of connexin43 adopts different conformations in the Golgi and gap junction as detected with structure-specific antibodies. Biochem J 408:375-385
46. Vandebrouck A, Sabourin J, Rivet J, Balghi H, Sebille S, Kitzis A, Raymond G, Cognard C, Bourmeyster N, Constantin B (2007) Regulation of capacitative calcium entries by 1-syntrophin: association of TRPC1 with dystrophin complex and the PDZ domain of 1-syntrophin. FASEB J 21:608-617
47. Stiber J, Hawkins A, Zhang ZS, Wang S, Burch J, Graham V, Ward CC, Seth M, Finch E, Malouf N, Williams RS, Eu JP, Rosenberg P (2008) STIM1 signaling controls store-operated calcium entry required for development and contractile function in skeletal muscle. Nat Cell Biol 10:688-697
48. Trovato-Salinaro A, Belluardo N, Frinchi M, von Maltzahn J, Willecke K, Condorelli DF, Mudò G (2009) Regulation of connexin gene expression during skeletal muscle regeneration in the adult rat. Am J Physiol Cell Physiol 296: C593-C606
49. Kalderon N, Epstein ML, Gilula NB (1977) Cell-to-cell communication and myogenesis. J Cell Biol 75:788-806
50. von Maltzahn J, Wulf V, Willecke K (2006) Spatiotemporal expression of connexin 39 and -43 during myoblast differentiation in cultured cells and in the mouse embryo. Cell Commun Adhes 13:55-60
51. Hervé JC, Derangeon M, Bahbouhi B, Mesnil M, Sarrouilhe D (2007) The connexin turnover, an important modulating factor of the level of cell-to-cell junctional communication: comparison with other integral membrane proteins. J Membr Biol 217:21-33
52. Rivedal E, Leithe E (2005) Connexin43 synthesis, phosphorylation, and degradation in regulation of transient inhibition of gap junction intercellular communication by the phorbol ester TPA in rat liver epithelial cells. Exp Cell Res 302:143-152
53. Bertipaglia I, Carafoli E (2007) Calpains and human disease. Subcell Biochem 45:29-53
54. Goel HL, Dey CS (2002) PKC-regulated myogenesis is associated with increased tyrosine phosphorylation of FAK, Cas, and paxillin, formation of Cas-CRK complex, and JNK activation. Differentiation 70:257-271
55. Kook SH, Choi KC, Son YO, Lee KY, Hwang IH, Lee HJ, Chung WT, Lee CB, Park JS, Lee JC (2008) Involvement of p38 MAPK-mediated signaling in the calpeptin-mediated suppression of myogenic differentiation and fusion in C2C12 cells. Mol Cell Biochem 310:85-92
56. Lin JS, Fitzgerald S, Dong Y, Knight C, Donaldson P, Kistler J (1997) Processing of the gap junction protein connexin50 in the ocular lens is accomplished by calpain. Eur J Cell Biol 73:141-149
57. Zhang W, Ma X, Zhong M, Zheng Z, Li L, Wang Z, Zhang Y (2009) Role of the calpain system in pulmonary vein connexin remodeling in dogs with atrial fibrillation. Cardiology 112:22-30
58. Vitale ML, Akpovi CD, Pelletier RM (2009) Cortactin/ tyrosinephosphorylated cortactin interaction with connexin 43 in mouse seminiferous tubules. Microsc Res Tech 72:856-867
59. Kardami E, Dang X, Iacobas DA, Nickel BE, Jeyaraman M, Srisakuldee W, Makazan J, Tanguy S, Spray DC (2007) The role of connexins in controlling cell growth and gene expression. Prog Biophys Mol Biol 94:245-264
60. 2+/PKC, p44/42 and p38 MAPKs pathways. Cell Prolif 41:786-802