Regulation of Skeletal Muscle Myoblast Differentiation and Proliferation by Pannexins

Chapter
First Online:
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 925)

Abstract

Pannexins are newly discovered channels that are now recognized as mediators of adenosine triphosphate release from several cell types allowing communication with the extracellular environment. Pannexins have been associated with various physiological and pathological processes including apoptosis, inflammation, and cancer. However, it is only recently that our work has unveiled a role for Pannexin 1 and Pannexin 3 as novel regulators of skeletal muscle myoblast proliferation and differentiation. Myoblast differentiation is an ordered multistep process that includes withdrawal from the cell cycle and the expression of key myogenic factors leading to myoblast differentiation and fusion into multinucleated myotubes. Eventually, myotubes will give rise to the diverse muscle fiber types that build the complex skeletal muscle architecture essential for body movement, postural behavior, and breathing. Skeletal muscle cell proliferation and differentiation are crucial processes required for proper skeletal muscle development during embryogenesis, as well as for the postnatal skeletal muscle regeneration that is necessary for muscle repair after injury or exercise. However, defects in skeletal muscle cell differentiation and/or deregulation of cell proliferation are involved in various skeletal muscle pathologies. In this review, we will discuss the expression of pannexins and their post-translational modifications in skeletal muscle, their known functions in various steps of myogenesis, including myoblast proliferation and differentiation, as well as their possible roles in skeletal muscle development, regeneration, and diseases such as Duchenne muscular dystrophy.

Keywords

Pannexin Skeletal muscle Myoblast Proliferation Differentiation 

Abbreviations

ATP

Adenosine triphosphate

Ca2+

Calcium

CBX

Carbenoxolone

DMD

Duchenne muscular dystrophy

HSMM

Human primary skeletal muscle myoblast

kDa

Kilodalton

P2R

P2 receptor

Panx

Pannexin

Panx1

Pannexin 1

Panx2

Pannexin 2

Panx3

Pannexin 3

RC

Reserve cell

RMS

Rhabdomyosarcoma

SC

Satellite cell

This is a preview of subscription content, log in to check access.

Notes

Acknowledgements

Our work is supported by the Department of Surgery at the Children’s Hospital of Eastern Ontario (Ottawa, Canada) and the Cancer Research Society.

Conflicts of Interest

No conflicts of interest, financial or otherwise, are declared by the authors.

References

  1. Araya R, Riquelme MA, Brandan E, Saez JC (2004) The formation of skeletal muscle myotubes requires functional membrane receptors activated by extracellular ATP. Brain Res Brain Res Rev 47(1–3):174–188. doi:S0165017304000761 [pii]  10.1016/j.brainresrev.2004.06.003 PubMedCrossRefGoogle Scholar
  2. Arias-Calderon M, Almarza G, Diaz-Vegas A, Contreras-Ferrat A, Valladares D, Casas M, Toledo H, Jaimovich E, Buvinic S (2016) Characterization of a multiprotein complex involved in excitation-transcription coupling of skeletal muscle. Skelet Muscle 6:15. doi: 10.1186/s13395-016-0087-5 PubMedPubMedCentralCrossRefGoogle Scholar
  3. Bao L, Locovei S, Dahl G (2004) Pannexin membrane channels are mechanosensitive conduits for ATP. FEBS Lett 572(1–3):65–68PubMedCrossRefGoogle Scholar
  4. Baranova A, Ivanov D, Petrash N, Pestova A, Skoblov M, Kelmanson I, Shagin D, Nazarenko S, Geraymovych E, Litvin O, Tiunova A, Born TL, Usman N, Staroverov D, Lukyanov S, Panchin Y (2004) The mammalian pannexin family is homologous to the invertebrate innexin gap junction proteins. Genomics 83(4):706–716PubMedCrossRefGoogle Scholar
  5. Bargiotas P, Krenz A, Hormuzdi SG, Ridder DA, Herb A, Barakat W, Penuela S, von Engelhardt J, Monyer H, Schwaninger M (2011) Pannexins in ischemia-induced neurodegeneration. Proc Natl Acad Sci U S A 108(51):20772–20777. doi: 10.1073/pnas.1018262108 PubMedPubMedCentralCrossRefGoogle Scholar
  6. Beckmann A, Grissmer A, Krause E, Tschernig T, Meier C (2016) Pannexin-1 channels show distinct morphology and no gap junction characteristics in mammalian cells. Cell Tissue Res 363(3):751–763. doi: 10.1007/s00441-015-2281-x PubMedCrossRefGoogle Scholar
  7. Bentzinger CF, Wang YX, Rudnicki MA (2012) Building muscle: molecular regulation of myogenesis. Cold Spring Harb Perspect Biol 4(2):pii: a008342. doi: 10.1101/cshperspect.a008342 CrossRefGoogle Scholar
  8. Biressi S, Molinaro M, Cossu G (2007) Cellular heterogeneity during vertebrate skeletal muscle development. Dev Biol 308(2):281–293. doi: 10.1016/j.ydbio.2007.06.006 PubMedCrossRefGoogle Scholar
  9. Boassa D, Ambrosi C, Qiu F, Dahl G, Gaietta G, Sosinsky G (2007) Pannexin1 channels contain a glycosylation site that targets the hexamer to the plasma membrane. J Biol Chem 282(43):31733–31743PubMedCrossRefGoogle Scholar
  10. Bond SR, Wang N, Leybaert L, Naus CC (2012) Pannexin 1 ohnologs in the teleost lineage. J Membr Biol 245(8):483–493. doi: 10.1007/s00232-012-9497-4 PubMedCrossRefGoogle Scholar
  11. Braun T, Gautel M (2011) Transcriptional mechanisms regulating skeletal muscle differentiation, growth and homeostasis. Nat Rev Mol Cell Biol 12(6):349–361. doi:nrm3118 [pii]  10.1038/nrm3118 PubMedCrossRefGoogle Scholar
  12. Bruzzone R, Hormuzdi SG, Barbe MT, Herb A, Monyer H (2003) Pannexins, a family of gap junction proteins expressed in brain. Proc Natl Acad Sci U S A 100(23):13644–13649PubMedPubMedCentralCrossRefGoogle Scholar
  13. Buvinic S, Almarza G, Bustamante M, Casas M, Lopez J, Riquelme M, Saez JC, Huidobro-Toro JP, Jaimovich E (2009) ATP released by electrical stimuli elicits calcium transients and gene expression in skeletal muscle. J Biol Chem 284(50):34490–34505. doi:M109.057315 [pii]  10.1074/jbc.M109.057315 PubMedPubMedCentralCrossRefGoogle Scholar
  14. Caskenette D, Penuela S, Lee V, Barr K, Beier F, Laird DW, Willmore KE (2016) Global deletion of Panx3 produces multiple phenotypic effects in mouse humeri and femora. J Anat. doi: 10.1111/joa.12437 PubMedGoogle Scholar
  15. Cea LA, Cisterna BA, Puebla C, Frank M, Figueroa XF, Cardozo C, Willecke K, Latorre R, Saez JC (2013) De novo expression of connexin hemichannels in denervated fast skeletal muscles leads to atrophy. Proc Natl Acad Sci U S A 110(40):16229–16234. doi: 10.1073/pnas.1312331110 PubMedPubMedCentralCrossRefGoogle Scholar
  16. Celetti SJ, Cowan KN, Penuela S, Shao Q, Churko J, Laird DW (2010) Implications of pannexin 1 and pannexin 3 for keratinocyte differentiation. J Cell Sci 123(Pt 8):1363–1372. doi:jcs.056093 [pii]  10.1242/jcs.056093 PubMedCrossRefGoogle Scholar
  17. Chekeni FB, Elliott MR, Sandilos JK, Walk SF, Kinchen JM, Lazarowski ER, Armstrong AJ, Penuela S, Laird DW, Salvesen GS, Isakson BE, Bayliss DA, Ravichandran KS (2010) Pannexin 1 channels mediate ‘find-me’ signal release and membrane permeability during apoptosis. Nature 467(7317):863–867. doi:nature09413 [pii]  10.1038/nature09413 PubMedPubMedCentralCrossRefGoogle Scholar
  18. Christ B, Ordahl CP (1995) Early stages of chick somite development. Anat Embryol (Berl) 191(5):381–396CrossRefGoogle Scholar
  19. Cinnamon Y, Kahane N, Bachelet I, Kalcheim C (2001) The sub-lip domain--a distinct pathway for myotome precursors that demonstrate rostral-caudal migration. Development 128(3):341–351PubMedGoogle Scholar
  20. Cowan KN, Langlois S, Penuela S, Cowan BJ, Laird DW (2012) Pannexin1 and Pannexin3 exhibit distinct localization patterns in human skin appendages and are regulated during keratinocyte differentiation and carcinogenesis. Cell Commun Adhes 19(3–4):45–53. doi: 10.3109/15419061.2012.712575 PubMedCrossRefGoogle Scholar
  21. D’Hondt C, Ponsaerts R, De Smedt H, Vinken M, De Vuyst E, De Bock M, Wang N, Rogiers V, Leybaert L, Himpens B, Bultynck G (2011) Pannexin channels in ATP release and beyond: an unexpected rendezvous at the endoplasmic reticulum. Cell Signal 23(2):305–316. doi:S0898-6568(10)00211-1 [pii]  10.1016/j.cellsig.2010.07.018 PubMedCrossRefGoogle Scholar
  22. Diezmos EF, Sandow SL, Markus I, Shevy Perera D, Lubowski DZ, King DW, Bertrand PP, Liu L (2013) Expression and localization of pannexin-1 hemichannels in human colon in health and disease. Neurogastroenterol Motil 25(6):e395–e405. doi: 10.1111/nmo.12130 PubMedCrossRefGoogle Scholar
  23. Dolmatova E, Spagnol G, Boassa D, Baum JR, Keith K, Ambrosi C, Kontaridis MI, Sorgen PL, Sosinsky GE, Duffy HS (2012) Cardiomyocyte ATP release through pannexin 1 aids in early fibroblast activation. Am J Physiol Heart Circ Physiol 303(10):H1208–H1218. doi: 10.1152/ajpheart.00251.2012 PubMedPubMedCentralCrossRefGoogle Scholar
  24. Ednie AR, Bennett ES (2012) Modulation of voltage-gated ion channels by sialylation. Compr Physiol 2(2):1269–1301. doi: 10.1002/cphy.c110044 PubMedGoogle Scholar
  25. Friday BB, Pavlath GK (2001) A calcineurin- and NFAT-dependent pathway regulates Myf5 gene expression in skeletal muscle reserve cells. J Cell Sci 114(Pt 2):303–310PubMedGoogle Scholar
  26. Friday BB, Horsley V, Pavlath GK (2000) Calcineurin activity is required for the initiation of skeletal muscle differentiation. J Cell Biol 149(3):657–666PubMedPubMedCentralCrossRefGoogle Scholar
  27. Goulding MD, Chalepakis G, Deutsch U, Erselius JR, Gruss P (1991) Pax-3, a novel murine DNA binding protein expressed during early neurogenesis. Embo J 10(5):1135–1147PubMedPubMedCentralGoogle Scholar
  28. Gros J, Manceau M, Thome V, Marcelle C (2005) A common somitic origin for embryonic muscle progenitors and satellite cells. Nature 435(7044):954–958. doi: 10.1038/nature03572 PubMedCrossRefGoogle Scholar
  29. Gulbransen BD, Sharkey KA (2012) Novel functional roles for enteric glia in the gastrointestinal tract. Nat Rev Gastroenterol Hepatol 9(11):625–632. doi:nrgastro.2012.138 [pii]  10.1038/nrgastro.2012.138 PubMedCrossRefGoogle Scholar
  30. Hirata A, Masuda S, Tamura T, Kai K, Ojima K, Fukase A, Motoyoshi K, Kamakura K, Miyagoe-Suzuki Y, Takeda S (2003) Expression profiling of cytokines and related genes in regenerating skeletal muscle after cardiotoxin injection: a role for osteopontin. Am J Pathol 163(1):203–215. doi: 10.1016/S0002-9440(10)63644-9 PubMedPubMedCentralCrossRefGoogle Scholar
  31. Huang YJ, Maruyama Y, Dvoryanchikov G, Pereira E, Chaudhari N, Roper SD (2007) The role of pannexin 1 hemichannels in ATP release and cell-cell communication in mouse taste buds. Proc Natl Acad Sci U S A 104(15):6436–6441PubMedPubMedCentralCrossRefGoogle Scholar
  32. Ishikawa M, Iwamoto T, Nakamura T, Doyle A, Fukumoto S, Yamada Y (2011) Pannexin 3 functions as an ER Ca2+ channel, hemichannel, and gap junction to promote osteoblast differentiation. J Cell Biol 193(7):1257–1274. doi:jcb.201101050 [pii]  10.1083/jcb.201101050 PubMedPubMedCentralCrossRefGoogle Scholar
  33. Ishikawa M, Iwamoto T, Fukumoto S, Yamada Y (2014) Pannexin 3 Inhibits Proliferation of Osteoprogenitor Cells by Regulating Wnt and p21 Signaling. J Biol Chem 289(5):2839–2851. doi:M113.523241 [pii]  10.1074/jbc.M113.523241 PubMedCrossRefGoogle Scholar
  34. Ishikawa M, Williams GL, Ikeuchi T, Sakai K, Fukumoto S, Yamada Y (2016) Pannexin 3 and connexin 43 modulate skeletal development through their distinct functions and expression patterns. J Cell Sci 129(5):1018–1030. doi: 10.1242/jcs.176883 PubMedPubMedCentralCrossRefGoogle Scholar
  35. Iwamoto T, Nakamura T, Doyle A, Ishikawa M, de Vega S, Fukumoto S, Yamada Y (2010) Pannexin 3 regulates intracellular ATP/cAMP levels and promotes chondrocyte differentiation. J Biol Chem 285(24):18948–18958. doi:M110.127027 [pii]  10.1074/jbc.M110.127027 PubMedPubMedCentralCrossRefGoogle Scholar
  36. Jorquera G, Altamirano F, Contreras-Ferrat A, Almarza G, Buvinic S, Jacquemond V, Jaimovich E, Casas M (2012) Cav1.1 controls frequency-dependent events regulating adult skeletal muscle plasticity. J Cell Sci 126(Pt 5):1189–1198. doi:jcs.116855 [pii]  10.1242/jcs.116855 Google Scholar
  37. Jostes B, Walther C, Gruss P (1990) The murine paired box gene, Pax7, is expressed specifically during the development of the nervous and muscular system. Mech Dev 33(1):27–37PubMedCrossRefGoogle Scholar
  38. Kahane N, Kalcheim C (1998) Identification of early postmitotic cells in distinct embryonic sites and their possible roles in morphogenesis. Cell Tissue Res 294(2):297–307PubMedCrossRefGoogle Scholar
  39. Kahane N, Cinnamon Y, Kalcheim C (1998) The cellular mechanism by which the dermomyotome contributes to the second wave of myotome development. Development 125(21):4259–4271PubMedGoogle Scholar
  40. Kassar-Duchossoy L, Giacone E, Gayraud-Morel B, Jory A, Gomes D, Tajbakhsh S (2005) Pax3/Pax7 mark a novel population of primitive myogenic cells during development. Genes Dev 19(12):1426–1431. doi: 10.1101/gad.345505 PubMedPubMedCentralCrossRefGoogle Scholar
  41. Kiefer JC, Hauschka SD (2001) Myf-5 is transiently expressed in nonmuscle mesoderm and exhibits dynamic regional changes within the presegmented mesoderm and somites I-IV. Dev Biol 232(1):77–90. doi: 10.1006/dbio.2000.0114 PubMedCrossRefGoogle Scholar
  42. Lai CP, Bechberger JF, Thompson RJ, MacVicar BA, Bruzzone R, Naus CC (2007) Tumor-suppressive effects of pannexin 1 in C6 glioma cells. Cancer Res 67(4):1545–1554PubMedCrossRefGoogle Scholar
  43. Lai CP, Bechberger JF, Naus CC (2009) Pannexin2 as a novel growth regulator in C6 glioma cells. Oncogene 28(49):4402–4408PubMedCrossRefGoogle Scholar
  44. Langlois S, Xiang X, Young K, Cowan BJ, Penuela S, Cowan KN (2014) Pannexin 1 and pannexin 3 channels regulate skeletal muscle myoblast proliferation and differentiation. J Biol Chem 289(44):30717–30731. doi:M114.572131 [pii]  10.1074/jbc.M114.572131 PubMedPubMedCentralCrossRefGoogle Scholar
  45. Le Vasseur M, Lelowski J, Bechberger JF, Sin WC, Naus CC (2014) Pannexin 2 protein expression is not restricted to the CNS. Front Cell Neurosci 8:392. doi: 10.3389/fncel.2014.00392 PubMedPubMedCentralCrossRefGoogle Scholar
  46. Liu N, Williams AH, Maxeiner JM, Bezprozvannaya S, Shelton JM, Richardson JA, Bassel-Duby R, Olson EN (2012) microRNA-206 promotes skeletal muscle regeneration and delays progression of Duchenne muscular dystrophy in mice. J Clin Invest 122(6):2054–2065. doi:62656 [pii]  10.1172/JCI62656 PubMedPubMedCentralCrossRefGoogle Scholar
  47. Locovei S, Bao L, Dahl G (2006a) Pannexin 1 in erythrocytes: function without a gap. Proc Natl Acad Sci U S A 103(20):7655–7659PubMedPubMedCentralCrossRefGoogle Scholar
  48. Locovei S, Wang J, Dahl G (2006b) Activation of pannexin 1 channels by ATP through P2Y receptors and by cytoplasmic calcium. FEBS Lett 580(1):239–244PubMedCrossRefGoogle Scholar
  49. Loeb DM, Thornton K, Shokek O (2008) Pediatric soft tissue sarcomas. Surg Clin North Am 88(3):615–627, vii. doi:S0039-6109(08)00042-X [pii]  10.1016/j.suc.2008.03.008 PubMedPubMedCentralCrossRefGoogle Scholar
  50. Lohman AW, Weaver JL, Billaud M, Sandilos JK, Griffiths R, Straub AC, Penuela S, Leitinger N, Laird DW, Bayliss DA, Isakson BE (2012) S-nitrosylation inhibits pannexin 1 channel function. J Biol Chem 287(47):39602–39612. doi:M112.397976 [pii]  10.1074/jbc.M112.397976 PubMedPubMedCentralCrossRefGoogle Scholar
  51. Lohman AW, Leskov IL, Butcher JT, Johnstone SR, Stokes TA, Begandt D, DeLalio LJ, Best AK, Penuela S, Leitinger N, Ravichandran KS, Stokes KY, Isakson BE (2015) Pannexin 1 channels regulate leukocyte emigration through the venous endothelium during acute inflammation. Nat Commun 6:7965. doi: 10.1038/ncomms8965 PubMedPubMedCentralCrossRefGoogle Scholar
  52. McNally EM, Pytel P (2007) Muscle diseases: the muscular dystrophies. Annu Rev Pathol 2:87–109. doi: 10.1146/annurev.pathol.2.010506.091936 PubMedCrossRefGoogle Scholar
  53. Moon PM, Penuela S, Barr K, Khan S, Pin CL, Welch I, Attur M, Abramson SB, Laird DW, Beier F (2015) Deletion of Panx3 Prevents the Development of Surgically Induced Osteoarthritis. J Mol Med (Berl). doi: 10.1007/s00109-015-1311-1 Google Scholar
  54. Nanni P, Nicoletti G, Palladini A, Astolfi A, Rinella P, Croci S, Landuzzi L, Monduzzi G, Stivani V, Antognoli A, Murgo A, Ianzano M, De Giovanni C, Lollini PL (2009) Opposing control of rhabdomyosarcoma growth and differentiation by myogenin and interleukin 4. Mol Cancer Ther 8(4):754–761. doi:1535–7163.MCT-08-0678 [pii]  10.1158/1535-7163.MCT-08-0678 PubMedCrossRefGoogle Scholar
  55. Oberlin O, Rey A, Lyden E, Bisogno G, Stevens MC, Meyer WH, Carli M, Anderson JR (2008) Prognostic factors in metastatic rhabdomyosarcomas: results of a pooled analysis from United States and European cooperative groups. J Clin Oncol 26(14):2384–2389. doi:26/14/2384 [pii]  10.1200/JCO.2007.14.7207 PubMedPubMedCentralCrossRefGoogle Scholar
  56. Oh SK, Shin JO, Baek JI, Lee J, Bae JW, Ankamerddy H, Kim MJ, Huh TL, Ryoo ZY, Kim UK, Bok J, Lee KY (2015) Pannexin 3 is required for normal progression of skeletal development in vertebrates.. doi:fj.15-273722 [pii]  10.1096/fj.15-273722 Google Scholar
  57. Ordahl CP, Berdougo E, Venters SJ, Denetclaw WF Jr (2001) The dermomyotome dorsomedial lip drives growth and morphogenesis of both the primary myotome and dermomyotome epithelium. Development 128(10):1731–1744PubMedGoogle Scholar
  58. Orellana JA, Velasquez S, Williams DW, Saez JC, Berman JW, Eugenin EA (2013) Pannexin1 hemichannels are critical for HIV infection of human primary CD4+ T lymphocytes. J Leukoc Biol 94(3):399–407. doi: 10.1189/jlb.0512249 PubMedPubMedCentralCrossRefGoogle Scholar
  59. Panchin YV (2005) Evolution of gap junction proteins--the pannexin alternative. J Exp Biol 208(Pt 8):1415–1419PubMedCrossRefGoogle Scholar
  60. Panchin Y, Kelmanson I, Matz M, Lukyanov K, Usman N, Lukyanov S (2000) A ubiquitous family of putative gap junction molecules. Curr Biol 10(13):R473–R474. doi:S0960-9822(00)00576-5 [pii]PubMedCrossRefGoogle Scholar
  61. Paoletti A, Raza SQ, Voisin L, Law F, Caillet M, Martins I, Deutsch E, Perfettini JL (2013) Editorial: Pannexin-1--the hidden gatekeeper for HIV-1. J Leukoc Biol 94(3):390–392. doi: 10.1189/jlb.0313148 PubMedCrossRefGoogle Scholar
  62. Paterson B, Strohman RC (1972) Myosin synthesis in cultures of differentiating chicken embryo skeletal muscle. Dev Biol 29(2):113–138PubMedCrossRefGoogle Scholar
  63. Pelegrin P, Surprenant A (2006) Pannexin-1 mediates large pore formation and interleukin-1beta release by the ATP-gated P2X7 receptor. Embo J 25(21):5071–5082PubMedPubMedCentralCrossRefGoogle Scholar
  64. Penuela S, Bhalla R, Gong XQ, Cowan KN, Celetti SJ, Cowan BJ, Bai D, Shao Q, Laird DW (2007) Pannexin 1 and pannexin 3 are glycoproteins that exhibit many distinct characteristics from the connexin family of gap junction proteins. J Cell Sci 120(Pt 21):3772–3783. doi:jcs.009514 [pii]  10.1242/jcs.009514 PubMedCrossRefGoogle Scholar
  65. Penuela S, Bhalla R, Nag K, Laird DW (2009) Glycosylation Regulates Pannexin Intermixing and Cellular Localization. Mol Biol Cell 20(20):4313–4323PubMedPubMedCentralCrossRefGoogle Scholar
  66. Penuela S, Gehi R, Laird DW (2013) The biochemistry and function of pannexin channels. Biochim Biophys Acta 1828(1):15–22. doi:S0005-2736(12)00021-1 [pii]  10.1016/j.bbamem.2012.01.017 PubMedCrossRefGoogle Scholar
  67. Penuela S, Kelly JJ, Churko JM, Barr KJ, Berger AC, Laird DW (2014a) Panx1 regulates cellular properties of keratinocytes and dermal fibroblasts in skin development and wound healing. J Invest Dermatol 134(7):2026–2035. doi: 10.1038/jid.2014.86 PubMedCrossRefGoogle Scholar
  68. Penuela S, Lohman AW, Lai W, Gyenis L, Litchfield DW, Isakson BE, Laird DW (2014b) Diverse post-translational modifications of the pannexin family of channel-forming proteins. Channels (Austin) 8(2):124–130. doi:27422 [pii]  10.4161/chan.27422 CrossRefGoogle Scholar
  69. Pillon NJ, Li YE, Fink LN, Brozinick JT, Nikolayev A, Kuo MS, Bilan PJ, Klip A (2014) Nucleotides released from palmitate-challenged muscle cells through pannexin-3 attract monocytes. Diabetes 63(11):3815–3826. doi:db14-0150 [pii]  10.2337/db14-0150 PubMedCrossRefGoogle Scholar
  70. Pinheiro AR, Paramos-de-Carvalho D, Certal M, Costa MA, Costa C, Magalhaes-Cardoso MT, Ferreirinha F, Sevigny J, Correia-de-Sa P (2013) Histamine induces ATP release from human subcutaneous fibroblasts, via pannexin-1 hemichannels, leading to Ca2+ mobilization and cell proliferation. J Biol Chem 288(38):27571–27583. doi: 10.1074/jbc.M113.460865 PubMedPubMedCentralCrossRefGoogle Scholar
  71. Pownall ME, Gustafsson MK, Emerson CP Jr (2002) Myogenic regulatory factors and the specification of muscle progenitors in vertebrate embryos. Annu Rev Cell Dev Biol 18:747–783. doi: 10.1146/annurev.cellbio.18.012502.105758 PubMedCrossRefGoogle Scholar
  72. Prochnow N, Abdulazim A, Kurtenbach S, Wildforster V, Dvoriantchikova G, Hanske J, Petrasch-Parwez E, Shestopalov VI, Dermietzel R, Manahan-Vaughan D, Zoidl G (2012) Pannexin1 stabilizes synaptic plasticity and is needed for learning. PLoS ONE 7(12):e51767. doi: 10.1371/journal.pone.0051767 PONE-D-12-23109 [pii]PubMedPubMedCentralCrossRefGoogle Scholar
  73. Qu Y, Misaghi S, Newton K, Gilmour LL, Louie S, Cupp JE, Dubyak GR, Hackos D, Dixit VM (2011) Pannexin-1 is required for ATP release during apoptosis but not for inflammasome activation. J Immunol 186(11):6553–6561. doi:jimmunol.1100478 [pii]  10.4049/jimmunol.1100478 PubMedCrossRefGoogle Scholar
  74. Relaix F, Rocancourt D, Mansouri A, Buckingham M (2005) A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 435(7044):948–953. doi: 10.1038/nature03594 PubMedCrossRefGoogle Scholar
  75. Riquelme MA, Cea LA, Vega JL, Boric MP, Monyer H, Bennett MV, Frank M, Willecke K, Saez JC (2013) The ATP required for potentiation of skeletal muscle contraction is released via pannexin hemichannels. Neuropharmacology 75:594–603. doi:S0028-3908(13)00118-4 [pii]  10.1016/j.neuropharm.2013.03.022 PubMedCrossRefGoogle Scholar
  76. Riquelme MA, Cea LA, Vega JL, Puebla C, Vargas AA, Shoji KF, Subiabre M, Saez JC (2015) Pannexin channels mediate the acquisition of myogenic commitment in C2C12 reserve cells promoted by P2 receptor activation. Front Cell Dev Biol 3:25. doi: 10.3389/fcell.2015.00025 PubMedPubMedCentralCrossRefGoogle Scholar
  77. Sambasivan R, Tajbakhsh S (2007) Skeletal muscle stem cell birth and properties. Semin Cell Dev Biol 18(6):870–882. doi: 10.1016/j.semcdb.2007.09.013 PubMedCrossRefGoogle Scholar
  78. Sassoon D, Lyons G, Wright WE, Lin V, Lassar A, Weintraub H, Buckingham M (1989) Expression of two myogenic regulatory factors myogenin and MyoD1 during mouse embryogenesis. Nature 341(6240):303–307. doi: 10.1038/341303a0 PubMedCrossRefGoogle Scholar
  79. Scaal M, Christ B (2004) Formation and differentiation of the avian dermomyotome. Anat Embryol (Berl) 208(6):411–424. doi: 10.1007/s00429-004-0417-y CrossRefGoogle Scholar
  80. Schienda J, Engleka KA, Jun S, Hansen MS, Epstein JA, Tabin CJ, Kunkel LM, Kardon G (2006) Somitic origin of limb muscle satellite and side population cells. Proc Natl Acad Sci U S A 103(4):945–950. doi: 10.1073/pnas.0510164103 PubMedPubMedCentralCrossRefGoogle Scholar
  81. Schultz E (1996) Satellite cell proliferative compartments in growing skeletal muscles. Dev Biol 175(1):84–94. doi: 10.1006/dbio.1996.0097 PubMedCrossRefGoogle Scholar
  82. Schwetz TA, Norring SA, Ednie AR, Bennett ES (2011) Sialic acids attached to O-glycans modulate voltage-gated potassium channel gating. J Biol Chem 286(6):4123–4132. doi: 10.1074/jbc.M110.171322 PubMedCrossRefGoogle Scholar
  83. Seror C, Melki MT, Subra F, Raza SQ, Bras M, Saidi H, Nardacci R, Voisin L, Paoletti A, Law F, Martins I, Amendola A, Abdul-Sater AA, Ciccosanti F, Delelis O, Niedergang F, Thierry S, Said-Sadier N, Lamaze C, Metivier D, Estaquier J, Fimia GM, Falasca L, Casetti R, Modjtahedi N, Kanellopoulos J, Mouscadet JF, Ojcius DM, Piacentini M, Gougeon ML, Kroemer G, Perfettini JL (2011) Extracellular ATP acts on P2Y2 purinergic receptors to facilitate HIV-1 infection. J Exp Med 208(9):1823–1834. doi: 10.1084/jem.20101805 PubMedPubMedCentralCrossRefGoogle Scholar
  84. Shestopalov VI, Panchin Y (2008) Pannexins and gap junction protein diversity. Cell Mol Life Sci 65(3):376–394PubMedCrossRefGoogle Scholar
  85. Silverman WR, de Rivero Vaccari JP, Locovei S, Qiu F, Carlsson SK, Scemes E, Keane RW, Dahl G (2009) The pannexin 1 channel activates the inflammasome in neurons and astrocytes. J Biol Chem 284(27):18143–18151PubMedPubMedCentralCrossRefGoogle Scholar
  86. Sosinsky GE, Boassa D, Dermietzel R, Duffy HS, Laird DW, MacVicar B, Naus CC, Penuela S, Scemes E, Spray DC, Thompson RJ, Zhao HB, Dahl G (2011) Pannexin channels are not gap junction hemichannels. Channels (Austin) 5(3):193–197. doi:15765 [pii]CrossRefGoogle Scholar
  87. Stewart MK, Plante I, Penuela S, Laird DW (2016) Loss of Panx1 Impairs Mammary Gland Development at Lactation: Implications for Breast Tumorigenesis. PLoS ONE 11(4):e0154162. doi: 10.1371/journal.pone.0154162 PubMedPubMedCentralCrossRefGoogle Scholar
  88. Stuelsatz P, Pouzoulet F, Lamarre Y, Dargelos E, Poussard S, Leibovitch S, Cottin P, Veschambre P (2010) Down-regulation of MyoD by calpain 3 promotes generation of reserve cells in C2C12 myoblasts. J Biol Chem 285(17):12670–12683. doi: 10.1074/jbc.M109.063966 PubMedPubMedCentralCrossRefGoogle Scholar
  89. Suadicani SO, Iglesias R, Wang J, Dahl G, Spray DC, Scemes E (2012) ATP signaling is deficient in cultured Pannexin1-null mouse astrocytes. Glia 60(7):1106–1116. doi: 10.1002/glia.22338 PubMedPubMedCentralCrossRefGoogle Scholar
  90. Swayne LA, Sorbara CD, Bennett SA (2010) Pannexin 2 is expressed by postnatal hippocampal neural progenitors and modulates neuronal commitment. J Biol Chem 285(32):24977–24986. doi:M110.130054 [pii]  10.1074/jbc.M110.130054 PubMedPubMedCentralCrossRefGoogle Scholar
  91. Tapscott SJ, Thayer MJ, Weintraub H (1993) Deficiency in rhabdomyosarcomas of a factor required for MyoD activity and myogenesis. Science 259(5100):1450–1453PubMedCrossRefGoogle Scholar
  92. Taulli R, Bersani F, Foglizzo V, Linari A, Vigna E, Ladanyi M, Tuschl T, Ponzetto C (2009) The muscle-specific microRNA miR-206 blocks human rhabdomyosarcoma growth in xenotransplanted mice by promoting myogenic differentiation. J Clin Invest 119(8):2366–2378. doi:38075 [pii]  10.1172/JCI38075 PubMedPubMedCentralGoogle Scholar
  93. Thompson RJ, Zhou N, MacVicar BA (2006) Ischemia opens neuronal gap junction hemichannels. Science 312(5775):924–927PubMedCrossRefGoogle Scholar
  94. Thompson RJ, Jackson MF, Olah ME, Rungta RL, Hines DJ, Beazely MA, MacDonald JF, MacVicar BA (2008) Activation of pannexin-1 hemichannels augments aberrant bursting in the hippocampus. Science 322(5907):1555–1559PubMedCrossRefGoogle Scholar
  95. Timoteo MA, Carneiro I, Silva I, Noronha-Matos JB, Ferreirinha F, Silva-Ramos M, Correia-de-Sa P (2014) ATP released via pannexin-1 hemichannels mediates bladder overactivity triggered by urothelial P2Y6 receptors. Biochem Pharmacol 87(2):371–379. doi: 10.1016/j.bcp.2013.11.007 PubMedCrossRefGoogle Scholar
  96. Turmel P, Dufresne J, Hermo L, Smith CE, Penuela S, Laird DW, Cyr DG (2011) Characterization of pannexin1 and pannexin3 and their regulation by androgens in the male reproductive tract of the adult rat. Mol Reprod Dev 78(2):124–138. doi: 10.1002/mrd.21280 PubMedCrossRefGoogle Scholar
  97. Valladares D, Almarza G, Contreras A, Pavez M, Buvinic S, Jaimovich E, Casas M (2013) Electrical stimuli are anti-apoptotic in skeletal muscle via extracellular ATP. Alteration of this signal in Mdx mice is a likely cause of dystrophy. PLoS ONE 8(11):e75340. doi: 10.1371/journal.pone.0075340 PubMedPubMedCentralCrossRefGoogle Scholar
  98. Vanden Abeele F, Bidaux G, Gordienko D, Beck B, Panchin YV, Baranova AV, Ivanov DV, Skryma R, Prevarskaya N (2006) Functional implications of calcium permeability of the channel formed by pannexin 1. J Cell Biol 174(4):535–546PubMedPubMedCentralCrossRefGoogle Scholar
  99. Wang H, Garzon R, Sun H, Ladner KJ, Singh R, Dahlman J, Cheng A, Hall BM, Qualman SJ, Chandler DS, Croce CM, Guttridge DC (2008) NF-kappaB-YY1-miR-29 regulatory circuitry in skeletal myogenesis and rhabdomyosarcoma. Cancer Cell 14(5):369–381. doi:S1535-6108(08)00330-9 [pii]  10.1016/j.ccr.2008.10.006 PubMedCrossRefGoogle Scholar
  100. Weilinger NL, Lohman AW, Rakai BD, Ma EM, Bialecki J, Maslieieva V, Rilea T, Bandet MV, Ikuta NT, Scott L, Colicos MA, Teskey GC, Winship IR, Thompson RJ (2016) Metabotropic NMDA receptor signaling couples Src family kinases to pannexin-1 during excitotoxicity. Nat Neurosci 19(3):432–442. doi: 10.1038/nn.4236 PubMedCrossRefGoogle Scholar
  101. Yaffe D (1968) Retention of differentiation potentialities during prolonged cultivation of myogenic cells. Proc Natl Acad Sci U S A 61(2):477–483PubMedPubMedCentralCrossRefGoogle Scholar
  102. Yaffe D, Saxel O (1977) Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 270(5639):725–727PubMedCrossRefGoogle Scholar
  103. Yin H, Price F, Rudnicki MA (2013) Satellite cells and the muscle stem cell niche. Physiol Rev 93(1):23–67. doi: 10.1152/physrev.00043.2011 PubMedPubMedCentralCrossRefGoogle Scholar
  104. Yoshida N, Yoshida S, Koishi K, Masuda K, Nabeshima Y (1998) Cell heterogeneity upon myogenic differentiation: down-regulation of MyoD and Myf-5 generates ‘reserve cells’. J Cell Sci 111(Pt 6):769–779PubMedGoogle Scholar
  105. Zoidl G, Kremer M, Zoidl C, Bunse S, Dermietzel R (2008) Molecular diversity of connexin and pannexin genes in the retina of the zebrafish Danio rerio. Cell Commun Adhes 15(1):169–183PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of Surgery, Division of SurgeryUniversity of Ottawa, Children’s Hospital of Eastern OntarioOttawaCanada
  2. 2.Molecular Biomedicine ProgramChildren’s Hospital of Eastern Ontario Research InstituteOttawaCanada
  3. 3.Department of Surgery, Division of SurgeryUniversity of Ottawa, Children’s Hospital of Eastern OntarioOttawaCanada
  4. 4.Department of Cellular and Molecular MedicineUniversity of OttawaOttawaCanada

Personalised recommendations