The ATP required for potentiation of skeletal muscle contraction is released via pannexin hemichannels

Neuropharmacology

Volumn 75, Issue , 2013, Pages 594-603

  Riquelme, Manuel A ^a   Cea, Luis A ^a,f   Vega, José L ^a,b,c   Boric, Mauricio P ^a   Monyer, Hannah ^b,c   Bennett, Michael V L ^d   Frank, Marina ^e   Willecke, Klaus ^e   Sáez, Juan C ^a,f  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b UNIVERSIDAD DE ANTOFAGASTA   (Chile)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^e UNIVERSITY OF BONN   (Germany)

^f Centro Interdisciplinario de Neurociencias de Valparaíso   (Chile)

Author keywords

Contractil force; Pannexin; Purinergic receptors

Indexed keywords

1,4 DIHYDROPYRIDINE RECEPTOR; ADENOSINE TRIPHOSPHATE; ETHIDIUM; GAP JUNCTION PROTEIN; GLUCOSE TRANSPORTER 4; PANNEXIN1; PURINERGIC P2X RECEPTOR; PURINERGIC P2Y RECEPTOR; RYANODINE RECEPTOR; UNCLASSIFIED DRUG;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; ELECTROSTIMULATION; EXTENSOR DIGITORUM LONGUS MUSCLE; FAST MUSCLE; GLUCOSE TRANSPORT; KNOCKOUT MOUSE; MALE; MOUSE; MUSCLE CELL; MUSCLE CONTRACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SLOW MUSCLE; SOLEUS MUSCLE; TRANSVERSE TUBULAR SYSTEM;

CONTRACTIL FORCE; ETD(+); ETHIDIUM; PANNEXIN; PANNEXIN1 HEMICHANNELS; PANX1 HCS; PURINERGIC RECEPTORS;

4-CHLORO-7-NITROBENZOFURAZAN; ACTION POTENTIALS; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANIMALS; CONNEXINS; DEOXYGLUCOSE; ETHIDIUM; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUSCLE CONTRACTION; MUSCLE, SKELETAL; MYOSINS; OLEIC ACIDS; PHOSPHORYLATION; PURINERGIC P2Y RECEPTOR ANTAGONISTS; RATS; RATS, SPRAGUE-DAWLEY; SERINE;

EID: 84890426112     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.03.022     Document Type: Article

References (52)

1. R. Araya, J.L. Liberona, J.C. Cárdenas, N. Riveros, M. Estrada, J.A. Powell, M.A. Carrasco, and E. Jaimovich Dihydropyridine receptors as voltage sensors for a depolarization-evoked, IP3R-mediated, slow calcium signal in skeletal muscle cells J. Gen. Physiol. 121 2003 3 16
2. R. Araya, M.A. Riquelme, E. Brandan, and J.C. Sáez The formation of skeletal muscle myotubes requires functional membrane receptors activated by extracellular ATP Brain Res. Rev. 47 2004 174 178
3. R. Augustin The protein family of glucose transport facilitators: it's not only about glucose after all IUBMB Life 62 2010 315 333
4. L. Bao, S. Locovei, and G. Dahl Pannexin membrane channels are mechanosensitive conduits for ATP FEBS Lett. 572 2004 65 68
5. A. Baranova, D. Ivanov, N. Petrash, A. Pestova, M. Skoblov, I. Kelmanson, D. Shagin, S. Nazarenko, E. Geraymovych, O. Litvin, A. Tiunova, T.L. Born, N. Usman, D. Staroverov, S. Lukyanov, and Y. Panchin The mammalian pannexin family is homologous to the invertebrate innexin gap junction proteins Genomics 83 2004 706 716
6. M.T. Barbe, H. Monyer, and R. Bruzzone Cell-cell communication beyond connexins: the pannexin channels Physiology (Bethesda) 21 2006 103 114
7. P. Bargiotas, A. Krenz, S.G. Hormuzdi, D.A. Ridder, A. Herb, W. Barakat, S. Peñuela, J. von Engelhardt, H. Monyer, and M. Schwaninger Pannexins in ischemia-induced neurodegeneration Proc. Natl. Acad. Sci. U. S. A. 108 2011 20772 20777
8. N. Belluardo, A. Trovato-Salinaro, G. Mudo, and D.F. Condorelli Expression of the rat connexin 39 (rCx39) gene in myoblasts and myotubes in developing and regenerating skeletal muscles: an in situ hybridization study Cell Tissue Res. 320 2005 299 310
9. D. Boassa, C. Ambrosi, F. Qiu, G. Dahl, G. Gaietta, and G. Sosinsky Pannexin1 channels contain a glycosylation site that targets the hexamer to the plasma membrane J. Biol. Chem. 282 2007 31733 31743
10. D. Boassa, F. Qiu, G. Dahl, and G. Sosinsky Trafficking dynamics of glycosylated pannexin 1 proteins Cell Commun. Adhes. 15 2008 119 132
11. J.L. Boyer, A. Mohanram, E. Camaioni, K.A. Jacobson, and T.K. Harden Competitive and selective antagonism of P2Y1 receptors by N6-methyl 2′-deoxyadenosine 3′,5′-bisphosphate Br. J. Pharmacol. 124 1998 1 3
12. R. Bruzzone, M.T. Barbe, N.J. Jakob, and H. Monyer Pharmacological properties of homomeric and heteromeric pannexin hemichannels expressed in Xenopus oocytes J. Neurochem. 92 2005 1033 1043
13. S. Buvinic, G. Almarza, M. Bustamante, M. Casas, J. López, M. Riquelme, J.C. Sáez, J.P. Huidobro-Toro, and E. Jaimovich ATP released by electrical stimuli elicits calcium transients and gene expression in skeletal muscle J. Biol. Chem. 284 2009 34490 34505
14. J.E. Contreras, J.C. Sáez, F.F. Bukauskas, and M.V. Bennett Gating and regulation of connexin 43 (Cx43) hemichannels Proc. Natl. Acad. Sci. U. S. A. 100 2003 11388 11393
15. R.A. Cunha, and A.M. Sebastiao Adenosine and adenine nucleotides are independently released from both the nerve terminals and the muscle fibres upon electrical stimulation of the innervated skeletal muscle of the frog Pflügers Arch. 424 1993 503 510
16. M.J. Dennis, L. Ziskind-Conhaim, and A.J. Harris Development of neuromuscular junctions in rat embryos Dev. Biol. 81 1981 266 279
17. G. Dvoriantchikova, D. Ivanov, Y. Panchin, and V.I. Shestopalov Expression of pannexin family of proteins in the retina FEBS Lett. 580 2006 2178 2182
18. P.T. Fueger, J. Shearer, T.M. Krueger, K.A. Posey, D.P. Bracy, S. Heikkinen, M. Laakso, J.N. Rottman, and D.H. Wasserman Hexokinase II protein content is a determinant of exercise endurance capacity in the mouse J. Physiol. 566 2005 533 541
19. P.T. Fueger, C.Y. Li, J.E. Ayala, J. Shearer, D.P. Bracy, M.J. Charron, J.N. Rottman, and D.H. Wasserman Glucose kinetics and exercise tolerance in mice lacking the GLUT4 glucose transporter J. Physiol. 582 2007 801 812
20. M. Gorselink, M.R. Drost, K.F. de Brouwer, G. Schaart, G.P. van Kranenburg, T.H. Roemen, M. van Bilsen, M.J. Charron, and G.J. van der Vusse Increased muscle fatigability in GLUT-4-deficient mice Am. J. Physiol. Endocrinol. Metab. 282 2002 E348 E354
21. B. Hellwig, and H.G. Joost Differentiation of erythrocyte-(GLUT1), liver-(GLUT2), and adipocyte-type (GLUT4) glucose transporters by binding of the inhibitory ligands cytochalasin B, forskolin, dipyridamole, and isobutylmethylxanthine Mol. Pharmacol. 40 1991 383 389
22. Y. Hitomi, T. Kizaki, S. Watanabe, G. Matsumura, Y. Fujioka, S. Haga, T. Izawa, N. Taniguchi, and H. Ohno Seven skeletal muscles rich in slow muscle fibers may function to sustain neutral position in the rodent hindlimb Comp. Biochem. Physiol. B Biochem. Mol. Biol. 140 2005 45 50
23. Y. Huang, J.B. Grinspan, C.K. Abrams, and S.S. Scherer Pannexin1 is expressed by neurons and glia but does not form functional gap junctions Glia 55 2007 46 56
24. 7 receptor-Pannexin1 complex: pharmacology and signaling Am. J. Physiol. 295 2008 C752 C760
25. J. Kang, N. Kang, D. Lovatt, A. Torres, Z. Zhao, J. Lin, and M. Nedergaard Connexin 43 hemichannels are permeable to ATP J. Neurosci. 28 2008 4702 4711
26. M.C. Kienitz, K. Bender, R. Dermietzel, L. Pott, and G. Zoidl Pannexin 1 constitutes the large conductance cation channel of cardiac myocytes J. Biol. Chem. 286 2011 290 298
27. J. Li, Z. Gao, V. Kehoe, J. Xing, N. King, and L. Sinoway Interstitial adenosine triphosphate modulates muscle afferent nerve-mediated pressor reflex Muscle Nerve 38 2008 972 977
28. S. Locovei, L. Bao, and G. Dahl Pannexin 1 in erythrocytes: function without a gap Proc. Natl. Acad. Sci. U. S. A. 103 2006 7655 7659
29. S. Locovei, J. Wang, and G. Dahl Activation of pannexin 1 channels by ATP through P2Y receptors and by cytoplasmic calcium FEBS Lett. 580 2006 239 244
30. J.P. Louboutin, V. Fichter-Gagnepain, and J. Noireaud Effects of external calcium on contractile responses in rat extensor digitorum longus muscles after sciatic nerve injury at birth Muscle Nerve 19 1996 1421 1428
31. W. Ma, H. Hui, P. Pelegrin, and A. Surprenant Pharmacological characterization of pannexin-1 currents expressed in mammalian cells J. Pharmacol. Exp. Ther. 328 2009 409 418
32. Y.V. Panchin Evolution of gap junction proteins - the pannexin alternative J. Exp. Biol. 208 2005 1415 1419
33. T. Pangrsic, M. Potokar, M. Stenovec, M. Kreft, E. Fabbretti, A. Nistri, E. Pryazhnikov, L. Khiroug, R. Giniatullin, and R. Zorec Exocytotic release of ATP from cultured astrocytes J. Biol. Chem. 282 2007 28749 28758
34. 7 receptor EMBO J. 25 2006 5071 5082
35. S. Peñuela, R. Bhalla, K. Nag, and D.W. Laird Glycosylation regulates pannexin intermixing and cellular localization Mol. Biol. Cell 20 2009 4313 4323
36. S. Peñuela, R. Bhalla, X.Q. Gong, K.N. Cowan, S.J. Celetti, B.J. Cowan, D. Bai, Q. Shao, and D.W. Laird Pannexin 1 and pannexin 3 are glycoproteins that exhibit many distinct characteristics from the connexin family of gap junction proteins J. Cell Sci. 120 2007 3772 3783
37. 2+-calmodulin-dependent protein kinase II of fast-twitch rat skeletal muscle J. Physiol. 580 2007 993 1005
38. A.J. Rose, B.J. Michell, B.E. Kemp, and M. Hargreaves Effect of exercise on protein kinase C activity and localization in human skeletal muscle J. Physiol. 561 2004 861 870
39. J.W. Ryder, Y. Kawano, D. Galuska, R. Fahlman, H. Wallberg-Henriksson, M.J. Charron, and J.R. Zierath Postexercise glucose uptake and glycogen synthesis in skeletal muscle from GLUT4-deficient mice FASEB J. 13 1999 2246 2256
40. J.C. Sáez, V.M. Berthoud, M.C. Brañes, A.D. Martínez, and E.C. Beyer Plasma membrane channels formed by connexins: their regulation and functions Physiol. Rev. 83 2003 1359 1400
41. D. Sandona, D. Danieli-Betto, E. Germinario, D. Biral, T. Martinello, A. Lioy, E. Tarricone, S. Gastaldello, and R. Betto The T-tubule membrane ATP-operated P2X4 receptor influences contractility of skeletal muscle FASEB J. 19 2005 1184 1186
42. J.M. Santos, S.B. Ribeiro, A.R. Gaya, H.J. Appell, and J.A. Duarte Skeletal muscle pathways of contraction-enhanced glucose uptake Int. J. Sports Med. 29 2008 785 794
43. K.A. Schalper, N. Palacios-Prado, J.A. Orellana, and J.C. Sáez Currently used methods for identification and characterization of hemichannels Cell Commun. Adhes. 15 2008 207 218
44. i responses Mol. Biol. Cell 19 2008 3501 3513
45. R.J. Thompson, N. Zhou, and B.A. MacVicar Ischemia opens neuronal gap junction hemichannels Science 312 2006 924 927
46. F. Vanden Abeele, G. Bidaux, D. Gordienko, B. Beck, Y.V. Panchin, A.V. Baranova, D.V. Ivanov, R. Skryma, and N. Prevarskaya Functional implications of calcium permeability of the channel formed by pannexin 1 J. Cell Biol. 174 2006 535 546
47. J. von Maltzahn, C. Euwens, K. Willecke, and G. Sohl The novel mouse connexin39 gene is expressed in developing striated muscle fibers J. Cell Sci. 117 2004 5381 5392
48. J. Wang, M. Ma, S. Locovei, R.W. Keane, and G. Dahl Modulation of membrane channel currents by gap junction protein mimetic peptides: size matters Am. J. Physiol. Cell Physiol. 293 2007 C1112 C1119
49. M.R. Yen, and M.H. Saier Jr. Gap junctional proteins of animals: the innexin/pannexin superfamily Prog. Biophys. Mol. Biol. 94 2007 5 14
50. L. Yiping, A. Denah, A.M. Kelly, and C. Franzini-Armstrong Differences in the histogenesis of EDL and diaphragm in rat Dev. Dyn. 193 1992 359 369
51. K. Yoshioka, M. Saito, K.B. Oh, Y. Nemoto, H. Matsuoka, M. Natsume, and H. Abe Intracellular fate of 2-NBDG, a fluorescent probe for glucose uptake activity, in Escherichia coli cells Biosci. Biotechnol. Biochem. 60 1996 1899 1901
52. G. Zhi, J.W. Ryder, J. Huang, P. Ding, Y. Chen, Y. Zhao, K.E. Kamm, and J.T. Stull Myosin light chain kinase and myosin phosphorylation effect frequency-dependent potentiation of skeletal muscle contraction Proc. Natl. Acad. Sci. U. S. A. 102 2005 17519 17524