A molecular signature in the pannexin1 intracellular loop confers channel activation by the α1 adrenoreceptor in smooth muscle cells

Science Signaling

Volumn 8, Issue 364, 2015, Pages

  Billaud, Marie ^a   Chiu, Yu Hsin ^a   Lohman, Alexander W ^a   Parpaite, Thibaud ^a   Butcher, Joshua T ^a   Mutchler, Stephanie M ^a   DeLalio, Leon J ^a   Artamonov, Mykhaylo V ^a   Sandilos, Joanna K ^a   Best, Angela K ^a   Somlyo, Avril V ^a   Thompson, Roger J ^b   Le, Thu H ^a   Ravichandran, Kodi S ^a   Bayliss, Douglas A ^a   Isakson, Brant E ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALPHA 1 ADRENERGIC RECEPTOR; ENDOTHELIN 1; INTERLEUKIN 2; MEMBRANE PROTEIN; MUTANT PROTEIN; NORADRENALIN; PANNEXIN1; PHENYLEPHRINE; PROBENECID; SEROTONIN; TAMOXIFEN; UNCLASSIFIED DRUG; GAP JUNCTION PROTEIN; NERVE PROTEIN; PANX1 PROTEIN, MOUSE;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE; BLOOD PRESSURE REGULATION; BLOOD VESSEL; BLOOD VESSEL TONE; CONTROLLED STUDY; HUMAN; HUMAN CELL; MALE; MEAN ARTERIAL PRESSURE; MOUSE; NONHUMAN; NORADRENERGIC SYSTEM; PRIORITY JOURNAL; PROTEIN EXPRESSION; SITE DIRECTED MUTAGENESIS; SMOOTH MUSCLE FIBER; THORACODORSAL ARTERY; VASOCONSTRICTION; ANALYSIS OF VARIANCE; ANIMAL; C57BL MOUSE; CYTOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; HEK293 CELL LINE; METABOLISM; MOLECULAR GENETICS; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; SIGNAL TRANSDUCTION; TELEMETRY; VASCULAR SMOOTH MUSCLE; WESTERN BLOTTING;

MUS;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; ANALYSIS OF VARIANCE; ANIMALS; BLOOD PRESSURE; BLOTTING, WESTERN; CONNEXINS; ENDOTHELIN-1; FLUORESCENT ANTIBODY TECHNIQUE; HEK293 CELLS; HUMANS; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; MUSCLE, SMOOTH, VASCULAR; MUTAGENESIS, SITE-DIRECTED; NERVE TISSUE PROTEINS; PATCH-CLAMP TECHNIQUES; RECEPTORS, ADRENERGIC, ALPHA-1; SEROTONIN; SIGNAL TRANSDUCTION; TELEMETRY; VASOCONSTRICTION;

EID: 84923093408     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2005824     Document Type: Article

References (74)

1. G. Burnstock, V. Ralevic, Purinergic signaling and blood vessels in health and disease. Pharmacol. Rev. 66, 102-192 (2014).
2. G. Burnstock, Dual control of vascular tone and remodelling by ATP released from nerves and endothelial cells. Pharmacol. Rep. 60, 12-20 (2008).
3. A. W. Lohman, M. Billaud, B. E. Isakson, Mechanisms of ATP release and signalling in the blood vessel wall. Cardiovasc. Res. 95, 269-280 (2012).
4. M. Billaud, A. W. Lohman, A. C. Straub, R. Looft-Wilson, S. R. Johnstone, C. A. Araj, A. K. Best, F. B. Chekeni, K. S. Ravichandran, S. Penuela, D. W. Laird, B. E. Isakson, Pannexin1 regulates α1-adrenergic receptor-mediated vasoconstriction. Circ. Res. 109, 80-85 (2011).
5. Y. Panchin, I. Kelmanson, M. Matz, K. Lukyanov, N. Usman, S. Lukyanov, A ubiquitous family of putative gap junction molecules. Curr. Biol. 10, R473-R474 (2000).
6. G. E. Sosinsky, D. Boassa, R. Dermietzel, H. S. Duffy, D.W. Laird, B. MacVicar, C. C. Naus, S. Penuela, E. Scemes, D. C. Spray, R. J. Thompson, H. B. Zhao, G. Dahl, Pannexin channels are not gap junction hemichannels. Channels 5, 193-197 (2011).
7. G. Spagnol, P. L. Sorgen, D. C. Spray, Structural order in Pannexin 1 cytoplasmic domains. Channels 8, 157-166 (2014).
8. M. R. Yen, M. H. Saier Jr., Gap junctional proteins of animals: The innexin/pannexin superfamily. Prog. Biophys. Mol. Biol. 94, 5-14 (2007).
9. S. R. Bond, C. C. Naus, The pannexins: Past and present. Front. Physiol. 5, 58 (2014).
10. S. Penuela, R. Bhalla, X. Q. Gong, K. N. Cowan, S. J. Celetti, B. J. Cowan, D. Bai, Q. Shao, 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, 3772-3783 (2007).
11. A. W. Lohman, M. Billaud, A. C. Straub, S. R. Johnstone, A. K. Best, M. Lee, K. Barr, S. Penuela, D. W. Laird, B. E. Isakson, Expression of pannexin isoforms in the systemic murine arterial network. J. Vasc. Res. 49, 405-416 (2012).
12. F. B. Chekeni, M. R. Elliott, J. K. Sandilos, S. F. Walk, J. M. Kinchen, E. R. Lazarowski, A. J. Armstrong, S. Penuela, D. W. Laird, G. S. Salvesen, B. E. Isakson, D. A. Bayliss, K. S. Ravichandran, Pannexin 1 channels mediate 'find-me' signal release and membrane permeability during apoptosis. Nature 467, 863-867 (2010).
13. I. K. Poon, Y. H. Chiu, A. J. Armstrong, J. M. Kinchen, I. J. Juncadella, D. A. Bayliss, K. S. Ravichandran, Unexpected link between an antibiotic, pannexin channels and apoptosis. Nature 507, 329-334 (2014).
14. S. E. Adamson, N. Leitinger, The role of pannexin1 in the induction and resolution of inflammation. FEBS Lett. 588, 1416-1422 (2014).
15. N. L. Weilinger, V. Maslieieva, J. Bialecki, S. S. Sridharan, P. L. Tang, R. J. Thompson, Ionotropic receptors and ion channels in ischemic neuronal death and dysfunction. Acta Pharmacol. Sin. 34, 39-48 (2013).
16. M. Sridharan, S. P. Adderley, E. A. Bowles, T. M. Egan, A. H. Stephenson, M. L. Ellsworth, R. S. Sprague, Pannexin 1 is the conduit for low oxygen tension-induced ATP release from human erythrocytes. Am. J. Physiol. Heart Circ. Physiol. 299, H1146-H1152 (2010).
17. B. E. Isakson, R. J. Thompson, Pannexin-1 as a potentiator of ligand-gated receptor signaling. Channels 8, 118-123 (2014).
18. A. W. Lohman, B. E. Isakson, Differentiating connexin hemichannels and pannexin channels in cellular ATP release. FEBS Lett. 588, 1379-1388 (2014).
19. J. K. Sandilos, D. A. Bayliss, Physiological mechanisms for the modulation of pannexin 1 channel activity. J. Physiol. 590, 6257-6266 (2012).
20. S. Gödecke, C. Roderigo, C. R. Rose, B. H. Rauch, A. Gödecke, J. Schrader, Thrombin-induced ATP release from human umbilical vein endothelial cells. Am. J. Physiol. Cell Physiol. 302, C915-C923 (2012).
21. N. L. Weilinger, P. L. Tang, R. J. Thompson, Anoxia-induced NMDA receptor activation opens pannexin channels via Src family kinases. J. Neurosci. 32, 12579-12588 (2012).
22. 2+ mobilization and cell proliferation. J. Biol. Chem. 288, 27571-27583 (2013).
23. 7 receptor-Pannexin1 complex: Pharmacology and signaling. Am. J. Physiol. Cell Physiol. 295, C752-C760 (2008).
24. M. Zhang, N. A. Piskuric, C. Vollmer, C. A. Nurse, P2Y2 receptor activation opens pannexin-1 channels in rat carotid body type II cells: Potential role in amplifying the neurotransmitter ATP. J. Physiol. 590, 4335-4350 (2012).
25. M. Billaud, A. W. Lohman, A. C. Straub, T. Parpaite, S. R. Johnstone, B. E. Isakson, Characterization of the thoracodorsal artery: Morphology and reactivity. Microcirculation 19, 360-372 (2012).
26. 2+ sensitization in smooth muscle: Redundancy of Rho guanine nucleotide exchange factors (RhoGEFs) and response kinetics, a caged compound study. J. Biol. Chem. 288, 34030-34040 (2013).
27. W. Silverman, S. Locovei, G. Dahl, Probenecid, a gout remedy, inhibits pannexin 1 channels. Am. J. Physiol. Cell Physiol. 295, C761-C767 (2008).
28. P. Pelegrin, A. Surprenant, Pannexin-1 mediates large pore formation and interleukin-1β release by the ATP-gated P2X7 receptor. EMBO J. 25, 5071-5082 (2006).
29. 1D-adrenergic receptor directly regulates arterial blood pressure via vasoconstriction. J. Clin. Invest. 109, 765-775 (2002).
30. E. Vivès, P. Brodin, B. Lebleu, A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. J. Biol. Chem. 272, 16010-16017 (1997).
31. J. Howl, I. D. Nicholl, S. Jones, The many futures for cell-penetrating peptides: How soon is now? Biochem. Soc. Trans. 35, 767-769 (2007).
32. J. K. Sandilos, Y. H. Chiu, F. B. Chekeni, A. J. Armstrong, S. F. Walk, K. S. Ravichandran, D. A. Bayliss, Pannexin 1, an ATP release channel, is activated by caspase cleavage of its pore-associated C-terminal autoinhibitory region. J. Biol. Chem. 287, 11303-11311 (2012).
33. A.W. Lohman, J. L. Weaver, M. Billaud, J. K. Sandilos, R. Griffiths, A. C. Straub, S. Penuela, N. Leitinger, D. W. Laird, D. A. Bayliss, B. E. Isakson, S-nitrosylation inhibits pannexin 1 channel function. J. Biol. Chem. 287, 39602-39612 (2012).
34. W. Ma, H. Hui, P. Pelegrin, A. Surprenant, Pharmacological characterization of pannexin-1 currents expressed in mammalian cells. J. Pharmacol. Exp. Ther. 328, 409-418 (2009).
35. 2+ in hamster cremaster arterioles. Br. J. Pharmacol. 155, 514-524 (2008).
36. E. B. Westcott, S. S. Segal, Ageing alters perivascular nerve function of mouse mesenteric arteries in vivo. J. Physiol. 591, 1251-1263 (2013).
37. S. W. Watts, Serotonin-induced contraction in mesenteric resistance arteries: Signaling and changes in deoxycorticosterone acetate-salt hypertension. Hypertension 39, 825-829 (2002).
38. S. W. Watts, R. P. Davis, 5-Hydroxtryptamine receptors in systemic hypertension: An arterial focus. Cardiovasc. Ther. 29, 54-67 (2011).
39. 1B/1D receptor-mediated contraction of the rabbit isolated renal artery. Br. J. Pharmacol. 130, 835-842 (2000).
40. L. N. Pierre, A. P. Davenport, Endothelin receptor subtypes and their functional relevance in human small coronary arteries. Br. J. Pharmacol. 124, 499-506 (1998).
41. D. Rizzoni, E. Porteri, A. Piccoli, M. Castellano, G. Bettoni, G. Pasini, E. Agabiti-Rosei, The vasoconstriction induced by endothelin-1 is mediated only by ETA receptors in mesenteric small resistance arteries of spontaneously hypertensive rats and Wistar Kyoto rats. J. Hypertens. 15, 1653-1657 (1997).
42. 12 receptors activation. Cell Commun. Signal. 11, 70 (2013).
43. 2+-dependent signaling pathways. J. Biol. Chem. 284, 20638-20648 (2009).
44. L. Seminario-Vidal, S. F. Okada, J. I. Sesma, S. M. Kreda, C. A. van Heusden, Y. Zhu, L. C. Jones, W. K. O'Neal, S. Penuela, D. W. Laird, R. C. Boucher, E. R. Lazarowski, Rho signaling regulates pannexin 1-mediated ATP release from airway epithelia. J. Biol. Chem. 286, 26277-26286 (2011).
45. 2+ sensitization in rat arterial smooth muscle. J. Physiol. 590, 5401-5423 (2012).
46. 2+ sensitization of vascular smooth muscle contractility. Circ. Res. 109, 993-1002 (2011).
47. M. H. Tsai, M. J. Jiang, Rho-kinase-mediated regulation of receptor-agonist-stimulated smooth muscle contraction. Pflugers Arch. 453, 223-232 (2006).
48. K. Budzyn, M. Paull, P. D. Marley, C. G. Sobey, Segmental differences in the roles of rho-kinase and protein kinase C in mediating vasoconstriction. J. Pharmacol. Exp. Ther. 317, 791-796 (2006).
49. G. Loirand, V. Sauzeau, P. Pacaud, Small G proteins in the cardiovascular system: Physiological and pathological aspects. Physiol. Rev. 93, 1659-1720 (2013).
50. H. C. Boonen, J. G. De Mey, G-proteins are involved in contractile responses of isolated mesenteric resistance arteries to agonists. Naunyn Schmiedebergs Arch. Pharmacol. 342, 462-468 (1990).
51. B. J. Heesen, J. G. De Mey, Effects of cyclic AMP-affecting agents on contractile reactivity of isolated mesenteric and renal resistance arteries of the rat. Br. J. Pharmacol. 101, 859-864 (1990).
52. A. J. Karsten, H. Derouet, M. Ziegler, R. E. Eckert, Involvement of cyclic nucleotides in renal artery smooth muscle relaxation. Urol. Res. 30, 367-373 (2003).
53. iβγ/PI3K-dependent activation of the RacGEF TIAM-1 is required for a1-adrenoceptor induced hypertrophy in neonatal rat cardiomyocytes. J. Mol. Cell. Cardiol. 53, 165-175 (2012).
54. M. Billaud, A. W. Lohman, S. R. Johnstone, L. A. Biwer, S. Mutchler, B. E. Isakson, Regulation of cellular communication by signaling microdomains in the blood vessel wall. Pharmacol. Rev. 66, 513-569 (2014).
55. A. W. Moore, W. F. Jackson, S. S. Segal, Regional heterogeneity of α-adrenoreceptor subtypes in arteriolar networks of mouse skeletal muscle. J. Physiol. 588, 4261-4274 (2010).
56. F. A. Dinenno, J. H. Eisenach, N. M. Dietz, M. J. Joyner, Post-junctional α-adrenoceptors and basal limb vascular tone in healthy men. J. Physiol. 540, 1103-1110 (2002).
57. 2-adrenoceptors on microvascular smooth muscle during sympathetic nerve stimulation. Circ. Res. 68, 232-244 (1991).
58. S. Guimarães, D. Moura, Vascular adrenoceptors: An update. Pharmacol. Rev. 53, 319-356 (2001).
59. T. Katsuragi, S. Tamesue, C. Sato, Y. Sato, T. Furukawa, ATP release by angiotensin II from segments and cultured smooth muscle cells of guinea-pig taenia coli. Naunyn Schmiedebergs Arch. Pharmacol. 354, 796-799 (1996).
60. Y. Cheng, K. J. Mansfield, S. L. Sandow, P. Sadananda, E. Burcher, K. H. Moore, Porcine bladder urothelial, myofibroblast, and detrusor muscle cells: Characterization and ATP release. Front. Pharmacol. 2, 27 (2011).
61. E. F. Diezmos, S. L. Sandow, I. Markus, D. Shevy Perera, D. Z. Lubowski, D. W. King, P. P. Bertrand, L. Liu, Expression and localization of pannexin-1 hemichannels in human colon in health and disease. Neurogastroenterol. Motil. 25, e395-e405 (2013).
62. 6 receptors. Biochem. Pharmacol. 87, 371-379 (2014).
63. T. A. Edwards, A. J. Wilson, Helix-mediated protein-protein interactions as targets for intervention using foldamers. Amino Acids 41, 743-754 (2011).
64. V. Azzarito, K. Long, N. S. Murphy, A. J. Wilson, Inhibition of a-helix-mediated protein-protein interactions using designed molecules. Nat. Chem. 5, 161-173 (2013).
65. J. Wang, G. Dahl, SCAM analysis of Panx1 suggests a peculiar pore structure. J. Gen. Physiol. 136, 515-527 (2010).
66. B. K. Kay, M. P. Williamson, M. Sudol, The importance of being proline: The interaction of proline-rich motifs in signaling proteins with their cognate domains. FASEB J. 14, 231-241 (2000).
67. B. N. Giepmans, Gap junctions and connexin-interacting proteins. Cardiovasc. Res. 62, 233-245 (2004).
68. M. A. Riquelme, L. A. Cea, J. L. Vega, M. P. Boric, H. Monyer, M. V. Bennett, M. Frank, K. Willecke, J. C. Sáez, The ATP required for potentiation of skeletal muscle contraction is released via pannexin hemichannels. Neuropharmacology 75, 594-603 (2013).
69. T. P. Robertson, J. N. Moore, E. Noschka, T. H. Lewis, S. J. Lewis, J. F. Peroni, Effects of Rho-kinase and Src protein tyrosine kinase inhibition on agonist-induced vasoconstriction of arteries and veins of the equine laminar dermis. Am. J. Vet. Res. 68, 886-894 (2007).
70. X. X. Xiong, L. J. Gu, J. Shen, X. H. Kang, Y. Y. Zheng, S. B. Yue, S. M. Zhu, Probenecid protects against transient focal cerebral ischemic injury by inhibiting HMGB1 release and attenuating AQP4 expression in mice. Neurochem. Res. 39, 216-224 (2014).
71. S. J. Coker, A. J. Batey, I. D. Lightbown, M. E. Díaz, D. A. Eisner, Effects of mefloquine on cardiac contractility and electrical activity in vivo, in isolated cardiac preparations, and in single ventricular myocytes. Br. J. Pharmacol. 129, 323-330 (2000).
72. R. Iglesias, D. C. Spray, E. Scemes, Mefloquine blockade of Pannexin1 currents: Resolution of a conflict. Cell Commun. Adhes. 16, 131-137 (2009).
73. 13-LARG-mediated signaling in vascular smooth muscle is required for salt-induced hypertension. Nat. Med. 14, 64-68 (2008).
74. S. Cechova, Q. Zeng, M. Billaud, S. Mutchler, C. K. Rudy, A. C. Straub, L. Chi, F. R. Chan, J. Hu, R. Griffiths, N. L. Howell, K.Madsen, B. L. Jensen, L. A. Palmer, R. M. Carey, S. S. Sung, S. M. Malakauskas, B. E. Isakson, T. H. Le, Loss of collectrin, an angiotensin-converting enzyme 2 homolog, uncouples endothelial nitric oxide synthase and causes hypertension and vascular dysfunction. Circulation 128, 1770-1780 (2013).