S-nitrosylation inhibits pannexin 1 channel function

Journal of Biological Chemistry

Volumn 287, Issue 47, 2012, Pages 39602-39612

  Lohman, Alexander W ^a   Weaver, Janelle L ^a   Billaud, Marie ^a   Sandilos, Joanna K ^a   Griffiths, Rachael ^a   Straub, Adam C ^a   Penuela, Silvia ^b   Leitinger, Norbert ^a   Laird, Dale W ^b   Bayliss, Douglas A ^a   Isakson, Brant E ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CHANNEL ACTIVITY; CHANNEL CURRENTS; CHANNEL FUNCTIONS; CYSTEINE RESIDUES; DITHIOTHREITOL; GUANYLATE CYCLASE; HUMAN EMBRYONIC KIDNEYS; NO DONOR; POST-TRANSLATIONAL MODIFICATIONS; PROTEIN FUNCTIONS; S-NITROSOGLUTATHIONE; S-NITROSYLATION; VASCULATURE; WILD TYPES;

ENDOTHELIAL CELLS; NITRIC OXIDE; TISSUE;

AMINO ACIDS;

1H [1,2,4]OXADIAZOLO[4,3 A]QUINAZOLIN 1 ONE; ADENOSINE TRIPHOSPHATE; ALANINE; AMMONIUM DERIVATIVE; BIOTIN; CYSTEINE; DIETHYLAMMONIUM 1 1(N,N DIETHYLAMINO)DIAZEN 1 IUM 1,2 DIOLATE; DITHIOTHREITOL; GUANYLATE CYCLASE; MEMBRANE PROTEIN; PANNEXIN 1; QUINAZOLINONE DERIVATIVE; S NITROSOGLUTATHIONE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTERY ENDOTHELIUM; ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME INHIBITION; GENE MUTATION; HUMAN; HUMAN CELL; INHIBITION KINETICS; ION CURRENT; MOUSE; NITROSYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; WILD TYPE;

ADENOSINE TRIPHOSPHATE; AMINO ACID SUBSTITUTION; ANIMALS; CONNEXINS; DITHIOTHREITOL; GLUTATHIONE; HEK293 CELLS; HUMANS; MICE; MUTATION; MUTATION, MISSENSE; NERVE TISSUE PROTEINS; NITRIC OXIDE; NITRIC OXIDE DONORS; NITRO COMPOUNDS; OXADIAZOLES; OXIDATION-REDUCTION; QUATERNARY AMMONIUM COMPOUNDS; QUINOXALINES;

EID: 84869234325     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.397976     Document Type: Article

References (43)

1. Ambrosi, C., Gassmann, O., Pranskevich, J. N., Boassa, D., Smock, A., Wang, J., Dahl, G., Steinem, C., and Sosinsky, G. E. (2010) Pannexin1 and Pannexin2 channels show quaternary similarities to connexons and different oligomerization numbers from each other. J. Biol. Chem. 285, 24420-24431
2. Dando, R., and Roper, S. D. (2009) Cell-to-cell communication in intact taste buds through ATP signalling from pannexin 1 gap junction hemichannels. J. Physiol. 587, 5899-5906
3. Reigada, D., Lu, W., Zhang, M., and Mitchell, C. H. (2008) Elevated pressure triggers a physiological release of ATP from the retina: possible role for pannexin hemichannels. Neuroscience 157, 396-404
4. Li, S., Bjelobaba, I., Yan, Z., Kucka, M., Tomic, M., and Stojilkovic, S. S. (2011) Expression and roles of pannexins in ATP release in the pituitary gland. Endocrinology 152, 2342-2352
5. Iwabuchi, S., and Kawahara, K. (2011) Functional significance of the negative-feedback regulation of ATP release via pannexin-1 hemichannels under ischemic stress in astrocytes. Neurochem. Int. 58, 376-384
6. Woehrle, T., Yip, L., Manohar, M., Sumi, Y., Yao, Y., Chen, Y., and Junger, W. G. (2010) Hypertonic stress regulates T cell function via pannexin-1 hemichannels and P2X receptors. J. Leukoc. Biol. 88, 1181-1189
7. Billaud, M., Lohman, A. W., Straub, A. C., Looft-Wilson, R., Johnstone, S. R., Araj, C. A., Best, A. K., Chekeni, F. B., Ravichandran, K. S., Penuela, S., Laird, D. W., and Isakson, B. E. (2011) Pannexin1 regulates α1-adrenergic receptor-mediated vasoconstriction. Circ. Res. 109, 80-85
8. Woehrle, T., Yip, L., Elkhal, A., Sumi, Y., Chen, Y., Yao, Y., Insel, P. A., and Junger, W. G. (2010) Pannexin-1 hemichannel-mediated ATP release together with P2X1 and P2X4 receptors regulate T-cell activation at the immune synapse. Blood 116, 3475-3484
9. Chekeni, F. B., Elliott, M. R., Sandilos, J. K., Walk, S. F., Kinchen, J. M., Lazarowski, E. R., Armstrong, A. J., Penuela, S., Laird, D. W., Salvesen, G. S., Isakson, B. E., Bayliss, D. A., and Ravichandran, K. S. (2010) Pannexin 1 channels mediate 'find-me' signal release and membrane permeability during apoptosis. Nature 467, 863-867
10. Ransford, G. A., Fregien, N., Qiu, F., Dahl, G., Conner, G. E., and Salathe, M. (2009) Pannexin 1 contributes to ATP release in airway epithelia. Am. J. Respir. Cell Mol. Biol. 41, 525-534
11. Sridharan, M., Adderley, S. P., Bowles, E. A., Egan, T. M., Stephenson, A. H., Ellsworth, M. L., and Sprague, R. S. (2011) Pannexin 1 is the conduit for low oxygen tension-induced ATP release from human erythrocytes. Am. J. Physiol. Heart Circ. Physiol. 299, H1146-H1152
12. Schenk, U., Westendorf, A. M., Radaelli, E., Casati, A., Ferro, M., Fumagalli, M., Verderio, C., Buer, J., Scanziani, E., and Grassi, F. (2008) Purinergic control of T cell activation by ATP released through pannexin-1 hemichannels. Sci. Signal. 1, ra6
13. Seminario-Vidal, L., Okada, S. F., Sesma, J. I., Kreda, S. M., van Heusden, C. A., Zhu, Y., Jones, L. C., O'Neal, W. K., Penuela, S., Laird, D. W., Boucher, R. C., and Lazarowski, E. R. (2011) Rho signaling regulates pannexin 1-mediated ATP release from airway epithelia. J. Biol. Chem. 286, 26277-26286
14. Gödecke, S., Roderigo, C., Rose, C. R., Rauch, B. H., Gödecke, A., and Schrader, J. (2012) Thrombin-induced ATP release from human umbilical vein endothelial cells. Am. J. Physiol. Cell Physiol. 302, C915-C923
15. Locovei, S., Bao, L., and Dahl, G. (2006) Pannexin 1 in erythrocytes: function without a gap. Proc. Natl. Acad. Sci. U.S.A. 103, 7655-7659
16. Silverman, W. R., de Rivero Vaccari, J. P., Locovei, S., Qiu, F., Carlsson, S. K., Scemes, E., Keane, R. W., and Dahl, G. (2009) The pannexin 1 channel activates the inflammasome in neurons and astrocytes. J. Biol. Chem. 284, 18143-18151
17. Iglesias, R., Dahl, G., Qiu, F., Spray, D. C., and Scemes, E. (2009) Pannexin 1: the molecular substrate of astrocyte "hemichannels." J. Neurosci. 29, 7092-7097
18. Lohman, A. W., Billaud, M., and Isakson, B. E. (2012) Mechanisms of ATP release and signalling in the blood vessel wall. Cardiovasc. Res. 95, 269-280
19. Burnstock, G. (2002) Purinergic signaling and vascular cell proliferation and death. Arterioscler. Thromb. Vasc. Biol. 22, 364-373
20. Rumjahn, S. M., Yokdang, N., Baldwin, K. A., Thai, J., and Buxton, I. L. (2009) Purinergic regulation of vascular endothelial growth factor signaling in angiogenesis. Br. J. Cancer 100, 1465-1470
21. Burnstock, G., and Ulrich, H. (2011) Purinergic signaling in embryonic and stem cell development. Cell. Mol. Life Sci. 68, 1369-1394
22. Burnstock, G. (2011) Purinergic signaling in the gastrointestinal tract. World J. Gastrointest. Pathophysiol. 2, 31-34
23. Bao, L., Locovei, S., and Dahl, G. (2004) Pannexin membrane channels are mechanosensitive conduits for ATP. FEBS Lett. 572, 65-68 (Pubitemid 39092514)
24. Weilinger, N. L., Tang, P. L., and Thompson, R. J. (2012) Anoxia-induced NMDA receptor activation opens pannexin channels via Src family kinases. J. Neurosci. 32, 12579-12588
25. Sandilos, J. K., Chiu, Y. H., Chekeni, F. B., Armstrong, A. J., Walk, S. F., Ravichandran, K. S., and Bayliss, D. A. (2012) 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
26. Penuela, S., Bhalla, R., Nag, K., and Laird, D. W. (2009) Glycosylation regulates pannexin intermixing and cellular localization. Mol. Biol. Cell 20, 4313-4323
27. Boassa, D., Ambrosi, C., Qiu, F., Dahl, G., Gaietta, G., and Sosinsky, G. (2007) Pannexin1 channels contain a glycosylation site that targets the hexamer to the plasma membrane. J. Biol. Chem. 282, 31733-31743 (Pubitemid 350044851)
28. Straub, A. C., Billaud, M., Johnstone, S. R., Best, A. K., Yemen, S., Dwyer, S. T., Looft-Wilson, R., Lysiak, J. J., Gaston, B., Palmer, L., and Isakson, B. E. (2011) Compartmentalized connexin 43 S-nitrosylation/ denitrosylation regulates heterocellular communication in the vessel wall. Arterioscler. Thromb. Vasc. Biol. 31, 399-407
29. Sun, J., Xin, C., Eu, J. P., Stamler, J. S., and Meissner, G. (2001) Cysteine-3635 is responsible for skeletal muscle ryanodine receptor modulation by NO. Proc. Natl. Acad. Sci. U.S.A. 98, 11158-11162 (Pubitemid 32928699)
30. Retamal, M. A., Cortés, C. J., Reuss, L., Bennett, M. V., and Sáez, J. C. (2006) S-Nitrosylation and permeation through connexin 43 hemichannels in astrocytes: induction by oxidant stress and reversal by reducing agents. Proc. Natl. Acad. Sci. U.S.A. 103, 4475-4480
31. Asada, K., Kurokawa, J., and Furukawa, T. (2009) Redox- and calmodulin-dependent S-nitrosylation of the KCNQ1 channel. J. Biol. Chem. 284, 6014-6020
32. Yoshida, T., Inoue, R., Morii, T., Takahashi, N., Yamamoto, S., Hara, Y., Tominaga, M., Shimizu, S., Sato, Y., and Mori, Y. (2006) Nitric oxide activates TRP channels by cysteine S-nitrosylation. Nat. Chem. Biol. 2, 596-607 (Pubitemid 44610344)
33. Penuela, S., Bhalla, R., Gong, X. Q., Cowan, K. N., Celetti, S. J., Cowan, B. J., Bai, D., Shao, Q., and Laird, D. W. (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, 3772-3783 (Pubitemid 350187359)
34. Jaffrey, S. R., and Snyder, S. H. (2001) The biotin switch method for the detection of S-nitrosylated proteins. Sci. STKE 2001, pl1
35. Lohman, A. W., Billaud, M., Straub, A. C., Johnstone, S. R., Best, A. K., Lee, M., Barr, K., Penuela, S., Laird, D. W., and Isakson, B. E. (2012) Expression of pannexin isoforms in the systemic murine arterial network. J. Vasc. Res. 49, 405-416
36. Schwartz, D., Chou, M. F., and Church, G. M. (2009) Predicting protein post-translational modifications using meta-analysis of proteome scale data sets. Mol. Cell. Proteomics 8, 365-379
37. Zhang, L., Deng, T., Sun, Y., Liu, K., Yang, Y., and Zheng, X. (2008) Role for nitric oxide in permeability of hippocampal neuronal hemichannels during oxygen glucose deprivation. J. Neurosci. Res. 86, 2281-2291
38. Swayne, L. A., Sorbara, C. D., and Bennett, S. A. (2010) Pannexin 2 is expressed by postnatal hippocampal neural progenitors and modulates neuronal commitment. J. Biol. Chem. 285, 24977-24986
39. Ray, A., Zoidl, G., Wahle, P., and Dermietzel, R. (2006) Pannexin expression in the cerebellum. Cerebellum 5, 189-192 (Pubitemid 44451609)
40. Bunse, S., Schmidt, M., Prochnow, N., Zoidl, G., and Dermietzel, R. (2010) Intracellular cysteine 346 is essentially involved in regulating Panx1 channel activity. J. Biol. Chem. 285, 38444-38452
41. Bunse, S., Schmidt, M., Hoffmann, S., Engelhardt, K., Zoidl, G., and Dermietzel, R. (2011) Single cysteines in the extracellular and transmembrane regions modulate pannexin 1 channel function. J. Membr. Biol. 244, 21-33
42. Ellsworth, M. L., Ellis, C. G., Goldman, D., Stephenson, A. H., Dietrich, H. H., and Sprague, R. S. (2009) Erythrocytes: oxygen sensors and modulators of vascular tone. Physiology 24, 107-116
43. Wang, J., and Dahl, G. (2010) SCAM analysis of Panx1 suggests a peculiar pore structure. J. Gen. Physiol. 136, 515-527