Unified patch clamp protocol for the characterization of Pannexin 1 channels in isolated cells and acute brain slices

Journal of Neuroscience Methods

Volumn 199, Issue 1, 2011, Pages 15-25

  Gründken, Christina ^a   Hanske, Julian ^a   Wengel, Stephanie ^a   Reuter, Wiebke ^a   Abdulazim, Amr ^a   Shestopalov, Valery I ^c   Dermietzel, Rolf ^a   Zoidl, Georg ^b   Prochnow, Nora ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b YORK UNIVERSITY   (Canada)

^c UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

Hippocampus; N2a cells; Neuron; Pannexin 1; Tail current

Indexed keywords

BRAIN PROTEIN; PANNEXIN 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN SLICE; CELL ISOLATION; CONTROLLED STUDY; GENETIC TRANSFECTION; HIPPOCAMPUS; HISTOCHEMISTRY; IN VITRO STUDY; MEMBRANE CURRENT; MOUSE; NERVE CELL; NONHUMAN; PATCH CLAMP; POLARIZATION AND DEPOLARIZATION; PRIORITY JOURNAL; VOLTAGE CLAMP;

ADENOSINE TRIPHOSPHATE; ANIMALS; BACTERIAL PROTEINS; CA1 REGION, HIPPOCAMPAL; CATIONS; CELL LINE, TUMOR; CONNEXINS; ELECTRIC STIMULATION; FLUORESCENT DYES; ION CHANNEL GATING; LUMINESCENT PROTEINS; MEFLOQUINE; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, FLUORESCENCE; NERVE TISSUE PROTEINS; NEUROBLASTOMA; NEURONS; PATCH-CLAMP TECHNIQUES; RECOMBINANT FUSION PROTEINS; TRANSFECTION; ZEBRAFISH PROTEINS;

EID: 79958096495     PISSN: 01650270     EISSN: 1872678X     Source Type: Journal    
DOI: 10.1016/j.jneumeth.2011.04.016     Document Type: Article

References (49)

1. Aoki T., Baraban S.C. Properties of a calcium-activated K(+) current on interneurons in the developing rat hippocampus. J Neurophysiol 2000, 83:3453-3461.
2. Bao L., Locovei S., Dahl G. Pannexin membrane channels are mechanosensitive conduits for ATP. FEBS Lett 2004, 572:65-68.
3. Baranova A., Ivanov D., Petrash N., Pestova A., Skoblov M., Kelmanson I., et al. The mammalian pannexin family is homologous to the invertebrate innexin gap junction proteins. Genomics 2004, 83:706-716.
4. Bargiotas P., Monyer H., Schwaninger M. Hemichannels in cerebral ischemia. Curr Mol Med 2009, 9:186-194.
5. Boassa D., Qiu F., Dahl G., Sosinsky G. Trafficking dynamics of glycosylated pannexin 1 proteins. Cell Commun Adhes 2008, 15:119-132.
6. Bruzzone R., Barbe M.T., Jakob N.J., Monyer H. Pharmacological properties of homomeric and heteromeric pannexin hemichannels expressed in Xenopus oocytes. J Neurochem 2005, 92:1033-1043.
7. Bruzzone R., Hormuzdi S.G., Barbe M.T., Herb A., Monyer H. Pannexins, a family of gap junction proteins expressed in brain. Proc Natl Acad Sci USA 2003, 100:13644-13649.
8. Bunse S., Locovei S., Schmidt M., Qiu F., Zoidl G., Dahl G., et al. The potassium channel subunit Kvbeta3 interacts with pannexin 1 and attenuates its sensitivity to changes in redox potentials. FEBS J 2009, 276:6258-6270.
9. Bunse S., Schmidt M., Prochnow N., Zoidl G., Dermietzel R. Intracellular cysteine C346 is essentially involved in regulating PANX1 channel activity. J Biol Chem 2010.
10. D'Hondt C., Ponsaerts R., De Smedt H., Bultynck G., Himpens B. Pannexins, distant relatives of the connexin family with specific cellular functions?. Bioessays 2009, 31:953-974.
11. Hodgkin A.L., Huxley A.F. The dual effect of membrane potential on sodium conductance in the giant axon of Loligo. J Physiol 1952, 116:497-506.
12. Huang Y., Grinspan J.B., Abrams C.K., Scherer S.S. Pannexin1 is expressed by neurons and glia but does not form functional gap junctions. Glia 2007, 55:46-56.
13. Iglesias R., Spray D.C., Scemes E. Mefloquine blockade of Pannexin1 currents: resolution of a conflict. Cell Commun Adhes 2009, 16:131-137.
14. Kamermans M., Fahrenfort I., Schultz K., Janssen-Bienhold U., Sjoerdsma T., Weiler R. Hemichannel-mediated inhibition in the outer retina. Science 2001, 292:1178-1180.
15. Kienitz M.C., Bender K., Dermietzel R., Pott L., Zoidl G. Pannexin 1 constitutes the large-conductance cation channel of cardiac myocytes. J Biol Chem 2011, 286:290-298.
16. Li H., Liu T.F., Lazrak A., Peracchia C., Goldberg G.S., Lampe P.D., et al. Properties and regulation of gap junctional hemichannels in the plasma membranes of cultured cells. J Cell Biol 1996, 134:1019-1030.
17. Locovei S., Bao L., Dahl G. Pannexin 1 in erythrocytes: function without a gap. Proc Natl Acad Sci USA 2006, 103:7655-7659.
18. Locovei S., Wang J., Dahl G. Activation of pannexin 1 channels by ATP through P2Y receptors and by cytoplasmic calcium. FEBS Lett 2006, 580:239-244.
19. Luthi A., Gahwiler B.H., Gerber U. 1S, 3R-ACPD induces a region of negative slope conductance in the steady-state current-voltage relationship of hippocampal pyramidal cells. J Neurophysiol 1997, 77:221-228.
20. Ma W., Hui H., Pelegrin P., Surprenant A. Pharmacological characterization of pannexin-1 currents expressed in mammalian cells. J Pharmacol Exp Ther 2009, 328:409-418.
21. MacVicar B.A., Thompson R.J. Non-junction functions of pannexin-1 channels. Trends Neurosci 2009, 33:93-102.
22. Martin E.D., Buno W. Caffeine-mediated presynaptic long-term potentiation in hippocampal CA1 pyramidal neurons. J Neurophysiol 2003, 89:3029-3038.
23. Muller D.J., Hand G.M., Engel A., Sosinsky G.E. Conformational changes in surface structures of isolated connexin 26 gap junctions. EMBO J 2002, 21:3598-3607.
24. Mylvaganam S., Zhang L., Wu C., Zhang Z.J., Samoilova M., Eubanks J., et al. Hippocampal seizures alter the expression of the pannexin and connexin transcriptome. J Neurochem 2010, 112:92-102.
25. Pelegrin P., Surprenant A. Pannexin-1 mediates large pore formation and interleukin-1beta release by the ATP-gated P2X7 receptor. EMBO J 2006, 25:5071-5082.
26. Penuela S., Bhalla R., Gong X.Q., Cowan K.N., Celetti S.J., Cowan B.J., et al. Pannexin 1 and pannexin 3 are glycoproteins that exhibit many distinct characteristics from the connexin family of gap junction proteins. J Cell Sci 2007, 120:3772-3783.
27. Penuela S., Bhalla R., Nag K., Laird D.W. Glycosylation regulates pannexin intermixing and cellular localization. Mol Biol Cell 2009, 20:4313-4323.
28. Pfahnl A., Dahl G. Gating of cx46 gap junction hemichannels by calcium and voltage. Pflugers Arch 1999, 437:345-353.
29. Prochnow N., Hoffmann S., Dermietzel R., Zoidl G. Replacement of a single cysteine in the fourth transmembrane region of zebrafish pannexin1 alters hemichannel gating behavior. Exp Brain Res 2009.
30. Prochnow N., Hoffmann S., Vroman R., Klooster J., Bunse S., Kamermans M., et al. Pannexin1 in the outer retina of the zebrafish, Danio rerio. Neuroscience 2009, 162:1039-1054.
31. Qiu F., Dahl G. A permeant regulating its permeation pore: inhibition of pannexin 1 channels by ATP. Am J Physiol Cell Physiol 2009, 296:C250-C255.
32. Quist A.P., Rhee S.K., Lin H., Lal R. Physiological role of gap-junctional hemichannels. Extracellular calcium-dependent isosmotic volume regulation. J Cell Biol 2000, 148:1063-1074.
33. Ray A., Zoidl G., Wahle P., Dermietzel R. Pannexin expression in the cerebellum. Cerebellum 2006, 5:189-192.
34. Ray A., Zoidl G., Weickert S., Wahle P., Dermietzel R. Site-specific and developmental expression of pannexin1 in the mouse nervous system. Eur J Neurosci 2005, 21:3277-3290.
35. Romanov R.A., Rogachevskaja O.A., Khokhlov A.A., Kolesnikov S.S. Voltage dependence of ATP secretion in mammalian taste cells. J Gen Physiol 2008, 132:731-744.
36. Shestopalov V.I., Panchin Y. Pannexins and gap junction protein diversity. Cell Mol Life Sci 2008, 65:376-394.
37. Srinivas M., Calderon D.P., Kronengold J., Verselis V.K. Regulation of connexin hemichannels by monovalent cations. J Gen Physiol 2006, 127:67-75.
38. Stout C., Charles A. Modulation of intercellular calcium signaling in astrocytes by extracellular calcium and magnesium. Glia 2003, 43:265-273.
39. Thimm J., Mechler A., Lin H., Rhee S., Lal R. Calcium-dependent open/closed conformations and interfacial energy maps of reconstituted hemichannels. J Biol Chem 2005, 280:10646-10654.
40. Thompson R.J., Jackson M.F., Olah M.E., Rungta R.L., Hines D.J., Beazely M.A., et al. Activation of pannexin-1 hemichannels augments aberrant bursting in the hippocampus. Science 2008, 322:1555-1559.
41. Thompson R.J., Zhou N., MacVicar B.A. Ischemia opens neuronal gap junction hemichannels. Science 2006, 312:924-927.
42. Trexler E.B., Bennett M.V., Bargiello T.A., Verselis V.K. Voltage gating and permeation in a gap junction hemichannel. Proc Natl Acad Sci USA 1996, 93:5836-5841.
43. Vanden Abeele F., Zholos A., Bidaux G., Shuba Y., Thebault S., Beck B., et al. Ca2+-independent phospholipase A2-dependent gating of TRPM8 by lysophospholipids. J Biol Chem 2006, 281:40174-40182.
44. Vogt A., Hormuzdi S.G., Monyer H. Pannexin1 and Pannexin2 expression in the developing and mature rat brain. Brain Res Mol Brain Res 2005, 141:113-120.
45. Wang J., Ma M., Locovei S., Keane R.W., Dahl G. Modulation of membrane channel currents by gap junction protein mimetic peptides: size matters. Am J Physiol Cell Physiol 2007, 293:C1112-C1119.
46. Ye Z.C., Wyeth M.S., Baltan-Tekkok S., Ransom B.R. Functional hemichannels in astrocytes: a novel mechanism of glutamate release. J Neurosci 2003, 23:3588-3596.
47. Yen M.R., Saier M.H. Gap junctional proteins of animals: the innexin/pannexin superfamily. Prog Biophys Mol Biol 2007, 94:5-14.
48. Zhang L., Deng T., Sun Y., Liu K., Yang Y., Zheng X. Role for nitric oxide in permeability of hippocampal neuronal hemichannels during oxygen glucose deprivation. J Neurosci Res 2008, 86:2281-2291.
49. Zoidl G., Petrasch-Parwez E., Ray A., Meier C., Bunse S., Habbes H.W., et al. Localization of the pannexin1 protein at postsynaptic sites in the cerebral cortex and hippocampus. Neuroscience 2007, 146:9-16.