Extracellular osmolarity modulates G protein-coupled receptor-dependent ATP release from 1321N1 astrocytoma cells

American Journal of Physiology - Cell Physiology

Volumn 298, Issue 2, 2010, Pages

  Blum, Andrew E ^a   Walsh, B Corbett ^a   Dubyak, George R ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Astrocyte; Hypotonic stress; Volume regulated anion channels; Volume sensitive organic osmolyte and anion channels

Indexed keywords

ADENOSINE TRIPHOSPHATE; G PROTEIN COUPLED RECEPTOR; PROBENECID; PROTEINASE ACTIVATED RECEPTOR 1; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; THROMBIN; 1,2 BIS(2 AMINOPHENOXY)ETHANE N,N,N',N' TETRAACETIC ACID ACETOXYMETHYL ESTER; 1,2-BIS(2-AMINOPHENOXY)ETHANE N,N,N',N'-TETRAACETIC ACID ACETOXYMETHYL ESTER; 1,9 DIDEOXYFORSKOLIN; 1,9-DIDEOXYFORSKOLIN; ANION; CARBENOXOLONE; CHELATING AGENT; DRUG DERIVATIVE; EGTAZIC ACID; FORSKOLIN; HYPERTONIC SOLUTION; HYPOTONIC SOLUTION; ION CHANNEL; TETANUS TOXIN;

ARTICLE; ASTROCYTOMA CELL; CALCIUM MOBILIZATION; HUMAN; HUMAN CELL; HYPOOSMOTIC STRESS; OSMOLARITY; PRIORITY JOURNAL; ASTROCYTOMA; CALCIUM SIGNALING; DOSE RESPONSE; DRUG EFFECT; ENZYME ACTIVATION; EXTRACELLULAR FLUID; KINETICS; METABOLISM; TUMOR CELL LINE;

ADENOSINE TRIPHOSPHATE; ANIONS; ASTROCYTOMA; CALCIUM SIGNALING; CARBENOXOLONE; CELL LINE, TUMOR; CHELATING AGENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; EGTAZIC ACID; ENZYME ACTIVATION; EXTRACELLULAR FLUID; FORSKOLIN; HUMANS; HYPERTONIC SOLUTIONS; HYPOTONIC SOLUTIONS; ION CHANNELS; KINETICS; OSMOLAR CONCENTRATION; PROBENECID; RECEPTOR, PAR-1; RHO GTP-BINDING PROTEINS; TETANUS TOXIN; THROMBIN;

EID: 75749101826     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00430.2009     Document Type: Article

References (75)

1. - currents in cultured rat astrocytes. J Physiol 572: 677-689, 2006.
2. Bader P, Weingart R. Pitfalls when examining gap junction hemichannels: interference from volume-regulated anion channels. Pflügers Arch 452: 396-406, 2006.
3. Bao L, Locovei S, Dahl G. Pannexin membrane channels are mechano-sensitive conduits for ATP. FEBS Lett 572: 65-68, 2004.
4. Bao L, Sachs F, Dahl G. Connexins are mechanosensitive. Am J Physiol Cell Physiol 287: C1389-C1395, 2004.
5. Bender AS, Neary JT, Norenberg MD. Role of phosphoinositide hydrolysis in astrocyte volume regulation. J Neurochem 61: 1506-1514, 1993.
6. Benfenati V, Caprini M, Nicchia GP, Rossi A, Dovizio M, Cervetto C, Nobile M, Ferroni S. Carbenoxolone inhibits volume-regulated anion conductance in cultured rat cortical astroglia. Channels (Austin) 3: 323-336, 2009.
7. 2+-dependent ATP release from astrocytes. Am J Physiol Cell Physiol 295: C231-C241, 2008.
8. Bruzzone R, Barbe MT, Jakob NJ, Monyer H. Pharmacological properties of homomeric and heteromeric pannexin hemichannels expressed in Xenopus oocytes. J Neurochem 92: 1033-1043, 2005.
9. Bunse S, Locovei S, Schmidt M, Qiu F, Zoidl G, Dahl G, Dermietzel R. The potassium channel subunit Kvbeta3 interacts with pannexin 1 and attenuates its sensitivity to changes in redox potentials. FEBS J 276: 6258-6270, 2009.
10. Burnstock G. Purine and pyrimidine receptors. Cell Mol Life Sci 64: 1471-1483, 2007.
11. Cheema TA, Pettigrew VA, Fisher SK. Receptor regulation of the volume-sensitive efflux of taurine and iodide from human SH-SY5Y neuroblastoma cells: differential requirements for Ca(2+) and protein kinase C. J Pharmacol Exp Ther 320: 1068-1077, 2007.
12. Cheema TA, Ward CE, Fisher SK. Subnanomolar concentrations of thrombin enhance the volume-sensitive efflux of taurine from human 1321N1 astrocytoma cells. J Pharmacol Exp Ther 315: 755-763, 2005.
13. Clarke LL, Boucher RC. Chloride secretory response to extracellular ATP in human normal and cystic fibrosis nasal epithelia. Am J Physiol Cell Physiol 263: C348-C356, 1992.
14. Cotrina ML, Lin JH, Alves-Rodrigues A, Liu S, Li J, Azmi-Ghadimi H, Kang J, Naus CC, Nedergaard M. Connexins regulate calcium signaling by controlling ATP release. Proc Natl Acad Sci USA 95: 15735-15740, 1998.
15. Dahl G, Locovei S. Pannexin: to gap or not to gap, is that a question? IUBMB Life 58: 409-419, 2006.
16. Darby M, Kuzmiski JB, Panenka W, Feighan D, MacVicar BA. ATP released from astrocytes during swelling activates chloride channels. J Neurophysiol 89: 1870-1877, 2003.
17. Diller KR, Zhu L. Hypothermia therapy for brain injury. Annu Rev Biomed Eng 11: 135-162, 2009.
18. Droogmans G, Maertens C, Prenen J, Nilius B. Sulphonic acid derivatives as probes of pore properties of volume-regulated anion channels in endothelial cells. Br J Pharmacol 128: 35-40, 1999.
19. Dutta AK, Sabirov RZ, Uramoto H, Okada Y. Role of ATP-conductive anion channel in ATP release from neonatal rat cardiomyocytes in ischaemic or hypoxic conditions. J Physiol 559: 799-812, 2004.
20. Eskandari S, Zampighi GA, Leung DW, Wright EM, Loo DD. Inhibition of gap junction hemichannels by chloride channel blockers. J Membr Biol 185: 93-102, 2002.
21. Franco R, Panayiotidis MI, de la Paz LD. Autocrine signaling involved in cell volume regulation: the role of released transmitters and plasma membrane receptors. J Cell Physiol 216: 14-28, 2008.
22. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 260: 3440-3450, 1985.
23. Halassa MM, Fellin T, Haydon PG. Tripartite synapses: roles for astrocytic purines in the control of synaptic physiology and behavior. Neuropharmacology 57: 343-346, 2009.
24. Heacock AM, Kerley D, Gurda GT, VanTroostenberghe AT, Fisher SK. Potentiation of the osmosensitive release of taurine and D-aspartate from SH-SY5Y neuroblastoma cells after activation of M3 muscarinic cholinergic receptors. J Pharmacol Exp Ther 311: 1097-1104, 2004.
25. Hisadome K, Koyama T, Kimura C, Droogmans G, Ito Y, Oike M. Volume-regulated anion channels serve as an auto/paracrine nucleotide release pathway in aortic endothelial cells. J Gen Physiol 119: 511-520, 2002.
26. Hoffmann EK, Lambert IH, Pedersen SF. Physiology of cell volume regulation in vertebrates. Physiol Rev 89: 193-277, 2009.
27. Iglesias R, Dahl G, Qiu F, Spray DC, Scemes E. Pannexin 1: the molecular substrate of astrocyte "hemichannels". J Neurosci 29: 7092-7097, 2009.
28. Joseph SM, Buchakjian MR, Dubyak GR. Colocalization of ATP release sites and ecto-ATPase activity at the extracellular surface of human astrocytes. J Biol Chem 278: 23331-23342, 2003.
29. Kang J, Kang N, Lovatt D, Torres A, Zhao Z, Lin J, Nedergaard M. Connexin 43 hemichannels are permeable to ATP. J Neurosci 28: 4702-4711, 2008.
30. Klausen TK, Hougaard C, Hoffmann EK, Pedersen SF. Cholesterol modulates the volume-regulated anion current in Ehrlich-Lettre ascites cells via effects on Rho and F-actin. Am J Physiol Cell Physiol 291: C757-C771, 2006.
31. Koyama T, Oike M, Ito Y. Involvement of Rho-kinase and tyrosine kinase in hypotonic stress-induced ATP release in bovine aortic endothelial cells. J Physiol 532: 759-769, 2001.
32. Lazarowski ER, Boucher RC, Harden TK. Mechanisms of release of nucleotides and integration of their action as P2X- and P2Y-receptor activating molecules. Mol Pharmacol 64: 785-795, 2003.
33. Lee YK, Kim HL, Kim YL, Im DS. Multiple actions of dimethylsphingosine in 1321N1 astrocytes. Mol Cells 23: 11-16, 2007.
34. Li G, Olson JE. Extracellular ATP activates chloride and taurine conductances in cultured hippocampal neurons. Neurochem Res 29: 239-246, 2004.
35. Li G, Olson JE. Purinergic activation of anion conductance and osmolyte efflux in cultured rat hippocampal neurons. Am J Physiol Cell Physiol 295: C1550-C1560, 2008.
36. Lin JH, Lou N, Kang N, Takano T, Hu F, Han X, Xu Q, Lovatt D, Torres A, Willecke K, Yang J, Kang J, Nedergaard M. A central role of connexin 43 in hypoxic preconditioning. J Neurosci 28: 681-695, 2008.
37. Liu HT, Akita T, Shimizu T, Sabirov RZ, Okada Y. Bradykinin-induced astrocyte-neuron signalling: glutamate release is mediated by ROS-activated volume-sensitive outwardly rectifying anion channels. J Physiol 587: 2197-2209, 2009.
38. Liu HT, Sabirov RZ, Okada Y. Oxygen-glucose deprivation induces ATP release via maxi-anion channels in astrocytes. Purinergic Signal 4: 147-154, 2008.
39. Liu HT, Toychiev AH, Takahashi N, Sabirov RZ, Okada Y. Maxianion channel as a candidate pathway for osmosensitive ATP release from mouse astrocytes in primary culture. Cell Res 18: 558-565, 2008.
40. Locovei S, Bao L, Dahl G. Pannexin 1 in erythrocytes: function without a gap. Proc Natl Acad Sci USA 103: 7655-7659, 2006.
41. Locovei S, Wang J, Dahl G. Activation of pannexin 1 channels by ATP through P2Y receptors and by cytoplasmic calcium. FEBS Lett 580: 239-244, 2006.
42. Ma W, Hui H, Pelegrin P, Surprenant A. Pharmacological characterization of pannexin-1 currents expressed in mammalian cells. J Pharmacol Exp Ther 328: 409-418, 2009.
43. Mall M, Wissner A, Gonska T, Calenborn D, Kuehr J, Brandis M, Kunzelmann K. Inhibition of amiloride-sensitive epithelial Na(+) absorption by extracellular nucleotides in human normal and cystic fibrosis airways. Am J Respir Cell Mol Biol 23: 755-761, 2000.
44. Mongin AA, Kimelberg HK. ATP potently modulates anion channel-mediated excitatory amino acid release from cultured astrocytes. Am J Physiol Cell Physiol 283: C569-C578, 2002.
45. 2+-sensitive mechanisms. Am J Physiol Cell Physiol 288: C204-C213, 2005.
46. Nilius B, Droogmans G. Amazing chloride channels: an overview. Acta Physiol Scand 177: 119-147, 2003.
47. - current by hypotonic volume increase in human endothelial cells. J Gen Physiol 103: 787-805, 1994.
48. Okada SF, Nicholas RA, Kreda SM, Lazarowski ER, Boucher RC. Physiological regulation of ATP release at the apical surface of human airway epithelia. J Biol Chem 281: 22992-23002, 2006.
49. Okada Y, Sato K, Numata T. Pathophysiology and puzzles of the volume-sensitive outwardly rectifying anion channel. J Physiol 587: 2141-2149, 2009.
50. Parr CE, Sullivan DM, Paradiso AM, Lazarowski ER, Burch LH, Olsen JC, Erb L, Weisman GA, Boucher RC, Turner JT. Cloning and expression of a human P2U nucleotide receptor, a target for cystic fibrosis pharmacotherapy. Proc Natl Acad Sci USA 91: 13067, 1994.
51. Pelegrin P, Surprenant A. Pannexin-1 mediates large pore formation and interleukin-1beta release by the ATP-gated P2X7 receptor. EMBO J 25: 5071-5082, 2006.
52. Post GR, Collins LR, Kennedy ED, Moskowitz SA, Aragay AM, Goldstein D, Brown JH. Coupling of the thrombin receptor to G12 may account for selective effects of thrombin on gene expression and DNA synthesis in 1321N1 astrocytoma cells. Mol Biol Cell 7: 1679-1690, 1996.
53. Ramos-Mandujano G, Vazquez-Juarez E, Hernandez-Benitez R, Pasantes-Morales H. Thrombin potently enhances swelling-sensitive glutamate efflux from cultured astrocytes. Glia 55: 917-925, 2007.
54. Ransford GA, Fregien N, Qiu F, Dahl G, Conner GE, Salathe M. Pannexin 1 contributes to ATP release in airway epithelia. Am J Respir Cell Mol Biol 41: 525-534, 2009.
55. Reyes JP, Hernandez-Carballo CY, Perez-Flores G, Perez-Cornejo P, Arreola J. Lack of coupling between membrane stretching and pannexin-1 hemichannels. Biochem Biophys Res Commun 380: 50-53, 2009.
56. Romanov RA, Rogachevskaja OA, Bystrova MF, Jiang P, Margolskee RF, Kolesnikov SS. Afferent neurotransmission mediated by hemichannels in mammalian taste cells. EMBO J 26: 657-667, 2007.
57. Rudkouskaya A, Chernoguz A, Haskew-Layton RE, Mongin AA. Two conventional protein kinase C isoforms, alpha and betaI, are involved in the ATP-induced activation of volume-regulated anion channel and glutamate release in cultured astrocytes. J Neurochem 105: 2260-2270, 2008.
58. Sabirov RZ, Dutta AK, Okada Y. Volume-dependent ATP-conductive large-conductance anion channel as a pathway for swelling-induced ATP release. J Gen Physiol 118: 251-266, 2001.
59. Sabirov RZ, Okada Y. ATP release via anion channels. Purinergic Signal 1: 311-328, 2005.
60. Sabirov RZ, Okada Y. The maxi-anion channel: a classical channel playing novel roles through an unidentified molecular entity. J Physiol Sci 59: 3-21, 2009.
61. Sanchez-Olea R, Morales M, Garcia O, Pasantes-Morales H. Cl channel blockers inhibit the volume-activated efflux of Cl and taurine in cultured neurons. Am J Physiol Cell Physiol 270: C1703-C1708, 1996.
62. 2+-dependent signaling pathways. J Biol Chem 284: 20638-20648, 2009.
63. Silverman W, Locovei S, Dahl G. Probenecid, a gout remedy, inhibits pannexin 1 channels. Am J Physiol Cell Physiol 295: C761-C767, 2008.
64. Spray DC, Ye ZC, Ransom BR. Functional connexin "hemichannels": a critical appraisal. Glia 54: 758-773, 2006.
65. Strange K, Emma F, Jackson PS. Cellular and molecular physiology of volume-sensitive anion channels. Am J Physiol Cell Physiol 270: C711-C730, 1996.
66. Takano T, Kang J, Jaiswal JK, Simon SM, Lin JH, Yu Y, Li Y, Yang J, Dienel G, Zielke HR, Nedergaard M. Receptor-mediated glutamate release from volume sensitive channels in astrocytes. Proc Natl Acad Sci USA 102: 16466-16471, 2005.
67. 2+- dependent ATP release from A549 cells involves synergistic autocrine stimulation by coreleased uridine nucleotides. J Physiol 584: 419-435, 2007.
68. Tatur S, Kreda S, Lazarowski E, Grygorczyk R. Calcium-dependent release of adenosine and uridine nucleotides from A549 cells. Purinergic Signal 4: 139-146, 2008.
69. Thompson RJ, Zhou N, MacVicar BA. Ischemia opens neuronal gap junction hemichannels. Science 312: 924-927, 2006.
70. Wang Y, Roman R, Lidofsky SD, Fitz JG. Autocrine signaling through ATP release represents a novel mechanism for cell volume regulation. Proc Natl Acad Sci USA 93: 12020-12025, 1996.
71. Wong CW, Christen T, Roth I, Chadjichristos CE, Derouette JP, Foglia BF, Chanson M, Goodenough DA, Kwak BR. Connexin37 protects against atherosclerosis by regulating monocyte adhesion. Nat Med 12: 950-954, 2006.
72. Xi G, Reiser G, Keep RF. The role of thrombin and thrombin receptors in ischemic, hemorrhagic and traumatic brain injury: deleterious or protective? J Neurochem 84: 3-9, 2003.
73. Ye ZC, Oberheim N, Kettenmann H, Ransom BR. Pharmacological "cross-inhibition" of connexin hemichannels and swelling activated anion channels. Glia 57: 258-269, 2009.
74. Zeng JW, Liu XH, He WJ, Du L, Zhang JH, Wu XG, Ruan HZ. Inhibition of ATP-induced glutamate release by MRS2179 in cultured dorsal spinal cord astrocytes. Pharmacology 82: 257-263, 2008.
75. Zsiros V, Maccaferri G. Noradrenergic modulation of electrical coupling in GABAergic networks of the hippocampus. J Neurosci 28: 1804-1815, 2008.