Reversal of rotenone-induced dysfunction of astrocytic connexin43 by opening mitochondrial ATP-sensitive potassium channels

Cellular and Molecular Neurobiology

Volumn 31, Issue 1, 2011, Pages 111-117

  Zhang, Shu ^a   Liang, Rui ^a   Zhou, Fang ^a   Huang, Xu ^a   Ding, Jian Hua ^a   Hu, Gang ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

Author keywords

Astrocyte; ATP sensitive potassium channel; Connexin 43; Iptakalim; Rotenone

Indexed keywords

5 HYDROXYDECANOIC ACID; ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; CONNEXIN 43; DIAZOXIDE; IPTAKALIM; ROTENONE;

ANIMAL CELL; APOPTOSIS; ARTICLE; ASTROCYTE; BRAIN MITOCHONDRION; CELL PROTECTION; CHANNEL GATING; CONTROLLED STUDY; DOWN REGULATION; GAP JUNCTION; NEUROPROTECTION; NEWBORN; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; ASTROCYTES; CELL MEMBRANE PERMEABILITY; CELLS, CULTURED; CONNEXIN 43; CYTOPROTECTION; DRUG EVALUATION, PRECLINICAL; GAP JUNCTIONS; ION CHANNEL GATING; POTASSIUM CHANNELS; PROPYLAMINES; RATS; RATS, SPRAGUE-DAWLEY; ROTENONE; UNCOUPLING AGENTS;

EID: 79151473668     PISSN: 02724340     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10571-010-9560-6     Document Type: Article

References (49)

1. M Alam WJ Schmidt 2002 Rotenone destroys dopaminergic neurons and induces parkinsonian symptoms in rats Behav Brain Res 136 317 324 1:CAS:528: DC%2BD38XnvVOltbs%3D 10.1016/S0166-4328(02)00180-8 12385818
2. M Amiry-Moghaddam OP Ottersen 2003 The molecular basis of water transport in the brain Nat Rev Neurosci 4 991 1001 1:CAS:528:DC%2BD3sXpslGhurs%3D 10.1038/nrn1252 14682361
3. R Bajgar S Seetharaman AJ Kowaltowski KD Garlid P Paucek 2001 Identification and properties of a novel intracellular (mitochondrial) ATP-sensitive potassium channel in brain J Biol Chem 276 33369 33374 1:CAS:528:DC%2BD3MXmslymu78%3D 10.1074/jbc.M103320200 11441006
4. R Betarbet TB Sherer G MacKenzie M Garcia-Osuna AV Panov JT Greenamyre 2000 Chronic systemic pesticide exposure reproduces features of Parkinson's disease Nat Neurosci 3 1301 1306 1:CAS:528:DC%2BD3cXosVGgsbg%3D 10.1038/81834 11100151
5. GF Blandini C Nappi E Tassorelli E Martignoni 2000 Functional changes of the basal ganglia circuitry in Parkinson's disease Prog Neurobiol 62 63 88 1:CAS:528:DC%2BD3cXltFWnurs%3D 10.1016/S0301-0082(99)00067-2 10821982
6. AE Cardona EP Pioro ME Sasse V Kostenko SM Cardona IM Dijkstra D Huang G Kidd S Dombrowski R Dutta JC Lee DN Cook S Jung SA Lira DR Littman RM Ransohoff 2006 Control of microglial neurotoxicity by the fractalkine receptor Nat Neurosci 9 917 924 1:CAS:528:DC%2BD28XmtFCmsbw%3D 10.1038/nn1715 16732273
7. Y Chen NE Vartiainen W Ying PH Chan J Koistinaho RA Swanson 2001 Astrocytes protect neurons from nitric oxide toxicity by a glutathione-dependent mechanism J Neurochem 77 1601 1610 1:CAS:528:DC%2BD3MXkslWnu70%3D 10.1046/j.1471-4159.2001.00374.x 11413243
8. JE Contreras HA Sanchez EA Eugenin, et al. 2002 Metabolic inhibition induces opening of unapposed connexin43 gap junction hemichannels and reduces gap junctional communication in cortical astrocytes in culture Proc Natl Acad Sci USA 99 495 500 1:CAS:528:DC%2BD38Xlt1Cruw%3D%3D 10.1073/pnas.012589799 11756680
9. JE Contreras HA Sanchez LP Veliz, et al. 2004 Role of connexin-based gap junction channels and hemichannels in ischemia-induced cell death in nervous tissue Brain Res Brain Res Rev 47 290 303 1:CAS:528:DC%2BD2cXhtVantLjM 10.1016/j.brainresrev.2004.08.002 15572178
10. R Dermietzel Y Gao E Scemes D Vieira M Urban M Kremer MV Bennett DC Spray 2000 Connexin43 null mice reveal that astrocytes express multiple connexins Brain Res Brain Res Rev 32 45 56 1:CAS:528:DC%2BD3cXit1WhtLo%3D 10.1016/S0165-0173(99)00067-3 10751656
11. FJ Diaz-Corrales M Asanuma I Miyazaki K Miyoshi N Ogawa 2005 Rotenone induces aggregation of gamma-tubulin protein and subsequent disorganization of the centrosome: relevance to formation of inclusion bodies and neurodegeneration Neuroscience 133 117 135 1:CAS:528:DC%2BD2MXktVOltLo%3D 10.1016/j.neuroscience. 2005.01.044 15893636
12. MH El-Fouly JE Trosko CC Chang 1987 A rapid and simple technique to study gap junctional intercellular communication Exp Cell Res 168 422 430 1:CAS:528:DyaL2sXhsFagtL0%3D 10.1016/0014-4827(87)90014-0 2433137
13. R Farahani MH Pina-Benabou A Kyrozis R Rozental, et al. 2005 Alterations in metabolism and gap junction expression may determine the role of astrocytes as ''good samaritans'' or executioners Glia 50 351 361 10.1002/glia.20213 15846800
14. C Giaume F Kirchhoff C Matute A Reichenbach A Verkhratsky 2007 Glia: the fulcrum of brain diseases Cell Death Differ 14 1324 1335 1:CAS:528: DC%2BD2sXms1Sru7c%3D 10.1038/sj.cdd.4402144 17431421
15. F Goubaeva M Mikami S Giardina B Ding J Abe J Yang 2007 Cardiac mitochondrial connexin 43 regulates apoptosis Biochem Biophys Res Commun 352 97 103 1:CAS:528:DC%2BD28Xht1Oht7nI 10.1016/j.bbrc.2006.10.177 17107662
16. B Hamprecht F Loffler 1985 Primary glial cultures as a model for studying hormone action Methods Enzymol 109 341 345 1:CAS:528:DyaL2MXktlagsrY%3D 10.1016/0076-6879(85)09097-8 2985921
17. L Helmuth 2000 Pesticide causes Parkinson's in rats Science 290 1068 1:CAS:528:DC%2BD3cXotVaqtr4%3D 10.1126/science.290.5494.1068a 11184997
18. LF Hu S Wang XR Shi HH Yao YH Sun JH Ding G Hu 2005 ATP-sensitive potassium channel opener iptakalim protected against the cytotoxicity of MPP+ on SH-SY5Y cells by decreasing extracellular glutamate level J Neurochem 94 1570 1579 1:CAS:528:DC%2BD2MXhtVaksbrL 10.1111/j.1471-4159.2005.03306.x 16000145
19. GR John E Scemes SO Suadicani JS Liu PC Charles, et al. 1999 IL-1beta differentially regulates calcium wave propagation between primary human fetal astrocytes via pathways involving P2 receptors and gap junction channels Proc Natl Acad Sci USA 96 11613 11618 1:CAS:528:DyaK1MXmvVCmtb0%3D 10.1073/pnas.96.20.11613 10500225
20. A Kawasaki T Hayashi K Nakachi JE Trosko K Sugihara Y Kotake S Ohta 2009 Modulation of connexin 43 in rotenone-induced model of Parkinson's disease Neuroscience 160 61 68 1:CAS:528:DC%2BD1MXksVaksbY%3D 10.1016/j.neuroscience. 2009.01.080 19232380
21. T Kielian 2008 Glial connexins and gap junctions in CNS inflammation and disease J Neurochem 106 1000 1016 1:CAS:528:DC%2BD1cXpsFOju7c%3D 10.1111/j.1471-4159.2008.05405.x 18410504
22. DV Krysko L Leybaert P Vandenabeele K D'Herde 2005 Gap junctions and the propagation of cell survival and cell death signals Apoptosis 10 459 469 1:STN:280:DC%2BD2M3msFGltw%3D%3D 10.1007/s10495-005-1875-2 15909108
23. CK Liao SM Wang YL Chen HS Wang JC Wu 2010 Lipopolysaccharide-induced inhibition of connexin 43 gap junction communication in astrocytes is mediated by downregulation of caveolin-3 Int J Biochem Cell Biol 42 762 770 1:CAS:528:DC%2BC3cXivFGqsro%3D 10.1016/j.biocel.2010.01.016 20093193
24. B Liss J Roeper 2001 Molecular physiology of neuronal K-ATP channels (Review) Mol Membr Biol 18 117 127 1:CAS:528:DC%2BD3MXlt1aktrs%3D 10.1080/09687680110047373 11463204
25. B Liss O Haeckel J Wildmann T Miki S Seino J Roeper 2005 K-ATP channels promote the differential degeneration of dopaminergic midbrain neurons Nat Neurosci 8 1742 1751 1:CAS:528:DC%2BD2MXht1Gis77N 10.1038/nn1570 16299504
26. M Mazzanti JY Sul PG Haydon 2001 Glutamate on demand: astrocytes as a ready source Neuroscientist 7 396 405 1:CAS:528:DC%2BD3MXnvVGisr0%3D 10.1177/107385840100700509 11597099
27. PL McGeer EG McGeer 2008 Glial reactions in Parkinson's disease Mov Disord 23 474 483 10.1002/mds.21751 18044695
28. JI Nagy JE Rash 2003 Astrocyte and oligodendrocyte connexins of the glial syncytium in relation to astrocyte anatomical domains and spatial buffering Cell Commun Adhes 10 401 406 1:CAS:528:DC%2BD2cXhtFKhsr8%3D 14681048
29. JI Nagy W Li EL Hertzberg CA Marotta 1996 Elevated connexin43 immunoreactivity at sites of amyloid plaques in Alzheimer's disease Brain Res 717 173 178 1:CAS:528:DyaK28XivFKquro%3D 10.1016/0006-8993(95)01526-4 8738268
30. T Nakase CC Naus 2004 Gap junctions and neurological disorders of the central nervous system Biochim Biophys Acta 1662 149 158 1:CAS:528: DC%2BD2cXisVKltL4%3D 10.1016/j.bbamem.2004.01.009 15033585
31. T Nakase S Fushiki CCG Naus 2003 Astrocytic gap junctions composed by connexin43 reduces apoptotic neuronal damage in cerebral ischemia Stroke 34 1987 1993 10.1161/01.STR.0000079814.72027.34 12843358
32. JL Perez Velazquez MV Frantseva CC Naus 2003 Gap junctions and neuronal injury: protectants or executioners? Neuroscientist 9 5 9 1:CAS:528: DC%2BD3sXhsVWrs78%3D 10.1177/1073858402239586 12580335
33. TM Scarabelli R Knight A Stephanou, et al. 2006 Clinical implications of apoptosis in ischemic myocardium Curr Probl Cardiol 31 181 264 10.1016/j.cpcardiol.2005.11.002 16503249
34. G Seifert K Schilling C Steinhauser 2006 Astrocyte dysfunction in neurological disorders: a molecular perspective Nat Rev Neurosci 7 194 206 1:CAS:528:DC%2BD28Xhs1Gqt7g%3D 10.1038/nrn1870 16495941
35. DC Spray ZC Ye BR Ransom 2006 Functional connexin 'hemichannels': a critical appraisal Glia 54 758 773 10.1002/glia.20429 17006904
36. A Tabernero JM Medina C Giaume 2006 Glucose metabolism and proliferation in glia: role of astrocytic gap junctions J Neurochem 99 1049 1061 1:CAS:528:DC%2BD28Xht1yks7rF 10.1111/j.1471-4159.2006.04088.x 16899068
37. KK Tai DD Truong 2002 Activation of adenosine triphosphate-sensitive potassium channels confers protection against rotenone-induced cell death: therapeutic implications for Parkinson's disease J Neurosci Res 69 559 566 1:CAS:528:DC%2BD38XmtVOgsrk%3D 10.1002/jnr.10309 12210849
38. A Thomzig M Wenzel C Karschin MJ Eaton SN Skatchkov, et al. 2001 Kir6.1 is the principal pore-forming subunit of astrocyte but not neuronal plasma membrane K-ATP channels Mol Cell Neurosci 18 671 690 1:CAS:528: DC%2BD3MXptFegtbs%3D 10.1006/mcne.2001.1048 11749042
39. H Wang 2003 Pharmacological characteristics of the novel antihypertensive drug, iptakalim hydrochloride, and its molecular mechanisms Drug Dev Res 58 65 68 1:CAS:528:DC%2BD3sXisFeltrw%3D 10.1002/ddr.10132
40. S Wang LF Hu Y Yang JH Ding G Hu 2005 Studies of ATP-sensitive potassium channels on 6-hydroxydopamine and haloperidol rat models of Parkinson's disease: implications for treating Parkinson's disease? Neuropharmacology 48 984 992 1:CAS:528:DC%2BD2MXjs1Omtbo%3D 10.1016/j.neuropharm.2005.01.009 15857625
41. S Wang LF Hu Y Zhang T Sun YH Sun SY Liu, et al. 2006 Effects of systemic administration of iptakalim on extracellular neurotransmitter levels in the striatum of unilateral 6-hydroxydopamine-lesioned rats Neuropsychopharmacology 31 933 940 1:CAS:528:DC%2BD28XjsFaht74%3D 10.1038/sj.npp.1300857 16123757
42. W Xie H Wang J Ding H Wang G Hu 2005 Anti-proliferating effect of iptakalim, a novel KATP channel opener, in cultured rabbit pulmonary arterial smooth muscle cells Eur J Pharmacol 511 81 87 1:CAS:528:DC%2BD2MXisFGqur8%3D 10.1016/j.ejphar.2005.01.039 15792775
43. Y Yang X Liu JH Ding J Sun Y Long F Wang, et al. 2004 Effects of iptakalim on rotenone-induced cytotoxicity and dopamine release from PC12 cells Neurosci Lett 366 53 57 1:CAS:528:DC%2BD2cXlsl2gsro%3D 10.1016/j.neulet.2004.05. 009 15265589
44. Y Yang X Liu Y Long F Wang JH Ding SY Liu, et al. 2005 Systematic administration of iptakalim, an ATP-sensitive potassium channel opener, prevents rotenone-induced motor and neurochemical alterations in rats J Neurosci Res 80 442 449 1:CAS:528:DC%2BD2MXjvFakt7o%3D 10.1002/jnr.20467 15795934
45. J Yang LF Hu X Liu F Zhou JH Ding G Hu 2006 Effects of iptakalim on extracellular glutamate and dopamine levels in the striatum of unilateral 6-hydroxydopamine-lesioned rats: a microdialysis study Life Sci 78 1940 1944 1:CAS:528:DC%2BD28XitVGgs78%3D 10.1016/j.lfs.2005.08.001 16216278
46. Y Yang X Liu Y Long F Wang JH Ding SY Liu, et al. 2006 Activation of mitochondrial ATP-sensitive potassium channels improves rotenone-related motor and neurochemical alterations in rats Int J Neuropsychopharmacol 9 51 61 1:CAS:528:DC%2BD28Xht1eiuw%3D%3D 10.1017/S1461145705005547 15927086
47. C Zawar TD Plant C Schirra A Konnerth B Neumcke 1999 Cell-type specific expression of ATP-sensitive potassium channels in the rat hippocampus J Physiol 514 327 341 1:CAS:528:DyaK1MXhsF2itLo%3D 10.1111/j.1469-7793.1999.315ae.x 9852317
48. +-induced astrocytic apoptosis via mitochondria and MAPK signal pathways J Neurochem 103 569 579 1:CAS:528:DC%2BD2sXht1KqsLzF 10.1111/j.1471-4159.2007.04775.x 17635669
49. F Zhou JY Wu XL Sun HH Yao JH Ding G Hu 2007 Iptakalim alleviates rotenone-induced degeneration of dopaminergic neurons through inhibiting microglia-mediated neuroinflammation Neuropsychopharmacology 32 2570 2580 1:CAS:528:DC%2BD2sXhtlWjsbnJ 10.1038/sj.npp.1301381 17356569