Modulation of Dopaminergic Neuronal Excitability by Zinc through the Regulation of Calcium-related Channels

다국어 초록 (Multilingual Abstract)

Depending on the intracellular buffering of calcium by chelation, zinc has the following two apparent effects on neuronal excitability: enhancement or reduction. Zinc increased tonic activity in the depolarized state when neurons were intracellularly dialyzed with EGTA but attenuated the neuronal activity when BAPTA was used as an intracellular calcium buffer. This suggests that neuronal excitability can be modulated by zinc, depending on the internal calcium buffering capacity. In this study, we elucidated the mechanisms of zinc-mediated alterations in neuronal excitability and determined the effect of calcium-related channels on zinc-mediated alterations in excitability. The zinc-induced augmentation of firing activity was mediated via the inhibition of small-conductance calcium-activated potassium (SK) channels with not only the contribution of voltage-gated L-type calcium channels (VGCCs) and ryanodine receptors (RyRs), but also through the activation of VGCCs via melastatin-like transient receptor potential channels. We suggest that zinc modulates the dopaminergic neuronal activity by regulating not only SK channels as calcium sensors, but also VGCCs or RyRs as calcium sources. Our results suggest that the cytosolic calcium-buffering capacity can tightly regulate zinc-induced neuronal firing patterns and that local calcium-signaling domains can determine the physiological and pathological state of synaptic activity in the dopaminergic system.

참고문헌 (Reference)

1 Eide DJ, "Zinc transporters and the cellular trafficking of zinc" 1763 : 711-722, 2006

2 Miralles F, "Zinc ions block rectifier potassium channels and calcium activated potassium channels at the frog motor nerve endings" 641 : 279-284, 1994

3 Chung J, "Zinc increases the excitability of dopaminergic neurons in rat substantia nigra" 286 : 183-186, 2000

4 Cardozo DL, "Voltage-dependent calcium channels in rat midbrain dopamine neurons : modulation by dopamine and GABAB receptors" 74 : 1137-1148, 1995

5 Neher E, "Vesicle pools and Ca2+ microdomains : new tools for understanding their roles in neurotransmitter release" 20 : 389-399, 1998

6 Guatteo E, "Temperature sensitivity of dopaminergic neurons of the substantia nigra pars compacta : involvement of transient receptor potential channels" 94 : 3069-3080, 2005

7 Hajós M, "Synaptic connections between pars compacta and pars reticulata neurones : electrophysiological evidence for functional modules within the substantia nigra" 660 : 216-224, 1994

8 Hardman CD, "Substantia nigra pars reticulata neurons in Parkinson's disease" 5 : 49-55, 1996

9 Sim JA, "Submicromolar concentrations of zinc irreversibly reduce a calcium-dependent potassium current in rat hippocampal neurons in vitro" 36 : 623-629, 1990

10 Lledo PM, "Stable transfection of calbindin-D28k into the GH3 cell line alters calcium currents and intracellular calcium homeostasis" 9 : 943-954, 1992

11 Vandecasteele M, "Spike frequency adaptation is developmentally regulated in substantia nigra pars compacta dopaminergic neurons" 192 : 1-10, 2011

12 하고은, "Spike Frequency Adaptation in Neurons of the Central Nervous System" 한국뇌신경과학회 26 (26): 179-185, 2017

13 Rousseau E, "Single cardiac sarcoplasmic reticulum Ca2+-release channel: activation by caffeine" 256 : H328-H333, 1989

14 Wolfart J, "Selective coupling of T-type calcium channels to SK potassium channels prevents intrinsic bursting in dopaminergic midbrain neurons" 22 : 3404-3413, 2002

15 Shepard PD, "Repetitive firing properties of putative dopamine-containing neurons in vitro : regulation by an apamin-sensitive Ca(2+)-activated K+ conductance" 86 : 141-150, 1991

16 Tarohda T, "Regional distributions of manganese, iron, copper, and zinc in the brains of 6-hydroxydopamine-induced parkinsonian rats" 383 : 224-234, 2005

17 Zhu X, "Receptor-activated Ca2+ influx via human Trp3 stably expressed in human embryonic kidney(HEK)293 cells. Evidence for a non-capacitative Ca2+ entry" 273 : 133-142, 1998

18 Prakriya M, "Potentiation and inhibition of Ca2+ release-activated Ca2+ channels by 2-aminoethyldiphenyl borate (2-APB) occurs independently of IP3 receptors" 536(Pt 1) : 3-19, 2001

19 Gonzales AL, "Pharmacological inhibition of TRPM4 hyperpolarizes vascular smooth muscle" 299 : C1195-C1202, 2010

20 Kim SH, "Nonselective cation channels are essential for maintaining intracellular Ca2+ levels and spontaneous firing activity in the midbrain dopamine neurons" 455 : 309-321, 2007

21 Nedergaard S, "Nifedipine-and omega-conotoxin-sensitive Ca2+ conductances in guinea-pig substantia nigra pars compacta neurones" 466 : 727-747, 1993

22 Berridge MJ, "Neuronal calcium signaling" 21 : 13-26, 1998

23 Takeda A, "Movement of zinc and its functional significance in the brain" 34 : 137-148, 2000

24 Roussel C, "Modulation of neuronal excitability by intracellular calcium buffering : from spiking to bursting" 39 : 455-466, 2006

25 Ma HT, "Modification of store-operated channel coupling and inositol trisphosphate receptor function by 2-aminoethoxydiphenyl borate in DT40 lymphocytes" 277 : 6915-6922, 2002

26 Durante P, "Low-threshold L-type calcium channels in rat dopamine neurons" 91 : 1450-1454, 2004

27 Augustine GJ, "Local calcium signaling in neurons" 40 : 331-346, 2003

28 Naraghi M, "Linearized buffered Ca2+ diffusion in microdomains and its implications for calculation of [Ca2+] at the mouth of a calcium channel" 17 : 6961-6973, 1997

29 Stork CJ, "Intracellular zinc elevation measured with a"calcium-specific"indicator during ischemia and reperfusion in rat hippocampus : a question on calcium overload" 26 : 10430-10437, 2006

30 Halaszovich CR, "Inhibition of TRP3 channels by lanthanides. Block from the cytosolic side of the plasma membrane" 275 : 37423-37428, 2000

31 Dexter DT, "Increased nigral iron content and alterations in other metal ions occurring in brain in Parkinson's disease" 52 : 1830-1836, 1989

32 Rogers JH, "Immunohistochemical markers in rat brain : colocalization of calretinin and calbindin-D28k with tyrosine hydroxylase" 587 : 203-210, 1992

33 이지연, "Functional Analysis and Immunochemical Analyses of Ca2+ Homeostasis-related Proteins Expression of Glaucoma-induced Retinal Degeneration in Rats" 한국뇌신경과학회 27 (27): 16-27, 2018

34 Gregory RB, "Evidence that 2-aminoethyl diphenylborate is a novel inhibitor of storeoperated Ca2+ channels in liver cells, and acts through a mechanism which does not involve inositol trisphosphate receptors" 354(Pt 2) : 285-290, 2001

35 Foehring RC, "Endogenous calcium buffering capacity of substantia nigral dopamine neurons" 102 : 2326-2333, 2009

36 Richards CD, "Electrophysiological and immunocytochemical characterization of GABA and dopamine neurons in the substantia nigra of the rat" 80 : 545-557, 1997

37 Noh J, "Effect of zinc ions on voltage-gated Ca2+ currents of rat nigral neurons" 9 : 25-28, 2000

38 Noh J, "Dual function of Zn2+ on the intrinsic excitability of dopaminergic neurons in rat substantia nigra" 175 : 85-92, 2011

39 Stocker M, "Differential distribution of three Ca(2+)-activated K(+)channel subunits, SK1, SK2, and SK3, in the adult rat central nervous system" 15 : 476-493, 2000

40 Kushal Sharma, "Differential Expression of Ca2+-buffering Protein Calretinin in Cochlear Afferent Fibers: A Possible Link to Vulnerability to Traumatic Noise" 한국뇌신경과학회 27 (27): 397-407, 2018

41 Kurobe N, "Developmental and age-dependent changes of 28-kDa calbindin-D in the central nervous tissue determined with a sensitive immunoassay method" 58 : 128-134, 1992

42 Fruen BR, "Dantrolene inhibition of sarcoplasmic reticulum Ca2+ release by direct and specific action at skeletal muscle ryanodine receptors" 272 : 26965-26971, 1997

43 Zhao F, "Dantrolene inhibition of ryanodine receptor Ca2+ release channels. Molecular mechanism and isoform selectivity" 276 : 13810-13816, 2001

44 Schwaller B, "Cytosolic Ca2+ buffers" 2 : a004051-, 2010

45 Leung YM, "Current perspectives in the pharmacological studies of store-operated Ca2+ entry blockers" 81 : 253-258, 1999

46 Fakler B, "Control of K(Ca)channels by calcium nano/microdomains" 59 : 873-881, 2008

47 Ullrich ND, "Comparison of functional properties of the Ca2+-activated cation channels TRPM4and TRPM5 from mice" 37 : 267-278, 2005

48 Sailer CA, "Comparative immunohistochemical distribution of three small-conductance Ca2+-activated potassium channel subunits, SK1, SK2, and SK3 in mouse brain" 26 : 458-469, 2004

49 Boulay G, "Cloning and expression of a novel mammalian homolog of Drosophila transient receptor potential(Trp)involved in calcium entry secondary to activation of receptors coupled by the Gq class of G protein" 272 : 29672-29680, 1997

50 De March Z, "Cellular localization of TRPC5 in the substantia nigra of rat" 402 : 35-39, 2006

51 Résibois A, "Calretinin in rat brain : an immunohistochemical study" 46 : 101-134, 1992

52 DeLorenzo RJ, "Calmodulin systems in neuronal excitability:a molecular approach to epilepsy" 16 (16): S104-S114, 1984

53 Mrejeru A, "Calcium-activated non-selective cation currents are involved in generation of tonic and bursting activity in dopamine neurons of the substantia nigra pars compacta" 589 (589): 2497-2514, 2011

54 Chan CS, "Calcium homeostasis, selective vulnerability and Parkinson's disease" 32 : 249-256, 2009

55 Chard PS, "Calcium buffering properties of calbindin D28k and parvalbumin in rat sensory neurones" 472 : 341-357, 1993

56 Celio MR, "Calbindin D-28k and parvalbumin in the rat nervous system" 35 : 375-475, 1990

57 Sausbier U, "Ca2+-activated K+ channels of the BK-type in the mouse brain" 125 : 725-741, 2006

58 조은혜, "Astrocytes, Microglia, and Parkinson’s Disease" 한국뇌신경과학회 27 (27): 77-87, 2018

59 Bakowski D, "An examination of the secretion-like coupling model for the activation of the Ca2+ release-activated Ca2+ current I(CRAC) in RBL-1 cells" 532(Pt 1) : 55-71, 2001

60 Dexter DT, "Alterations in the levels of iron, ferritin and other trace metals in Parkinson's disease and other neurodegenerative diseases affecting the basal ganglia" 114 (114): 1953-1975, 1991

61 Hoesch RE, "A novel Ca(2+)influx pathway in mammalian primary sensory neurons is activated by caffeine" 86 : 190-196, 2001

62 Grynkiewicz G, "A new generation of Ca2+ indicators with greatly improved fluorescence properties" 260 : 3440-3450, 1985

63 Grand T, "9-phenanthrol inhibits human TRPM4 but not TRPM5 cationic channels" 153 : 1697-1705, 2008

64 Iwasaki H, "2-Aminoethoxydiphenyl borate(2-APB)inhibits capacitative calcium entry independently of the function of inositol 1, 4, 5-trisphosphate receptors" 7 : 429-439, 2001

65 Chan CS, "'Rejuvenation' protects neurons in mouse models of Parkinson's disease" 447 : 1081-1086, 2007