Dopaminergic neurons exhibit an age-dependent decline in electrophysiological parameters in the MitoPark mouse model of Parkinson’s disease

Journal of Neuroscience

Volumn 36, Issue 14, 2016, Pages 4026-4037

  Branch, Sarah Y ^a   Chen, Cang ^a   Sharma, Ramaswamy ^a   Lechleiter, James D ^a   Li, Senlin ^a   Beckstead, Michael J ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

Dopamine; Electrophysiology; Mice; MitoPark; Neurotransmission; Parkinson s

Indexed keywords

DOPAMINE; DNA BINDING PROTEIN; ION CHANNEL; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL TRANSCRIPTION FACTOR A; TRANSCRIPTION FACTOR;

AGE; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CONTROLLED STUDY; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; MOTOR DYSFUNCTION; MOUSE; NEUROTRANSMISSION; NONHUMAN; PARKINSON DISEASE; REAL TIME POLYMERASE CHAIN REACTION; SUBSTANTIA NIGRA; AGING; ANIMAL; BIOLOGICAL RHYTHM; C57BL MOUSE; DENDRITE; ELECTRIC CAPACITANCE; ELECTROPHYSIOLOGY; FEMALE; GENETICS; MALE; NERVE CONDUCTION; PATHOLOGY; PATHOPHYSIOLOGY; SYNAPTIC TRANSMISSION;

AGING; ANIMALS; BIOLOGICAL CLOCKS; DENDRITES; DNA-BINDING PROTEINS; DOPAMINERGIC NEURONS; ELECTRIC CAPACITANCE; ELECTROPHYSIOLOGICAL PHENOMENA; FEMALE; ION CHANNELS; MALE; MICE; MICE, INBRED C57BL; MITOCHONDRIAL PROTEINS; NEURAL CONDUCTION; PARKINSON DISEASE; SUBSTANTIA NIGRA; SYNAPTIC TRANSMISSION; TRANSCRIPTION FACTORS;

EID: 84964089878     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1395-15.2016     Document Type: Article

References (60)

1. Ahn KC, Bernier BE, Harnett MT, Morikawa H (2010) IP3 receptor sensitization during in vivo amphetamine experience enhances NMDA receptor plasticity in dopamine neurons of the ventral tegmental area. J Neurosci 30:6689-6699. CrossRef Medline
2. Beckstead MJ, Grandy DK, Wickman K, Williams JT (2004) Vesicular dopamine release elicits an inhibitory postsynaptic current in midbrain dopamine neurons. Neuron 42:939-946. CrossRef Medline
3. Birkmayer W, Hornykiewicz O (1961) The L-3,4-dioxyphenylalanine (DOPA)-effect in Parkinson-akinesia (in German). Wien Klin Wochenschr 73:787-788. Medline
4. Branch SY, Beckstead MJ (2012) Methamphetamine produces bidirectional, concentration-dependent effects on dopamine neuron excitability and dopamine-mediated synaptic currents. J Neurophysiol 108:802-809. CrossRef Medline
5. Branch SY, Sharma R, Beckstead MJ (2014) Aging decreases L-type calcium channel currents and pacemaker firing fidelity in substantia nigra dopamine neurons. J Neurosci 34:9310-9318. CrossRef Medline
6. Carli M, Evenden JL, Robbins TW (1985) Depletion of unilateral striatal dopamine impairs initiation of contralateral actions and not sensory attention. Nature 313:679-682. CrossRef Medline
7. Catterall WA, Goldin AL, Waxman SG (2005) International union of pharmacology: XLVII. Nomenclature and structure-function relationships of voltage-gated sodium channels. Pharmacol Rev 57:397-409. CrossRef Medline
8. Collier TJ, Kanaan NM, Kordower JH (2011) Ageing as a primary risk factor for Parkinson's disease: evidence from studies of non-human primates. Nat Rev Neurosci 12:359-366. CrossRef Medline
9. Dauer W, Przedborski S (2003) Parkinson's disease: mechanisms and models. Neuron 39:889-909. CrossRef Medline
10. Dawson TM, Ko HS, Dawson VL (2010) Genetic animal models of Parkinson's disease. Neuron 66:646-661. CrossRef Medline
11. de la Fuente-Fernández R, Schulzer M, Kuramoto L, Cragg J, Ramachandiran N, Au WL, Mak E, McKenzie J, McCormick S, Sossi V, Ruth TJ, Lee CS, Calne DB, Stoessl AJ (2011) Age-specific progression of nigrostriatal dysfunction in Parkinson's disease. Ann Neurol 69:803-810. CrossRef Medline
12. Duty S, Jenner P (2011) Animal models of Parkinson's disease: a source of novel treatments and clues to the cause of the disease. Br J Pharmacol 164:1357-1391. CrossRef Medline
13. Ekstrand MI, Galter D (2009) The MitoPark mouse: an animal model of Parkinson's disease with impaired respiratory chain function in dopamine neurons. Parkinsonism Relat Disord 15:S185-S188. CrossRef Medline
14. Ekstrand MI, Falkenberg M, Rantanen A, Park CB, Gaspari M, Hultenby K, Rustin P, Gustafsson CM, Larsson NG (2004) Mitochondrial transcription factor A regulates mtDNA copy number in mammals. Hum Mol Genet 13:935-944. CrossRef Medline
15. Ekstrand MI, Terzioglu M, Galter D, Zhu S, Hofstetter C, Lindqvist E, Thams S, Bergstrand A, Hansson FS, Trifunovic A, Hoffer B, Cullheim S, Mohammed AH, Olson L, Larsson NG (2007) Progressive Parkinsonism in mice with respiratory-chain-deficient dopamine neurons. Proc Natl Acad Sci U S A 104:1325-1330. CrossRef Medline
16. Ford CP, Mark GP, Williams JT (2006) Properties and opioid inhibition of mesolimbic dopamine neurons vary according to target location. J Neurosci 26:2788-2797. CrossRef Medline
17. Galter D, Pernold K, Yoshitake T, Lindqvist E, Hoffer B, Kehr J, Larsson NG, Olson L (2010) MitoPark mice mirror the slow progression of key symptoms and L-DOPA response in Parkinson's disease. Genes Brain Behav 9:173-181. CrossRef Medline
18. Gantz SC, Ford CP, Neve KA, Williams JT (2011) Loss of Mecp2 in substantia nigra dopamine neurons compromises the nigrostriatal pathway. J Neurosci 31:12629-12637. CrossRef Medline
19. George AL Jr (2005) Inherited disorders of voltage-gated sodium channels. J Clin Invest 115:1990-1999. CrossRef Medline
20. Goldberg MS, Pisani A, Haburcak M, Vortherms TA, Kitada T, Costa C, Tong Y, Martella G, Tscherter A, Martins A, Bernardi G, Roth BL, Pothos EN, Calabresi P, Shen J (2005) Nigrostriatal dopaminergic deficits and hypokinesia caused by inactivation of the familial Parkinsonism-linked gene DJ-1. Neuron 45:489-496. CrossRef Medline
21. Gonon FG, Buda MJ (1985) Regulation of dopamine release by impulse flow and by auto receptors as studied by in vivo voltammetry in the rat striatum. Neuroscience 14:765-774. CrossRef Medline
22. Good CH, Hoffman AF, Hoffer BJ, Chefer VI, Shippenberg TS, Bäckman CM, Larsson NG, Olson L, Gellhaar S, Galter D, Lupica CR (2011) Impaired nigrostriatal function precedes behavioral deficits in a genetic mitochondrial model of Parkinson's disease. FASEB J 25:1333-1344. CrossRef Medline
23. Grace AA, Onn SP (1989) Morphology and electrophysiological properties of immunocytochemically identified rat dopamine neurons recorded in vitro. J Neurosci 9:3463-3481. Medline
24. Grauer SM, Hodgson R, Hyde LA (2014) MitoPark mice, an animal model of Parkinson's disease, show enhanced prepulse inhibition of acoustic startle and no loss of gating in response to the adenosine A(2A) antagonist SCH 412348. Psychopharmacology 231:1325-1337. CrossRef Medline
25. Greenamyre JT, Hastings TG (2004) Biomedicine: Parkinson's-divergent causes, convergent mechanisms. Science 304:1120-1122. CrossRef Medline
26. Groves PM, Linder JC (1983) Dendro-dendritic synapses in substantia nigra: descriptions based on analysis of serial sections. Exp Brain Res 49:209-217. Medline
27. Guzman JN, Sanchez-Padilla J, Wokosin D, Kondapalli J, Ilijic E, Schumacker PT, Surmeier DJ (2010) Oxidant stress evoked by pacemaking in dopaminergic neurons is attenuated by DJ-1. Nature 468:696-700. CrossRef Medline
28. Harrington KA, Augood SJ, Kingsbury AE, Foster OJ, Emson PC (1996) Dopamine transporter (Dat) and synaptic vesicle amine transporter (VMAT2) gene expression in the substantia nigra of control and Parkinson's disease. Brain Res Mol Brain Res 36:157-162. CrossRef Medline
29. Hauser RA (2009) Levodopa: past, present, and future. Eur Neurol 62:1-8. CrossRef Medline
30. HornykiewiczO (1975) Parkinson's disease and its chemotherapy. Biochem Pharmacol 24:1061-1065. CrossRef Medline
31. Ilijic E, Guzman JN, Surmeier DJ (2011) The L-type channel antagonist isradipine is neuroprotective in a mouse model of Parkinson's disease. Neurobiol Dis 43:364-371. CrossRef Medline
32. Janezic S, Threlfell S, Dodson PD, Dowie MJ, Taylor TN, Potgieter D, Parkkinen L, Senior SL, Anwar S, Ryan B, Deltheil T, Kosillo P, Cioroch M, Wagner K, Ansorge O, Bannerman DM, Bolam JP, Magill PJ, Cragg SJ, Wade-Martins R (2013) Deficits in dopaminergic transmission precede neuron loss and dysfunction in a new Parkinson model. Proc Natl Acad Sci U S A 110:E4016-4025. CrossRef Medline
33. Jang J, Um KB, Jang M, Kim SH, Cho H, Chung S, Kim HJ, Park MK (2014) Balance between the proximal dendritic compartment and the soma determines spontaneous firing rate in midbrain dopamine neurons. J Physiol 592:2829-2844. CrossRef Medline
34. Jones SR, Gainetdinov RR, Wightman RM, Caron MG (1998) Mechanisms of amphetamine action revealed in mice lacking the dopamine transporter. J Neurosci 18:1979-1986. Medline
35. Kang Y, Kitai ST (1993) Calcium spike underlying rhythmic firing in dopaminergic neurons of the rat substantia nigra. Neurosci Res 18:195-207. CrossRef Medline
36. Kitada T, Pisani A, Porter DR, Yamaguchi H, Tscherter A, Martella G, Bonsi P, Zhang C, Pothos EN, Shen J (2007) Impaired dopamine release and synaptic plasticity in the striatum of PINK1-deficient mice. Proc Natl Acad Sci U S A 104:11441-11446. CrossRef Medline
37. Lacey MG, Mercuri NB, North RA (1987) Dopamine acts on D2 receptors to increase potassium conductance in neurons of the rat substantia nigra zona compacta. J Physiol 392:397-416. CrossRef Medline
38. Larsson NG, Wang J, Wilhelmsson H, Oldfors A, Rustin P, Lewandoski M, Barsh GS, Clayton DA (1998) Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat Genet 18:231-236. CrossRef Medline
39. Lee CS, Samii A, Sossi V, Ruth TJ, Schulzer M, Holden JE, Wudel J, Pal PK, de la Fuente-Fernandez R, Calne DB, Stoessl AJ (2000) In vivo positron emission tomographic evidence for compensatory changes in presynaptic dopaminergic nerve terminals in Parkinson's disease. Ann Neurol 47: 493-503. CrossRef Medline
40. Li X, Redus L, Chen C, Martinez PA, Strong R, Li S, O'Connor JC (2013) Cognitive dysfunction precedes the onset of motor symptoms in the MitoPark mouse model of Parkinson's disease. PLoS One 8:e71341. CrossRef Medline
41. Lin X, Parisiadou L, Gu XL, Wang L, Shim H, Sun L, Xie C, Long CX, Yang WJ, Ding J, Chen ZZ, Gallant PE, Tao-Cheng JH, Rudow G, Troncoso JC, Liu Z, Li Z, Cai H (2009) Leucine-rich repeat kinase 2 regulates the progression of neuropathology induced by Parkinson's-disease-related mutant alpha-synuclein. Neuron 64:807-827. CrossRef Medline
42. Lundblad M, Decressac M, Mattsson B, Björklund A (2012) Impaired neu-rotransmission caused by overexpression of α-synuclein in nigral dopamine neurons. Proc Natl Acad Sci U S A 109:3213-3219. CrossRef Medline
43. Margolis EB, Coker AR, Driscoll JR, Lemaître AI, Fields HL (2010) Reliability in the identification of midbrain dopamine neurons. PLoS One 5:e15222. CrossRef Medline
44. Neuhoff H, Neu A, Liss B, Roeper J (2002) Ih channels contribute to the different functional properties of identified dopaminergic subpopulations in the midbrain. J Neurosci 22:1290-1302. Medline
45. Oyama G, Yoshimi K, Natori S, Chikaoka Y, Ren YR, Funayama M, Shimo Y, Takahashi R, Nakazato T, Kitazawa S, HattoriN (2010) Impaired in vivo dopamine release in parkin knockout mice. Brain Res 1352:214-222. CrossRef Medline
46. Panayotis N, Pratte M, Borges-Correia A, Ghata A, Villard L, Roux JC (2011) Morphological and functional alterations in the substantia nigra pars compacta of the Mecp2-null mouse. Neurobiol Dis 41:385-397. CrossRef Medline
47. Rice ME, Patel JC, Cragg SJ (2011) Dopamine release in the basal ganglia. Neuroscience 198:112-137. CrossRef Medline
48. Scherfler C, Khan NL, Pavese N, Eunson L, Graham E, Lees AJ, Quinn NP, Wood NW, Brooks DJ, Piccini PP (2004) Striatal and cortical pre-and postsynaptic dopaminergic dysfunction in sporadic parkin-linked parkinsonism. Brain 127:1332-1342. CrossRef Medline
49. Schober A (2004) Classic toxin-induced animal models of Parkinson's disease: 6-OHDA and MPTP. Cell Tissue Res 318:215-224. CrossRef Medline
50. Sharma R, Tsuchiya M, Skobe Z, Tannous BA, Bartlett JD (2010) The acid test of fluoride: how pH modulates toxicity. PLoS One 5:e10895. CrossRef Medline
51. Shepard PD, Bunney BS (1991) Repetitive firing properties of putative DA containing neurons in vitro: regulation by an apamin sensitive Ca activated K conductance. Exp Brain Res 86:141-150. Medline
52. Sulzer D, Rayport S (1990) Amphetamine and other psychostimulants reduce pH gradients in midbrain dopaminergic neurons and chromaffin granules: a mechanism of action. Neuron 5:797-808. CrossRef Medline
53. Sulzer D, Maidment NT, Rayport S (1993) Amphetamine and other weak bases act to promote reverse transport of dopamine in ventral midbrain neurons. J Neurochem 60:527-535. CrossRef Medline
54. Tepper JM, Sawyer SF, Groves PM (1987) Electrophysiologically identified nigral dopaminergic neurons intracellularly labeled with HRP: light-microscopic analysis. J Neurosci 7:2794-2806. Medline
55. Tepper JM, Creese I, Schwartz DH (1991) Stimulus-evoked changes in neostriatal dopamine levels in awake and anesthetized rats as measured by microdialysis. Brain Res 559:283-292. CrossRef Medline
56. Terzioglu M, Galter D (2008) Parkinson's disease: genetic versus toxininduced rodent models. FEBS J 275:1384-1391. CrossRef Medline
57. Wilson CJ, Callaway JC (2000) Coupled oscillator model of the dopaminergic neuron of the substantia nigra. J Neurophysiol 83:3084-3100. Medline
58. Wilson CJ, Groves PM, Fifková E (1977) Monoaminergic synapses, including dendro-dendritic synapses in the rat substantia nigra. Exp Brain Res 30:161-174. Medline
59. Wolfart J, Neuhoff H, Franz O, Roeper J (2001) Differential expression of the small-conductance, calcium-activated potassium channel SK3 is critical for pacemaker control in dopaminergic midbrain neurons. J Neurosci 21:3443-3456. Medline
60. Zhang TA, Placzek AN, Dani JA (2010) In vitro identification and electrophysiological characterization of dopamine neurons in the ventral tegmental area. Neuropharmacology 59:431-436. CrossRef Medline