Dual effects of l-DOPA on nigral dopaminergic neurons

Experimental Neurology

Volumn 247, Issue , 2013, Pages 582-594

  Guatteo, Ezia ^a   Yee, Andrew ^b   McKearney, James ^b   Cucchiaroni, Maria L ^a,c   Armogida, Marta ^a,c   Berretta, Nicola ^a   Mercuri, Nicola B ^a,c   Lipski, Janusz ^b  

^a IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

^c UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

Brain slice; Calcium; Dopamine; Electrophysiology; Rodents; Substantia nigra

Indexed keywords

4 AMINOBUTYRIC ACID B RECEPTOR; ALPHA 1 ADRENERGIC RECEPTOR; AMPA RECEPTOR; CALCIUM ION; DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; IONOTROPIC RECEPTOR; KAINIC ACID RECEPTOR; LEVODOPA; METABOTROPIC RECEPTOR 1;

ANIMAL TISSUE; ARTICLE; AUTOOXIDATION; BRAIN SLICE; CELL SURVIVAL; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DRUG MECHANISM; EVOKED RESPONSE; MICROFLUOROMETRY; MOUSE; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL STIMULATION; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; RAT; STIMULUS RESPONSE; UPREGULATION;

2,4,5-TRIHYDROXYPHENYLALANINE; AADC; ACSF; AROMATIC L-AMINO ACID DECARBOXYLASE; ARTIFICIAL CEREBRO-SPINAL FLUID; BRAIN SLICE; CALCIUM; CPA; CYCLOPIAZONIC ACID; DA; DAT; DOPAMINE; DOPAMINE TRANSPORTER; ELECTROPHYSIOLOGY; ENDOPLASMIC RETICULUM; ER; PARKINSON'S DISEASE; PD; RODENTS; SEPSC; SNC; SNR; SPONTANEOUS EXCITATORY POSTSYNAPTIC CURRENT; STN; SUBSTANTIA NIGRA; SUBSTANTIA NIGRA PARS COMPACTA; SUBSTANTIA NIGRA PARS RETICULATA; SUBTHALAMIC NUCLEUS; TETRODOTOXIN; TOPA; TTX;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; CALCIUM; DOPAMINE AGENTS; DOPAMINERGIC NEURONS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; ELECTRIC STIMULATION; EXCITATORY AMINO ACID AGENTS; LEVODOPA; MICE; PATCH-CLAMP TECHNIQUES; RATS; RATS, WISTAR; SUBSTANTIA NIGRA; TIME FACTORS;

EID: 84881368865     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2013.02.009     Document Type: Article

References (83)

1. Aghajanian G.K., Bunney B.S. Dopamine autoreceptors: pharmacological characterization by microiontophoretic single cell recording studies. Naunyn Schmiedebergs Arch. Pharmacol. 1977, 297:1-7.
2. Aizenman E., White W.F., Loring R.H., Rosenberg P.A. A 3,4-dihydroxyphenylalanine oxidation product is a non-N-methyl-d-aspartate glutamatergic agonist in rat cortical neurons. Neurosci. Lett. 1990, 116:168-171.
3. Amini B., Clark J.W., Canavier C.C. Calcium dynamics underlying pacemaker-like and burst firing oscillations in midbrain dopaminergic neurons: a computational study. J. Neurophysiol. 1999, 82:2249-2261.
4. Andreassen O.A., Ferrante R.J., Aamo T.O., Beal M.F., Jørgensen H.A. Oral dyskinesias and histopathological alterations in substantia nigra after long-term haloperidol treatment of old rats. Neuroscience 2003, 122:717-725.
5. Bernardini G.L., Speciale S.G., German D.C. Increased midbrain dopaminergic cell activity following 2'CH3-MPTP-induced dopaminergic cell loss: an in vitro electrophysiological study. Brain Res. 1990, 527:123-129.
6. Biscoe T.J., Evans R.H., Headley P.M., Martin M.R., Watkins J.C. Structure-activity relations of excitatory amino acids on frog and rat spinal neurones. Br. J. Pharmacol. 1976, 58:373-382.
7. Brodin L., Grillner S., Rovainen C.M. N-Methyl-D-aspartate (NMDA), kainate and quisqualate receptors and the generation of fictive locomotion in the lamprey spinal cord. Brain Res. 1985, 325:302-306.
8. Cha J.H., Dure L.S., Sakurai S.Y., Penney J.B., Young A.B. 2,4,5-Trihydroxyphenylalanine (6-hydroxy-dopa) displaces [3H]AMPA binding in rat striatum. Neurosci. Lett. 1991, 132:55-58.
9. 2+]c dynamics in spontaneously firing dopamine neurons of the rat substantia nigra pars compacta. J. Cell Sci. 2003, 116:2665-2675.
10. Chung K.K., Freestone P.S., Lipski J. Expression and functional properties of TRPM2 channels in dopaminergic neurons of the substantia nigra of the rat. J. Neurophysiol. 2011, 106:2865-2875.
11. Cohen G. Monoamine oxidase, hydrogen peroxide, and Parkinson's disease. Adv. Neurol. 1987, 45:119-125.
12. Cucchiaroni M.L., Freestone P.S., Berretta N., Viscomi M.T., Bisicchia E., Okano H., Molinari M., Bernardi G., Lipski J., Mercuri N.B., Guatteo E. Properties of dopaminergic neurons in organotypic mesencephalic-striatal co-cultures: evidence for a facilitatory effect of dopamine on the glutamatergic input mediated by α-1 adrenergic receptors. Eur. J. Neurosci. 2011, 33:1622-1636.
13. Dawson T.M., Dawson V.L. Molecular pathways of neurodegeneration in Parkinson's disease. Science 2003, 302:819-822.
14. De March Z., Giampà C., Patassini S., Bernardi G., Fusco F.R. Cellular localization of TRPC5 in the substantia nigra of rat. Neurosci. Lett. 2006, 402:35-39.
15. Double K.L., Reyes S., Werry E.L., Halliday G.M. Selective cell death in neurodegeneration: why are some neurons spared in vulnerable regions?. Prog. Neurobiol. 2010, 92:316-329.
16. Drion G., Massotte L., Sepulchre R., Seutin V. How modeling can reconcile apparently discrepant experimental results: the case of pacemaking in dopaminergic neurons. PLoS Comput. Biol. 2011, 7:1-14.
17. Durán-Ferreras E., Chacón-Peña J.R., Durán-Quintana J.A. The role of olanzapine in Parkinsonian dopaminergic psychosis. Rev. Neurol. 2002, 35:691-696.
18. + channel by stimulation of glutamate phosphoinositide-coupled receptors in cultured cerebellar granule cells. Eur. J. Neurosci. 1991, 3:778-789.
19. Federici M., Natoli S., Bernardi G., Mercuri N.B. Dopamine selectively reduces GABA(B) transmission onto dopaminergic neurones by an unconventional presynaptic action. J. Physiol. 2002, 540:119-128.
20. Foubert-Samier A., Helmer C., Perez F., Le Goff M., Auriacombe S., Elbaz A., Dartigues J.F., Tison F. Past exposure to neuroleptic drugs and risk of Parkinson disease in an elderly cohort. Neurology 2012, 79:1615-1621.
21. 2+ homeostasis. Eur. J. Neurosci. 2009, 30:1849-1859.
22. Friedman J.H., Factor S.A. Atypical antipsychotics in the treatment of drug-induced psychosis in Parkinson's disease. Mov. Disord. 2000, 15:201-211.
23. Furukawa N., Arai N., Goshima Y., Miyamae T., Ohshima E., Suzuki F., Fujita K., Misu Y. Endogenously released DOPA is a causal factor for glutamate release and resultant delayed neuronal cell death by transient ischemia in rat striata. J. Neurochem. 2001, 76:815-824.
24. Garrido M., Tereshchenko Y., Zhevtsova Z., Taschenberger G., Bähr M., Kügler S. Glutathione depletion and overproduction both initiate degeneration of nigral dopaminergic neurons. Acta Neuropathol. 2011, 121:475-485.
25. Grace A.A., Bunney B.S. Induction of depolarization block in midbrain dopamine neurons by repeated administration of haloperidol: analysis using in vivo intracellular recording. J. Pharmacol. Exp. Ther. 1986, 238:1092-1100.
26. Greengard P. The neurobiology of slow synaptic transmission. Science 2001, 294:1024-1030.
27. Grynkiewicz G., Poenie M., Tsien R.Y. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 1985, 260:3440-3450.
28. Guatteo E., Mercuri N.B., Bernardi G., Knöpfel T. Group I metabotropic glutamate receptors mediate an inward current in rat substantia nigra dopamine neurons that is independent from calcium mobilization. J. Neurophysiol. 1999, 82:1974-1981.
29. Guatteo E., Bengtson C.P., Bernardi G., Mercuri N.B. Voltage-gated calcium channels mediate intracellular calcium increase in weaver dopaminergic neurons during stimulation of D2 and GABAB receptors. J. Neurophysiol. 2004, 92:3368-3374.
30. Guatteo E., Chung K.K., Bowala T.K., Bernardi G., Mercuri N.B., Lipski J. Temperature sensitivity of dopaminergic neurons of the substantia nigra pars compacta: involvement of transient receptor potential channels. J. Neurophysiol. 2005, 94:3069-3080.
31. Guatteo E., Cucchiaroni M.L., Sebastianelli L., Bernardi G., Mercuri N.B. The midbrain slice preparation. An in vitro model to select potential anti-parkinsonian drugs?. Parkinsonism Relat. Disord. 2008, 14(Suppl. 2):S150-S153.
32. Guzman J.N., Sánchez-Padilla J., Chan C.S., Surmeier D.J. Robust pacemaking in substantia nigra dopaminergic neurons. J. Neurosci. 2009, 29:11011-11019.
33. Han P., Nakanishi S.T., Tran M.A., Whelan P.J. Dopaminergic modulation of spinal neuronal excitability. J. Neurosci. 2007, 27:13192-13204.
34. Hastings T.G. The role of dopamine oxidation in mitochondrial dysfunction: implications for Parkinson's disease. J. Bioenerg. Biomembr. 2009, 41:469-472.
35. Ingram S.L., Prasad B.M., Amara S.G. Dopamine transporter-mediated conductances increase excitability of midbrain dopamine neurons. Nat. Neurosci. 2002, 5:971-978.
36. Jomphe C., Bourque M.J., Fortin G.D., St-Gelais F., Okano H., Kobayashi K., Trudeau L.E. Use of TH-EGFP transgenic mice as a source of identified dopaminergic neurons for physiological studies in postnatal cell culture. J. Neurosci. Methods 2005, 146:1-12.
37. Kim S.H., Choi Y.M., Jang J.Y., Chung S., Kang Y.K., Park M.K. Nonselective cation channels are essential for maintaining intracellular Ca2+ levels and spontaneous firing activity in the midbrain dopamine neurons. Pflugers Arch. 2007, 455:309-321.
38. Konitsiotis S., Blanchet P.J., Verhagen L., Lamers E., Chase T.N. AMPA receptor blockade improves levodopa-induced dyskinesia in MPTP monkeys. Neurology 2000, 54:1589-1595.
39. Kostrzewa R.M., Harper J.W. Comparison of the neonatal effects of 6-hydroxydopa and 6-hydroxydopamine on growth and development of central ctecholaminergic neurins. Chemical Tools in Catecholamine Research 1975, vol. 1:181-196. North-Holland, Amsterdam. G. Jonsson, T. Malmfors, C. Sachs (Eds.).
40. Lacey M.G., Mercuri N.B., North R.A. Dopamine acts on D2 receptors to increase potassium conductance in neurones of the rat substantia nigra zona compacta. J. Physiol. 1987, 392:397-416.
41. Lacey M.G., Mercuri N.B., North R.A. Two cell types in rat substantia nigra zona compacta distinguished by membrane properties and the actions of dopamine and opioids. J. Neurosci. 1989, 9:1233-1241.
42. Lee C.R., Witkovsky P., Rice M.E. Regulation of substantia nigra pars reticulata GABAergic neuron activity by H[U+2082]O[U+2082] via flufenamic acid-sensitive channels and K(ATP) channels. Front. Syst. Neurosci. 2011, 5:1-12.
43. Li X., Qi J., Yamaguchi T., Wang H.L., Morales M. Heterogeneous composition of dopamine neurons of the rat A10 region: molecular evidence for diverse signaling properties. Brain Struct. Funct. 2012, (Aug 29, [Epub ahead of print]).
44. Lin J.Y., van Wyk M., Bowala T.K., Teo M.Y., Lipski J. Dendritic projections and dye-coupling in dopaminergic neurons of the substantia nigra examined in horizontal brain slices from young rats. J. Neurophysiol. 2003, 90:2531-2535.
45. Lipski J., Nistico R., Berretta N., Guatteo E., Bernardi G., Mercuri N.B. l-DOPA: a scapegoat for accelerated neurodegeneration in Parkinson's disease?. Prog. Neurobiol. 2011, 94:389-407.
46. Lüscher C., Slesinger P.A. Emerging roles for G protein-gated inwardly rectifying potassium (GIRK) channels in health and disease. Nat. Rev. Neurosci. 2010, 11:301-315.
47. Margolis E.B., Mitchell J.M., Ishikawa J., Hjelmstad G.O., Fields H.L. Midbrain dopamine neurons: projection target determines action potential duration and dopamine D(2) receptor inhibition. J. Neurosci. 2008, 28:8908-8913.
48. Marinelli S., Federici M., Giacomini P., Bernardi G., Mercuri N.B. Hypoglycemia enhances ionotropic but reduces metabotropic glutamate responses in substantia nigra dopaminergic neurons. J. Neurophysiol. 2001, 85:1159-1166.
49. Mena M.A., Pardo B., Paino C.L., De Yebenes J.G. Levodopa toxicity in foetal rat midbrain neurones in culture: modulation by ascorbic acid. Neuroreport 1993, 4:438-440.
50. Mena M.A., Casarejos M.J., Solano R.M., de Yébenes J.G. Half a century of l-DOPA. Curr. Top. Med. Chem. 2009, 9:880-893.
51. Mercuri N.B., Calabresi P., Bernardi G. Responses of rat substantia nigra compacta neurones to l-DOPA. Br. J. Pharmacol. 1990, 100:257-260.
52. Mercuri N.B., Calabresi P., Bernardi G. Dopamine uptake inhibition potentiates the effects of l-DOPA on rat substantia nigra zona compacta neurons. Neurosci. Lett. 1991, 126:79-82.
53. Michel P.P., Hefti F. Toxicity of 6-hydroxydopamine and dopamine for dopaminergic neurons in culture. J. Neurosci. Res. 1990, 26:428-435.
54. Misu Y., Kitahama K., Goshima Y. l-3,4-Dihydroxyphenylalanine as a neurotransmitter candidate in the central nervous system. Pharmacol. Ther. 2003, 97:117-137.
55. Miyazaki I., Asanuma M., Kikkawa Y., Takeshima M., Murakami S., Miyoshi K., Sogawa N., Kita T. Astrocyte-derived metallothionein protects dopaminergic neurons from dopamine quinone toxicity. Glia 2011, 59:435-451.
56. Morikawa H., Paladini C.A. Dynamic regulation of midbrain dopamine neuron activity: intrinsic, synaptic, and plasticity mechanisms. Neuroscience 2011, 198:95-111.
57. Mosharov E.V., Larsen K.E., Kanter E., Phillips K.A., Wilson K., Schmitz Y., Krantz D.E., Kobayashi K., Edwards R.H., Sulzer D. Interplay between cytosolic dopamine, calcium, and alpha-synuclein causes selective death of substantia nigra neurons. Neuron 2009, 62:218-229.
58. Mrejeru A., Wei A., Ramirez J.M. Calcium-activated non-selective cation currents are involved in generation of tonic and bursting activity in dopamine neurons of the substantia nigra pars compacta. J. Physiol. 2011, 589:2497-2514.
59. Mytilineou C., Walker R.H., JnoBaptiste R., Olanow C.W. Levodopa is toxic to dopamine neurons in an in vitro but not an in vivo model of oxidative stress. J. Pharmacol. Exp. Ther. 2003, 304:792-800.
60. Newcomer T.A., Rosenberg P.A., Aizenman E. Iron-mediated oxidation of 3,4-dihydroxyphenylalanine to an excitotoxin. J. Neurochem. 1995, 64:1742-1748.
61. Olanow C.W., Stern M.B., Sethi K. The scientific and clinical basis for the treatment of Parkinson disease (2009). Neurology 2009, 72(Suppl. 4):S1-S136.
62. Olney J.W., Zorumski C.F., Stewart G.R., Price M.T., Wang G.J., Labruyere J. Excitotoxicity of l-dopa and 6-OH-dopa: implications for Parkinson's and Huntington's diseases. Exp. Neurol. 1990, 108:269-272.
63. Paladini C.A., Fiorillo C.D., Morikawa H., Williams J.T. Amphetamine selectively blocks inhibitory glutamate transmission in dopamine neurons. Nat. Neurosci. 2001, 4:275-281.
64. Pedarzani P., Storm J.F. Dopamine modulates the slow Ca(2+)-activated K+ current IAHP via cyclic AMP-dependent protein kinase in hippocampal neurons. J. Neurophysiol. 1995, 74:2749-2753.
65. Rosenberg P.A., Loring R., Xie Y., Zaleskas V., Aizenman E. 2,4,5-trihydroxyphenylalanine in solution forms a non-N-methyl-d-aspartate glutamatergic agonist and neurotoxin. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:4865-4869.
66. Ruffieux A., Schultz W. Dopaminergic activation of reticulata neurones in the substantia nigra. Nature 1980, 285:240-241.
67. Schapira A.H. Mitochondria in the aetiology and pathogenesis of Parkinson's disease. Lancet Neurol. 2008, 7:97-109.
68. Schapira A.H., Emre M., Jenner P., Poewe W. Levodopa in the treatment of Parkinson's disease. Eur. J. Neurol. 2009, 16:982-989.
69. Schotland J., Shupliakov O., Wikström M., Brodin L., Srinivasan M., You Z.B., Herrera-Marschitz M., Zhang W., Hökfelt T., Grillner S. Control of lamprey locomotor neurons by colocalized monoamine transmitters. Nature 1995, 374:266-268.
70. Sebastianelli L., Ledonne A., Marrone M.C., Bernardi G., Mercuri N.B. The L-amino acid carrier inhibitor 2-aminobicyclo[2.2.1]heptane-2-carboxylic acid (BCH) reduces L-dopa-elicited responses in dopaminergic neurons of the substantia nigra pars compacta. Exp. Neurol. 2008, 212:230-233.
71. Surmeier D.J., Guzman J.N., Sanchez-Padilla J. Calcium, cellular aging, and selective neuronal vulnerability in Parkinson's disease. Cell Calcium 2010, 47:175-182.
72. Surmeier D.J., Guzman J.N., Sanchez-Padilla J., Schumacker P.T. The role of calcium and mitochondrial oxidant stress in the loss of substantia nigra pars compacta dopaminergic neurons in Parkinson's disease. Neuroscience 2011, 198:221-231.
73. Takahashi N., Kozai D., Kobayashi R., Ebert M., Mori Y. Roles of TRPM2 in oxidative stress. Cell Calcium 2011, 50:279-287.
74. Tepper J.M., Sawyer S.F., Groves P.M. Electrophysiologically identified nigral dopaminergic neurons intracellularly labeled with HRP: light-microscopic analysis. J. Neurosci. 1987, 7:2794-2806.
75. Ting S. Liquid chromatographic determination of levodopa, levodopa-carbidopa, and related impurities in solid dosage forms. J. Assoc. Off. Anal. Chem. 1986, 69:169-173.
76. Tofighy A., Abbott A., Centonze D., Cooper A.J., Noor E., Pearce S.M., Puntis M., Stanford I.M., Wigmore M.A., Lacey M.G. Excitation by dopamine of rat subthalamic nucleus neurones in vitro-a direct action with unconventional pharmacology. Neuroscience 2003, 116:157-166.
77. Werkman T.R., Kruse C.G., Nievelstein H., Long S.K., Wadman W.J. In vitro modulation of the firing rate of dopamine neurons in the rat substantia nigra pars compacta and the ventral tegmental area by antipsychotic drugs. Neuropharmacology 2001, 40:927-936.
78. Yamamoto S., Takahashi N., Mori Y. Chemical physiology of oxidative stress-activated TRPM2 and TRPC5 channels. Prog. Biophys. Mol. Biol. 2010, 103:18-27.
79. Zhang T.A., Hendricson A.W., Morrisett R.A. Dual synaptic sites of D(1)-dopaminergic regulation of ethanol sensitivity of NMDA receptors in nucleus accumbens. Synapse 2005, 58:30-44.
80. Zhou F.W., Jin Y., Matta S.G., Xu M., Zhou F.M. An ultra-short dopamine pathway regulates basal ganglia output. J. Neurosci. 2009, 29:10424-10435.
81. Zhu Z., Bartol M., Shen K., Johnson S.W. Excitatory effects of dopamine on subthalamic nucleus neurons: in vitro study of rats pretreated with 6-hydroxydopamine and levodopa. Brain Res. 2002, 945:31-40.
82. Zhu Z.T., Shen K.Z., Johnson S.W. Pharmacological identification of inward current evoked by dopamine in rat subthalamic neurons in vitro. Neuropharmacology 2002, 42:772-781.
83. Zigmond M.J., Hastings T.G., Perez R.G. Increased dopamine turnover after partial loss of dopaminergic neurons: compensation or toxicity?. Parkinsonism Relat. Disord. 2002, 8:389-393.