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

European Journal of Neuroscience

Volumn 33, Issue 9, 2011, Pages 1622-1636

  Cucchiaroni, Maria L ^a   Freestone, Peter S ^a,b   Berretta, Nicola ^a   Viscomi, Maria T ^a   Bisicchia, Elisa ^a,c   Okano, Hideyuki ^d   Molinari, Marco ^a   Bernardi, Giorgio ^a,e   Lipski, Janusz ^b   Mercuri, Nicola B ^a,e   Guatteo, Ezia ^a  

^a IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

^c UNIVERSITY OF TERAMO   (Italy)

^d KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

D2 receptors; Dopamine; GABA; Glutamate; Patch clamp technique; TH GFP mouse

Indexed keywords

ALPHA ADRENERGIC RECEPTOR; DOPAMINE; DOPAMINE 2 RECEPTOR; DOPAMINE TRANSPORTER; GREEN FLUORESCENT PROTEIN; MESSENGER RNA; TYROSINE 3 MONOOXYGENASE; VESICULAR GLUTAMATE TRANSPORTER 2;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; COCULTURE; CONTROLLED STUDY; CORPUS STRIATUM; CULTURE TECHNIQUE; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; DOWN REGULATION; GENE EXPRESSION REGULATION; HYPERPOLARIZATION; IN VIVO STUDY; MESENCEPHALON; MOUSE; NEUROMODULATION; NEUROTRANSMITTER RELEASE; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SLOW INWARD CURRENT; SYNAPSE VESICLE;

ACTION POTENTIALS; ANIMALS; CELLS, CULTURED; COCULTURE TECHNIQUES; CORPUS STRIATUM; DOPAMINE; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; GLUTAMIC ACID; GREEN FLUORESCENT PROTEINS; MESENCEPHALON; MICE; MICE, TRANSGENIC; NEURONS; PATCH-CLAMP TECHNIQUES; RECEPTORS, ADRENERGIC, ALPHA-1; RECEPTORS, GABA-A; SODIUM CHANNEL BLOCKERS; SYNAPSES; SYNAPTIC TRANSMISSION; TETRODOTOXIN; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2;

EID: 79955548476     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2011.07659.x     Document Type: Article

References (77)

1. Adams, B.E., Reid, C.A., Myers, D., Ng, C., Powell, K., Phillips, A.M., Zheng, T., O'Brien, T.J. & Williams, D.A. (2009) Excitotoxic-mediated transcriptional decreases in HCN2 channel function increase network excitability in CA1. Exp. Neurol., 219, 249-257.
2. Akaike, A., Katsuki, H., Kume, T. & Maeda, T. (1999) Reactive oxygen species in NMDA receptor-mediated glutamate neurotoxicity. Parkinsonism Relat. Disord., 4, 203-207.
3. Augood, S.J., Westmore, K., McKenna, P.J. & Emson, P.C. (1993) Co-expression of dopamine transporter mRNA and tyrosine hydroxylase mRNA in ventral mesencephalic neurones. Brain Res. Mol. Brain Res., 20, 328-334.
4. Biel, M., Wahl-Schott, C., Michalakis, S. & Zong, X. (2009) Hyperpolarization-activated cation channels: from genes to function. Physiol. Rev., 89, 847-885.
5. Birgner, C., Nordenankar, K., Lundblad, M., Mendez, J.A., Smith, C., le Grevès, M., Galter, D., Olson, L., Fredriksson, A., Trudeau, L.E., Kullander, K. & Wallèn-Mackenzie, A. (2010) VGLUT2 in dopamine neurons is required for psycostimulant-induced behavioural activation. Proc. Natl. Acad. Sci. USA, 107, 389-394.
6. Bolte, S. & Cordelières, F.P. (2006) A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc., 224, 213-232.
7. Bourque, M.J. & Trudeau, L.E. (2000) GDNF enhances the synaptic efficacy of dopaminergic neurons in culture. Eur. J. Neurosci., 12, 3172-3180.
8. Bunney, B.S., Chiodo, L.A. & Grace, A.A. (1991) Midbrain dopamine system electrophysiological functioning: a review and new hypothesis. Synapse, 9, 79-94.
9. Cepeda, C. & Levine, M.S. (1998) Dopamine and N-methyl-d-aspartate receptor interactions in the neostriatum. Dev. Neurosci., 20, 1-18.
10. Cepeda, C., Buchwald, N.A. & Levine, M.S. (1993) Neuromodulatory actions of dopamine in the neostriatum are dependent upon the excitatory amino acid receptor subtypes activated. Proc. Natl. Acad. Sci. USA, 90, 9576-9580.
11. Cepeda, C., Colwell, C.S., Itri, J.N., Chandler, S.H. & Levine, M.S. (1998) Dopaminergic modulation of NMDA-induced whole cell currents in neostriatal neurons in slices: contribution of calcium conductances. J. Neurophysiol., 79, 82-94.
12. Cerruti, C., Walther, D.M., Kuhar, M.J. & Uhl, G.R. (1993) Dopamine transporter mRNA expression is intense in rat midbrain neurons and modest outside midbrain. Brain Res. Mol. Brain Res., 18, 181-186.
13. Chuhma, N., Choi, W.Y., Mingote, S. & Rayport, S. (2009) Dopamine neuron glutamate cotransmission: frequency-dependent modulation in the mesoventromedial projection. Neuroscience, 164, 1068-1083.
14. Ciliax, B.J., Heilman, C., Demchyshyn, L.L., Pristupa, Z.B., Ince, E., Hersch, S.M., Niznik, H.B. & Levey, A.I. (1995) The dopamine transporter: immunochemical characterization and localization in brain. J. Neurosci., 15, 1714-1723.
15. Dal Bo, G., St-Gelais, F., Danik, M., Williams, S., Cotton, M. & Trudeau, L.E. (2004) Dopamine neurons in culture express VGLUT2 explaining their capacity to release glutamate at synapses in addition to dopamine. J. Neurochem., 88, 1398-1405.
16. Dal Bo, G., Bérubé-Carrière, N., Mendez, J.A., Leo, D., Riad, M., Descarries, L., Lévesque, D. & Trudeau, L.E. (2008) Enhanced glutamatergic phenotype of mesencephalic dopamine neurons after neonatal 6-hydroxydopamine lesion. Neuroscience, 156, 59-70.
17. Franke, H., Schelhorn, N. & Illes, P. (2003) Dopaminergic neurons develop axonal projections to their target areas in organotypic co-cultures of the ventral mesencephalon and the striatum/prefrontal cortex. Neurochem. Int., 42, 431-439.
18. Franz, O., Liss, B., Neu, A. & Roeper, J. (2000) Single-cell mRNA expression of HCN1 correlates with a fast gating phenotype of hyperpolarization-activated cyclic nucleotide-gated ion channels (Ih) in central neurons. Eur. J. Neurosci., 12, 2685-2693.
19. 2+ homeostasis. Eur. J. Neurosci., 30, 1849-1859.
20. Fremeau, R.T., Voglmaier, S., Seal, R.P. & Edwards, R.H. (2004) VGLUTs define subsets of excitatory neurons and suggest novel roles for glutamate. Trends Neurosci., 27, 98-103.
21. Gähwiler, B., Capogna, M., Debanne, D., McKinney, R.A. & Thompson, S.M. (1997) Organotypic slice cultures: a technique has come of age. Trends Neurosci., 20, 471-477.
22. Grace, A.A. (1988) In vivo and in vitro intracellular recordings from rat midbrain dopamine neurons. Ann. N Y Acad. Sci., 537, 51-76.
23. Grace, A.A. (1992) The depolarization block hypothesis of neuroleptic action: implications for the etiology and treatment of schizophrenia. J. Neural Transm. Suppl., 36, 91-131.
24. Grace, A.A. & Bunney, B.S. (1986) Induction of depolarization block in midbrain dopamine neurons by repeated administration of haloperidol: analysis using in vivo intracellular recording. J. Pharmacol. Exp. Ther., 238, 1092-1100.
25. Grace, A.A., Bunney, B.S., Moore, H. & Todd, C.L. (1997) Dopamine-cell depolarization block as a model for the therapeutic actions of antipsychotic drugs. Trends Neurosci., 20, 31-37.
26. Gramsbergen, J., Sandberg, M., Møller Dall, A., Kornblit, B. & Zimmer, J. (2002) Glutathione depletion in nigrostriatal slice cultures: GABA loss, dopamine resistance and protection by the tetrahydrobiopterin precursor sepiapterin. Brain Res., 935, 47-58.
27. Grenhoff, J., North, R.A. & Johnson, S.W. (1995) Alpha 1-adrenergic effects on dopamine neurons recorded intracellularly in the rat midbrain slice. Eur. J. Neurosci., 7, 1707-1713.
28. Guatteo, E., Fusco, F.R., Giacomini, P., Bernardi, G. & Mercuri, N.B. (2000) The weaver mutation reverses the function of dopamine and GABA in mouse dopaminergic neurons. J. Neurosci., 20, 6013-6020.
29. Guatteo, E., Cucchiaroni, M.L., Freestone, P.S., Okano, H., Bernardi, G., Lipski, J. & Mercuri, N.B. (2007) Comparison of electrophysiological and pharmacological properties of identified dopaminergic neurons in acute vs. organotypic midbrain slices. Society for Neuroscience 37th Annual Meeting, 2007, San Diego, CA, USA, Abstract N. 893.5.
30. Hersch, S.M., Yi, H., Heilman, C.J., Edwards, R.H. & Levey, A.I. (1997) Subcellular localization and molecular topology of the dopamine transporter in the striatum and substantia nigra. J. Comp. Neurol., 388, 211-227.
31. Hnasko, T.S., Chuhma, N., Zhang, H., Goh, G.Y., Sulzer, D., Palmiter, R.D., Rayport, S. & Edwards, R.H. (2010) Vesicular glutamate transport promotes dopamine storage and glutamate corelease in vivo. Neuron, 65, 643-656.
32. Holmes, C., Jones, S.A. & Greenfield, S.A. (1995) The influence of target and non-target brain regions on the development of mid-brain dopaminergic neurons in organotypic slice culture. Brain Res. Dev. Brain Res., 88, 212-219.
33. Hummon, A.B., Lim, S.R., Difilippantonio, M.J. & Ried, T. (2007) Isolation and solubilization of proteins after TRIzol extraction of RNA and DNA from patient material following prolonged storage. BioTechniques, 42, 467-472.
34. Jakobsen, B., Gramsbergen, J.B., Møller Dall, A., Rosenblad, C. & Zimmer, J. (2005) Characterization of organotypic ventral mesencephalic cultures from embryonic mice and protection against MPP toxicity by GDNF. Eur. J. Neurosci., 21, 2939-2948.
35. Johnson, S.W. & North, R.A. (1992) Opioids excite dopamine neurons by hyperpolarization of local interneurons. J. Neurosci., 12, 483-488.
36. Jomphe, C., Bourque, M.J., Fortin, G.D., St-Gelais, F., Okano, H., Kobayashi, K. & Trudeau, L.E. (2005) Use of TH-EGFP transgenic mice as a source of identified dopaminergic neurons for physiological studies in postnatal cell culture. J. Neurosci. Methods, 146, 1-12.
37. Jung, A.B. & Bennett, J.P. (1996) Development of striatal dopaminergic function. I. Pre-and postnatal development of mRNAs and binding sites for striatal D1 (D1a) and D2(D2a) receptors. Brain Res. Dev. Brain Res., 94, 109-120.
38. Kashani, A., Betancur, C., Giros, B., Hirsch, E. & El Mestikawy, S. (2007) Altered expression of vesicular glutamate transporters VGLUT1 and VGLUT2 in Parkinson disease. Neurobiol. Aging, 28, 568-578.
39. Kawano, M., Kawasaki, A., Sakata-Haga, H., Fukui, Y., Kawano, H., Nogami, H. & Hisano, S. (2006) Particular subpopulations of midbrain and hypothalamic dopamine neurons express vesicular glutamate transporter 2 in the rat brain. J. Comp. Neurol., 498, 581-592.
40. Kearns, S.M., Scheffler, B., Goetz, A.K., Lin, D.D., Baker, H.D., Roper, S.N., Mandel, R.J. & Steindler, D.A. (2006) A method for a more complete in vitro Parkinson's model: slice culture bioassay for modeling maintenance and repair of the nigrostriatal circuit. J. Neurosci. Methods, 157, 1-9.
41. Kress, G. & Reynolds, I.J. (2005) Dopaminergic neurotoxins require excitotoxic stimulation in organotypic cultures. Neurobiol. Dis., 20, 639-645.
42. Lacey, M.G., Mercuri, N.B. & North, R.A. (1987) Dopamine acts on D2 receptors to increase potassium conductance in neurones of the rat substantia nigra zona compacta. J. Physiol., 392, 397-416.
43. Lacey, M.G., Mercuri, N.B. & North, R.A. (1988) On the potassium conductance increase activated by GABAB and dopamine D2 receptors in rat substantia nigra neurones. J. Physiol., 401, 437-453.
44. Lacey, M.G., Mercuri, N.B. & North, R.A. (1989) Two cell types in rat substantia nigra zona compacta distinguished by membrane properties and the actions of dopamine and opioids. J. Neurosci., 9, 1233-1241.
45. Larsen, T.R., Rossen, S. & Gramsbergen, J.B. (2008) Dopamine release in organotypic cultures of foetal mouse mesencephalon: effects of depolarizing agents, pargyline, nomifensine, tetrodotoxin and calcium. Eur. J. Neurosci., 28, 569-576.
46. Lavin, A., Nogueira, L., Lapish, C.C., Wightman, R.M., Phillips, P.E. & Seamans, J.K. (2005) Mesocortical dopamine neurons operate in distinct temporal domains using multimodal signaling. J. Neurosci., 25, 5013-5023.
47. Manders, E.M.M., Verbeek, F.J. & Aten, J.A. (1993) Measurement of colocalization of objects in dual-colour confocal images. J. Microsc., 169, 375-382.
48. Margolis, E.B., Lock, H., Hjelmstad, G.O. & Fields, H.L. (2006) The ventral tegmental area revisited: is there an electrophysiological marker for dopaminergic neurons? J. Physiol., 577 (Pt 3), 907-924.
49. Matsushita, N., Okada, H., Yasoshima, Y., Takahashi, K., Kiuchi, K. & Kobayashi, K. (2002) Dynamics of tyrosine hydroxylase promoter activity during midbrain dopaminergic neuron development. J. Neurochem., 82, 295-304.
50. Mendez, J.A., Bourque, M.J., Dal Bo, G., Bourdeau, M.L., Danik, M., Williams, S., Lacaille, J.C. & Trudeau, L.E. (2008) Developmental and target-dependent regulation of vesicular glutamate transporter expression by dopamine neurons. J. Neurosci., 28, 6309-6318.
51. Mercuri, N.B., Bonci, A., Calabresi, P., Stefani, A. & Bernardi, G. (1995) Properties of the hyperpolarization-activated cation current Ih in rat midbrain dopaminergic neurons. Eur. J. Neurosci., 7, 462-469.
52. Neuhoff, H., Neu, A., Liss, B. & Roeper, J. (2002) I(h) channels contribute to the different functional properties of identified dopaminergic subpopulations in the midbrain. J. Neurosci., 22, 1290-1302.
53. Paladini, C.A. & Williams, J.T. (2004) Noradrenergic inhibition of midbrain dopamine neurons. J. Neurosci., 24, 4568-4575.
54. Paladini, C.A., Fiorillo, C.D., Morikawa, H. & Williams, J.T. (2001) Amphetamine selectively blocks inhibitory glutamate transmission in dopamine neurons. Nat. Neurosci., 4, 275-281.
55. Plenz, D. & Kitai, S.T. (1998) Regulation of the nigrostriatal pathway by metabotropic glutamate receptors during development. J. Neurosci., 18, 4133-4144.
56. Richichi, C., Brewster, A.L., Bender, R.A., Simeone, T.A., Zha, Q., Yin, H.Z., Weiss, J.H. & Baram, T.Z. (2008) Mechanisms of seizure-induced 'transcriptional channelopathy' of hyperpolarization-activated cyclic nucleotide gated (HCN) channels. Neurobiol. Dis., 29, 297-305.
57. Rohrbacher, J., Ichinohe, N. & Kitai, S.T. (2000) Electrophysiological characteristics of substantia nigra neurons in organotypic cultures: spontaneous and evoked activities. Neuroscience, 97, 703-714.
58. Rommelfanger, K.S., Mitrano, D.A., Smith, Y. & Weinshenker, D. (2009) Light and electron microscopic localization of alpha-1 adrenergic receptor immunoreactivity in the rat striatum and ventral midbrain. Neuroscience, 158, 1530-1540.
59. Sawamoto, K., Nakao, N., Kakishita, K., Ogawa, Y., Toyama, Y., Yamamoto, A., Yamaguchi, M., Mori, K., Goldman, S.A., Itakura, T. & Okano, H. (2001) Generation of dopaminergic neurons in the adult brain from mesencephalic precursor cells labeled with a nestin-GFP transgene. J. Neurosci., 21, 3895-3903.
60. Sherer, T., Richardson, J.R., Testa, C.M., Seo, B.B., Panov, A.V., Yagi, T., Matsuno-Yagi, A., Miller, G.W. & Greenamyre, J.T. (2007) Mechanism of toxicity of pesticides acting at complex I: relevance to environmental etiologies of Parkinson's disease. J. Neurochem., 100, 1469-1479.
61. Shi, W.X., Pun, C.L., Zhang, X.X., Jones, M.D. & Bunney, B.S. (2000) Dual effects of d-amphetamine on dopamine neurons mediated by dopamine and nondopamine receptors. J. Neurosci., 20, 3504-3511.
62. Shimada, S., Kitayama, S., Walther, D. & Uhl, G. (1992) Dopamine transporter mRNA: dense expression in ventral midbrain neurons. Brain Res. Mol. Brain Res., 13, 359-362.
63. Shimizu, K., Matsubara, K., Ohtaki, K. & Shiono, H. (2003) Paraquat leads to dopaminergic neural vulnerability in organotypic midbrain culture. Neurosci. Res., 46, 523-532.
64. Snyder-Keller, A., Tseng, K.Y., Lyng, G.D., Graber, D.J. & O'Donnell, P. (2008) Afferent influences on striatal development in organotypic cocultures. Synapse, 62, 487-500.
65. Stahl, K., Skare, Ø. & Torp, R. (2009) Organotypic cultures as a model of Parkinson's disease. A twist to an old model. Sci. World J., 9, 811-821.
66. Steensen, B.H., Nedergaard, S., Ostergaard, K. & Lambert, J.D. (1995) Electrophysiological characterization of dopaminergic and non-dopaminergic neurones in organotypic slice cultures of the rat ventral mesencephalon. Exp. Brain Res., 106, 205-214.
67. Stuber, G.D., Hnasko, T.S., Britt, J.P., Edwards, R.H. & Bonci, A. (2010) Dopaminergic terminals in the nucleus accumbens but not the dorsal striatum corelease glutamate. J. Neurosci., 30, 8229-8233.
68. Sulzer, D., Joyce, M.P., Lin, L., Geldwert, D., Haber, S.N., Hattori, T. & Rayport, S. (1998) Dopamine neurons make glutamatergic synapses in vitro. J. Neurosci., 18, 4588-4602.
69. Takamori, S. (2006) VGLUTs: 'exciting' times for glutamatergic research? Neurosci. Res., 55, 343-351.
70. Tecuapetla, F., Patel, J.C., Xenias, H., English, D., Tadros, I., Shah, F., Berlin, J., Deisseroth, K., Rice, M.E., Tepper, J.M. & Koos, T. (2010) Glutamatergic signaling by mesolimbic dopamine neurons in the nucleus accumbens. J. Neurosci., 30, 7105-7110.
71. Testa, C.M., Sherer, T.B. & Greenamyre, J.T. (2005) Rotenone induces oxidative stress and dopaminergic neuron damage in organotypic substantia nigra cultures. Brain Res. Mol. Brain Res., 134, 109-118.
72. Tseng, K.Y., Snyder-Keller, A. & O'Donnell, P. (2007) Dopaminergic modulation of striatal plateau depolarizations in corticostriatal organotypic cocultures. Psychopharmacology (Berl), 191, 627-640.
73. Van der Kloot, W. (1991) The regulation of quantal size. Prog. Neurobiol., 36, 93-130.
74. Washio, H., Takigachi-Hayashi, K. & Konishi, S. (1999) Early postnatal development of substantia nigra neurons in rat midbrain slices: hyperpolarization-activated inward current and dopamine-activated current. Neurosci. Res., 34, 91-101.
75. Yamaguchi, T., Sheen, W. & Morales, M. (2007) Glutamatergic neurons are present in the rat ventral tegmental area. Eur. J. Neurosci., 25, 106-118.
76. Yung, W.H., Häusser, M.A. & Jack, J.J. (1991) Electrophysiology of dopaminergic and non-dopaminergic neurones of the guinea-pig substantia nigra pars compacta in vitro. J. Physiol., 436, 643-667.
77. Zhang, T.A., Placzek, A.N. & Dani, J.A. (2010) In vitro identification and electrophysiological characterization of dopamine neurons in the ventral tegmental area. Neuropharmacology, 59, 431-436.