Dopamine specifically inhibits forebrain neural stem cell proliferation, suggesting a novel effect of antipsychotic drugs

Journal of Neuroscience

Volumn 25, Issue 24, 2005, Pages 5815-5823

  Kippin, Tod E ^a,c   Kapur, Shitij ^b   Van Der Kooy, Derek ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Dopamine; Dopamine receptor; Haloperidol; Neurogenesis; Neuronal progenitor cell; Proliferation; Stem cells

Indexed keywords

2,3,4,5 TETRAHYDRO 7,8 DIHYDROXY 1 PHENYL 1H 3 BENZAZEPINE; DOMPERIDONE; DOPAMINE; DOPAMINE 2 RECEPTOR; DOPAMINE 2 RECEPTOR BLOCKING AGENT; DOPAMINE RECEPTOR; GENOMIC DNA; HALOPERIDOL; NEUROLEPTIC AGENT; QUINPIROLE; RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DOPAMINERGIC SYSTEM; DRUG EFFECT; FEMALE; FOREBRAIN; GROWTH INHIBITION; MALE; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PSYCHOPHARMACOLOGY; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; ANTIPSYCHOTIC AGENTS; CELL DIVISION; DOPAMINE; FEMALE; HALOPERIDOL; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS; PROSENCEPHALON; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, DOPAMINE D3; STEM CELLS;

EID: 20544452612     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1120-05.2005     Document Type: Article

References (66)

1. Andersson C, Hamerm RM, Lawlerm CP, Mailman RB, Lieberman JA (2002) Striatal volume changes in the rat following long-term administration of typical and atypical antipsychotic drugs. Neuropsychopharmacology 27:143-151.
2. Asa SL, Kelly MA, Grandy DK, Low MJ (1999) Pituitary lactotroph adenomas develop after prolonged lactotroph hyperplasia in dopamine D2 receptor-deficient mice. Endocrinology 140:5348-5355.
3. Baker SA, Baker KA, Hagg T (2004) Dopaminergic nigrostriatal projections regulate neural precursor proliferation in the adult mouse subventricular zone. Eur J Neurosci 20:575-579.
4. Benes FM, Paskevich PA, Davidson J, Bomesick VB (1985) The effects of haloperidol on synaptic patterns in the rat striatum. Brain Res 329:265-274.
5. Benraiss A, Chmielnicki E, Lerner K, Roh D, Goldman SA (2001) Adenoviral brain-derived neurotrophic factor induces both neostriatal and olfactory neuronal recruitment from endogenous progenitor cells in the adult forebrain. J Neurosci 21:6718-6731.
6. Chakos MH, Lieberman JA, Bilder RM, Borenstein M, Lerner G, Bogerts B, Wu H, Kinon B, Ashtari M (1994) Increase in caudate nuclei volumes of first-episode schizophrenic patients taking antipsychotic drugs. Am J Psychiatry 15:1430-1436.
7. Chakos MH, Shirakawa O, Lieberman J, Lee H, Bilder R, Tamminga CA (1998) Striatal enlargement in rats chronically treated with neuroleptic. Biol Psychiatry 44:675-684.
8. Craig CG, Tropepe V, Morshead CM, Reynolds BA, Weiss S, van der Kooy D (1996) In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J Neurosci 16:2649-2658.
9. Dawirs RR, Hildebrandt K, Teuchert-Noodt G (1998) Adult treatment with haloperidol increases dentate granule cell proliferation in the gerbil hippocampus. J Neural Transm 105:317-327.
10. Deisseroth K, Singla S, Toda H, Monje M, Palmer TD, Malenka RC (2004) Excitation-neurogenesis coupling in adult neural stem/progenitor cells. Neuron 42:535-552.
11. Duman RS, Nakagawa S, Malberg J (2001) Regulation of adult neurogenesis by antidepressant treatment. Neuropsychopharmacology 25:836-844.
12. Frielingsdorf H, Schwarz K, Brundin P, Mohapel P (2004) No evidence for new dopaminergic neurons in the adult mammalian substantia nigra. Proc Natl Acad Sci USA 101:10177-10182.
13. Gage FH (2000) Mammalian neural stem cells. Science 287:1433-1438.
14. Gur RE, Cowell P, Turetsky BI, Gallacher F, Cannon T, Bilker W, Gur RC (1998) A follow-up magnetic resonance imaging study of schizophrenia: relationship of neuroanatomical changes to clinical and neurobehavioral measures. Arch Gen Psychiatry 55:145-152.
15. Halim ND, Weichert CS, McClintock BW, Weinberger DR, Lipska BK (2004) Effects of chronic haloperidol and clozapine treatment on neurogenesis in the adult rat hippocampus. Neuropsychopharmacology 29:1063-1069.
16. Harrison PJ (1999) The neuropathological effects of antipsychotic drugs. Schizoprhenia Res 40:87-99.
17. Hitoshi S, Alexson T, Tropepe V, Donoviel D, Elia AJ, Nye JS, Conlon RA, Mak TW, Bernstein A, van der Kooy D (2002) Notch pathway molecules are essential for the maintenance, but not the generation, of mammalian neural stem cells. Genes Dev 16:846-858.
18. Hoglinger GU, Rizk P, Muriel MP, Duyckaerts C, Oertel WH, Caille I, Hirsch EC (2004) Dopamine depletion impairs precursor cell proliferation in Parkinson disease. Nat Neurosci 7:726-735.
19. Iaccarino C, Samad TA, Mathis C, Kercret H, Piceti R, Borrelli E (2002) Control of lactotrop proliferation by dopamine: Essential role of signaling through D2 receptors and ERKs. Proc Natl Acad Sci USA 99:14530-14535.
20. Ingham, CA, Hood, SH, van Maldegen, B, Weenink, A, Arbuthnott, GW (1993) Morphological changes in the rat neostriatum after unilateral 6-hyproxydopamine injections into the nigrostriatal pathway. Exp Brain Res 93:17-27.
21. Ingham CA, Hood SH, Taggart P, Arbuthnott GW (1998) Plasticity of synapses in the rat neostriatum after unilateral lesion of the nigrostriatal dopaminergic pathway. J Neurosci 18:4732-4743.
22. Jeste DV, Lohr JB, Eastham JH, Rockwell E, Caligiuri MP (1998) Adverse neurobiological effects of long-term use of neuroleptics: human and animal studies. J Psychiatr Res 32:201-214.
23. Kapur S, Remington G (2001) Dopamine D2 receptors and their role in atypical antipsychotic action: still necessary and may even be sufficient. Biol Psychiatry 50:873-883.
24. Kapur S, Seeman P (2001) Does fast dissociation from the dopamine D2 receptor explain the action of atypical antipsychotics?: a new hypothesis. Am J Psychiatry 158:360-369.
25. Kapur S, Zipurshk R, Jones C, Remington G, Houle S (2000) Relationship between dopamine D(2) occupancy, clinical response, and side effects: a double-blind PET study of first-episode schizophrenia. Am J Psychiatry 157:514-520.
26. Kapur S, VanderSpek SC, Brownlee BA, Nobrega JN (2003) Antipsychotic dosing in preclinical models is often unrepresentative of clinical condition-a suggested solution based on in vivo occupancy. J Pharmacol Exp Ther 305:625-631.
27. Kay JN, Blum M (2000) Differential response of ventral midbrain and striatal progenitor cells to lesions of the nigrostriatal dopaminergic projection. Dev Neurosci 22:56-67.
28. Kelley MA, Rubinstein M, Asa S, Zhang G, Saez C, Bunzow JR, Allen R, Hnasko R, Ben-Honathan N, Grandy DK, Low MJ (1997) Pituitary lactotroph hyperplasia and chronic hyperprolactinemia in dopamine D2 receptor-deficient mice. Neuron 19:103-113.
29. Kerns JM, Sierins DK, Kao LC, Klawans HL, Carvey PM (1992) Synaptic plasticity in the rat striatum following chronic haloperidol treatment. Clin Neuropharmacol 15:488-500.
30. Keshavan MS, Bagwell WW, Haas GL, Sweeney JA, Schooler NR, Pettegrew JW (1994) Changes in caudate volume with neuroleptic treatment. Lancet 344:1434.
31. Konradi C, Heckers S (2001) Antipsychotic drugs and neuroplastidty: Insights into the treatment and neurobiology of schizophrenia. Biol Psychiatry 50:729-742.
32. Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264:1145-1148.
33. Luskin MB (1994) Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11:173-189.
34. Malberg JE, Duman RS (2003) Cell proliferation in adult hippocampus is decreased by inescapable stress: reversal by fluoxetine treatment. Neuropsychopharmacology 28:1562-1571.
35. Malberg JE, Eisch AJ, Nestler EJ, Duman RS (2000) Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 20:9104-9110.
36. Mao L, Wang JQ (2001) Gliogenesis in the striatum of the adult rat: alteration in neural progenitor population after psychostimulant exposure. Dev Brain Res 130:41-51.
37. Mao L, Wang JQ (2003) Adult neural stem/progenitor cells in neurodegenerative repair. Sheng Li Xue Bao 55:233-244.
38. Mao L, Lau YS, Petroske E, Wang JQ (2001) Profound astrogenesis in the striatum of adult mice following nigrostriatal dopaminergic lesion by repeated MPTP administration. Brain Res Dev Brain Res 131:57-65.
39. Martens DJ, Tropepe V, van Der Kooy D (2000) Separate proliferation kinetics of fibroblast growth factor-responsive and epidermal growth factor-responsive neural stem cells within the embryonic forebrain germinal zone. J Neurosci 20:1085-1095.
40. Martens DJ, Seaberg RM, van der Kooy D (2002) In vivo infusions of exogenous growth factors into the fourth ventricle of the adult mouse brain increase the proliferation of neural progenitors around the fourth ventricle and central canal of the spinal cord. Eur J Neurosci 16:1045-1057.
41. Meshul CK, Casey DE (1989) Regional, reversible ultrastructural changes in rat brain with chronic neuroleptic treatment. Brain Res 489:338-346.
42. Morshead CM, van der Kooy D (1992) Postmitotic death is the fate of constitutively proliferating cells in the subependymal layer of the adult mouse brain. J Neurosci 12:249-256.
43. Morshead CM, Reynolds BA, Craig CG, McBurney MW, Staines WA, Morassutti D, Weiss S, van der Kooy D (1994) Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron 13:1071-1082.
44. Morshead CM, Craig CG, van der Kooy D (1998) In vivo clonal analyses reveal the properties of endogenous neural stem cell proliferation in the adult mammalian forebrain. Development 125:2251-2261.
45. Morshead CM, Garcia AD, Sofroniew MV, van Der Kooy D (2003) The ablation of glial fibrillary acidic protein-positive cells from the adult central nervous system results in the loss of forebrain neural stem cells but not retinal stem cells. Eur J Neurosci 18:76-84.
46. Nagatsu T, Mogi M, Ichinose H, Togari A (2000) Changes in cytokines and neurotrophins in Parkinson's disease. J Neural Transm Suppl 60:277-290.
47. Nakajima K, Hida H, Shimano Y, Fujimoto I, Hashitani T, Kumazaki M, Sakurai T, Nishino H (2001) GDNF is a major component of trophic activity in DA-depleted striatum for survival and neurite extension of DAergic neurons. Brain Res 916:76-84.
48. Nitsch C, Riesenberg R (1995) Synaptic reorganization in the rat striatum after dopaminergic deafferentation: an ultrastructural study using glutamate decarboxylase immunocytochemistry. Synapse 19:247-263.
49. Nyberg S, Farde L (2000) Non-equipotent doses partly explain difference among antipsychotics-implications of PET studies. Psychopharmacology 148:22-23.
50. Ohtani N, Goto T, Waeber C, Bhide PG (2003) Dopamine modulates cell cycle in the lateral ganglionic eminence. J Neurosci 23:2840-2850.
51. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. New York: Academic.
52. Pencea V, Bingaman KD, Wiegand SJ, Luskin MB (2001) Infusion of brain-derived neurotrophic factor into the lateral ventricle of the adult rat leads to new neurons in the parenchyma of the striatum, septum, thalamus, and hypothalamus. J Neurosci 21:6706-6717.
53. Reynolds BA, Weiss S (1996) Clonal population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev Biol 175:1-13.
54. Saiardi A, Bozzi Y, Bail JH, Borrelli E (1997) Antiproliferative role of dopamine: loss of D2 receptors causes hormonal dysfunction and pituitary hyperplasia. Neuron 19:115-126.
55. Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S, Weisstaub N, Lee J, Duman R, Arancio O, Belzung C, Hen R (2003) Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301:805-809.
56. Schmitt A, Weber S, Jatzko A, Braus DF, Henn FA (2004) Hippocampal volume and cell proliferation after acute and chronic clozapine or haloperidol treatment. J Neural Transm 111:91-100.
57. Seaberg RM, van der Kooy D (2003) Stem and progenitor cells: the premature desertion of rigorous definitions. Trends Neurosci 26:125-131.
58. Seeman P (2002) Atypical antipsychotics: mechanism of action. Can J Psychiatry 47:27-38.
59. Uranova NA, Orlovskawa DD, Apel K, Kintzova AJ, Haselhorst U, Schenk H (1991) Morphometric study of synaptic patterns in the rat caudate nucleus and hippocampus under haloperidol treatment. Synapse 7:253-259.
60. van der Kooy D, Weiss S (2000) Why stem cells? Science 287:1439-1441.
61. Van Kampen JM, Hagg T, Robertson HA (2004) Induction of neurogenesis in the adult rat subventricular zone and neostriatum following dopamine D receptor stimulation. Eur J Neurosci 19:2377-2387.
62. Wakade CG, Mahadik SP, Waller JL, Chiu F-C (2002) Atypical neuroleptics stimulate neurogenesis in adult rat brain. J Neurosci Res 69:72-79.
63. Wang H-D, Dunnavant FD, Jarman T, Deutch AY (2004) Effects of antipsychotic drugs on neurogenesis in the forebrain of the adult rat. Neuropsychopharmacology 29:1230-1238.
64. Yamada M, Onodera M, Mizuno Y, Mochizuki H (2004) Neurogenesis in olfactory bulb identified by retroviral labeling in normal and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated adult mice. Neuroscience 124:173-181.
65. Yurek DM, Fletcher-Turner A (2001) Differential expression of GDNF, BDNF, and NT-3 in the aging nigrostriatal system following a neurotoxic lesion. Brain Res 891:228-235.
66. Zhao M, Momma S, Delfani K, Carlen M, Cassidy RM, Johansson CB, Brismar H, Shupliakov O, Frisen J, Janson AM (2003) Evidence for neurogenesis in the adult mammalian substantia nigra. Proc Natl Acad Sci USA 100:7925-7930.