Neurotransmitter CART as a new therapeutic candidate for Parkinson's disease

Pharmaceuticals

Volumn 6, Issue 1, 2013, Pages 108-123

  Mao, Peizhong ^a,b   Meshul, Charles K ^a,c   Thuillier, Philippe ^a   Reddy, P Hemachandra ^a,b  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c PORTLAND VA MEDICAL CENTER   (United States)

Author keywords

Antioxidant; Cocaine and amphetamine regulated transcript; Dopamine; Mitochondria; Neuroprotection; Oxidative stress

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALPHA SYNUCLEIN; CALCIUM ION; COCAINE AMPHETAMINE REGULATED TRANSCRIPT; DJ 1 PROTEIN; DOPAMINE; LEUCINE RICH REPEAT KINASE 2; MITOCHONDRIAL PROTEIN; NEUROPEPTIDE; PARKIN; PARKIN 2; PARKIN 5; PTEN INDUCED KINASE 1; SUCCINATE DEHYDROGENASE; SUCCINATE DEHYDROGENASE (UBIQUINONE); UNCLASSIFIED DRUG;

ALPHA SYNUCLEIN GENE; ARTICLE; CALCIUM HOMEOSTASIS; DISEASE ASSOCIATION; DISEASE MODEL; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DOPAMINERGIC SYSTEM; ENZYME ACTIVITY; GENE; GENE MUTATION; GENETIC ASSOCIATION; HUMAN; LRRK2 GENE; NEUROPATHOLOGY; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PARKINSON DISEASE; PATHOPHYSIOLOGY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; SUBSTANTIA NIGRA;

EID: 84872852087     PISSN: None     EISSN: 14248247     Source Type: Journal    
DOI: 10.3390/ph6010108     Document Type: Article

References (96)

1. Tanner, C.M.; Goldman, S.M. Epidemiology of Parkinson's Disease. Neurol. Clin. 1996, 14, 317-335.
2. Barzilai, A.; Melamed, E. Molecular Mechanisms of Selective Dopaminergic Neuronal Death in Parkinson's Disease. Trends Mol. Med. 2003, 9, 126-132.
3. Moore, D.J.; West, A.B.; Dawson, V.L.; Dawson, T.M. Molecular Pathophysiology of Parkinson's Disease. Annu. Rev. Neurosci. 2005, 28, 57-87.
4. Thomas, B.; Beal, M.F. Parkinson's Disease. Hum. Mol. Genet. 2007, 16 Spec No. 2, R183-94.
5. Banerjee, R.; Starkov, A.A.; Beal, M.F.; Thomas, B. Mitochondrial Dysfunction in the Limelight of Parkinson's Disease Pathogenesis. Biochim. Biophys. Acta 2009, 1792, 651-663.
6. Schapira, A.H. Targeting Mitochondria for Neuroprotection in Parkinson's Disease. Antioxid. Redox Signal. 2012, 16, 965-973.
7. Schapira, A.H. Mitochondrial Diseases. Lancet 2012, 379, 1825-1834.
8. Wood-Kaczmar, A.; Gandhi, S.; Wood, N.W. Understanding the Molecular Causes of Parkinson's Disease. Trends Mol. Med. 2006, 12, 521-528.
9. Winklhofer, K.F.; Haass, C. Mitochondrial Dysfunction in Parkinson's Disease. Biochim. Biophys. Acta 2010, 1802, 29-44.
10. Mao, P.; Ardeshiri, A.; Jacks, R.; Yang, S.; Hurn, P.D.; Alkayed, N.J. Mitochondrial Mechanism of Neuroprotection by CART. Eur. J. Neurosci. 2007, 26, 624-632.
11. Mao, P.; Meshul, C.K.; Thuillier, P.; Goldberg, N.R.; Reddy, P.H. CART Peptide is a Potential Endogenous Antioxidant and Preferentially Localized in Mitochondria. PLoS One 2012, 7, e29343.
12. Warner, T.T.; Schapira, A.H. Genetic and Environmental Factors in the Cause of Parkinson's Disease. Ann. Neurol. 2003, 53 Suppl 3, S16-23; discussion S23-5.
13. Schapira, A.H. Etiology and Pathogenesis of Parkinson Disease. Neurol. Clin. 2009, 27, 583-603,
14. Schapira, A.H. Etiology of Parkinson's Disease. Neurology 2006, 66, S10-23.
15. Lansbury, P.T., Jr; Brice, A. Genetics of Parkinson's Disease and Biochemical Studies of Implicated Gene Products. Curr. Opin. Cell Biol. 2002, 14, 653-660.
16. Dodson, M.W.; Guo, M. Pink1, Parkin, DJ-1 and Mitochondrial Dysfunction in Parkinson's Disease. Curr. Opin. Neurobiol. 2007, 17, 331-337.
17. Nuytemans, K.; Theuns, J.; Cruts, M.; Van Broeckhoven, C. Genetic Etiology of Parkinson Disease Associated with Mutations in the SNCA, PARK2, PINK1, PARK7, and LRRK2 Genes: A Mutation Update. Hum. Mutat. 2010, 31, 763-780.
18. Martin, L.J. Biology of Mitochondria in Neurodegenerative Diseases. Prog. Mol. Biol. Transl. Sci. 2012, 107, 355-415.
19. Polymeropoulos, M.H.; Lavedan, C.; Leroy, E.; Ide, S.E.; Dehejia, A.; Dutra, A.; Pike, B.; Root, H.; Rubenstein, J.; Boyer, R.; et al. Mutation in the Alpha-Synuclein Gene Identified in Families with Parkinson's Disease. Science 1997, 276, 2045-2047.
20. Spillantini, M.G.; Schmidt, M.L.; Lee, V.M.; Trojanowski, J.Q.; Jakes, R.; Goedert, M. Alpha-Synuclein in Lewy Bodies. Nature 1997, 388, 839-840.
21. Uversky, V.N.; Li, J.; Bower, K.; Fink, A.L. Synergistic Effects of Pesticides and Metals on the Fibrillation of Alpha-Synuclein: Implications for Parkinson's Disease. Neurotoxicology 2002, 23, 527-536.
22. Maraganore, D.M.; de Andrade, M.; Elbaz, A.; Farrer, M.J.; Ioannidis, J.P.; Kruger, R.; Rocca, W.A.; Schneider, N.K.; Lesnick, T.G.; Lincoln, S.J.; et al. Collaborative Analysis of Alpha-Synuclein Gene Promoter Variability and Parkinson Disease. JAMA 2006, 296, 661-670.
23. Galvin, J.E.; Pollack, J.; Morris, J.C. Clinical Phenotype of Parkinson Disease Dementia. Neurology 2006, 67, 1605-1611.
24. Galvin, J.E. Cognitive Change in Parkinson Disease. Alzheimer Dis. Assoc. Disord. 2006, 20, 302-310.
25. Janda, E.; Isidoro, C.; Carresi, C.; Mollace, V. Defective Autophagy in Parkinson's Disease: Role of Oxidative Stress. Mol. Neurobiol. 2012.
26. Betarbet, R.; Sherer, T.B.; MacKenzie, G.; Garcia-Osuna, M.; Panov, A.V.; Greenamyre, J.T. Chronic Systemic Pesticide Exposure Reproduces Features of Parkinson's Disease. Nat. Neurosci. 2000, 3, 1301-1306.
27. Langston, J.W.; Sastry, S.; Chan, P.; Forno, L.S.; Bolin, L.M.; Di Monte, D.A. Novel Alpha-Synuclein-Immunoreactive Proteins in Brain Samples from the Contursi Kindred, Parkinson's, and Alzheimer's Disease. Exp. Neurol. 1998, 154, 684-690.
28. Forno, L.S. Neuropathology of Parkinson's Disease. J. Neuropathol. Exp. Neurol. 1996, 55, 259-272.
29. Kitada, T.; Asakawa, S.; Hattori, N.; Matsumine, H.; Yamamura, Y.; Minoshima, S.; Yokochi, M.; Mizuno, Y.; Shimizu, N. Mutations in the Parkin Gene Cause Autosomal Recessive Juvenile Parkinsonism. Nature 1998, 392, 605-608.
30. Giasson, B.I.; Lee, V.M. Are Ubiquitination Pathways Central to Parkinson's Disease? Cell 2003, 114, 1-8.
31. Valente, E.M.; Abou-Sleiman, P.M.; Caputo, V.; Muqit, M.M.; Harvey, K.; Gispert, S.; Ali, Z.; Del Turco, D.; Bentivoglio, A.R.; Healy, D.G. et al. Hereditary Early-Onset Parkinson's Disease Caused by Mutations in PINK1. Science 2004, 304, 1158-1160.
32. Silvestri, L.; Caputo, V.; Bellacchio, E.; Atorino, L.; Dallapiccola, B.; Valente, E.M.; Casari, G. Mitochondrial Import and Enzymatic Activity of PINK1 Mutants Associated to Recessive Parkinsonism. Hum. Mol. Genet. 2005, 14, 3477-3492.
33. Bonifati, V.; Rizzu, P.; van Baren, M.J.; Schaap, O.; Breedveld, G.J.; Krieger, E.; Dekker, M.C.; Squitieri, F.; Ibanez, P.; Joosse, M.; et al. Mutations in the DJ-1 Gene Associated with Autosomal Recessive Early-Onset Parkinsonism. Science 2003, 299, 256-259.
34. Matsuda, N.; Sato, S.; Shiba, K.; Okatsu, K.; Saisho, K.; Gautier, C.A.; Sou, Y.S.; Saiki, S.; Kawajiri, S.; Sato, F.; et al. PINK1 Stabilized by Mitochondrial Depolarization Recruits Parkin to Damaged Mitochondria and Activates Latent Parkin for Mitophagy. J. Cell Biol. 2010, 189, 211-221.
35. Guzman, J.N.; Sanchez-Padilla, J.; Wokosin, D.; Kondapalli, J.; Ilijic, E.; Schumacker, P.T.; Surmeier, D.J. Oxidant Stress Evoked by Pacemaking in Dopaminergic Neurons is Attenuated by DJ-1. Nature 2010, 468, 696-700.
36. Papkovskaia, T.D.; Chau, K.Y.; Inesta-Vaquera, F.; Papkovsky, D.B.; Healy, D.G.; Nishio, K.; Staddon, J.; Duchen, M.R.; Hardy, J.; Schapira, A.H.; et al. G2019S Leucine-Rich Repeat Kinase 2 Causes Uncoupling Protein-Mediated Mitochondrial Depolarization. Hum. Mol. Genet. 2012, 21, 4201-4213.
37. Abeliovich, A. Parkinson's Disease: Mitochondrial Damage Control. Nature 2010, 463, 744-745.
38. Schapira, A.H.; Mann, V.M.; Cooper, J.M.; Dexter, D.; Daniel, S.E.; Jenner, P.; Clark, J.B.; Marsden, C.D. Anatomic and Disease Specificity of NADH CoQ1 Reductase (Complex I) Deficiency in Parkinson's Disease. J. Neurochem. 1990, 55, 2142-2145.
39. Jenner, P. Oxidative Stress in Parkinson's Disease. Ann. Neurol. 2003, 53 Suppl 3, S26-36; discussion S36-8.
40. Lin, M.T.; Beal, M.F. Mitochondrial Dysfunction and Oxidative Stress in Neurodegenerative Diseases. Nature 2006, 443, 787-795.
41. Moran, M.; Moreno-Lastres, D.; Marin-Buera, L.; Arenas, J.; Martin, M.A.; Ugalde, C. Mitochondrial Respiratory Chain Dysfunction: Implications in Neurodegeneration. Free Radic. Biol. Med. 2012, 53, 595-609.
42. Jenner, P. Presymptomatic Detection of Parkinson's Disease. J. Neural Transm. Suppl. 1993, 40, 23-36.
43. Zhou, C.; Huang, Y.; Przedborski, S. Oxidative Stress in Parkinson's Disease: A Mechanism of Pathogenic and Therapeutic Significance. Ann. N. Y. Acad. Sci. 2008, 1147, 93-104.
44. Schapira, A.H.; Cooper, J.M.; Dexter, D.; Clark, J.B.; Jenner, P.; Marsden, C.D. Mitochondrial Complex I Deficiency in Parkinson's Disease. J. Neurochem. 1990, 54, 823-827.
45. Dauer, W.; Przedborski, S. Parkinson's Disease: Mechanisms and Models. Neuron 2003, 39, 889-909.
46. Gunzler, S.A.; Shakil, S.; Carlson, N.E.; Nutt, J.G.; Meshul, C.K. Low Doses of Apomorphine Transiently Reduce Locomotor Activity in MPTP-Treated Mice. Neurosci. Lett. 2007, 428, 64-67.
47. Meshul, C.K.; Emre, N.; Nakamura, C.M.; Allen, C.; Donohue, M.K.; Buckman, J.F. Time-Dependent Changes in Striatal Glutamate Synapses Following a 6-Hydroxydopamine Lesion. Neuroscience 1999, 88, 1-16.
48. Robinson, S.; Freeman, P.; Moore, C.; Touchon, J.C.; Krentz, L.; Meshul, C.K. Acute and Subchronic MPTP Administration Differentially Affects Striatal Glutamate Synaptic Function. Exp. Neurol. 2003, 180, 74-87.
49. Fox, S.H.; Brotchie, J.M. The MPTP-Lesioned Non-Human Primate Models of Parkinson's Disease. Past, Present, and Future. Prog. Brain Res. 2010, 184, 133-157.
50. Iderberg, H.; Francardo, V.; Pioli, E.Y. Animal Models of L-DOPA-Induced Dyskinesia: An Update on the Current Options. Neuroscience 2012, 211, 13-27.
51. Wilhelmus, M.M.; Nijland, P.G.; Drukarch, B.; de Vries, H.E.; van Horssen, J. Involvement and Interplay of Parkin, PINK1, and DJ1 in Neurodegenerative and Neuroinflammatory Disorders. Free Radic. Biol. Med. 2012, 53, 983-992.
52. Manning-Bog, A.B.; McCormack, A.L.; Li, J.; Uversky, V.N.; Fink, A.L.; Di Monte, D.A. The Herbicide Paraquat Causes Up-Regulation and Aggregation of Alpha-Synuclein in Mice: Paraquat and Alpha-Synuclein. J. Biol. Chem. 2002, 277, 1641-1644.
53. Dawson, T.M.; Dawson, V.L. Molecular Pathways of Neurodegeneration in Parkinson's Disease. Science 2003, 302, 819-822.
54. Chan, C.S.; Guzman, J.N.; Ilijic, E.; Mercer, J.N.; Rick, C.; Tkatch, T.; Meredith, G.E.; Surmeier, D.J. 'Rejuvenation' Protects Neurons in Mouse Models of Parkinson's Disease. Nature 2007, 447, 1081-1086.
55. Chinta, S.J.; Andersen, J.K. Reversible Inhibition of Mitochondrial Complex I Activity Following Chronic Dopaminergic Glutathione Depletion in Vitro: Implications for Parkinson's Disease. Free Radic. Biol. Med. 2006, 41, 1442-1448.
56. Chinta, S.J.; Kumar, M.J.; Hsu, M.; Rajagopalan, S.; Kaur, D.; Rane, A.; Nicholls, D.G.; Choi, J.; Andersen, J.K. Inducible Alterations of Glutathione Levels in Adult Dopaminergic Midbrain Neurons Result in Nigrostriatal Degeneration. J. Neurosci. 2007, 27, 13997-14006.
57. Sarkar, C.; Basu, B.; Chakroborty, D.; Dasgupta, P.S.; Basu, S. The Immunoregulatory Role of Dopamine: An Update. Brain Behav. Immun. 2010, 24, 525-528.
58. Rasheed, N.; Alghasham, A. Central Dopaminergic System and its Implications in Stress-Mediated Neurological Disorders and Gastric Ulcers: Short Review. Adv. Pharmacol. Sci. 2012, 2012, 182671.
59. Hastings, T.G. The Role of Dopamine Oxidation in Mitochondrial Dysfunction: Implications for Parkinson's Disease. J. Bioenerg. Biomembr. 2009, 41, 469-472.
60. Mao, P.; Reddy, P.H. Aging and Amyloid Beta-Induced Oxidative DNA Damage and Mitochondrial Dysfunction in Alzheimer's Disease: Implications for Early Intervention and Therapeutics. Biochim. Biophys. Acta 2011.
61. Duncan, J.; Johnson, S.; Ou, X.M. Monoamine Oxidases in Major Depressive Disorder and Alcoholism. Drug Discov. Ther. 2012, 6, 112-122.
62. Alam, Z.I.; Jenner, A.; Daniel, S.E.; Lees, A.J.; Cairns, N.; Marsden, C.D.; Jenner, P.; Halliwell, B. Oxidative DNA Damage in the Parkinsonian Brain: An Apparent Selective Increase in 8-Hydroxyguanine Levels in Substantia Nigra. J. Neurochem. 1997, 69, 1196-1203.
63. Alam, Z.I.; Daniel, S.E.; Lees, A.J.; Marsden, D.C.; Jenner, P.; Halliwell, B. A Generalised Increase in Protein Carbonyls in the Brain in Parkinson's but Not Incidental Lewy Body Disease. J. Neurochem. 1997, 69, 1326-1329.
64. Jenner, P. Oxidative Stress and Parkinson's Disease. Handb. Clin. Neurol. 2007, 83, 507-520.
65. Seet, R.C.; Lee, C.Y.; Lim, E.C.; Tan, J.J.; Quek, A.M.; Chong, W.L.; Looi, W.F.; Huang, S.H.; Wang, H.; Chan, Y.H.; et al. Oxidative Damage in Parkinson Disease: Measurement using Accurate Biomarkers. Free Radic. Biol. Med. 2010, 48, 560-566.
66. Douglass, J.; McKinzie, A.A.; Couceyro, P. PCR Differential Display Identifies a Rat Brain mRNA that is Transcriptionally Regulated by Cocaine and Amphetamine. J. Neurosci. 1995, 15, 2471-2481.
67. Thim, L.; Kristensen, P.; Nielsen, P.F.; Wulff, B.S.; Clausen, J.T. Tissue-Specific Processing of Cocaine-and Amphetamine-Regulated Transcript Peptides in the Rat. Proc. Natl. Acad. Sci. U. S. A. 1999, 96, 2722-2727.
68. Larsen, P.J.; Seier, V.; Fink-Jensen, A.; Holst, J.J.; Warberg, J.; Vrang, N. Cocaine-and Amphetamine-Regulated Transcript is Present in Hypothalamic Neuroendocrine Neurones and is Released to the Hypothalamic-Pituitary Portal Circuit. J. Neuroendocrinol. 2003, 15, 219-226.
69. Koylu, E.O.; Couceyro, P.R.; Lambert, P.D.; Ling, N.C.; DeSouza, E.B.; Kuhar, M.J. Immunohistochemical Localization of Novel CART Peptides in Rat Hypothalamus, Pituitary and Adrenal Gland. J. Neuroendocrinol. 1997, 9, 823-833.
70. Koylu, E.O.; Balkan, B.; Kuhar, M.J.; Pogun, S. Cocaine and Amphetamine Regulated Transcript (CART) and the Stress Response. Peptides 2006, 27, 1956-1969.
71. Mao, P. Potential Antidepressant Role of Neurotransmitter CART: Implications for Mental Disorders. Depress Res. Treat. 2011, 2011, 762139.
72. Kuhar, M.J.; Adams, S.; Dominguez, G.; Jaworski, J.; Balkan, B. CART Peptides. Neuropeptides 2002, 36, 1-8.
73. Hunter, R.G.; Kuhar, M.J. CART Peptides as Targets for CNS Drug Development. Curr. Drug Targets CNS Neurol. Disord. 2003, 2, 201-205.
74. Rogge, G.; Jones, D.; Hubert, G.W.; Lin, Y.; Kuhar, M.J. CART Peptides: Regulators of Body Weight, Reward and Other Functions. Nat. Rev. Neurosci. 2008, 9, 747-758.
75. del Giudice, E.M.; Santoro, N.; Cirillo, G.; D'Urso, L.; Di Toro, R.; Perrone, L. Mutational Screening of the CART Gene in Obese Children: Identifying a Mutation (Leu34Phe) Associated with Reduced Resting Energy Expenditure and Cosegregating with Obesity Phenotype in a Large Family. Diabetes 2001, 50, 2157-2160.
76. Yanik, T.; Dominguez, G.; Kuhar, M.J.; Del Giudice, E.M.; Loh, Y.P. The Leu34Phe ProCART Mutation Leads to Cocaine-and Amphetamine-Regulated Transcript (CART) Deficiency: A Possible Cause for Obesity in Humans. Endocrinology 2006, 147, 39-43.
77. Mao, P.; Jacks, R. Transcriptional Activity by Cocaine-Amphetamine-Regulated Transcript. Mol. Psychiatry 2007, 12, 223-224.
78. Wu, B.; Hu, S.; Yang, M.; Pan, H.; Zhu, S. CART Peptide Promotes the Survival of Hippocampal Neurons by Upregulating Brain-Derived Neurotrophic Factor. Biochem. Biophys. Res. Commun. 2006, 347, 656-661.
79. Xu, Y.; Zhang, W.; Klaus, J.; Young, J.; Koerner, I.; Sheldahl, L.C.; Hurn, P.D.; Martinez-Murillo, F.; Alkayed, N.J. Role of Cocaine-and Amphetamine-Regulated Transcript in Estradiol-Mediated Neuroprotection. Proc. Natl. Acad. Sci. USA 2006, 103, 14489-14494.
80. Zhang, M.; Han, L.; Xu, Y. Roles of Cocaine-and Amphetamine-Regulated Transcript in the Central Nervous System. Clin. Exp. Pharmacol. Physiol. 2012, 39, 586-592.
81. Mao, P. Recent progress and concerns in dementia: distinguishing Alzheimer's disease and dementia with Lewy bodies via biochemical markers in the cerebrospinal fluid. Advances in Biological Chemistry 2012, 2, 176-190.
82. Swerdlow, R.H.; Newell, K.L. "Untangling" the Relationship between Alzheimer Disease and Dementia with Lewy Bodies. Neurology 2012, 79, 1938-1939.
83. Cecchini, G. Function and Structure of Complex II of the Respiratory Chain. Annu. Rev. Biochem. 2003, 72, 77-109.
84. Rustin, P.; Rotig, A. Inborn Errors of Complex II--Unusual Human Mitochondrial Diseases. Biochim. Biophys. Acta 2002, 1553, 117-122.
85. Bertoni-Freddari, C.; Fattoretti, P.; Paoloni, R.; Caselli, U.; Galeazzi, L.; Meier-Ruge, W. Synaptic Structural Dynamics and Aging. Gerontology 1996, 42, 170-180.
86. Gimenez-Roqueplo, A.P.; Favier, J.; Rustin, P.; Rieubland, C.; Kerlan, V.; Plouin, P.F.; Rotig, A.; Jeunemaitre, X. Functional Consequences of a SDHB Gene Mutation in an Apparently Sporadic Pheochromocytoma. J. Clin. Endocrinol. Metab. 2002, 87, 4771-4774.
87. Maier-Woelfle, M.; Brandle, M.; Komminoth, P.; Saremaslani, P.; Schmid, S.; Locher, T.; Heitz, P.U.; Krull, I.; Galeazzi, R.L.; Schmid, C. et al. A Novel Succinate Dehydrogenase Subunit B Gene Mutation, H132P, Causes Familial Malignant Sympathetic Extraadrenal Paragangliomas. J. Clin. Endocrinol. Metab. 2004, 89, 362-367.
88. Chinta, S.J.; Andersen, J.K. Dopaminergic Neurons. Int. J. Biochem. Cell Biol. 2005, 37, 942-946.
89. Fagergren, P.; Hurd, Y. CART mRNA Expression in Rat Monkey and Human Brain: Relevance to Cocaine Abuse. Physiol. Behav. 2007, 92, 218-225.
90. Dallvechia-Adams, S.; Smith, Y.; Kuhar, M.J. CART Peptide-Immunoreactive Projection from the Nucleus Accumbens Targets Substantia Nigra Pars Reticulata Neurons in the Rat. J. Comp. Neurol. 2001, 434, 29-39.
91. Dallvechia-Adams, S.; Kuhar, M.J.; Smith, Y. Cocaine-and Amphetamine-Regulated Transcript Peptide Projections in the Ventral Midbrain: Colocalization with Gamma-Aminobutyric Acid, Melanin-Concentrating Hormone, Dynorphin, and Synaptic Interactions with Dopamine Neurons. J. Comp. Neurol. 2002, 448, 360-372.
92. Upadhya, M.A.; Nakhate, K.T.; Kokare, D.M.; Singh, U.; Singru, P.S.; Subhedar, N.K. CART Peptide in the Nucleus Accumbens Shell Acts Downstream to Dopamine and Mediates the Reward and Reinforcement Actions of Morphine. Neuropharmacology 2012, 62, 1823-1833.
93. Moffett, M.C.; Song, J.; Kuhar, M.J. CART Peptide Inhibits Locomotor Activity Induced by Simultaneous Stimulation of D1 and D2 Receptors, but Not by Stimulation of Individual Dopamine Receptors. Synapse 2011, 65, 1-7.
94. Hostetler, C.M.; Kowalczyk, A.S.; Griffin, L.L.; Bales, K.L. CART Peptide Following Social Novelty in the Prairie Vole (Microtus Ochrogaster). Brain Res. 2011, 1414, 32-40.
95. Brischoux, F.; Griffond, B.; Fellmann, D.; Risold, P.Y. Early and Transient Ontogenetic Expression of the Cocaine-and Amphetamine-Regulated Transcript Peptide in the Rat Mesencephalon: Correlation with Tyrosine Hydroxylase Expression. J. Neurobiol. 2002, 52, 221-229.
96. Goldberg, N.R.; Haack, A.K.; Lim, N.S.; Janson, O.K.; Meshul, C.K. Dopaminergic and Behavioral Correlates of Progressive Lesioning of the Nigrostriatal Pathway with 1-Methyl-4-Phenyl-1,2,3,6-Tetrahydropyridine. Neuroscience 2011, 180, 256-271.