In vivo dopamine release and uptake impairments in rats treated with 3-nitropropionic acid

Neuroscience

Volumn 161, Issue 3, 2009, Pages 940-949

  Kraft, J C ^a   Osterhaus, G L ^a   Ortiz, A N ^a   Garris, P A ^b   Johnson, M A ^a  

^a UNIVERSITY OF KANSAS   (United States)

^b ILLINOIS STATE UNIVERSITY   (United States)

Author keywords

3 nitropropionic acid; cyclic voltammetry; dopamine; Huntington's disease; microelectrode; striatum

Indexed keywords

3 NITROPROPIONIC ACID; DOPAMINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CORPUS STRIATUM; DOPAMINE RELEASE; DOPAMINE UPTAKE; ELECTROSTIMULATION; MALE; NONHUMAN; POTENTIOMETRY; PRIORITY JOURNAL; RAT;

3,4-DIHYDROXYPHENYLACETIC ACID; ANALYSIS OF VARIANCE; ANIMALS; CENTRAL NERVOUS SYSTEM AGENTS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; DOPAMINE; ELECTRIC STIMULATION; HOMOVANILLIC ACID; HUNTINGTON DISEASE; KINETICS; MALE; MICROELECTRODES; MOTOR ACTIVITY; NITRO COMPOUNDS; PROPIONIC ACIDS; RATS; RATS, INBRED LEW;

EID: 67349240384     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.03.083     Document Type: Article

References (72)

1. Abercrombie ED, Russo ML (2002). Neurochemistry in the R6/2 transgenic mouse model of Huntington's disease. Program number 19512 in Society for Neuroscience 2002, Orlando, FL.
2. Akopian G., Crawford C., Beal M.F., Cappelletti M., Jakowec M.W., Petzinger G.M., Zheng L., Gheorghe S.L., Reichel C.M., Chow R., and Walsh J.P. Decreased striatal dopamine release underlies increased expression of long-term synaptic potentiation at corticostriatal synapses 24 h after 3-nitropropionic-acid-induced chemical hypoxia. J Neurosci 28 (2008) 9585-9597
3. Alston T.A., Mela L., and Bright H.J. 3-Nitropropionate, the toxic substance of Indigofera, is a suicide inactivator of succinate dehydrogenase. Proc Natl Acad Sci U S A 74 (1977) 3767-3771
4. Amara S.G., and Kuhar M.J. Neurotransmitter transporters: recent progress. Annu Rev Neurosci 16 (1993) 73-93
5. Beal M.F., Brouillet E., Jenkins B., Henshaw R., Rosen B., and Hyman B.T. Age-dependent striatal excitotoxic lesions produced by the endogenous mitochondrial inhibitor malonate. J Neurochem 61 (1993) 1147-1150
6. Beal M.F., Brouillet E., Jenkins B.G., Ferrante R.J., Kowall N.W., Miller J.M., Storey E., Srivastava R., Rosen B.R., and Hyman B.T. Neurochemical and histologic characterization of striatal excitotoxic lesions produced by the mitochondrial toxin 3-nitropropionic acid. J Neurosci 13 (1993) 4181-4192
7. Beal M.F., Swartz K.J., Hyman B.T., Storey E., Finn S.F., and Koroshetz W. Aminooxyacetic acid results in excitotoxin lesions by a novel indirect mechanism. J Neurochem 57 (1991) 1068-1073
8. Bizat N., Hermel J.M., Boyer F., Jacquard C., Creminon C., Ouary S., Escartin C., Hantraye P., Kajewski S., and Brouillet E. Calpain is a major cell death effector in selective striatal degeneration induced in vivo by 3-nitropropionate: implications for Huntington's disease. J Neurosci 23 (2003) 5020-5030
9. Blum D., Galas M.C., Cuvelier L., and Schiffmann S.N. Chronic intoxication with 3-nitropropionic acid in rats induces the loss of striatal dopamine terminals without affecting nigral cell viability. Neurosci Lett 354 (2004) 234-238
10. Blum D., Hemming F.J., Galas M.C., Torch S., Cuvelier L., Schiffmann S.N., and Sadoul R. Increased Alix (apoptosis-linked gene-2 interacting protein X) immunoreactivity in the degenerating striatum of rats chronically treated by 3-nitropropionic acid. Neurosci Lett 368 (2004) 309-313
11. Blum D., Galas M.C., Gall D., Cuvelier L., and Schiffmann S.N. Striatal and cortical neurochemical changes induced by chronic metabolic compromise in the 3-nitropropionic model of Huntington's disease. Neurobiol Dis 10 (2002) 410-426
12. Blum D., Gall D., Galas M.C., d'Alcantara P., Bantubungi K., and Schiffmann S.N. The adenosine A1 receptor agonist adenosine amine congener exerts a neuroprotective effect against the development of striatal lesions and motor impairments in the 3-nitropropionic acid model of neurotoxicity. J Neurosci 22 (2002) 9122-9133
13. Blum D., Gall D., Cuvelier L., and Schiffmann S.N. Topological analysis of striatal lesions induced by 3-nitropropionic acid in the Lewis rat. Neuroreport 12 (2001) 1769-1772
14. Bolivar V.J., Manley K., and Messer A. Early exploratory behavior abnormalities in R6/1 Huntington's disease transgenic mice. Brain Res 1005 (2004) 29-35
15. Brouillet E., Conde F., Beal M.F., and Hantraye P. Replicating Huntington's disease phenotype in experimental animals. Prog Neurobiol 59 (1999) 427-468
16. Brouillet E., Hantraye P., Ferrante R.J., Dolan R., Leroy-Willig A., Kowall N.W., and Beal M.F. Chronic mitochondrial energy impairment produces selective striatal degeneration and abnormal choreiform movements in primates. Proc Natl Acad Sci U S A 92 (1995) 7105-7109
17. Brouillet E., Jacquard C., Bizat N., and Blum D. 3-Nitropropionic acid: a mitochondrial toxin to uncover physiopathological mechanisms underlying striatal degeneration in Huntington's disease. J Neurochem 95 (2005) 1521-1540
18. Brouillet E., Jenkins B.G., Hyman B.T., Ferrante R.J., Kowall N.W., Srivastava R., Roy D.S., Rosen B.R., and Beal M.F. Age-dependent vulnerability of the striatum to the mitochondrial toxin 3-nitropropionic acid. J Neurochem 60 (1993) 356-359
19. Cakala M., Drabik J., Kazmierczak A., Kopczuk D., and Adamczyk A. Inhibition of mitochondrial complex II affects dopamine metabolism and decreases its uptake into striatal synaptosomes. Folia Neuropathol 44 (2006) 238-243
20. Coles C.J., Edmondson D.E., and Singer T.P. Inactivation of succinate dehydrogenase by 3-nitropropionate. J Biol Chem 254 (1979) 5161-5167
21. Cooper J.R., Bloom F.E., and Roth R.H. The biochemical basis of neuropharmacology (2003), Oxford University Press, New York
22. 2+ channel currents in cultured bovine adrenal chromaffin cells. Neuron 16 (1996) 1027-1036
23. Diverse-Pierluissi M., Dunlap K., and Westhead E.W. Multiple actions of extracellular ATP on calcium currents in cultured bovine chromaffin cells. Proc Natl Acad Sci U S A 88 (1991) 1261-1265
24. Ellison D.W., Beal M.F., and Martin J.B. Amino acid neurotransmitters in postmortem human brain analyzed by high performance liquid chromatography with electrochemical detection. J Neurosci Methods 19 (1987) 305-315
25. El Massioui N., Ouary S., Cheruel F., Hantraye P., and Brouillet E. Perseverative behavior underlying attentional set-shifting deficits in rats chronically treated with the neurotoxin 3-nitropropionic acid. Exp Neurol 172 (2001) 172-181
26. Eradiri O.L., and Starr M.S. Striatal dopamine depletion and behavioural sensitization induced by methamphetamine and 3-nitropropionic acid. Eur J Pharmacol 386 2-3 (1999) 217-226
27. Fernagut P.O., Diguet E., Jaber M., Bioulac B., and Tison F. Dopamine transporter knock-out mice are hypersensitive to 3-nitropropionic acid-induced striatal damage. Eur J Neurosci 15 (2002) 2053-2056
28. Fowler S.C., Birkestrand B.R., Chen R., Moss S.J., Vorontsova E., Wang G., and Zarcone T.J. A force-plate actometer for quantitating rodent behaviors: illustrative data on locomotion, rotation, spatial patterning, stereotypies, and tremor. J Neurosci Methods 107 (2001) 107-124
29. Gandia L., Garcia A.G., and Morad M. ATP modulation of calcium channels in chromaffin cells. J Physiol 470 (1993) 55-72
30. Garris P.A., and Wightman R.M. Different kinetics govern dopaminergic transmission in the amygdala, prefrontal cortex, and striatum: an in vivo voltammetric study. J Neurosci 14 (1994) 442-450
31. Greenamyre J.T., Higgins D.S., and Eller R.V. Quantitative autoradiography of dihydrorotenone binding to complex I of the electron transport chain. J Neurochem 59 (1992) 746-749
32. Guyot M.C., Hantraye P., Dolan R., Palfi S., Maziere M., and Brouillet E. Quantifiable bradykinesia, gait abnormalities and Huntington's disease-like striatal lesions in rats chronically treated with 3-nitropropionic acid. Neuroscience 79 (1997) 45-56
33. Harper P. Huntington's disease (1991), W. B. Saunders, London
34. Heien M.L.A.V., and Wightman R.M. Phasic dopamine signaling during behavior, reward, and disease states. CNS Neurol Disord Drug Targets 5 1 (2006) 99-108
35. Henry J.P., Botton D., Sagne C., Isambert M.F., Desnos C., Blanchard V., Raisman-Vozari R., Krejci E., Massoulie J., and Gasnier B. Biochemistry and molecular biology of the vesicular monoamine transporter from chromaffin granules. J Exp Biol 196 (1994) 251-262
36. Hickey M.A., Reynolds G.P., and Morton A.J. The role of dopamine in motor symptoms in the R6/2 transgenic mouse model of Huntington's disease. J Neurochem 81 (2002) 46-59
37. Johnson M.A., Rajan V., Miller C.E., and Wightman R.M. Dopamine release is severely compromised in the R6/2 mouse model of Huntington's disease. J Neurochem 97 (2006) 737-746
38. Johnson M.A., Villanueva M., Haynes C.L., Seipel A.T., Buhler L.A., and Wightman R.M. Catecholamine exocytosis is diminished in R6/2 Huntington's disease model mice. J Neurochem 103 (2007) 2102-2110
39. Johnson Jr. R.G. Accumulation of biological amines into chromaffin granules: a model for hormone and neurotransmitter transport. Physiol Rev 68 (1988) 232-307
40. Kandel E.R., Schwartz J.H., and Jessell T.M. Principles of neural science (2000), McGraw-Hill, New York
41. Kawagoe K.T., Jankowski J.A., and Wightman R.M. Etched carbon-fiber electrodes as amperometric detectors of catecholamine secretion from isolated biological cells. Anal Chem 63 (1991) 1584-1594
42. Lee S.T., Chu K., Park J.E., Hong N.H., Im W.S., Kang L., Han Z., Jung K.H., Kim M.W., and Kim M. Atorvastatin attenuates mitochondrial toxin-induced striatal degeneration, with decreasing iNOS/c-Jun levels and activating ERK/Akt pathways. J Neurochem 104 (2008) 1190-1200
43. Lee S.T., Park J.E., Kim D.H., Kim S., Im W.S., Kang L., Jung S.H., Kim M.W., Chu K., and Kim M. Granulocyte-colony stimulating factor attenuates striatal degeneration with activating survival pathways in 3-nitropropionic acid model of Huntington's disease. Brain Res 1194 (2008) 130-137
44. Leventhal L., Sortwell C.E., Hanbury R., Collier T.J., Kordower J.H., and Palfi S. Cyclosporin A protects striatal neurons in vitro and in vivo from 3-nitropropionic acid toxicity. J Comp Neurol 425 (2000) 471-478
45. Mangiarini L., Sathasivam K., Seller M., Cozens B., Harper A., Hetherington C., Lawton M., Trottier Y., Lehrach H., Davies S.W., and Bates G.P. Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell 87 (1996) 493-506
46. Maragos W.F., Zhu J., Chesnut M.D., and Dwoskin L.P. Mitochondrial toxin inhibition of [(3)H]dopamine uptake into rat striatal synaptosomes. Biochem Pharmacol 63 (2002) 1499-1505
47. Mathews C.K., and van Holde K.E. Biochemistry (1996), Benjamin/Cummings, Menlo Park, CA
48. McBride J.L., During M.J., Wuu J., Chen E.Y., Leurgans S.E., and Kordower J.H. Structural and functional neuroprotection in a rat model of Huntington's disease by viral gene transfer of GDNF. Exp Neurol 181 (2003) 213-223
49. McGeer E.G., and McGeer P.L. Duplication of biochemical changes of Huntington's chorea by intrastriatal injections of glutamic and kainic acids. Nature 263 (1976) 517-519
50. Michael D., Travis E.R., and Wightman R.M. Color images for fast-scan CV measurements in biological systems. Anal Chem 70 (1998) 586A-592A
51. Moriyama Y., Yamamoto A., Yamada H., Tashiro Y., and Futai M. Role of endocrine cell microvesicles in intercellular chemical transduction. Biol Chem Hoppe Seyler 377 (1996) 155-165
52. Newcomb J.D., Brown W.D., Rodriguez A.I., Garbuzova-Davis S., Saporta S., Sanberg P.R., and Willing A.E. Behavioral alterations in Lewis rats following two-day continuous 3-nitropropionic acid administration. Neurotox Res 8 (2005) 259-266
53. Ouary S., Bizat N., Altairac S., Menetrat H., Mittoux V., Conde F., Hantraye P., and Brouillet E. Major strain differences in response to chronic systemic administration of the mitochondrial toxin 3-nitropropionic acid in rats: implications for neuroprotection studies. Neuroscience 97 (2000) 521-530
54. Ouary S., Bizat N., Altairac S., Menetrat H., Mittoux V., Conde F., Hantraye P., and Brouillet E. Major strain differences in response to chronic systemic administration of the mitochondrial toxin 3-nitropropionic acid in rats: implications for neuroprotection studies. Neuroscience 97 (2000) 521-530
55. Park J.E., Lee S.T., Im W.S., Chu K., and Kim M. Galantamine reduces striatal degeneration in 3-nitropropionic acid model of Huntington's disease. Neurosci Lett 448 (2008) 143-147
56. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates (2005), Elsevier Academic, San Diego
57. Petersén A., Puschban Z., Lotharius J., NicNiocaill B., Wiekop P., O'Connor W.T., and Brundin P. Evidence for dysfunction of the nigrostriatal pathway in the R6/1 line of transgenic Huntington's disease mice. Neurobiol Dis 11 (2002) 134-146
58. Press W.H., Flanery B.P., Teukolsky S.A., and Fetterline W.T. Numerical recipes in Pascal (1989), Cambridge University Press, Cambridge
59. Rice M.E., and Nicholson C. Diffusion and ion shifts in the brain extracellular microenvironment and their relevance for voltammetric measurements. In: Boulton A.A., et al. (Ed). Neuromethods: voltammetric methods in brain systems (1995), Humana Press, Totowa, NJ 27-79
60. Roberts R.C., Ahn A., Swartz K.J., Beal M.F., and DiFiglia M. Intrastriatal injections of quinolinic acid or kainic acid: differential patterns of cell survival and the effects of data analysis on outcome. Exp Neurol 124 (1993) 274-282
61. Sagredo O., Ramos J.A., Decio A., Mechoulam R., and Fernandez-Ruiz J. Cannabidiol reduced the striatal atrophy caused 3-nitropropionic acid in vivo by mechanisms independent of the activation of cannabinoid, vanilloid TRPV1 and adenosine A2A receptors. Eur J Neurosci 26 (2007) 843-851
62. Schuldiner S., Shirvan A., and Linial M. Vesicular neurotransmitter transporters: from bacteria to humans. Physiol Rev 75 (1995) 369-392
63. Schulz J.B., Henshaw D.R., Jenkins B.G., Ferrante R.J., Kowall N.W., Rosen B.R., and Beal M.F. 3-Acetylpyridine produces age-dependent excitotoxic lesions in rat striatum. J Cereb Blood Flow Metab 14 (1994) 1024-1029
64. Storey E., Hyman B.T., Jenkins B., Brouillet E., Miller J.M., Rosen B.R., and Beal M.F. 1-Methyl-4-phenylpyridinium produces excitotoxic lesions in rat striatum as a result of impairment of oxidative metabolism. J Neurochem 58 (1992) 1975-1978
65. Sulzer D., Sonders M.S., Poulsen N.W., and Galli A. Mechanisms of neurotransmitter release by amphetamines: a review. Prog Neurobiol 75 (2005) 406-433
66. The Huntington's Disease Collaborative Research Group. A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. The Huntington's Disease Collaborative Research Group. Cell 72 (1993) 971-983
67. Van Raamsdonk J.M., Pearson J., Slow E.J., Hossain S.M., Leavitt B.R., and Hayden M.R. Cognitive dysfunction precedes neuropathology and motor abnormalities in the YAC128 mouse model of Huntington's disease. J Neurosci 25 (2005) 4169-4180
68. Venton B.J., Michael D.J., and Wightman R.M. Correlation of local changes in extracellular oxygen and pH that accompany dopaminergic terminal activity in the rat caudate-putamen. J Neurochem 84 (2003) 373-381
69. Walker Q.D., Rooney M.B., Wightman R.M., and Kuhn C.M. Dopamine release and uptake are greater in female than male rat striatum as measured by fast cyclic voltammetry. Neuroscience 95 (2000) 1061-1070
70. Wang L.H., and Qin Z.H. Animal models of Huntington's disease: implications in uncovering pathogenic mechanisms and developing therapies. Acta Pharmacol Sin 27 (2006) 1287-1302
71. Wightman R.M., Amatore C., Engstrom R.C., Hale P.D., Kristensen E.W., Kuhr W.G., and May L.J. Real-time characterization of dopamine overflow and uptake in the rat striatum. Neuroscience 25 (1988) 513-523
72. Wu Q., Reith M.E.A., Wightman R.M., Kawagoe K.T., and Garris P.A. Determination of release and uptake parameters from electrically evoked dopamine dynamics measured by real-time voltammetry. J Neurosci Methods 112 (2001) 119-133