Neurotoxic (+)-methamphetamine treatment in rats increases brain-derived neurotrophic factor and tropomyosin receptor kinase B expression in multiple brain regions

Neuroscience

Volumn 184, Issue , 2011, Pages 164-171

  Braun, A A ^a,b   Herring, N R ^c   Schaefer, T L ^a   Hemmerle, A M ^a,b   Dickerson, J W ^a,b   Seroogy, K B ^a,b   Vorhees, C V ^a,b   Williams, M T ^a,b  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF CINCINNATI   (United States)

^c University of Louisville School of Medicine   (United States)

Author keywords

BDNF; Brain derived neurotrophic factor; Methamphetamine; TrkB; Tropomyosin receptor kinase b

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CORTICOSTERONE; MESSENGER RNA; METHAMPHETAMINE; TYROSINE 3 MONOOXYGENASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; CORTICOSTERONE BLOOD LEVEL; ENTORHINAL CORTEX; FRONTAL CORTEX; GENE EXPRESSION; HIPPOCAMPAL CA1 REGION; LOCUS CERULEUS; MALE; NEUROTOXICITY; NONHUMAN; PARIETAL CORTEX; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRIFORM CORTEX; RAT; RNA PROBE; SUBSTANTIA NIGRA PARS COMPACTA; TISSUE SECTION;

ANIMALS; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CORTICOSTERONE; MALE; METHAMPHETAMINE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, TRKB; RNA, MESSENGER;

EID: 79955983761     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.03.045     Document Type: Article

References (91)

1. Altar C.A., Cai N., Bliven T., Juhasz M., Conner J.M., Acheson A.L., Lindsay R.M., Wiegand S.J. Anterograde transport of brain-derived neurotrophic factor and its role in the brain. Nature 1997, 389:856-860.
2. Barbacid M. Neurotrophic factors and their receptors. Curr Opin Cell Biol 1995, 7:148-155.
3. Barr A.M., Panenka W.J., MacEwan G.W., Thornton A.E., Lang D.J., Honer W.G., Lecomte T. The need for speed: an update on methamphetamine addiction. J Psychiatry Neurosci 2006, 31:301-313.
4. Belcher A.M., O'Dell S.J., Marshall J.F. Impaired object recognition memory following methamphetamine, but not p-chloroamphetamine- or d-amphetamine-induced neurotoxicity. Neuropsychopharmacology 2005, 30:2026-2034.
5. Bisagno V., Ferguson D., Luine V.N. Short toxic methamphetamine schedule impairs object recognition task in male rats. Brain Res 2002, 940:95-101.
6. Blochl A., Sirrenberg C. Neurotrophins stimulate the release of dopamine from rat mesencephalic neurons via Trk and p75Lntr receptors. J Biol Chem 1996, 271:21100-21107.
7. Broad K.D., Mimmack M.L., Keverne E.B., Kendrick K.M. Increased BDNF and trk-B mRNA expression in cortical and limbic regions following formation of a social recognition memory. Eur J Neurosci 2002, 16:2166-2174.
8. Broadbent N.J., Gaskin S., Squire L.R., Clark R.E. Object recognition memory and the rodent hippocampus. Learn Mem 2010, 17:5-11.
9. Butters N., Soeldner C., Fedio P. Comparison of parietal and frontal lobe spatial deficits in man: extrapersonal vs personal (egocentric) space. Percept Mot Skills 1972, 34:27-34.
10. Byrne R.W. Geographical knowledge and orientation. Normality and pathology in cognitive functions 1982, 239-264. Academic press, London.
11. Cadet J.L., Krasnova I.N. Molecular bases of methamphetamine-induced neurodegeneration. Int Rev Neurobiol 2009, 88:101-119.
12. Canals J.M., Checa N., Marco S., Akerud P., Michels A., Perez-Navarro E., Tolosa E., Arenas E., Alberch J. Expression of brain-derived neurotrophic factor in cortical neurons is regulated by striatal target area. J Neurosci 2001, 21:117-124.
13. Canals J.M., Checa N., Marco S., Michels A., Perez-Navarro E., Alberch J. The neurotrophin receptors trkA, trkB and trkC are differentially regulated after excitotoxic lesion in rat striatum. Brain Res Mol Brain Res 1999, 69:242-248.
14. Canals J.M., Marco S., Checa N., Michels A., Perez-Navarro E., Arenas E., Alberch J. Differential regulation of the expression of nerve growth factor, brain-derived neurotrophic factor, and neurotrophin-3 after excitotoxicity in a rat model of Huntington's disease. Neurobiol Dis 1998, 5:357-364.
15. Cappon G.D., Pu C., Vorhees C.V. Time-course of methamphetamine-induced neurotoxicity in rat caudate-putamen after single-dose treatment. Brain Res 2000, 863:106-111.
16. Cass W.A., Peters L.E., Harned M.E., Seroogy K.B. Protection by GDNF and other trophic factors against the dopamine-depleting effects of neurotoxic doses of methamphetamine. Ann N Y Acad Sci 2006, 1074:272-281.
17. Chapman D.E., Hanson G.R., Kesner R.P., Keefe K.A. Long-term changes in basal ganglia function after a neurotoxic regimen of methamphetamine. J Pharmacol Exp Ther 2001, 296:520-527.
18. Cook D., Kesner R.P. Caudate nucleus and memory for egocentric localization. Behav Neural Biol 1988, 49:332-343.
19. Daberkow D.P., Kesner R.P., Keefe K.A. Relation between methamphetamine-induced monoamine depletions in the striatum and sequential motor learning. Pharmacol Biochem Behav 2005, 81:198-204.
20. Dalley J.W., Cardinal R.N., Robbins T.W. Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates. Neurosci Biobehav Rev 2004, 28:771-784.
21. Dixon J.E., McKinnon D. Expression of the trk gene family of neurotrophin receptors in prevertebral sympathetic ganglia. Brain Res Dev Brain Res 1994, 77:177-182.
22. Dluzen D.E. The effect of gender and the neurotrophin, BDNF, upon methamphetamine-induced neurotoxicity of the nigrostriatal dopaminergic system in mice. Neurosci Lett 2004, 359:135-138.
23. Dluzen D.E., Anderson L.I., McDermott J.L., Kucera J., Walro J.M. Striatal dopamine output is compromised within +/- BDNF mice. Synapse 2002, 43:112-117.
24. Dong M., Wu Y., Fan Y., Xu M., Zhang J. c-fos modulates brain-derived neurotrophic factor mRNA expression in mouse hippocampal CA3 and dentate gyrus neurons. Neurosci Lett 2006, 400:177-180.
25. Edwards R.H., Selby M.J., Garcia P.D., Rutter W.J. Processing of the native nerve growth factor precursor to form biologically active nerve growth factor. J Biol Chem 1988, 263:6810-6815.
26. Fehm H.L., Holl R., Steiner K., Klein E., Voigt K.H. Evidence for ACTH-unrelated mechanisms in the regulation of cortisol secretion in man. Klin Wochenschr 1984, 62:19-24.
27. Fornai F., Alessandri M.G., Torracca M.T., Bassi L., Scalori V., Corsini G.U. Noradrenergic modulation of methamphetamine-induced striatal dopamine depletion. Ann N Y Acad Sci 1998, 844:166-177.
28. Fornai F., Bassi L., Torracca M.T., Scalori V., Corsini G.U. Norepinephrine loss exacerbates methamphetamine-induced striatal dopamine depletion in mice. Eur J Pharmacol 1995, 283:99-102.
29. Friedman S.D., Castaneda E., Hodge G.K. Long-term monoamine depletion, differential recovery, and subtle behavioral impairment following methamphetamine-induced neurotoxicity. Pharmacol Biochem Behav 1998, 61:35-44.
30. Fukumura M., Cappon G.D., Broening H.W., Vorhees C.V. Methamphetamine-induced dopamine and serotonin reductions in neostriatum are not gender specific in rats with comparable hyperthermic responses. Neurotoxicol Teratol 1998, 20:441-448.
31. Gall C.M. Seizure-induced changes in neurotrophin expression: implications for epilepsy. Exp Neurol 1993, 124:150-166.
32. Grace C.E., Schaefer T.L., Herring N.R., Skelton M.R., McCrea A.E., Vorhees C.V., Williams M.T. (+)-Methamphetamine increases corticosterone in plasma and BDNF in brain more than forced swim or isolation in neonatal rats. Synapse 2008, 62:110-121.
33. Guillin O., Diaz J., Carroll P., Griffon N., Schwartz J.C., Sokoloff P. BDNF controls dopamine D3 receptor expression and triggers behavioural sensitization. Nature 2001, 411:86-89.
34. Haughey H.M., Fleckenstein A.E., Hanson G.R. Differential regional effects of methamphetamine on the activities of tryptophan and tyrosine hydroxylase. J Neurochem 1999, 72:661-668.
35. He J., Yang Y., Yu Y., Li X., Li X.M. The effects of chronic administration of quetiapine on the methamphetamine-induced recognition memory impairment and dopaminergic terminal deficit in rats. Behav Brain Res 2006, 172:39-45.
36. Herring N.R., Schaefer T.L., Gudelsky G.A., Vorhees C.V., Williams M.T. Effect of +-methamphetamine on path integration learning, novel object recognition, and neurotoxicity in rats. Psychopharmacology (Berl) 2008, 199:637-650.
37. Herring N.R., Schaefer T.L., Tang P.H., Skelton M.R., Lucot J.P., Gudelsky G.A., Vorhees C.V., Williams M.T. Comparison of time-dependent effects of (+)-methamphetamine or forced swim on monoamines, corticosterone, glucose, creatine, and creatinine in rats. BMC Neurosci 2008, 9:49.
38. Hicks R.R., Li C., Zhang L., Dhillon H.S., Prasad M.R., Seroogy K.B. Alterations in BDNF and trkB mRNA levels in the cerebral cortex following experimental brain trauma in rats. J Neurotrauma 1999, 16:501-510.
39. Hicks R.R., Martin V.B., Zhang L., Seroogy K.B. Mild experimental brain injury differentially alters the expression of neurotrophin and neurotrophin receptor mRNAs in the hippocampus. Exp Neurol 1999, 160:469-478.
40. Hicks R.R., Numan S., Dhillon H.S., Prasad M.R., Seroogy K.B. Alterations in BDNF and NT-3 mRNAs in rat hippocampus after experimental brain trauma. Brain Res Mol Brain Res 1997, 48:401-406.
41. Hicks R.R., Zhang L., Dhillon H.S., Prasad M.R., Seroogy K.B. Expression of trkB mRNA is altered in rat hippocampus after experimental brain trauma. Brain Res Mol Brain Res 1998, 59:264-268.
42. Hotchkiss A.J., Gibb J.W. Long-term effects of multiple doses of methamphetamine on tryptophan hydroxylase and tyrosine hydroxylase activity in rat brain. J Pharmacol Exp Ther 1980, 214:257-262.
43. Hotchkiss A.J., Morgan M.E., Gibb J.W. The long-term effects of multiple doses of methamphetamine on neostriatal tryptophan hydroxylase, tyrosine hydroxylase, choline acetyltransferase and glutamate decarboxylase activities. Life Sci 1979, 25:1373-1378.
44. Hyman C., Hofer M., Barde Y.A., Juhasz M., Yancopoulos G.D., Squinto S.P., Lindsay R.M. BDNF is a neurotrophic factor for dopaminergic neurons of the substantia nigra. Nature 1991, 350:230-232.
45. Isackson P.J., Huntsman M.M., Murray K.D., Gall C.M. BDNF mRNA expression is increased in adult rat forebrain after limbic seizures: temporal patterns of induction distinct from NGF. Neuron 1991, 6:937-948.
46. Johnson L.D., O'Malley P.M., Bachman J.G., Schulenberg J.E. Monitoring the future national survey results on drug use, 1975-2008. Vol. II: College students and adults ages 19-50 (NIH Publication No. 09-7403) 2009, National Institute of Drug Abuse, Bethesda, MD.
47. Joyce J.N., Renish L., Osredkar T., Walro J.M., Kucera J., Dluzen D.E. Methamphetamine-induced loss of striatal dopamine innervation in BDNF heterozygote mice does not further reduce D3 receptor concentrations. Synapse 2004, 52:11-19.
48. Kim D.J., Roh S., Kim Y., Yoon S.J., Lee H.K., Han C.S., Kim Y.K. High concentrations of plasma brain-derived neurotrophic factor in methamphetamine users. Neurosci Lett 2005, 388:112-115.
49. Kish S.J., Fitzmaurice P.S., Boileau I., Schmunk G.A., Ang L.C., Furukawa Y., Chang L.J., Wickham D.J., Sherwin A., Tong J. Brain serotonin transporter in human methamphetamine users. Psychopharmacology (Berl) 2009, 202:649-661.
50. Kitamura O., Tokunaga I., Gotohda T., Kubo S. Immunohistochemical investigation of dopaminergic terminal markers and caspase-3 activation in the striatum of human methamphetamine users. Int J Legal Med 2007, 121:163-168.
51. Kokaia Z., Andsberg G., Yan Q., Lindvall O. Rapid alterations of BDNF protein levels in the rat brain after focal ischemia: evidence for increased synthesis and anterograde axonal transport. Exp Neurol 1998, 154:289-301.
52. Krasnova I.N., Cadet J.L. Methamphetamine toxicity and messengers of death. Brain Res Rev 2009, 60:379-407.
53. Le Foll B., Diaz J., Sokoloff P. A single cocaine exposure increases BDNF and D3 receptor expression: implications for drug-conditioning. Neuroreport 2005, 16:175-178.
54. Lee R., Kermani P., Teng K.K., Hempstead B.L. Regulation of cell survival by secreted proneurotrophins. Science 2001, 294:1945-1948.
55. Lyons W.E., Mamounas L.A., Ricaurte G.A., Coppola V., Reid S.W., Bora S.H., Wihler C., Koliatsos V.E., Tessarollo L. Brain-derived neurotrophic factor-deficient mice develop aggressiveness and hyperphagia in conjunction with brain serotonergic abnormalities. Proc Natl Acad Sci U S A 1999, 96:15239-15244.
56. Madinier A., Bertrand N., Mossiat C., Prigent-Tessier A., Beley A., Marie C., Garnier P. Microglial involvement in neuroplastic changes following focal brain ischemia in rats. PLoS One 2009, 4:e8101.
57. Martinez-Serrano A., Bjorklund A. Protection of the neostriatum against excitotoxic damage by neurotrophin-producing, genetically modified neural stem cells. J Neurosci 1996, 16:4604-4616.
58. Matsuzaki H., Namikawa K., Kiyama H., Mori N., Sato K. Brain-derived neurotrophic factor rescues neuronal death induced by methamphetamine. Biol Psychiatry 2004, 55:52-60.
59. McAllister A.K., Katz L.C., Lo D.C. Neurotrophins and synaptic plasticity. Annu Rev Neurosci 1999, 22:295-318.
60. Meredith C.W., Jaffe C., Ang-Lee K., Saxon A.J. Implications of chronic methamphetamine use: a literature review. Harv Rev Psychiatry 2005, 13:141-154.
61. Meredith G.E., Callen S., Scheuer D.A. Brain-derived neurotrophic factor expression is increased in the rat amygdala, piriform cortex and hypothalamus following repeated amphetamine administration. Brain Res 2002, 949:218-227.
62. Merlio J.P., Ernfors P., Jaber M., Persson H. Molecular cloning of rat trkC and distribution of cells expressing messenger RNAs for members of the trk family in the rat central nervous system. Neuroscience 1992, 51:513-532.
63. Merlio J.P., Ernfors P., Kokaia Z., Middlemas D.S., Bengzon J., Kokaia M., Smith M.L., Siesjo B.K., Hunter T., Lindvall O. Increased production of the TrkB protein tyrosine kinase receptor after brain insults. Neuron 1993, 10:151-164.
64. Metsis M., Timmusk T., Arenas E., Persson H. Differential usage of multiple brain-derived neurotrophic factor promoters in the rat brain following neuronal activation. Proc Natl Acad Sci U S A 1993, 90:8802-8806.
65. Moser E.I., Kropff E., Moser M.B. Place cells, grid cells, and the brain's spatial representation system. Annu Rev Neurosci 2008, 31:69-89.
66. Narita M., Aoki K., Takagi M., Yajima Y., Suzuki T. Implication of brain-derived neurotrophic factor in the release of dopamine and dopamine-related behaviors induced by methamphetamine. Neuroscience 2003, 119:767-775.
67. Nibuya M., Morinobu S., Duman R.S. Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments. J Neurosci 1995, 15:7539-7547.
68. Numan S., Lane-Ladd S.B., Zhang L., Lundgren K.H., Russell D.S., Seroogy K.B., Nestler E.J. Differential regulation of neurotrophin and trk receptor mRNAs in catecholaminergic nuclei during chronic opiate treatment and withdrawal. J Neurosci 1998, 18:10700-10708.
69. Numan S., Gall C.M., Seroogy K.B. Developmental expression of neurotrophins and their receptors in postnatal rat ventral midbrain. J Mol Neurosci 2005, 27:245-260.
70. Numan S., Seroogy K.B. Expression of trkB and trkC mRNAs by adult midbrain dopamine neurons: a double-label in situ hybridization study. J Comp Neurol 1999, 403:295-308.
71. O'Dell S.J., Feinberg L.M., Marshall J.F. A neurotoxic regimen of methamphetamine impairs novelty recognition as measured by a social odor-based task. Behav Brain Res 2011, 216:396-401.
72. Packard M.G., Knowlton B.J. Learning and memory functions of the basal ganglia. Annu Rev Neurosci 2002, 25:563-593.
73. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1986, Academic Press, Inc, San Diego.
74. Perez-Navarro E., Canudas A.M., Akerund P., Alberch J., Arenas E. Brain-derived neurotrophic factor, neurotrophin-3, and neurotrophin-4/5 prevent the death of striatal projection neurons in a rodent model of Huntington's disease. J Neurochem 2000, 75:2190-2199.
75. Rocamora N., Welker E., Pascual M., Soriano E. Upregulation of BDNF mRNA expression in the barrel cortex of adult mice after sensory stimulation. J Neurosci 1996, 16:4411-4419.
76. Sato N., Sakata H., Tanaka Y.L., Taira M. Navigation-associated medial parietal neurons in monkeys. Proc Natl Acad Sci U S A 2006, 103:17001-17006.
77. Schaaf M.J., de Kloet E.R., Vreugdenhil E. Corticosterone effects on BDNF expression in the hippocampus. Implications for memory formation. Stress 2000, 3:201-208.
78. Schaaf M.J., de Jong J., de Kloet E.R., Vreugdenhil E. Downregulation of BDNF mRNA and protein in the rat hippocampus by corticosterone. Brain Res 1998, 813:112-120.
79. Schroder N., O'Dell S.J., Marshall J.F. Neurotoxic methamphetamine regimen severely impairs recognition memory in rats. Synapse 2003, 49:89-96.
80. Sekine Y., Ouchi Y., Takei N., Yoshikawa E., Nakamura K., Futatsubashi M., Okada H., Minabe Y., Suzuki K., Iwata Y., Tsuchiya K.J., Tsukada H., Iyo M., Mori N. Brain serotonin transporter density and aggression in abstinent methamphetamine abusers. Arch Gen Psychiatry 2006, 63:90-100.
81. Seroogy K.B., Herman J.P. In situ hybridization approaches to the study of the nervous system. Neurochemistry: a practical approach 1997, 121-150. Oxford University Press, Oxford, UK. A.J. Turner, H.S. Bachelard (Eds.).
82. Seroogy K.B., Lundgren K.H., Tran T.M., Guthrie K.M., Isackson P.J., Gall C.M. Dopaminergic neurons in rat ventral midbrain express brain-derived neurotrophic factor and neurotrophin-3 mRNAs. J Comp Neurol 1994, 342:321-334.
83. Skelton M.R., Williams M.T., Schaefer T.L., Vorhees C.V. Neonatal (+)-methamphetamine increases brain derived neurotrophic factor, but not nerve growth factor, during treatment and results in long-term spatial learning deficits. Psychoneuroendocrinology 2007, 32:734-745.
84. Smith M.A., Makino S., Kvetnansky R., Post R.M. Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus. J Neurosci 1995, 15:1768-1777.
85. The DASIS report: primary methampetamine/amphetamine admissions to substance abuse treatment: 2005 2008, Substance Abuse and Mental Health Services Administration OoAS, Rockville, MD.
86. Szumlinski K.K., Haskew R.E., Balogun M.Y., Maisonneuve I.M., Glick S.D. Iboga compounds reverse the behavioural disinhibiting and corticosterone effects of acute methamphetamine: implications for their antiaddictive properties. Pharmacol Biochem Behav 2001, 69:485-491.
87. Thoenen H. Neurotrophins and neuronal plasticity. Science 1995, 270:593-598.
88. Weinshenker D., Ferrucci M., Busceti C.L., Biagioni F., Lazzeri G., Liles L.C., Lenzi P., Pasquali L., Murri L., Paparelli A., Fornai F. Genetic or pharmacological blockade of noradrenaline synthesis enhances the neurochemical, behavioral, and neurotoxic effects of methamphetamine. J Neurochem 2008, 105:471-483.
89. Wilson J.M., Kalasinsky K.S., Levey A.I., Bergeron C., Reiber G., Anthony R.M., Schmunk G.A., Shannak K., Haycock J.W., Kish S.J. Striatal dopamine nerve terminal markers in human, chronic methamphetamine users. Nat Med 1996, 2:699-703.
90. Yang J., Siao C.J., Nagappan G., Marinic T., Jing D., McGrath K., Chen Z.Y., Mark W., Tessarollo L., Lee F.S., Lu B., Hempstead B.L. Neuronal release of proBDNF. Nat Neurosci 2009, 12:113-115.
91. Yurek D.M., Seroogy K.B. Neurotrophic factor protection of dopaminergic neurons. Neurobiology of the neurotrophins 2001, 355-397. F.P. Graham Publishing, Johnson City, TN. I. Mocchetti (Ed.).