Fluoxetine potentiation of methylphenidate-induced neuropeptide expression in the striatum occurs selectively in direct pathway (striatonigral) neurons

Journal of Neurochemistry

Volumn 122, Issue 5, 2012, Pages 1054-1064

  Van Waes, Vincent ^a,b   Carr, Betsy ^a   Beverley, Joel A ^a   Steiner, Heinz ^a  

^a ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

^b UNIVERSITÉ DE FRANCHE COMTÉ   (France)

Author keywords

dynorphin; methylphenidate; psychostimulant; SSRI; striatum; substance P

Indexed keywords

COCAINE; DYNORPHIN; ENKEPHALIN; FLUOXETINE; METHYLPHENIDATE; SUBSTANCE P;

ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; BRAIN TISSUE; CONTROLLED STUDY; CORPUS STRIATUM; DRUG EFFECT; DRUG POTENTIATION; GENE CONTROL; GENE EXPRESSION; HISTOCHEMISTRY; IMMEDIATE EARLY GENE; IN SITU HYBRIDIZATION; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; RAT; STRIATONIGRAL NEURON;

ANIMALS; AUTORADIOGRAPHY; CENTRAL NERVOUS SYSTEM STIMULANTS; CORPUS STRIATUM; DRUG SYNERGISM; DYNORPHINS; EARLY GROWTH RESPONSE PROTEIN 1; ENKEPHALINS; FLUOXETINE; GENE EXPRESSION REGULATION; MALE; METHYLPHENIDATE; NEURAL PATHWAYS; NEURONS; NEUROPEPTIDES; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; SEROTONIN UPTAKE INHIBITORS; SUBSTANCE P; SUBSTANTIA NIGRA;

EID: 84865328236     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2012.07852.x     Document Type: Article

References (68)

1. Alburges M. E., Hoonakker A. J., Horner K. A., Fleckenstein A. E., and, Hanson G. R., (2011) Methylphenidate alters basal ganglia neurotensin systems through dopaminergic mechanisms: a comparison with cocaine treatment. J. Neurochem. 117, 470-478.
2. Berke J. D., and, Hyman S. E., (2000) Addiction, dopamine, and the molecular mechanisms of memory. Neuron 25, 515-532.
3. Bhat R. V., and, Baraban J. M., (1993) Activation of transcription factor genes in striatum by cocaine: role of both serotonin and dopamine systems. J. Pharmacol. Exp. Ther. 267, 496-505. (Pubitemid 23325045)
4. Bhatara V., Feil M., Hoagwood K., Vitiello B., and, Zima B., (2004) National trends in concomitant psychotropic medication with stimulants in pediatric visits: practice versus knowledge. J. Atten. Disord. 7, 217-226. (Pubitemid 38891300)
5. Brandon C. L., and, Steiner H., (2003) Repeated methylphenidate treatment in adolescent rats alters gene regulation in the striatum. Eur. J. Neurosci. 18, 1584-1592. (Pubitemid 37215111)
6. Brandon C. L., Marinelli M., Baker L. K., and, White F. J., (2001) Enhanced reactivity and vulnerability to cocaine following methylphenidate treatment in adolescent rats. Neuropsychopharmacology 25, 651-661. (Pubitemid 32995947)
7. Bubar M. J., and, Cunningham K. A., (2008) Prospects for serotonin 5-HT2R pharmacotherapy in psychostimulant abuse. Prog. Brain Res. 172, 319-346.
8. Cenci M. A., and, Björklund A., (1993) Transection of corticostriatal afferents reduces amphetamine- and apomorphine-induced striatal Fos expression and turning behaviour in unilaterally 6-hydroxydopamine-lesioned rats. Eur. J. Neurosci. 5, 1062-1070. (Pubitemid 23239792)
9. Cotterly L., Beverley J. A., Yano M., and, Steiner H., (2007) Dysregulation of gene induction in corticostriatal circuits after repeated methylphenidate treatment in adolescent rats: differential effects on zif 268 and homer 1a. Eur. J. Neurosci. 25, 3617-3628. (Pubitemid 47020439)
10. Csoka A., Bahrick A., and, Mehtonen O. P., (2008) Persistent sexual dysfunction after discontinuation of selective serotonin reuptake inhibitors. J. Sex. Med. 5, 227-233.
11. Di Chiara G., and, Imperato A., (1988) Opposite effects of mu and kappa opiate agonists on dopamine release in the nucleus accumbens and in the dorsal caudate of freely moving rats. J. Pharmacol. Exp. Ther. 244, 1067-1080. (Pubitemid 18090131)
12. DSMMD (2000) Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition. American Psychiatric Association, Washington, DC.
13. Everitt B. J., and, Robbins T. W., (2005) Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat. Neurosci. 8, 1481-1489. (Pubitemid 41573659)
14. Ferguson S. M., and, Robinson T. E., (2004) Amphetamine-evoked gene expression in striatopallidal neurons: regulation by corticostriatal afferents and the ERK/MAPK signaling cascade. J. Neurochem. 91, 337-348. (Pubitemid 39363433)
15. Frankel P. S., Alburges M. E., Bush L., Hanson G. R., and, Kish S. J., (2008) Striatal and ventral pallidum dynorphin concentrations are markedly increased in human chronic cocaine users. Neuropharmacology 55, 41-46.
16. Fuchs R. A., Branham R. K., and, See R. E., (2006) Different neural substrates mediate cocaine seeking after abstinence versus extinction training: a critical role for the dorsolateral caudate-putamen. J. Neurosci. 26, 3584-3588.
17. Gardier A. M., Moratalla R., Cuellar B., Sacerdote M., Guibert B., Lebrec H., and, Graybiel A. M., (2000) Interaction between the serotoninergic and dopaminergic systems in d-fenfluramine-induced activation of c-fos and jun B genes in rat striatal neurons. J. Neurochem. 74, 1363-1373. (Pubitemid 30163955)
18. Gerfen C. R., and, Young W. S. III, (1988) Distribution of striatonigral and striatopallidal peptidergic neurons in both patch and matrix compartments: an in situ hybridization histochemistry and fluorescent retrograde tracing study. Brain Res. 460, 161-167.
19. Gerfen C. R., Engber T. M., Mahan L. C., Susel Z., Chase T. N., Monsma F. J. Jr, and, Sibley D. R., (1990) D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. Science 250, 1429-1432. (Pubitemid 120031867)
20. Gerfen C. R., McGinty J. F., and, Young W. S. III, (1991) Dopamine differentially regulates dynorphin, substance P, and enkephalin expression in striatal neurons: in situ hybridization histochemical analysis. J. Neurosci. 11, 1016-1031.
21. Greely H., Sahakian B., Harris J., Kessler R. C., Gazzaniga M., Campbell P., and, Farah M. J., (2008) Towards responsible use of cognitive-enhancing drugs by the healthy. Nature 456, 702-705.
22. Guerra M. J., Liste I., and, Labandeira-Garcia J. L., (1998) Interaction between the serotonergic, dopaminergic, and glutamatergic systems in fenfluramine-induced Fos expression in striatal neurons. Synapse 28, 71-82. (Pubitemid 128770605)
23. Hanson G. R., Singh N., Merchant K., Johnson M., and, Gibb J. W., (1995) The role of NMDA receptor systems in neuropeptide responses to stimulants of abuse. Drug Alcohol Depend. 37, 107-110.
24. Heiman M., Schaefer A., Gong S., et al. (2008) A translational profiling approach for the molecular characterization of CNS cell types. Cell 135, 738-748.
25. Horner K. A., Adams D. H., Hanson G. R., and, Keefe K. A., (2005) Blockade of stimulant-induced preprodynorphin mRNA expression in the striatal matrix by serotonin depletion. Neuroscience 131, 67-77. (Pubitemid 40170489)
26. Hurd Y. L., and, Herkenham M., (1993) Molecular alterations in the neostriatum of human cocaine addicts. Synapse 13, 357-369. (Pubitemid 23104541)
27. Hyman S. E., and, Nestler E. J., (1996) Initiation and adaptation: a paradigm for understanding psychotropic drug action. Am. J. Psychiatry 153, 151-162. (Pubitemid 26038955)
28. Ishii M., Tatsuzawa Y., Yoshino A., and, Nomura S., (2008) Serotonin syndrome induced by augmentation of SSRI with methylphenidate. Psychiatry Clin Neurosci 62, 246. (Pubitemid 351537721)
29. Keefe K. A., and, Horner K. A,. (2010) Neurotransmitter regulation of basal ganglia gene expression, in Handbook of Basal Ganglia Structure and Function (, Steiner H., and, Tseng K. Y,., eds), pp. 461-490. Academic Press/Elsevier, London.
30. Kim Y., Teylan M. A., Baron M., Sands A., Nairn A. C., and, Greengard P., (2009) Methylphenidate-induced dendritic spine formation and DeltaFosB expression in nucleus accumbens. Proc. Natl Acad. Sci. USA 106, 2915-2920.
31. Knapska E., and, Kaczmarek L., (2004) A gene for neuronal plasticity in the mammalian brain: zif268/Egr-1/NGFI-A/Krox-24/TIS8/ZENK? Prog. Neurobiol. 74, 183-211. (Pubitemid 39535508)
32. Kollins S. H., (2008) ADHD, substance use disorders, and psychostimulant treatment: current literature and treatment guidelines. J. Atten. Disord. 12, 115-125.
33. Kollins S. H., MacDonald E. K., and, Rush C. R., (2001) Assessing the abuse potential of methylphenidate in nonhuman and human subjects: a review. Pharmacol. Biochem. Behav. 68, 611-627.
34. Lavretsky H., Kim M. D., Kumar A., and, Reynolds C. F., (2003) Combined treatment with methylphenidate and citalopram for accelerated response in the elderly: an open trial. J Clin. Psychiatry 64, 1410-1414. (Pubitemid 41270097)
35. Le Moine C., and, Bloch B., (1995) D1 and D2 dopamine receptor gene expression in the rat striatum: sensitive cRNA probes demonstrate prominent segregation of D1 and D2 mRNAs in distinct neuronal populations of the dorsal and ventral striatum. J. Comp. Neurol. 355, 418-426.
36. Lobo M. K., and, Nestler E. J., (2011) The striatal balancing act in drug addiction: distinct roles of direct and indirect pathway medium spiny neurons. Front. Neuroanat. 5, 41.
37. Marinelli M., Barrot M., Simon H., Oberlander C., Dekeyne A., Le Moal M., and, Piazza P. V., (1998) Pharmacological stimuli decreasing nucleus accumbens dopamine can act as positive reinforcers but have a low addictive potential. Eur. J. Neurosci. 10, 3269-3275. (Pubitemid 29070623)
38. Muller C. P., and, Huston J. P., (2006) Determining the region-specific contributions of 5-HT receptors to the psychostimulant effects of cocaine. Trends Pharmacol. Sci. 27, 105-112. (Pubitemid 43184032)
39. Nelson J. C., (2007) Augmentation strategies in the treatment of major depressive disorder. Recent findings and current status of augmentation strategies. CNS Spectr. 12 (Suppl. 22), 6-9.
40. Nestler E. J., and, Carlezon W. A. J., (2006) The mesolimbic dopamine reward circuit in depression. Biol. Psychiatry 59, 1151-1159. (Pubitemid 44192421)
41. Paxinos G., and, Watson C,. (1998) The Rat Brain in Stereotaxic Coordinates. Academic Press, New York.
42. Ravindran A. V., Kennedy S. H., O'Donovan M. C., Fallu A., Camacho F., and, Binder C. E., (2008) Osmotic-release oral system methylphenidate augmentation of antidepressant monotherapy in major depressive disorder: results of a double-blind, randomized, placebo-controlled trial. J Clin. Psychiatry 69, 87-94. (Pubitemid 351282001)
43. Reiner A., and, Anderson K. D., (1990) The patterns of neurotransmitter and neuropeptide cooccurrence among striatal projection neurons: conclusions based on recent findings. Brain Res. Rev. 15, 251-265.
44. Safer D. J., Zito J. M., and, DosReis S., (2003) Concomitant psychotropic medication for youths. Am. J. Psychiatry 160, 438-449. (Pubitemid 41102118)
45. See R. E., Elliott J. C., and, Feltenstein M. W., (2007) The role of dorsal vs ventral striatal pathways in cocaine-seeking behavior after prolonged abstinence in rats. Psychopharmacology 194, 321-331. (Pubitemid 47389350)
46. Shippenberg T. S., Zapata A., and, Chefer V. I., (2007) Dynorphin and the pathophysiology of drug addiction. Pharmacol. Ther. 116, 306-321. (Pubitemid 47454747)
47. Spanagel R., Herz A., and, Shippenberg T. S., (1992) Opposing tonically active endogenous opioid systems modulate the mesolimbic dopaminergic pathway. Proc. Natl Acad. Sci. USA 89, 2046-2050.
48. Spangler R., Zhou Y., Maggos C. E., Schlussman S. D., Ho A., and, Kreek M. J., (1997) Prodynorphin, proenkephalin and kappa opioid receptor mRNA responses to acute 'binge' cocaine. Mol. Brain Res. 44, 139-142. (Pubitemid 27050870)
49. Steiner H,. (2010) Psychostimulant-induced gene regulation in corticostriatal circuits, in Handbook of Basal Ganglia Structure and Function (, Steiner H., and, Tseng K. Y,., eds), pp 501-525. Academic Press/Elsevier, London.
50. Steiner H., and, Gerfen C. R., (1993) Cocaine-induced c-fos messenger RNA is inversely related to dynorphin expression in striatum. J. Neurosci. 13, 5066-5081. (Pubitemid 24000994)
51. Steiner H., and, Gerfen C. R., (1998) Role of dynorphin and enkephalin in the regulation of striatal output pathways and behavior. Exp. Brain Res. 123, 60-76. (Pubitemid 28495297)
52. Steiner H., and, Gerfen C. R., (1999) Enkephalin regulates acute D2 dopamine receptor antagonist-induced immediate-early gene expression in striatal neurons. Neuroscience 88, 795-810. (Pubitemid 28518258)
53. Steiner H., and, Kitai S. T., (2000) Regulation of rat cortex function by D1 dopamine receptors in the striatum. J. Neurosci. 20, 5449-5460. (Pubitemid 30457741)
54. Steiner H., and, Van Waes V,. (2012) Addiction-related gene regulation: risks of exposure to cognitive enhancers and other psychostimulants. ILAR J. 53, in press.
55. Steiner H., Van Waes V., and, Marinelli M., (2010) Fluoxetine potentiates methylphenidate-induced gene regulation in addiction-related brain regions: concerns for use of cognitive enhancers? Biol. Psychiatry 67, 592-594.
56. Surmeier D. J., Song W.-J., and, Yan Z., (1996) Coordinated expression of dopamine receptors in neostriatal medium spiny neurons. J. Neurosci. 16, 6579-6591. (Pubitemid 26337379)
57. Swanson J. M., and, Volkow N. D., (2008) Increasing use of stimulants warns of potential abuse. Nature 453, 586. (Pubitemid 351769275)
58. Unal C. T., Beverley J. A., Willuhn I., and, Steiner H., (2009) Long-lasting dysregulation of gene expression in corticostriatal circuits after repeated cocaine treatment in adult rats: effects on zif 268 and homer 1a. Eur. J. Neurosci. 29, 1615-1626.
59. Van Waes V., Beverley J., Marinelli M., and, Steiner H., (2010) Selective serotonin reuptake inhibitor antidepressants potentiate methylphenidate (Ritalin)-induced gene regulation in the adolescent striatum. Eur. J. Neurosci. 32, 435-447.
60. Vanderschuren L. J., Di Ciano P., and, Everitt B. J., (2005) Involvement of the dorsal striatum in cue-controlled cocaine seeking. J. Neurosci. 25, 8665-8670. (Pubitemid 41362043)
61. Wang J. Q., and, McGinty J. F., (1996) D1 and D2 receptor regulation of preproenkephalin and preprodynorphin mRNA in rat striatum following acute injection of amphetamine or methamphetamine. Synapse 22, 114-122. (Pubitemid 26041230)
62. Warren B. L., Iñiguez S. D., Alcantara L. F., Wright K. N., Parise E. M., Weakley S. K., and, Bolaños-Guzmán C. A., (2011) Juvenile administration of concomitant methylphenidate and fluoxetine alters behavioral reactivity to reward- and mood-related stimuli and disrupts ventral tegmental area gene expression in adulthood. J. Neurosci. 31, 10347-10358.
63. Weikop P., Yoshitake T., and, Kehr J., (2007) Differential effects of adjunctive methylphenidate and citalopram on extracellular levels of serotonin, noradrenaline and dopamine in the rat brain. Eur. Neuropsychopharmacol. 17, 658-671. (Pubitemid 47277501)
64. Willuhn I., Sun W., and, Steiner H., (2003) Topography of cocaine-induced gene regulation in the rat striatum: relationship to cortical inputs and role of behavioural context. Eur. J. Neurosci. 17, 1053-1066. (Pubitemid 36411602)
65. Yano M., and, Steiner H., (2005a) Methylphenidate (Ritalin) induces Homer 1a and zif 268 expression in specific corticostriatal circuits. Neuroscience 132, 855-865.
66. Yano M., and, Steiner H., (2005b) Topography of methylphenidate (Ritalin)-induced gene regulation in the striatum: differential effects on c-fos, substance P and opioid peptides. Neuropsychopharmacology 30, 901-915. (Pubitemid 40570906)
67. Yano M., and, Steiner H., (2007) Methylphenidate and cocaine: the same effects on gene regulation? Trends Pharmacol. Sci. 28, 588-596. (Pubitemid 350026614)
68. Yano M., Beverley J. A., and, Steiner H., (2006) Inhibition of methylphenidate-induced gene expression in the striatum by local blockade of D1 dopamine receptors: interhemispheric effects. Neuroscience 140, 699-709.