κ-opioid system regulates the long-lasting behavioral adaptations induced by early-life exposure to methylphenidate

Neuropsychopharmacology

Volumn 34, Issue 5, 2009, Pages 1339-1350

  Wiley, Matthew D ^a   Poveromo, Laura B ^a   Antapasis, John ^a   Herrera, Carolina M ^a   Bolãos Guzmán, Carlos A ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

Author keywords

Depression; Methylphenidate; nor BNI; Rat; U 50488

Indexed keywords

3,4 DICHLORO N METHYL N [2 (1 PYRROLIDINYL)CYCLOHEXYL]BENZENEACETAMIDE; BINALTORPHIMINE; COCAINE; DYNORPHIN; KAPPA OPIATE RECEPTOR; LIGAND; METHYLPHENIDATE; SODIUM CHLORIDE; SUCROSE;

ADAPTATION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; AVERSIVE BEHAVIOR; CONDITIONING; CONTROLLED STUDY; DEPRESSION; DRUG DOSE INCREASE; EMOTION; FOOD PREFERENCE; FORCED SWIMMING TEST; MALE; MAZE TEST; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; SPRAGUE DAWLEY RAT; STRESS;

3,4-DICHLORO-N-METHYL-N-(2-(1-PYRROLIDINYL)-CYCLOHEXYL)-BENZENEACETAMIDE, (TRANS)-ISOMER; ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; CENTRAL NERVOUS SYSTEM STIMULANTS; COCAINE; CONDITIONING (PSYCHOLOGY); FOOD PREFERENCES; MALE; METHYLPHENIDATE; MOTOR ACTIVITY; NALTREXONE; PSYCHOTROPIC DRUGS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, OPIOID, KAPPA; STRESS, PSYCHOLOGICAL;

EID: 62349092331     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/npp.2008.188     Document Type: Article

References (72)

1. Andersen SL, Arvanitogiannis A, Pliakas AM, LeBlanc C, Carlezon Jr WA (2002). Altered responsiveness to cocaine in rats exposed to methylphenidate during development. Nat Neurosci 5: 13-14.
2. Andersen SL, Navalta CP (2004). Altering the course of neurodevelopment: a framework for understanding the enduring effects of psychotropic drugs. Int J Dev Neurosci 22: 423-440.
3. Arnsten AF (2006). Stimulants: therapeutic actions in ADHD. Neuropsychopharmacology 31: 2376-2383.
4. Askenasy EP, Taber KH, Yang PB, Dafny N (2007). Methylphenidate (Ritalin): behavioral studies in the rat. Int J Neurosci 117: 757-794.
5. Badiani A, Rajabi H, Nencini P, Stewart J (2001). Modulation of food intake by the kappa opioid U-50,488H: evidence for an effect on satiation. Behav Brain Res 118: 179-186.
6. Berton O, McClung CA, Dileone RJ, Krishnan V, Renthal W, Russo SJ et al. (2006). Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311: 864-868.
7. Biederman J, Faraone SV (2004). Attention deficit hyperactivity disorder: a worldwide concern. J Nerv Ment Dis 192: 453-454.
8. Biederman J, Faraone SV (2005). Attention-deficit hyperactivity disorder. Lancet 366: 237-248.
9. Bolaños CA, Barrot M, Berton O, Wallace-Black D, Nestler EJ (2003). Methylphenidate treatment during pre- and periadolescence alters behavioral responses to emotional stimuli at adulthood. Biol Psychiatry 54: 1317-1329.
10. Bolaños CA, Garmsen GM, Clair MA, McDougall SA (1996). Effects of the kappa-opioid receptor agonist U-50,488 on morphine-induced place preference conditioning in the developing rat. Eur J Pharmacol 317: 1-8.
11. Bolaños CA, Wiley MD, Maffeo ML, Powers KD, Kinka DW, Grausam KB et al. (2008). Antidepressant treatment can normalize adult behavioral deficits induced by early-life exposure to methylphenidate. Biol Psychiatry 63: 309-316.
12. Britton GB, Segan AT, Sejour J, Mancebo SE (2007). Early exposure to methylphenidate increases fear responses in an aversive context in adult rats. Dev Psychobiol 49: 265-275.
13. Carlezon Jr WA, Beguin C, DiNieri JA, Baumann MH, Richards MR, Todtenkopf MS et al. (2006). Depressive-like effects of the kappa-opioid receptor agonist salvinorin A on behavior and neurochemistry in rats. J Pharmacol Exp Ther 316: 440-447.
14. Carlezon Jr WA, Konradi C (2004). Understanding the neurobiological consequences of early exposure to psychotropic drugs: linking behavior with molecules. Neuropharmacology 47: 47-60.
15. Carlezon Jr WA, Mague SD, Andersen SL (2003). Enduring behavioral effects of early exposure to methylphenidate in rats. Biol Psychiatry 54: 1330-1337.
16. Carlezon Jr WA, Thome J, Olson VG, Lane-Ladd SB, Brodkin ES, Hiroi N et al. (1998). Regulation of cocaine reward by CREB. Science 282: 2272-2275.
17. Charntikov S, Halladay LR, Herbert MS, Marquez EM, McDougall SA (2008). Effects of dorsal striatal infusions of R(-)-propylnorapomorphine on kappa-opioid-mediated locomotor activity in the young rat: possible role of the indirect pathway. Neuroscience 155: 603-612.
18. Chavkin C, James IF, Goldstein A (1982). Dynorphin is a specific endogenous ligand of the kappa opioid receptor. Science 215: 413-415.
19. Collins RL, Zavala AR, Ingersoll VY, Duke MA, Crawford CA, McDougall SA (1998). Kappa opioid-mediated behavioral sensitization in the preweanling rat: relationship to Fos immunoreactivity. Psychopharmacology (Berl) 137: 282-291.
20. Corbett AD, Paterson SJ, McKnight AT, Magnan J, Kosterlitz HW (1982). Dynorphin and dynorphin are ligands for the kappa-subtype of opiate receptor. Nature 299: 79-81.
21. Crawford CA, McDougall SA, Bolanos CA, Hall S, Berger SP (1995). The effects of the kappa agonist U-50488 on cocaine-induced conditioned and unconditioned behaviors and Fos immunoreactivity. Psychopharmacology (Berl) 120: 392-399.
22. Crawford CA, Villafranca SW, Cyr MC, Farley CM, Reichel CM, Gheorghe SL et al. (2007). Effects of early methylphenidate exposure on morphine- and sucrose-reinforced behaviors in adult rats: relationship to dopamine D2 receptors. Brain Res 1139: 245-253.
23. Cryan JF, Markou A, Lucki I (2002). Assessing antidepressant activity in rodents: recent developments and future needs. Trends Pharmacol Sci 23: 238-245.
24. Di Chiara G, 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.
25. Endoh T, Matsuura H, Tanaka C, Nagase H (1992). Norbinaltorphimine: a potent and selective kappa-opioid receptor antagonist with long-lasting activity in vivo. Arch Int Pharmacodyn Ther 316: 30-42.
26. Ettenberg A (2004). Opponent process properties of self-administered cocaine. Neurosci Biobehav Rev 27: 721-728.
27. Federici M, Geracitano R, Bernardi G, Mercuri NB (2005). Actions of methylphenidate on dopaminergic neurons of the ventral midbrain. Biol Psychiatry 57: 361-365.
28. Gualtieri CT, Wargin W, Kanoy R, Patrick K, Shen CD, Youngblood W et al. (1982). Clinical studies of methylphenidate serum levels in children and adults. J Am Acad Child Psychiatry 21: 19-26.
29. Horan P, Taylor J, Yamamura HI, Porreca F (1992). Extremely long-lasting antagonistic actions of nor-binaltorphimine (nor-BNI) in the mouse tail-flick test. J Pharmacol Exp Ther 260: 1237-1243.
30. Hyman SE (2003). Methylphenidate-induced plasticity: what should we be looking for? Biol Psychiatry 54: 1310-1311.
31. Iñiguez SD, Warren BL, Neve RL, Nestler EJ, Russo SJ, Bolaños-Guzmán CA (2008). Insulin receptor substrate-2 in the ventral tegmental area regulates behavioral responses to cocaine. Synapse 122: 1172-1177.
32. Jewett DC, Woods JH (1995). Nor-binaltorphimine: an ultra-long acting kappa-opioid antagonist in pigeons. Behav Pharmacol 6: 815-820.
33. Knoll AT, Meloni EG, Thomas JB, Carroll FI, Carlezon Jr WA (2007). Anxiolytic-like effects of kappa-opioid receptor antagonists in models of unlearned and learned fear in rats. J Pharmacol Exp Ther 323: 838-845.
34. Koob GF, Sanna PP, Bloom FE (1998). Neuroscience of addiction. Neuron 21: 467-476.
35. Krishnan V, Han MH, Mazei-Robison M, Iniguez SD, Ables JL, Vialou V et al. (2008). AKT signaling within the ventral tegmental area regulates cellular and behavioral responses to stressful stimuli. Biol Psychiatry 64: 691-700.
36. Kuczenski R, Segal DS (2005). Stimulant actions in rodents: implications for attention-deficit/hyperactivity disorder treatment and potential substance abuse. Biol Psychiatry 57: 1391-1396.
37. Kuzmin A, Sandin J, Terenius L, Ogren SO (2000). Dose- and time-dependent bimodal effects of kappa-opioid agonists on locomotor activity in mice. J Pharmacol Exp Ther 295: 1031-1042.
38. Kuzmin AV, Semenova S, Gerrits MA, Zvartau EE, Van Ree JM (1997). Kappa-opioid receptor agonist U50,488H modulates cocaine and morphine self-administration in drug-naive rats and mice. Eur J Pharmacol 321: 265-271.
39. Land BB, Bruchas MR, Lemos JC, Xu M, Melief EJ, Chavkin C (2008). The dysphoric component of stress is encoded by activation of the dynorphin kappa-opioid system. J Neurosci 28: 407-414.
40. Lucki I (1997). The forced swimming test as a model for core and component behavioral effects of antidepressant drugs. Behav Pharmacol 8: 523-532.
41. Mague SD, Andersen SL, Carlezon Jr WA (2005). Early developmental exposure to methylphenidate reduces cocaine-induced potentiation of brain stimulation reward in rats. Biol Psychiatry 57: 120-125.
42. Mague SD, Pliakas AM, Todtenkopf MS, Tomasiewicz HC, Zhang Y, Stevens Jr WC et al. (2003). Antidepressant-like effects of kappa-opioid receptor antagonists in the forced swim test in rats. J Pharmacol Exp Ther 305: 323-330.
43. Maisonneuve IM, Archer S, Glick SD (1994). U50488, a kappa opioid receptor agonist, attenuates cocaine-induced increases in extracellular dopamine in the nucleus accumbens of rats. Neurosci Lett 181: 57-60.
44. Manzanares J, Lookingland KJ, Moore KE (1991). Kappa opioid receptor-mediated regulation of dopaminergic neurons in the rat brain. J Pharmacol Exp Ther 256: 500-505.
45. McDougall SA, Garmsen GM, Meier TL, Crawford CA (1997). Kappa opioid mediated locomotor activity in the preweanling rat: role of pre- and postsynaptic dopamine receptors. Psychopharmacology (Berl) 133: 62-68.
46. McLaughlin JP, Marton-Popovici M, Chavkin C (2003). Kappa opioid receptor antagonism and prodynorphin gene disruption block stress-induced behavioral responses. J Neurosci 23: 5674-5683.
47. Mucha RF, Herz A (1985). Motivational properties of kappa and mu opioid receptor agonists studied with place and taste preference conditioning. Psychopharmacology (Berl) 86: 274-280.
48. Nestler EJ, Barrot M, DiLeone RJ, Eisch AJ, Gold SJ, Monteggia LM (2002). Neurobiology of depression. Neuron 34: 13-25.
49. Nestler EJ, Carlezon Jr WA (2006). The mesolimbic dopamine reward circuit in depression. Biol Psychiatry 59: 1151-1159.
50. Olson VG, Zabetian CP, Bolanos CA, Edwards S, Barrot M, Eisch AJ et al. (2005). Regulation of drug reward by cAMP response element-binding protein: evidence for two functionally distinct subregions of the ventral tegmental area. J Neurosci 25: 5553-5562.
51. Pliakas AM, Carlson RR, Neve RL, Konradi C, Nestler EJ, Carlezon Jr WA (2001). Altered responsiveness to cocaine and increased immobility in the forced swim test associated with elevated cAMP response element-binding protein expression in nucleus accumbens. J Neurosci 21: 7397-7403.
52. Rey JM, Sawyer MG (2003). Are psychostimulant drugs being used appropriately to treat child and adolescent disorders? Br J Psychiatry 182: 284-286.
53. Ruegg H, Yu WZ, Bodnar RJ (1997). Opioid-receptor subtype agonist-induced enhancements of sucrose intake are dependent upon sucrose concentration. Physiol Behav 62: 121-128.
54. Sampson D, Muscat R, Phillips G, Willner P (1992). Decreased reactivity to sweetness following chronic exposure to mild unpredictable stress or acute administration of pimozide. Neurosci Biobehav Rev 16: 519-524.
55. Shippenberg TS, Herz A (1986). Differential effects of mu and kappa opioid systems on motivational processes. NIDA Res Monogr 75: 563-566.
56. Shippenberg TS, Zapata A, Chefer VI (2007). Dynorphin and the pathophysiology of drug addiction. Pharmacol Ther 116: 306-321.
57. Spanagel R, Herz A, Shippenberg TS (1992). Opposing tonically active endogenous opioid systems modulate the mesolimbic dopaminergic pathway. Proc Natl Acad Sci USA 89: 2046-2050.
58. Spangler R, Ho A, Zhou Y, Maggos CE, Yuferov V, Kreek MJ (1996). Regulation of kappa opioid receptor mRNA in the rat brain by 'binge' pattern cocaine administration and correlation with preprodynorphin mRNA. Brain Res Mol Brain Res 38: 71-76.
59. Spear LP (2007). Assessment of adolescent neurotoxicity: rationale and methodological considerations. Neurotoxicol Teratol 29: 1-9.
60. Spruijt BM, Welbergen P, Brakkee J, Gispen WH (1988). An ethological analysis of excessive grooming in young and aged rats. Ann N Y Acad Sci 525: 89-100.
61. Takemori AE, Ho BY, Naeseth JS, Portoghese PS (1988). Norbinaltorphimine, a highly selective kappa-opioid antagonist in analgesic and receptor binding assays. J Pharmacol Exp Ther 246: 255-258.
62. Trujillo KA, Akil H (1990). Pharmacological regulation of striatal prodynorphin peptides. Prog Clin Biol Res 328: 223-226.
63. Turchan J, Przewlocka B, Lason W, Przewlocki R (1998). Effects of repeated psychostimulant administration on the prodynorphin system activity and kappa opioid receptor density in the rat brain. Neuroscience 85: 1051-1059.
64. Unterwald EM, Rubenfeld JM, Kreek MJ (1994). Repeated cocaine administration upregulates kappa and mu, but not delta, opioid receptors. Neuroreport 5: 1613-1616.
65. Vitiello B (2001). Psychopharmacology for young children: clinical needs and research opportunities. Pediatrics 108: 983-989.
66. Volkow ND (2004). The reality of comorbidity: depression and drug abuse. Biol Psychiatry 56: 714-717.
67. Volkow ND, Insel TR (2003). What are the long-term effects of methylphenidate treatment? Biol Psychiatry 54: 1307-1309.
68. Wooters TE, Neugebauer NM, Rush CR, Bardo MT (2008). Methylphenidate enhances the abuse-related behavioral effects of nicotine in rats: intravenous self-administration, drug discrimination, and locomotor cross-sensitization. Neuropsychopharmacology 33: 1137-1148.
69. Yano M, Steiner H (2005). Topography of methylphenidate (ritalin)-induced gene regulation in the striatum: differential effects on c-fos, substance P and opioid peptides. Neuropsychopharmacology 30: 901-915.
70. You ZB, Herrera-Marschitz M, Terenius L (1999). Modulation of neurotransmitter release in the basal ganglia of the rat brain by dynorphin peptides. J Pharmacol Exp Ther 290: 1307-1315.
71. Zhang H, Shi YG, Woods JH, Watson SJ, Ko MC (2007). Central kappa-opioid receptor-mediated antidepressant-like effects of nor-Binaltorphimine: behavioral and BDNF mRNA expression studies. Eur J Pharmacol 570: 89-96.
72. Zito JM, Safer DJ, dosReis S, Gardner JF, Boles M, Lynch F (2000). Trends in the prescribing of psychotropic medications to preschoolers. JAMA 283: 1025-1030.