Intermittent Morphine Administration Induces Dependence and is a Chronic Stressor in Rats

Neuropsychopharmacology

Volumn 28, Issue 11, 2003, Pages 1960-1972

  Houshyar, Hani ^a   Gomez, Francisca ^a   Manalo, Sotara ^a   Bhargava, Aditi ^a   Dallman, Mary F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Dependence; Energy balance; HPA axis; Morphine; Stress; Withdrawal

Indexed keywords

CORTICOTROPIN; CORTICOTROPIN RELEASING FACTOR; INSULIN; LEPTIN; MORPHINE; SODIUM CHLORIDE; TESTOSTERONE;

ADOLESCENT; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; DOSE RESPONSE; ENERGY BALANCE; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; INSULIN BLOOD LEVEL; MALE; MORPHINE ADDICTION; NONHUMAN; PRIORITY JOURNAL; RAT; STRESS; STRIA TERMINALIS; TESTOSTERONE BLOOD LEVEL; THALAMUS MIDLINE NUCLEUS; WEIGHT GAIN; WEIGHT REDUCTION;

EID: 0242491721     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.npp.1300271     Document Type: Article

References (70)

1. Ahtee L, Atilla MJ, Calson KR, Haikala (1989). Changes in brain monoamine metabolism during withdrawal from oral self-administration of morphine and in response to a morphine challenge in the withdrawn state. J Pharmacol Exp Ther 249: 303-310.
2. Akana SF, Cascio CS, Shinsako J, Dallman MF (1985). Corticosterone: narrow range required for normal body and thymus weight and ACTH. Am J Physiol 249: R527-R532.
3. Akana SF, Strack AM, Hanson ES, Horsley CJ, Milligan ED, Bhatnagar S et al (1999). Interactions among chronic cold, corticosterone and puberty on energy intake and deposition. Stress 3: 131-146.
4. Bartness TJ (1998). Innervation of mammalian white adipose tissue: implications for the regulation of total body fat. Am J Physiol 275: R1399-R1411.
5. Blanchard RJ, Nikulina JN, Sakai RR, McKittrick C, McEwen B, Blanchard DC (1998). Behavioral and endocrine change following chronic predatory stress. Physiol Behav 63: 561-569.
6. Boghossian S, Jourdan D, Dacher M, Alliot J (2001). Effect of morphine on caloric intake and macronutrient selection in male and female Lou/c/jall rats during aging. Mech Ageing Dev 122: 1825-1839.
7. Brown MR, Fisher LA, Rivier J, Spiess J, Rivier C, Vale W (1981). Corticotropin-releasing factor: effects on the sympathetic nervous system and oxygen consumption. Life Sci 30: 207-210.
8. Buckingham JC (1982). Effects of adrenocortical and gonadal steroids on the secretion in vitro of corticotrophin and its hypothalamic releasing factor. J Endocrinol 93: 123-132.
9. Buwalda B, de Boer SF, Van Kalkeren AA, Koolhaas JM (1997). Physiological and behavioral effects of chronic intracerebroventricular infusion of corticotropin-releasing factor in the rat. Psychoneuroendocrinology 22: 297-309.
10. Cami J, Gilabert CM, San L, de la Torre R (1992). Hypercortisolism after opioid discontinuation in rapid detoxification of heroin addicts. Br J Addict 87: 1145-1151.
11. Cano G, Card JP, Rinaman L, Sved A (2000). Connections of Barrington's nucleus to the sympathetic nervous system in rats. J Autonomic Nervous System 79: 117-128.
12. Chang SL, Patel NA, Romero AA, Thompson J, Zadina JE (1996). FOS expression induced by interleukin-1 or acute morphine treatment in the rat hypothalamus is attenuated by chronic exposure to morphine. Brain Res 736: 227-236.
13. Dallman MF (2001). Stress, and sickness decrease food intake and body weight: how does this happen?. In: Broome DR (ed). Dahlem Workshop: Coping with Challenge: Welfare in Animals Including Humans. Free University of Berlin: Berlin. pp 301-316.
14. Dallman MF, Akana SF, Scribner KA, Bradbury MJ, Walker C-D, Strack AM et al (1992). Stress, feedback and facilitation in the hypothalamo-pituitary- adrenal axis. J Neuroendocrinol 4: 517-526.
15. Dallman MF, Bhatnagar S (2001). Chronic Stress and Energy Balance: Role of the Hypothalamo-Pituitary-Adrenal Axis. Oxford University Press: New York.
16. Dallman MF, Viau V, Bhatnagar S, Gomez F, Laugero K, Bell ME (2002). Corticotropin-releasing factor (CRF), corticosteroids, stress and sugar: energy balance the brain and behavior. In: Pfaff DW (ed). Hormones, Brain and Behavior. Academic Press: San Diego. Vol 1, pp 571-632.
17. Davis M, Whalen PJ (2001). The amygdala: vigilance and emotion. Mol Psychiatry 6: 13-34.
18. Eisenberg RM (1985). Effects of chronic treatment with diazepam, phenobarbital, or amphetamine on naloxone-precipitated morphine withdrawal. Drug Alcohol Depend 15: 375-381.
19. Fisher LA, Rivier J, Rivier C, Spiess J, Vale W, Brown MR (1982). Corticotropin-releasing factor: effects on the autonomic nervous system and visceral systems. Endocrinology 110: 2222-2224.
20. Fuertes G, Milanes MV, Rodrigues-Gago M, Marin MT, Laorden ML (2000). Changes in hypothalamic paraventricular nucleus catecholaminergic activity after acute and chronic morphine administration. Eur J Pharmacol 388: 49-56.
21. Gerra G, Zaimovic A, Raggi MA, Giusti F, Delsignore R, Bertacca S et al (2001). Aggressive responding of male heroin addicts under methadone treatment: psychometric and neuroendocrine correlates. Drug Alcohol Depend 65: 85-95.
22. Gomez F, Dallman MF (2001). Manipulation of androgens causes different energetic responses to cold in 60-and 40-day-old rats. Am J Physiol 280: R262-R273.
23. Gomez F, Houshyar H, Dallman MF (2002). Marked regulatory shifts in gonadal, adrenal and metabolic system responses to repeated restraint stress occur within a 3-week period in pubertal male rats. Endocrinology 143: 2852-2862.
24. Gray TS (1993). Amygdaloid CRF pathways. Role in autonomic, neuroendocrine, and behavioral responses to stress. Ann N Y Acad Sci 697: 53-60.
25. Helmreich DL, Watkins LR, Deak T, Maier SF, Akil H, Watson SJ (1999). The effect of stressor controllability on stress-induced neuropeptide mRNA expression within the paraventricular nucleus of the hypothalamus. J Neuroendocrinol 11: 121-128.
26. House SD, Mao X, Wu G-d, Espinelli D, Li WX, Chang SL (2001). Chronic morphine potentiates the inflammatory response by disrupting interleukin-1B modulation of the hypothalamo-pituitary-adrenal axis. J Neuroimmunol 118: 277-285.
27. Houshyar H, Cooper ZD, Woods JH (2001a). Paradoxical effects of chronic morphine treatment on the temperature and pituitary-adrenal responses to acute restraint stress: a chronic stress paradigm. J Neuroendocrinol 13: 862-874.
28. Houshyar H, Galigniana MD, Pratt WB, Woods JH (2001b). Differential responsivity of the HPA axis to glucocorticoid negative feedback and corticotropin-releasing hormone in rats undergoing acute and chronic morphine withdrawal: possible mechanisms involved in facilitated and attenuated stress responses. J Neuroendocrinol 13: 875-886.
29. Hsu DT, Chen F-L, Takahashi LK, Kalin NH (1998). Rapid stress-induced elevations in corticotropin-releasing hormone mRNA in rat central amygdala nucleus and hypothalamic paraventricular nucleus: an in situ hybridization analysis. Brain Res 788: 305-310.
30. Imaki T, Nahan JL, Rivier C, Sawchenko PE, Vale WW (1991). Differential regulation of corticotropin-releasing factor mRNA in rat brain regions by glucocorticoids and stress. J Neurosci 11: 585-599.
31. Jacobson L, Akana SF, Cascio CS, Scribner K, Shinsako J, Dallman MF (1989). The adrenocortical system responds slowly to the removal of corticosterone in the absence of stress. Endocrinology 124: 2144-2152.
32. Koob GF (1999). Corticotropin-releasing factor, norepinephrine and stress. Biol Psychiatry 46: 1167-1180.
33. Koob GF, Heinrichs SC (1999). A role for corticotropin releasing factor and urocortin in behavioral responses to stressors. Brain Res 848: 141-152.
34. Koob GF, Le Moal M (2001). Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology 24: 97-129.
35. Kreek MJ, Borg L, Schluger JH (2002). Relationships between endocrine functions and substance abuse syndromes: heroin and related short-acting opiates in addiction contrasted with methadone and other long-acting opioid agonists used in the pharmacology of addiction. In: Pfaff DW (ed). Hormones, Brain and Behavior. Elsevier Science (USA): San Diego. Vol 5, pp 781-830.
36. Kreek MJ, Koob GF (1998). Drug dependence: stress and dysregulation of brain reward pathways. Drug Alcohol Depend 51: 23-47.
37. Krukoff TL, MacTavish D, Jhamandas JH (1999). Hypertensive rats exhibit heightened expression of corticotropin-releasing factor in activated central neurons in response to restraint stress. Mol Brain Res 65: 70-79.
38. Langerman L, Piscoun B, Bansinath M, Shemesh Y, Turndorf H, Grant GJ (2001). Quantifiable dose-dependent withdrawal after morphine discontinuation in a rat model. Pharm Biochem Behav 68: 1-6.
39. Laorden ML, Fuertes G, Gonzalez-Cuello A, Milanes MV (2000). Changes in catecholaminergic pathways innervating paraventricular nucleus and pituitary-adrenal axis responses during morphine dependence: implications of al and a2-adrenoceptors. J Pharmacol Exp Ther 293: 578-584.
40. Laugero KD (2001). A new perspective on glucocorticoid feedback: relation to stress, carbohydrate feeding and feeling better. J Neuroendocrinol 13: 827-835.
41. Leshem M (1988). Morphine induces delayed anorexia in rats. Psychopharmacology 94: 254-258.
42. Leshner AL, Koob GF (1999). Drugs of abuse and the brain. Proc Assoc Am Physicians 111: 99-108.
43. Levine AS, Grace M, Billington CJ, Gosnell BA, Krahn DD, Brown DM et al (1988). Effect of morphine and nalmefene on energy balance in diabetic and non-diabetic rats. Pharm Biochem Behav 29: 495-500.
44. Lightman SL, Young III WS (1988). Corticotrophin-releasing factor, vasopressin and pro-opiomelanocortin mRNA responses to stress and opiates in the rat. J Physiol 403: 511-523.
45. Ma XM, Aguilera G (1999). Transcriptional responses of the vasopressin and corticotropin-releasing hormone genes to acute and repeated intraperitoneal hypertonic saline injection in rats. Mol Brain Res 68: 129-140.
46. Ma XM, Lightman SL, Aguilera G (1999). Vasopressin and corticotropin-releasing hormone gene responses to novel restraint in rats adapted to repeated restraint. Endocrinology 140: 3623-3632.
47. Makino S, Schulkin J, Smith MA, Pacak K, Palkovits M, Gold PW (1995). Regulation of corticotropin-releasing hormone receptor messenger ribonucleic acid in the rat brain and pituitary by glucocorticoids and stress. Endocrinology 136: 4517-4525.
48. Makino S, Shibasaki T, Yamauchi N, Nishioka T, Miamoto T, Wakabayashi I, Gold PW et al (1999). Psychological stress increased corticotropin-releasing hormone mRNA and content in the central nucleus of amygdala but not in the hypothalamic paraventricular nuclei of the rat. Brain Res 850: 136-143.
49. Marti O, Marti J, Armario A (1994). Effects of chronic stress on food intake in rats: influence of Stressor intensity and duration of daily exposure. Physiol Behav 55: 747-755.
50. McNally GP, Akil H (2002). Role of corticotropin-releasing hormone in the amygdala and bed nucleus of the stria terminalis in the behavioral, pain modulatory, and endocrine consequences of opiate withdrawal. Neuroscience 12: 605-617.
51. Milanes MV, Laorden ML, Chapleur-Chateau M (1997). Differential regulation of corticotropin-releasing factor and vasopressin in discrete brain regions after morphine administration: correlations with hypothalamic noradrenergic activity and pituitary-adrenal response. Naunyn-Schmiedeberg's Arch Pharmacol 356: 603-610.
52. Milanes MV, Laorden ML, Chapleur-Chateau M, Burlet A (1998). Alterations in corticotropin-releasing factor and vasopressin content in rat brain during morphine withdrawal: correlation with hypothalamic noradrenergic activity and pituitary-adrenal response. J Pharmacol Exp Ther 285: 700-706.
53. Milanes MV, Puig MM, Vargas ML (1993). Simultaneous changes in hypothalamic catecholamine levels and plasma corticosterone concentration in the rat after acute morphine and during tolerance. Neuropeptides 24: 279-284.
54. Mutti A, Folli D, Van der Venne MT, Berlin A, Gerra G, Caccavari R et al (1992). Long-lasting impairment of neuroendocrine response to psychological stress in heroin addicts. Neurotoxicology 13: 255-260.
55. Pechnick RN (1993). Effect of opioids on the hypothalamo-pituitary- adrenal axis. Annu Rev Pharmacol Toxicol 32: 353-382.
56. Pinelli A, Trivulzio S, Spezia R (1998). Effects of tizanidine administration in precipitated opioid withdrawal signs in rats. Drug Alcohol Depend 50: 81-88.
57. Rayner DV, Trayhurn P (2001). Regulation of leptin production: sympathetic nervous system interactions. J Mol Med 79: 8-20.
58. Sarnyai B, Shaham Y, Heinrichs SC (2001). The role of corticotropin-releasing factor in drug addiction. Pharm Rev 53: 209-243.
59. Schulkin J, Gold PW, McEwen BS (1998). Induction of corticotropin- releasing hormone gene expression by glucocorticoids: implication for understanding the states of fear and anxiety and allostatic load. Psychoneuroendocrinology 23: 219-243.
60. Scribner KA, Akana SF, Walker C-D, Dallman MF (1993). Streptozotocin-diabetic rats exhibit facilitated adrenocorticotropin responses to acute stress, but normal sensitivity to feedback by corticosteroids. Endocrinology 133: 2667-2674.
61. Shaham Y, Funk D, Erb S, Brown TJ, Walker C-D, Stewart J (1997). Corticotropin-releasing factor, but not corticosterone, is involved in stress-induced relapse to heroin seeking in rats. J Neurosci 17: 2605-2614.
62. Shaham YSE, Leung S, Buczek Y, Stewart J (1998). CP-154,526, a selective non-peptide antagonist of the corticotropin-releasing factor1 receptor attenuates stress-induced relapse to drug seeking in cocaine-and heroin-treated rats. Psychopharmacology 137: 184-190.
63. Shalev U, Morales M, Hope B, Yap J, Shaham Y (2001). Time-dependent changes in extinction behavior and stress-induced reinstatement of drug seeking following withdrawal from heroin in rats. Psychopharmacology 156: 98-107.
64. Shibasaki T, Yamauchi N, Kato Y, Masuda A, Imaki T, Hotta M et al (1988). Involvement of corticotropin-releasing factor in restraint stress-induced anorexia and reversion of the anorexia by somatostatin in the rat. Life Sci 43: 1103-1110.
65. Smagin GN, Howell LA, Redmann Jr S, Ryan DH, Harris RBH (1999). Prevention of stress-induced weight loss by third ventricular CRF receptor antagonist. Am J Physiol 268: R1461-R1469.
66. Valentino RJ, Kosboth M, Colflesh M, Miselis RR (2000). Transneuronal labeling from the rat distal colon: anatomic evidence for regulation of distal colon function by a pontine corticotropin-releasing factor system. J Comp Neurol 417: 399-414.
67. Vescovi PP, Pedrazzoni M, Gerra G, Pioli G, Maninetti L, Michelini M et al (1989). Impaired ACTH and B-endorphin response to sauna-induced hyperthermia in heroin addicts. Acta Endocrinol 121: 484-488.
68. Viau V, Soriano L, Dallman MF (2001). Androgens alter corticotropin-releasing hormone and vasopressin mRNA within forebrain sites known to regulate activity in the hypothalamic-pituitary-adrenal axis. J Neuroendocrinol 13: 442-452.
69. Walker DL, Davis M (1997). Double dissociation between involvement of the bed nucleus of the strial terminalis and the central nucleus of the amygdala in startle increases produced by conditioned versus unconditioned fear. J Neurosci 17: 9375-9383.
70. Zhou Y, Spangler R, Maggos CE, LaForge KS, Ho A, Kreek MJ (1996). Steady-state methadone in rats does not change mRNA levels of corticotropin-releasing factor, its pituitary receptor or proopiomelanocortin. Eur J Pharmacol 315: 31-35.