From mouse to man: The 5-HT3 receptor modulates physical dependence on opioid narcotics

Pharmacogenetics and Genomics

Volumn 19, Issue 3, 2009, Pages 193-205

  Chu, Larry F ^a   Liang, De Yong ^a   Li, Xiangqi ^a   Sahbaie, Peyman ^c   D'Arcy, Nicole ^a   Liao, Guochun ^b   Peltz, Gary ^a   Clark, J David ^a,c  

^a STANFORD UNIVERSITY   (United States)

^b Roche Palo Alto   (United States)

^c VA PALO ALTO HEALTH CARE SYSTEM   (United States)

Author keywords

Addiction; Hyperalgesia; Morphine; Ondansetron; Opioid; Serotonin

Indexed keywords

MESSENGER RNA; MORPHINE; NALOXONE; ONDANSETRON; SEROTONIN 3 RECEPTOR;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CLINICAL ARTICLE; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; CROSSOVER PROCEDURE; DISEASE PREDISPOSITION; DORSAL RAPHE NUCLEUS; DOUBLE BLIND PROCEDURE; DRUG EFFECT; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENE MAPPING; GENETIC VARIABILITY; GNETOPHYTA; HAPLOTYPE; HERITABILITY; HTR3A GENE; HUMAN; MALE; MOUSE; NONHUMAN; OPIATE ADDICTION; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; RECEPTOR INTRINSIC ACTIVITY;

ANALGESICS, OPIOID; ANIMALS; BEHAVIOR, ANIMAL; BRAIN; COMPUTATIONAL BIOLOGY; GENETIC VARIATION; HAPLOTYPES; HUMANS; MALE; MICE; MICE, INBRED STRAINS; MORPHINE; NARCOTICS; RECEPTORS, SEROTONIN, 5-HT3; RNA, MESSENGER; SUBSTANCE WITHDRAWAL SYNDROME; SUBSTANCE-RELATED DISORDERS;

ANIMALIA; MUS;

EID: 62349093322     PISSN: 17446872     EISSN: 17446880     Source Type: Journal    
DOI: 10.1097/FPC.0b013e328322e73d     Document Type: Article

References (68)

1. Results from the 2006 National Survey on Drug Use and Health: National Findings. Substance Abuse and Mental Health Services Administration, Department of Health and Human Services 2006.
2. Birnbaum HG, White AG, Reynolds JL, Greenberg PE, Zhang M, Vallow S, et al. Estimated costs of prescription opioid analgesic abuse in the United States in 2001: a societal perspective. Clin J Pain 2006; 22:667-676.
3. Gruber SA, Silveri MM, Yurgelun-Todd DA. Neuropsychological consequences of opiate use. Neuropsychol Rev 2007; 17:299-315.
4. Manchikanti L. Prescription drug abuse: what is being done to address this new drug epidemic? Testimony before the Subcommittee on Criminal Justice, Drug Policy and Human Resources. Pain Physician 2006; 9: 287-321.
5. Handelsman L, Cochrane KJ, Aronson MJ, Ness R, Rubinstein KJ, Kanof PD. Two new rating scales for opiate withdrawal. Am J Drug Alcohol Abuse 1987; 13:293-308.
6. Kendler KS, Jacobson KC, Prescott CA, Neale MC. Specificity of genetic and environmental risk factors for use and abuse/dependence of cannabis, cocaine, hallucinogens, sedatives, stimulants, and opiates in male twins. Am J Psychiatry 2003; 160:687-695.
7. Kest B, Palmese CA, Juni A, Chester EJ, Mogil JS. Mapping of a quantitative trait locus for morphine withdrawal severity. Mamm Genome 2004; 15: 610-617.
8. Kest B, Hopkins E, Palmese CA, Adler M, Mogil JS. Genetic variation in morphine analgesic tolerance: a survey of 11 inbred mouse strains. Pharmacol Biochem Behav 2002; 73:821-828.
9. Liang DY, Guo T, Liao G, Kingery WS, Peltz G, Clark JD. Chronic pain and genetic background interact and influence opioid analgesia, tolerance, and physical dependence. Pain 2006; 121:232-240.
10. Bickel WK, Stitzer ML, Wazlavek BE, Liebson IA. Naloxone-precipitated withdrawal in humans after acute morphine administration. NIDA Res Monogr 1986; 67:349-354.
11. Wang J, Liao G, Usuka J, Peltz G. Computational genetics: from mouse to human? Trends Genet 2005; 21:526-532.
12. Liao G, Wang J, Guo J, Allard J, Cheng J, Ng A, et al. In silico genetics: identification of a functional element regulating H2-Ealpha gene expression. Science 2004; 306:690-695.
13. Liang DY, Liao G, Lighthall GK, Peltz G, Clark DJ. Genetic variants of the P-gtycoprotein gene Abcb1b modulate opioid-induced hyperalgesia, tolerance and dependence. Pharmacogenet Genomics 2006; 16:825-835.
14. Liang DY, Liao G, Wang J, Usuka J, Guo Y, Peltz G, et al. A genetic analysis of opioid-induced hyperalgesia in mice. Anesthesiology 2006; 104:1054-1062.
15. Smith SB, Marker CL, Perry C, Liao G, Sotocinal SG, Austin JS, et al. Quantitative trait locus and computational mapping identifies Kcnj9 (GIRK3) as a candidate gene affecting analgesia from multiple drug classes. Pharmacogenet Genomics 2008; 18:231-241.
16. Lin RJ, Sternsdorf T, Tini M, Evans RM. Transcriptional regulation in acute promyelocytic leukemia. Oncogene 2001; 20:7204-7215.
17. Kest B, Palmese CA, Hopkins E, Adler M, Juni A, Mogil JS. Naloxone-precipitated withdrawal jumping in 11 inbred mouse strains: evidence for common genetic mechanisms in acute and chronic morphine physical dependence. Neuroscience 2002; 115:463-469.
18. Pedigo NW, Dewey WL, Harris LS. Determination and characterization of the antinociceptive activity of intraventricularly administered acetylcholine in mice. J Pharmacol Exp Ther 1975; 193:845-852.
19. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 1994; 53:55-63.
20. Li X, Angst MS, Clark JD. A murine model of opioid-induced hyperalgesia. Brain Res Mol Brain Res 2001; 86:56-62.
21. Poree LR, Guo TZ, Kingery WS, Maze M. The analgesic potency of dexmedetomidine is enhanced after nerve injury: a possible role for peripheral alpha2-adrenoceptors. Anesth Analg 1998; 87:941-948.
22. Bardo MT, Rowlett JK, Harris MJ. Conditioned place preference using opiate and stimulant drugs: a meta-analysis. Neurosci Biobehav Rev 1995; 19:39-51.
23. Reid LD, Marglin SH, Mattie ME, Hubbell CL. Measuring morphine's capacity to establish a place preference. Pharmacol Biochem Behav 1989; 33:765-775.
24. Guo Y, Weller P, Farrell E, Cheung P, Fitch B, Clark D, et al. In silico pharmacogenetics of warfarin metabolism. Nat Biotechnol 2006; 24: 531-536.
25. Liang DY, Shi X, Li X, Li J, Clark JD. The beta2 adrenergic receptor regulates morphine tolerance and physical dependence. Behav Brain Res 2007; 181:118-126.
26. Li X, Lighthall G, Liang DY, Clark JD. Alterations in spinal cord gene expression after hindpaw formalin injection. J Neurosci Res 2004; 78:533-541.
27. Liang D, Li X, Lighthall G, Clark JD. Heme oxygenase type 2 modulates behavioral and molecular changes during chronic exposure to morphine. Neuroscience 2003; 121:999-1005.
28. Feldman AL, Costouros NG, Wang E, Qian M, Marincola FM, Alexander HR, et al. Advantages of mRNA amplification for microarray analysis. Biotechniques 2002; 33:906-914.
29. Liang DY, Clark JD. Modulation of the NO/CO-cGMP signaling cascade during chronic morphine exposure in mice. Neurosci Lett 2004; 365: 73-77.
30. Compton P, Miotto K, Elashoff D. Precipitated opioid withdrawal across acute physical dependence induction methods. Pharmacol Biochem Behav 2004; 77:263-268.
31. Hoehe M. Influence of the menstrual cycle on neuroendocrine and behavioral responses to an opiate agonist in humans: preliminary results. Psychoneuroendocrinology 1988; 13:339-344.
32. Costall B, Naylor RJ. 5-HT3 receptors. Curr Drug Targets CNS Neurol Disord 2004; 3:27-37.
33. Roychoudhury M, Kulkarni SK. Prevention of morphine discontinuation phenomenon in mice by ondansetron, a selective 5-HT3 antagonist. Methods Find Exp Clin Pharmacol 1996; 18:677-683.
34. Angst MS, Clark JO. Opioid-induced hyperalgesia: a qualitative systematic review. Anesthesiology 2006; 104:570-587.
35. Chu LF, Clark DJ, Angst MS. Opioid tolerance and hyperalgesia in chronic pain patients after one month of oral morphine therapy: a preliminary prospective study. J Pain 2006; 7:43-48.
36. Kayan S, Woods LA, Mitchell CL. Morphine-induced hyperalgesia in rats tested on the hot plate. J Pharmacol Exp Ther 1971; 177: 509-513.
37. VonVoigtlander PF, Lewis RA. A withdrawal hyperalgesia test for physical dependence: evaluation of mu and mixed-partial opioid agonists. J Pharmacol Methods 1983; 10:277-282.
38. Costall B, Jones BJ, Kelly ME, Naylor RJ, Onaivi ES, Tyers MB. Sites of action of ondansetron to inhibit withdrawal from drugs of abuse. Pharmacol Biochem Behav 1990; 36:97-104.
39. Gulati A, Bhargava HN. Brain and spinal cord 5-HT2 receptors of morphine-tolerant-dependent and -abstinent rats. Eur J Pharmacol 1989; 167:185-192.
40. Tao R, Ma Z, Auerbach SB. Alteration in regulation of seratonin release in rat dorsal raphe nucleus after prolonged exposure to morphine. J Pharmacol Exp Ther 1998; 286:481-488.
41. Ingram SL, Vaughan CW, Bagley EE, Connor M, Christie MJ. Enhanced opioid efficacy in opioid dependence is caused by an altered signal transduction pathway. J Neurosci 1998; 18:10269-10276.
42. Brady CA, Stanford IM, Ali I, Lin L, Williams JM, Dubin AE, et al. Pharmacological comparison of human homomeric 5-HT3A receptors versus heteromeric 5-HT3A/3B receptors. Neuropharmacology 2001; 41:282-284.
43. Gyermek L. 5-HT3 receptors: pharmacologic and therapeutic aspects. J Clin Pharmacol 1995; 35:845-855.
44. Tricklebank MD. Interactions between dopamine and 5-HT3 receptors suggest new treatments for psychosis and drug addiction. Trends Pharmacol Sci 1989; 10:127-129.
45. Kauer JA, Malenka RC. Synaptic plasticity and addiction. Nat Rev Neurosci 2007; 8:844-858.
46. Hodge CW, Bratt AM, Kelley SP. Deletion of the 5-HT(3A)-receptor subunit blunts the induction of cocaine sensitization. Genes Brain Behav 2008; 7:96-102.
47. Carboni E, Acquas E, Leone P, Perezzani L, Di Chiara G. 5-HT3 receptor antagonists block morphine- and nicotine-induced place-preference conditioning. Eur J Pharmacol 1988; 151:159-160.
48. Higgins GA, Nguyen P, Joharchi N, Sellers EM. Effects of 5-HT3 receptor antagonists on behavioural measures of naloxone-precipitated opioid withdrawal. Psychopharmacology (Berl) 1991; 105:322-328.
49. Hui SC, Seville EL, Ogle CW. Prevention by the 5-HT3 receptor antagonist, ondansetron, of morphine-dependence and tolerance in the rat. Br J Pharmacol 1996; 118:1044-1050.
50. Pinelli A, Trivulzio S, Tomasoni L. Effects of ondansetron administration on opioid withdrawal syndrome observed in rats. Eur J Pharmacol 1997; 340:111-119.
51. Acquas E, Carboni E, Leone P, Di Chiara G. 5-HT3 receptors antagonists block morphine- and nicotine- but not amphetamine-induced place-preference conditioning. Pharmacol Res Commun 1988; 20: 1113-1114.
52. Borg PJ, Taylor DA. Voluntary oral morphine self-administration in rats: effect of haloperidol or ondansetron. Pharmacol Biochem Behav 1994; 47:633-646.
53. Joharchi N, Sellers EM, Higgins GA. Effect of 5-HT3 receptor antagonists on the discriminative stimulus properties of morphine in rats. Psychopharmacology (Berl) 1993; 112:111-115.
54. Higgins GA, Wang Y, Corrigall WA, Sellers EM. Influence of 5-HT3 receptor antagonists and the indirect 5-HT agonist, dexfenfluramine, on heroin self-administration in rats. Psychopharmacology (Berl) 1994; 114:611-619.
55. Sell LA, Cowen PJ, Robson PJ. Ondansetron and opiate craving. A novel pharmacological approach to addiction. Br J Psychiatry 1995; 166:511-514.
56. Tecott LH, Maricq AV, Julius D. Nervous system distribution of the serotonin 5-HT3 receptor mRNA. Proc Natl Acad Sci U S A 1993; 90: 1430-1434.
57. Maldonado R, Stinus L, Gold LH, Koob GF. Role of different brain structures in the expression of the physical morphine withdrawal syndrome. J Pharmacol Exp Ther 1992; 261:669-677.
58. Tremblay EC, Charton G. Anatomical correlates of morphine-withdrawal syndrome: differential participation of structures located within the limbic system and striatum. Neurosci Lett 1981; 23:137-142.
59. Koob GF, Le Moal M. Addiction and the brain antireward system. Annu Rev Psychol 2008; 59:29-53.
60. Doverty M, Somogyi AA, White JM, Bochner F, Beare CH, Menelaou A, et al. Methadone maintenance patients are cross-tolerant to the antinociceptive effects of morphine. Pain 2001; 93:155-163.
61. Vera-Portocarrero LP, Zhang ET, King T, Ossipov MH, Vanderah TW, Lai J, et al. Spinal NK-1 receptor expressing neurons mediate opioid-induced hyperalgesia and antinociceptive tolerance via activation of descending pathways. Pain 2007; 129:35-45.
62. Krzywkowski K, Jensen AA, Connolly CN, Brauner-Osborne H. Naturally occurring variations in the human 5-HT3A gene profoundly impact 5-HT3 receptor function and expression. Pharmacogenet Genomics 2007; 17:255-266.
63. Walstab J, Hammer C, Bonisch H, Rappold G, Niesler B. Naturally occurring variants in the HTR3B gene significantly alter properties of human heteromeric 5-hydroxytryptamine-3A/B receptors. Pharmacogenet Genomics 2008; 18:793-802.
64. Tanaka M, Kobayashi D, Murakami Y, Ozaki N, Suzuki T, Iwata N, et al. Genetic polymorphisms in the 5-hydroxytryptamine type 3B receptor gene and paroxetine-induced nausea. Int J Neuropsychopharmacol 2008; 11:261-267.
65. Yamada K, Hattori E, Iwayama Y, Ohnishi T, Ohba H, Toyota T, et al. Distinguishable haplotype blocks in the HTR3A and HTR3B region in the Japanese reveal evidence of association of HTR3B with female major depression. Biol Psychiatry 2006; 60:192-201.
66. Koob GF. The neurobiology of addiction: a neuroadaptational view relevant for diagnosis. Addiction 2006; 101 (Suppl 1):23-30.
67. Nestler EJ. Is there a common molecular pathway for addiction? Nat Neurosci 2005; 8:1445-1449.
68. Mao J. Opioid-induced abnormal pain sensitivity: implications in clinical opioid therapy. Pain 2002; 100:213-217.