Mouse model of OPRM1 (A118G) polymorphism increases sociability and dominance and confers resilience to social defeat

Journal of Neuroscience

Volumn 35, Issue 8, 2015, Pages 3582-3590

  Briand, Lisa A ^a,c   Hilario, Monica ^a   Dow, Holly C ^b   Brodkin, Edward S ^b   Blendy, Julie A ^a   Berton, Olivier ^b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c TEMPLE UNIVERSITY   (United States)

Author keywords

Anhedonia; Intracranial self stimulation; OPRM1 A118G; Social defeat; Social interaction; opioid

Indexed keywords

MU OPIATE RECEPTOR; NALOXONE; NARCOTIC ANTAGONIST; OPRM PROTEIN, MOUSE; PROTEIN C FOS;

ADULT; ALLELE; ANHEDONIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DEPTH STIMULATION; CONTROLLED STUDY; DNA POLYMORPHISM; EXPERIMENTAL BEHAVIORAL TEST; FEMALE; GENE; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPRM1 GENE; PRIORITY JOURNAL; QUANTITATIVE ASSAY; RESIDENT INTRUDER TEST; SELF STIMULATION; SINGLE NUCLEOTIDE POLYMORPHISM; SMELLING; SOCIAL AVOIDANCE BEHAVIOR; SOCIAL INTERACTION; SOCIAL STRESS; THREE CHAMBER SOCIABILITY TEST; AGGRESSION; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; GENETICS; HETEROZYGOTE; METABOLISM; MISSENSE MUTATION; NUCLEUS ACCUMBENS; PERIAQUEDUCTAL GRAY MATTER; PHYSIOLOGY; SOCIAL DOMINANCE;

AGGRESSION; ANHEDONIA; ANIMALS; DOMINANCE-SUBORDINATION; FEMALE; HETEROZYGOTE; MALE; MICE; MICE, INBRED C57BL; MUTATION, MISSENSE; NALOXONE; NARCOTIC ANTAGONISTS; NUCLEUS ACCUMBENS; PERIAQUEDUCTAL GRAY; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTO-ONCOGENE PROTEINS C-FOS; RECEPTORS, OPIOID, MU;

EID: 84923348025     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4685-14.2015     Document Type: Article

References (53)

1. American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders, fifth edition. Arlington, VA: American Psychiatric.
2. Barr CS, Schwandt ML, Lindell SG, Higley JD, Maestripieri D, Goldman D, Suomi SJ, Heilig M (2008) Variation at the mu-opioid receptor gene (OPRM1) influences attachment behavior in infant primates. Proc Natl Acad Sci U S A 105:5277-5281. CrossRef Medline.
3. Baumeister RF, DeWall CN, Ciarocco NJ, Twenge JM (2005) Social exclusion impairs self-regulation. J Pers Soc Psychol 88:589-604. CrossRef Medline.
4. Bergen AW, Kokoszka J, Peterson R, Long JC, Virkkunen M, Linnoila M, Goldman D (1997) Mu opioid receptor gene variants: lack of association with alcohol dependence. Mol Psychiatry 2:490-494. CrossRef Medline.
5. Bertoletti E, Zanoni A, Giorda R, Battaglia M (2012) Influence of the OPRM1 gene polymorphism upon children’s degree of withdrawal and brain activation in response to facial expressions. Dev Cogn Neurosci 2:103-109. CrossRef Medline.
6. Berton O, Covington HE III, Ebner K, Tsankova NM, Carle TL, Ulery P, Bhonsle A, Barrot M, Krishnan V, Singewald GM, Singewald N, Birnbaum S, Neve RL, Nestler EJ (2007) Induction of deltaFosB in the periaqueductal gray by stress promotes active coping responses. Neuron 55: 289-300. CrossRef Medline.
7. Bilbao A, Robinson JE, Heilig M, Malanga CJ, Spanagel R, Sommer WH, Thorsell A (2014) A pharmacogenetic determinant of mu-opioid receptor antagonist effects on alcohol reward and consumption: evidence from humanized mice. Biol Psychiatry pii:S0006-3223(14)00653-2. CrossRef Medline.
8. Brodkin ES, Hagemann A, Nemetski SM, Silver LM (2004) Social approachavoidance behavior of inbred mouse strains towards DBA/2 mice. Brain Res 1002:151-157. CrossRef Medline.
9. Carlezon WA Jr, Chartoff EH (2007) Intracranial self-stimulation (ICSS) in rodents to study the neurobiology of motivation. Nat Protoc 2:2987-2995. CrossRef Medline.
10. Chaijale NN, Curtis AL, Wood SK, Zhang XY, Bhatnagar S, Reyes BA, Van Bockstaele EJ, Valentino RJ (2013) Social stress engages opioid regulation of locus coeruleus norepinephrine neurons and induces a state of cellular and physical opiate dependence. Neuropsychopharmacology 38: 1833-1843. CrossRef Medline.
11. Challis C, Boulden J, Veerakumar A, Espallergues J, Vassoler FM, Pierce RC, Beck SG, Berton O (2013) Raphe GABAergic neurons mediate the acquisition of avoidance after social defeat. J Neurosci 33:13978-13988, 13988a. CrossRef Medline.
12. Chong RY, Oswald L, Yang X, Uhart M, Lin PI, Wand GS (2006) The mu-opioid receptor polymorphism A118G predicts cortisol responses to naloxone and stress. Neuropsychopharmacology 31:204-211. Medline.
13. Commons KG, Aicher SA, Kow LM, Pfaff DW (2000) Presynaptic and postsynaptic relations of mu-opioid receptors to gamma-aminobutyric acidimmunoreactive and medullary-projecting periaqueductal gray neurons. J Comp Neurol 419:532-542. CrossRef Medline.
14. Copeland WE, Sun H, Costello EJ, Angold A, Heilig MA, Barr CS (2011) Child mu-opioid receptor gene variant influences parent-child relations. Neuropsychopharmacology 36:1165-1170. CrossRef Medline.
15. Donahue RJ, Muschamp JW, Russo SJ, Nestler EJ, Carlezon WA Jr (2014) Effects of striatal _FosB overexpression and ketamine on social defeat stress-induced anhedonia in mice. Biol Psychiatry 76:550-558. CrossRef Medline.
16. Floyd NS, Keay KA, Arias CM, Sawchenko PE, Bandler R (1996) Projections from the ventrolateral periaqueductal gray to endocrine regulatory subdivisions of the paraventricular nucleus of the hypothalamus in the rat. Neurosci Lett 220:105-108. CrossRef Medline.
17. Francis TC, Chandra R, Friend DM, Finkel E, Dayrit G, Miranda J, Brooks JM, Iniguez SD, O’Donnell P, Kravitz A, Lobo MK (2015) Nucleus accumbens medium spiny neuron subtypes mediate depression-related outcomes to social defeat stress. Biol Psychiatry 77:212-222. CrossRef Medline.
18. Frank E, Salchner P, Aldag JM, Salome´ N, Singewald N, Landgraf R, Wigger A (2006) Genetic predisposition to anxiety-related behavior determines coping style, neuroendocrine responses, and neuronal activation during social defeat. Behav Neurosci 120:60-71. CrossRef Medline.
19. Franklin K, Paxinos G (2007) The mouse brain in stereotaxic coordinates, 3rd edition. San Diego: Academic.
20. Gelernter J, Kranzler H, Cubells J (1999) Genetics of two mu opioid receptor gene (OPRM1) exon I polymorphisms: population studies, and allele frequencies in alcohol-and drug-dependent subjects. Mol Psychiatry 4:476-483. CrossRef Medline.
21. Herman BH, Panksepp J (1978) Effects of morphine and naloxone on separation distress and approach attachment: evidence for opiate mediation of social affect. Pharmacol Biochem Behav 9:213-220. CrossRef Medline.
22. Hsu DT, Sanford BJ, Meyers KK, Love TM, Hazlett KE, Wang H, Ni L, Walker SJ, Mickey BJ, Korycinski ST, Koeppe RA, Crocker JK, Langenecker SA, Zubieta JK (2013) Response of the mu-opioid system to social rejection and acceptance. Mol Psychiatry 18:1211-1217. CrossRef Medline.
23. Huang P, Chen C, Mague SD, Blendy JA, Liu-Chen LY (2012) A common single nucleotide polymorphism A118G of the mu opioid receptor alters its N-glycosylation and protein stability. Biochem J 441:379-386. CrossRef Medline.
24. Kalin NH, Shelton SE, Lynn DE (1995) Opiate systems in mother and infant primates coordinate intimate contact during reunion. Psychoneuroendocrinology 20:735-742. CrossRef Medline.
25. Knowles PA, Conner RL, Panksepp J (1989) Opiate effects on social behavior of juvenile dogs as a function of social deprivation. Pharmacol Biochem Behav 33:533-537. CrossRef Medline.
26. Kollack-Walker S, Watson SJ, Akil H (1997) Social stress in hamsters: defeat activates specific neurocircuits within the brain. J Neurosci 17:8842-8855. Medline.
27. Kroes RA, Burgdorf J, Otto NJ, Panksepp J, Moskal JR (2007) Social defeat, a paradigm of depression in rats that elicits 22 kHz vocalizations, preferentially activates the cholinergic signaling pathway in the periaqueductal gray. Behav Brain Res 182:290-300. CrossRef Medline.
28. Mague SD, Blendy JA (2010) OPRM1 SNP (A118G): involvement in disease development, treatment response, and animal models. Drug Alcohol Depend 108:172-182. CrossRef Medline.
29. Mague SD, Isiegas C, Huang P, Liu-Chen LY, Lerman C, Blendy JA (2009) Mouse model of OPRM1 (A118G) polymorphism has sex-specific effects on drug-mediated behavior. Proc Natl Acad Sci U S A 106:10847-10852. CrossRef Medline.
30. Mallott MA, Maner JK, DeWall N, Schmidt NB (2009) Compensatory deficits following rejection: the role of social anxiety in disrupting affiliative behavior. Depress Anxiety 26:438-446. CrossRef Medline.
31. Messeri P, Eleftheriou BE, Oliverio A (1975) Dominance behavior: a phylogenetic analysis in the mouse. Physiol Behav 14:53-58. CrossRef Medline.
32. Miller GM, Bendor J, Tiefenbacher S, Yang H, Novak MA, Madras BK (2004) A mu-opioid receptor single nucleotide polymorphism in rhesus monkey: association with stress response and aggression. Mol Psychiatry 9:99-108. CrossRef Medline.
33. Moles A, Kieffer BL, D’Amato FR (2004) Deficit in attachment behavior in mice lacking the mu-opioid receptor gene. Science 304:1983-1986. CrossRef Medline.
34. Morrison KE, Swallows CL, Cooper MA (2011) Effects of dominance status on conditioned defeat and expression of 5-HT1A and 5-HT2A receptors. Physiol Behav 104:283-290. CrossRef Medline.
35. Morrison KE, Curry DW, Cooper MA (2012) Social status alters defeatinduced neural activation in Syrian hamsters. Neuroscience 210:168-178. CrossRef Medline.
36. Moy SS, Nadler JJ, Young NB, Perez A, Holloway LP, Barbaro RP, Barbaro JR, Wilson LM, Threadgill DW, Lauder JM, Magnuson TR, Crawley JN (2007) Mouse behavioral tasks relevant to autism:phenotypes of 10 inbred strains. Behav Brain Res 176:4-20. CrossRef Medline.
37. Nugent NR, Lally MA, Brown L, Knopik VS, McGeary JE (2012) OPRM1 and diagnosis-related posttraumatic stress disorder in binge-drinking patients living with HIV. AIDS Behav 16:2171-2180. CrossRef Medline.
38. Panksepp J, Herman B, Conner R, Bishop P, Scott JP (1978) The biology of social attachments: opiates alleviate separation distress. Biol Psychiatry 13:607-618. Medline.
39. Paxinos G, Franklin K (2004) The mouse brain in stereotaxic coordinates, compact 2nd edition. Amsterdam: Elsevier Academic.
40. Poulin JF, Laforest S, Drolet G (2014) Enkephalin downregulation in the nucleus accumbens underlies chronic stress-induced anhedonia. Stress 17:88-96. CrossRef Medline.
41. Slavich GM, O’Donovan A, Epel ES, Kemeny ME (2010) Black sheep get the blues: a psychobiological model of social rejection and depression. Neurosci Biobehav Rev 35:39-45. CrossRef Medline.
42. Tan EC, Tan CH, Karupathivan U, Yap EP (2003) Mu opioid receptor gene polymorphisms and heroin dependence in Asian populations. Neuroreport 14:569-572. CrossRef Medline.
43. Teskey GC, Kavaliers M, Hirst M (1984) Social conflict activates opioid analgesic and ingestive behaviors in male mice. Life Sci 35:303-315. CrossRef Medline.
44. Timmer M, Cordero MI, Sevelinges Y, Sandi C (2011) Evidence for a role of oxytocin receptors in the long-term establishment of dominance hierarchies. Neuropsychopharmacology 36:2349-2356. CrossRef Medline.
45. Trezza V, Damsteegt R, Achterberg EJ, Vanderschuren LJ (2011) Nucleus accumbens µ-opioid receptors mediate social reward. J Neurosci 31: 6362-6370. CrossRef Medline.
46. Troisi A, Frazzetto G, Carola V, Di Lorenzo G, Coviello M, D’Amato FR, Moles A, Siracusano A, Gross C (2011) Social hedonic capacity is associated with the A118G polymorphism of the mu-opioid receptor gene (OPRM1) in adult healthy volunteers and psychiatric patients. Soc Neurosci 6:88-97. CrossRef Medline.
47. Troisi A, Frazzetto G, Carola V, Di Lorenzo G, Coviello M, Siracusano A, Gross C (2012) Variation in the mu-opioid receptor gene (OPRM1) moderates the influence of early maternal care on fearful attachment. Soc Cogn Affect Neurosci 7:542-547. CrossRef Medline.
48. Vialou V, Robison AJ, Laplant QC, Covington HE III, Dietz DM, Ohnishi YN, Mouzon E, Rush AJ III, Watts EL, Wallace DL, Iñiguez SD, Ohnishi YH, Steiner MA, Warren BL, Krishnan V, Bolaños CA, Neve RL, Ghose S, Berton O, Tamminga CA et al. (2010) DeltaFosB in brain reward circuits mediates resilience to stress and antidepressant responses. Nat Neurosci 13:745-752. CrossRef Medline.
49. Vivian JA, Miczek KA (1998) Effects of mu and delta opioid agonists and antagonists on affective vocal and reflexive pain responses during social stress in rats. Psychopharmacology 139:364-375. CrossRef Medline.
50. Wang YJ, Huang P, Ung A, Blendy JA, Liu-Chen LY (2012) Reduced expression of the mu opioid receptor in some, but not all, brain regions in mice with OPRM1 A112G. Neuroscience 205:178-184. CrossRef Medline.
51. Way BM, Lieberman MD (2010) Is there a genetic contribution to cultural differences? Collectivism, individualism and genetic markers of social sensitivity. Soc Cogn Affect Neurosci 5:203-211. CrossRef Medline.
52. Way BM, Taylor SE, Eisenberger NI (2009) Variation in the mu-opioid receptor gene (OPRM1) is associated with dispositional and neural sensitivity to social rejection. Proc Natl Acad Sci U S A 106:15079-15084. CrossRef Medline.
53. Williams KD (2007) Ostracism. Annu Rev Psychol 58:425-452. CrossRef Medline.