PER1 rs3027172 genotype interacts with early life stress to predict problematic alcohol use, but not reward-related ventral striatum activity

Frontiers in Psychology

Volumn 7, Issue MAR, 2016, Pages

  Baranger, David A A ^a   Ifrah, Chloé ^a   Prather, Aric A ^b   Carey, Caitlin E ^a   Corral Frías, Nadia S ^c   Conley, Emily Drabant ^d   Hariri, Ahmad R ^e   Bogdan, Ryan ^a,c  

^a WASHINGTON UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Duke University ^*  (United States)

^e DUKE UNIVERSITY   (United States)

Author keywords

Alcohol; Circadian; Early life stress; GxE; PER1; Stress; Ventral striatum

Indexed keywords

EID: 84961990465     PISSN: None     EISSN: 16641078     Source Type: Journal    
DOI: 10.3389/fpsyg.2016.00464     Document Type: Article

References (70)

1. Abarca, C., Albrecht, U., and Spanagel, R. (2002). Cocaine sensitization and reward are under the influence of circadian genes and rhythm. Proc. Natl. Acad. Sci. U.S.A. 99, 9026-9030. doi: 10.1073/pnas.142039099
2. Beck, A., Schlagenhauf, F., Wüstenberg, T., Hein, J., Kienast, T., Kahnt, T., et al. (2009). Ventral striatal activation during reward anticipation correlates with impulsivity in alcoholics. Biol. Psychiatry 66, 734-742. doi: 10.1016/j.biopsych.2009.04.035
3. Bernstein, D. P., Stein, J. A., Newcomb, M. D., Walker, E., Pogge, D., Ahluvalia, T., et al. (2003). Development and validation of a brief screening version of the childhood trauma questionnaire. Child Abuse Negl. 27, 169-190. doi: 10.1016/S0145-2134(02)00541-0
4. Berridge, K. C., Robinson, T. E., and Aldridge, J. W. (2009). Dissecting components of reward: "liking", "wanting", and learning. Curr. Opin. Pharmacol. 9, 65-73. doi: 10.1016/j.coph.2008.12.014
5. Blomeyer, D., Buchmann, A. F., Lascorz, J., Zimmermann, U. S., Esser, G., Desrivieres, S., et al. (2013). Association of PER2 genotype and stressful life events with alcohol drinking in young adults. PLoS ONE 8:e59136. doi: 10.1371/journal.pone.0059136
6. Boecker, R., Holz, N. E., Buchmann, A. F., Blomeyer, D., Plichta, M. M., Wolf, I., et al. (2014). Impact of early life adversity on reward processing in young adults: EEG-fMRI results from a prospective study over 25 years. PLoS ONE 9:e104185. doi: 10.1371/journal.pone.0104185
7. Buysse, D. J., Reynolds, C. F., Monk, T. H., Berman, S. R., and Kupfer, D. J. (1989). The pittsburgh sleep quality index: a new instrument for psychiatric practice and research. Psychiatry Res. 28, 193-213. doi: 10.1016/0165-1781(89)90047-4
8. Carré, J. M., Fisher, P. M., Manuck, S. B., and Hariri, A. R. (2012). Interaction between trait anxiety and trait anger predict amygdala reactivity to angry facial expressions in men but not women. Soc. Cogn. Affect. Neurosci. 7, 213-221. doi: 10.1093/scan/nsq101
9. Cheng, X., Zhao, X., Khurana, S., Bruggeman, L. A., and Kao, H.-Y. (2013). Microarray analyses of glucocorticoid and vitamin D3 target genes in differentiating cultured human podocytes. PLoS ONE 8:e60213. doi: 10.1371/journal.pone.0060213
10. Chong, S. Y. C., Ptáček, L. J., and Fu, Y.-H. (2012). Genetic insights on sleep schedules: this time, it's PERsonal. Trends Genet. 28, 598-605. doi: 10.1016/j.tig.2012.08.002
11. Corral-Frías, N. S., Nikolova, Y. S., Michalski, L. J., Baranger, D. A. A., Hariri, A. R., Bogdan, R., et al. (2016). Stress-related anhedonia is associated with ventral striatum reactivity to reward and transdiagnostic psychiatric symptomatology. Psychol. Med. 45, 2605-2617. doi: 10.1017/s0033291715000525
12. Dallmann, R., Touma, C., Palme, R., Albrecht, U., and Steinlechner, S. (2006). Impaired daily glucocorticoid rhythm in Per1 (Brd) mice. J. Comp. Physiol. A. Neuroethol. Sens. Neural. Behav. Physiol. 192, 769-775. doi: 10.1007/s00359-006-0114-9
13. Delgado, M. R., Nystrom, L. E., Fissell, C., Noll, D. C., and Fiez, J. A. (2000). Tracking the hemodynamic responses to reward and punishment in the striatum. J. Neurophysiol. 84, 3072-3077. Available online at: http://jn.physiology.org/content/84/6/3072.long
14. Dillon, D. G., Holmes, A. J., Birk, J. L., Brooks, N., Lyons-Ruth, K., and Pizzagalli, D. A. (2009). Childhood adversity is associated with left basal ganglia dysfunction during reward anticipation in adulthood. Biol. Psychiatry 66, 206-213. doi: 10.1016/j.biopsych.2009.02.019
15. Do, C. B., Tung, J. Y., Dorfman, E., Kiefer, A. K., Drabant, E. M., Francke, U., et al. (2011). Web-based genome-wide association study identifies two novel loci and a substantial genetic component for parkinson's disease. PLoS Genet. 7:e1002141. doi: 10.1371/journal.pgen.1002141
16. Dong, L., Bilbao, A., Laucht, M., Henriksson, R., Yakovleva, T., Ridinger, M., et al. (2011). Effects of the circadian rhythm gene period 1 (per1) on psychosocial stress-induced alcohol drinking. Am. J. Psychiatry 168, 1090-1098. doi: 10.1176/appi.ajp.2011.10111579
17. Duncan, L., and Keller, M. (2011). A critical review of the first 10 years of candidate gene-by-environmental interaction research in psychiatry. Am. J. Psychiatry 168, 1041-1049. doi: 10.1176/appi.ajp.2011.11020191
18. Enoch, M.-A. (2011). The role of early life stress as a predictor for alcohol and drug dependence. Psychopharmacology (Berl.) 214, 17-31. doi: 10.1007/s00213-010-1916-6
19. Eriksson, N., Macpherson, J. M., Tung, J. Y., Hon, L. S., Naughton, B., Saxonov, S., et al. (2010). Web-based, participant-driven studies yield novel genetic associations for common traits. PLoS Genet. 6:e1000993. doi: 10.1371/journal.pgen.1000993
20. Fillmore, K. M., Hartka, E., Johnstone, B. M., Leino, E. V, Motoyoshi, M., and Temple, M. T. (1991). A meta-analysis of life course variation in drinking. Br. J. Addict. 86, 1221-1267. doi: 10.1111/j.1360-0443.1991.tb01702.x
21. First, M. B., Gibbon, M., Spitzer, R. L., Williams, J. B. W., and Benjamin, L. S. (1997). Structured Clinical Interview for DSM-IV Axis II Personality Disorders, (SCID-II). Washington, DC: American Psychiatric Press.
22. Gamsby, J. J., Templeton, E. L., Bonvini, L. A., Wang, W., Loros, J. J., Dunlap, J. C., et al. (2013). The circadian Per1 and Per2 genes influence alcohol intake, reinforcement, and blood alcohol levels. Behav. Brain Res. 249, 15-21. doi: 10.1016/j.bbr.2013.04.016
23. Gauderman, W. J. (2002a). Sample size requirements for association studies of gene-gene interaction. Am. J. Epidemiol. 155, 478-484. doi: 10.1093/aje/155.5.478
24. Gauderman, W. J. (2002b). Sample size requirements for matched case-control studies of gene-environment interaction. Stat. Med. 21, 35-50. doi: 10.1002/sim.973
25. Hariri, A., Brown, S. M., Williamson D. E., Flory, J. D., de Wit, H., and Manuck, S. B. (2006). Preference for immediate over delayed rewards is associated with magnitude of ventral striatal activity. J. Neurosci. 26, 13213-13217. doi: 10.1523/JNEUROSCI.3446-06.2006
26. Hasin, D. S., Stinson, F. S., Ogburn, E., and Grant, B. F. (2007). Prevalence, correlates, disability, and comorbidity of DSM-IV alcohol abuse and dependence in the United States. Arch. Gen. Psychiatry 64, 830-842. doi: 10.1001/archpsyc.64.7.830
27. Hayes, A. (2013). Introduction to Mediation, Moderation, and Conditional Process Analysis. New York, NY: Guilford Press.
28. Holm, S. M., Forbes, E. E., Ryan, N. D., Phillips, M. L., Tarr, J. A., and Dahl, R. E. (2009). Reward-related brain function and sleep in pre/early pubertal and mid/late pubertal adolescents. J. Adolesc. Health 45, 326-334. doi: 10.1016/j.jadohealth.2009.04.001
29. Hu, Y., Shmygelska, A., Tran, D., Eriksson, N., Tung, J., and Hinds, D. (2016). GWAS of 89,283 individuals identifies genetic variants associated with being a morning person. Nat. Commun. 7, 1-9. doi: 10.1038/ncomms10448
30. Jackson, K. M., Sher, K. J., Gotham, H. J., and Wood, P. K. (2001). Transitioning into and out of large-effect drinking in young adulthood. J. Abnorm. Psychol. 110, 378-391. doi: 10.1037/0021-843X.110.3.378
31. Keller, M. C. (2014). Gene × environment interaction studies have not properly controlled for potential confounders: the problem and the (simple) solution. Biol. Psychiatry 75, 18-24. doi: 10.1016/j.biopsych.2013.09.006
32. Kokotailo, P. K., Egan, J., Gangnon, R., Brown, D., Mundt, M., and Fleming, M. (2004). Validity of the alcohol use disorders identification test in college students. Alcohol. Clin. Exp. Res. 28, 914-920. doi: 10.1097/01.ALC.0000128239.87611.F5
33. Kovanen, L., Saarikoski, S. T., Haukka, J., Pirkola, S., Aromaa, A., Lönnqvist, J., et al. (2010). Circadian clock gene polymorphisms in alcohol use disorders and alcohol consumption. Alcohol Alcohol 45, 303-311. doi: 10.1093/alcalc/agq035
34. Lancaster, J. L., Woldorff, M. G., Parsons, L. M., Liotti, M., Freitas, C. S., Rainey, L., et al. (2000). Automated Talairach Atlas labels for functional brain mapping. Hum. Brain Mapp. 10, 120-131. doi: 10.1002/1097-0193(200007)10:3<120::AID-HBM30>3.0.CO;2-8
35. Li, M., Xue, X., Shao, S., Shao, F., and Wang, W. (2013). Cognitive, emotional and neurochemical effects of repeated maternal separation in adolescent rats. Brain Res. 1518, 82-90. doi: 10.1016/j.brainres.2013.04.026
36. Liu, Y., Wang, Y., Jiang, Z., Wan, C., Zhou, W., and Wang, Z. (2007). The extracellular signal-regulated kinase signaling pathway is involved in the modulation of morphine-induced reward by mPer1. Neuroscience 146, 265-271. doi: 10.1016/j.neuroscience.2007.01.009
37. Maldjian, J. A., Laurienti, P. J., Kraft, R. A., and Burdette, J. H. (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19, 1233-1239. doi: 10.1016/S1053-8119(03)00169-1
38. McCarthy, M. J., Fernandes, M., Kranzler, H. R., Covault, J. M., and Welsh, D. K. (2013). Circadian clock period inversely correlates with illness severity in cells from patients with alcohol use disorders. Alcohol. Clin. Exp. Res. 37, 1304-1310. doi: 10.1111/acer.12106
39. Meerlo, P., Sgoifo, A., and Turek, F. W. (2002). The effects of social defeat and other stressors on the expression of circadian rhythms. Stress 5, 15-22. doi: 10.1080/102538902900012323
40. Monroe, S. M. (2008). Modern approaches to conceptualizing and measuring human life stress. Annu. Rev. Clin. Psychol. 4, 33-52. doi: 10.1146/annurev.clinpsy.4.022007.141207
41. Mullin, B. C., Phillips, M. L., Siegle, G. J., Buysse, D. J., Forbes, E. E., and Franzen, P. L. (2013). Sleep deprivation amplifies striatal activation to monetary reward. Psychol. Med. 43, 2215-2225. doi: 10.1017/S0033291712002875
42. Nader, N., Chrousos, G. P., and Kino, T. (2009). Circadian rhythm transcription factor CLOCK regulates the transcriptional activity of the glucocorticoid receptor by acetylating its hinge region lysine cluster: potential physiological implications. FASEB J. 23, 1572-1583. doi: 10.1096/fj.08-117697
43. Nader, N., Chrousos, G. P., and Kino, T. (2010). Interactions of the circadian CLOCK system and the HPA axis. Trends Endocrinol. Metab. 21, 277-286. doi: 10.1016/j.tem.2009.12.011
44. Naimi, T. S., Brewer, R. D., Mokdad, A., Denny, C., Serdula, M. K., and Marks, J. S. (2003). Binge drinking among US adults. JAMA J. Am. Med. Assoc. 289, 70-75. doi: 10.1001/jama.289.1.70
45. Nesan, D., and Vijayan, M. M. (2013). The transcriptomics of glucocorticoid receptor signaling in developing zebrafish. PLoS ONE 8:e80726. doi: 10.1371/journal.pone.0080726
46. Nieto, M. A. (2002). The snail superfamily of zinc-finger transcription factors. Nat. Rev. Mol. Cell Biol. 3, 155-166. doi: 10.1038/nrm757
47. Nikolova, Y. S., Bogdan, R., Brigidi, B. D., and Hariri, A. R. (2012). Ventral striatum reactivity to reward and recent life stress interact to predict positive affect. Biol. Psychiatry 72, 157-163. doi: 10.1016/j.biopsych.2012.03.014
48. Polman, J. A. E., Welten, J. E., Bosch, D. S., de Jonge, R. T., Balog, J., van der Maarel, S. M., et al. (2012). A genome-wide signature of glucocorticoid receptor binding in neuronal PC12 cells. BMC Neurosci. 13:118. doi: 10.1186/1471-2202-13-118
49. Price, A. L., Patterson, N. J., Plenge, R. M., Weinblatt, M. E., Shadick, N. A., and Reich, D. (2006). Principal components analysis corrects for stratification in genome-wide association studies. Nat. Genet. 38, 904-909. doi: 10.1038/ng1847
50. Reddy, T. E., Gertz, J., Crawford, G. E., Garabedian, M. J., and Myers, R. M. (2012). The hypersensitive glucocorticoid response specifically regulates period 1 and expression of circadian genes. Mol. Cell. Biol. 32, 3756-3767. doi: 10.1128/MCB.00062-12
51. Reddy, T. E., Pauli, F., Sprouse, R. O., Neff, N. F., Newberry, K. M., Garabedian, M. J., et al. (2009). Genomic determination of the glucocorticoid response reveals unexpected mechanisms of gene regulation. Genome Res. 19, 2163-2171. doi: 10.1101/gr.097022.109
52. Sarkar, D. K. (2012). Circadian genes, the stress axis, and alcoholism. Alcohol Res. 34, 362-366. Available online at: http://pubs.niaaa.nih.gov/publications/arcr343/362-366.htm
53. Saunders, J. B., Aasland, O. G., Babor, T. F., de la Fuente, J. R., and Grant, M. (1993). Development of the Alcohol Use Disorders Identification Test (AUDIT): WHO collaborative project on early detection of persons with harmful alcohol consumption-II. Addiction 88, 791-804. doi: 10.1111/j.1360-0443.1993.tb02093.x
54. Schäfer, I., Reininghaus, U., Langeland, W., Voss, A., Zieger, N., Haasen, C., et al. (2007). Dissociative symptoms in alcohol-dependent patients: associations with childhood trauma and substance abuse characteristics. Compr. Psychiatry 48, 539-545. doi: 10.1016/j.comppsych.2007.05.013
55. Scher, C. D., Stein, M. B., Asmundson, G. J. G., McCreary, D. R., and Forde, D. R. (2001). The childhood trauma questionnaire in a community sample: psychometric properties and normative data. J. Trauma. Stress 14, 843-857. doi: 10.1023/A:1013058625719
56. Schulenberg, J., Maggs, J. L., Long, S. W., Sher, K. J., Gotham, H. J., Baer, J. S., et al. (2001). The problem of college drinking: insights from a developmental perspective. Alcohol. Clin. Exp. Res. 25, 473-477. doi: 10.1111/j.1530-0277.2001.tb02237.x
57. Shan, T., Cui, X., Li, W., Lin, W., Li, Y., Chen, X., et al. (2014). Novel regulatory program for norepinephrine-induced epithelial-mesenchymal transition in gastric adenocarcinoma cell lines. Cancer Sci. 105, 847-856. doi: 10.1111/cas.12438
58. Sheehan, D. V., Lecrubier, Y., Sheehan, K. H., Amorim, P., Janavs, J., Weiller, E., et al. (1998). The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J. Clin. Psychiatry 59(Suppl. 2), 22-33.
59. Spanagel, R., Rosenwasser, A. M., Schumann, G., and Sarkar, D. K. (2005). Alcohol consumption and the body's biological clock. Alcohol. Clin. Exp. Res. 29, 1550-1557. doi: 10.1097/01.alc.0000175074.70807.fd
60. Spencer, S., Falcon, E., Kumar, J., Krishnan, V., Mukherjee, S., Birnbaum, S. G., et al. (2013). Circadian genes Period 1 and Period 2 in the nucleus accumbens regulate anxiety-related behavior. Eur. J. Neurosci. 37, 242-250. doi: 10.1111/ejn.12010
61. Spreckelmeyer, K. N., Krach, S., Kohls, G., Rademacher, L., Irmak, A., Konrad, K., et al. (2009). Anticipation of monetary and social reward differently activates mesolimbic brain structures in men and women. Soc. Cogn. Affect. Neurosci. 4, 158-165. doi: 10.1093/scan/nsn051
62. Tung, J. Y., Do, C. B., Hinds, D. A., Kiefer, A. K., Macpherson, J. M., Chowdry, A. B., et al. (2011). Efficient replication of over 180 genetic associations with self-reported medical data. PLoS ONE 6:e23473. doi: 10.1371/journal.pone.0023473
63. Venkatraman, V., Huettel, S. A., Chuah, L. Y. M., Payne, J. W., and Chee, M. W. L. (2011). Sleep deprivation biases the neural mechanisms underlying economic preferences. J. Neurosci. 31, 3712-3718. doi: 10.1523/JNEUROSCI.4407-10.2011
64. Watson, S., Owen, B. M., Gallagher, P., Hearn, A. J., Young, A. H., and Ferrier, I. N. (2007). Family history, early adversity and the hypothalamic-pituitary-adrenal (HPA) axis: Mediation of the vulnerability to mood disorders. Neuropsychiatr. Dis. Treat. 3, 647-653. Available online at: https://www.dovepress.com/articles.php?article_id=939
65. Wirth, M., Burch, J., Violanti, J., Burchfiel, C., Fekedulegn, D., Andrew, M., et al. (2013). Association of the Period3 clock gene length polymorphism with salivary cortisol secretion among police officers. Neuro Endocrinol. Lett. 34, 27-37. Available online at: http://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23524621/
66. Wong, M. M., Brower, K. J., Nigg, J. T., and Zucker, R., a. (2010). Childhood sleep problems, response inhibition, and alcohol and drug outcomes in adolescence and young adulthood. Alcohol. Clin. Exp. Res. 34, 1033-1044. doi: 10.1111/j.1530-0277.2010.01178.x
67. Wright, K. D., Asmundson, G. J., McCreary, D. R., Scher, C., Hami, S., and Stein, M. B. (2001). Factorial validity of the childhood trauma questionnaire in men and women. Depress. Anxiety 13, 179-183. doi: 10.1002/da.1034
68. Wulff, K., Porcheret, K., Cussans, E., and Foster, R. G. (2009). Sleep and circadian rhythm disturbances: multiple genes and multiple phenotypes. Curr. Opin. Genet. Dev. 19, 237-246. doi: 10.1016/j.gde.2009.03.007
69. Yamamoto, T., Nakahata, Y., Tanaka, M., Yoshida, M., Soma, H., Shinohara, K., et al. (2005). Acute physical stress elevates mouse period1 mRNA expression in mouse peripheral tissues via a glucocorticoid-responsive element. J. Biol. Chem. 280, 42036-42043. doi: 10.1074/jbc.M509600200
70. Yau, W.-Y. W., Zubieta, J.-K., Weiland, B. J., Samudra, P. G., Zucker, R. A., and Heitzeg, M. M. (2012). Nucleus accumbens response to incentive stimuli anticipation in children of alcoholics: relationships with precursive behavioral risk and lifetime alcohol use. J. Neurosci. 32, 2544-2551. doi: 10.1523/JNEUROSCI.1390-11.2012