Involvement of the BDNF gene in loneliness in adolescence: A report of opposite gene effects in boys and girls

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Verhagen, Maaike ^a   Van Roekel, Eeske ^a,b   Engels, Rutger C M E ^a  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR;

ADOLESCENT; ARTICLE; BRAIN DERIVED NEUROTROPHIC FACTOR GENE; FEMALE; GENETIC POLYMORPHISM; GENOTYPE; HUMAN; LONELINESS; LONGITUDINAL STUDY; MALE; SEX DIFFERENCE;

ADOLESCENT; BRAIN-DERIVED NEUROTROPHIC FACTOR; CHILD; FEMALE; GENE-ENVIRONMENT INTERACTION; GENOTYPE; HUMANS; LONELINESS; MALE;

EID: 84898603201     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0092768     Document Type: Article

References (65)

1. Baumeister RF, Leary MR (1995) The need to belong: desire for interpersonal attachments as a fundamental human motivation. Psychol Bull 117: 497-529.
2. Perlman D, Peplau LA (1981) Toward a social psychology of loneliness. In: Gillmour R, Duck S, editors. Personal Relationships 3: Personal Relationships in Disorder. London: Academic Press. 31-56.
3. Cacioppo JT, Hawkley LC (2009) Perceived social isolation and cognition. Trends in Cognitive Sciences 13: 447-454.
4. Gardner WL, Pickett CL, Jefferis V, Knowles M (2005) On the outside looking in: loneliness and social monitoring. Pers Soc Psychol Bull 31: 1549-1560. (Pubitemid 41560520)
5. Rotenberg KJ, Addis N, Betts LR, Corrigan A, Fox C, et al. (2010) The relation between trust beliefs and loneliness during early childhood, middle childhood, and adulthood. Pers Soc Psychol Bull 36: 1086-1100.
6. Barrientos RM, Sprunger DB, Campeau S, Higgins EA, Watkins LR, et al. (2003) Brain-derived neurotrophic factor mRNA downregulation produced by social isolation is blocked by intrahippocampal interleukin-1 receptor antagonist. Neuroscience 121: 847-853. (Pubitemid 37324583)
7. Schumacher J, Jamra RA, Becker T, Ohlraun S, Klopp N, et al. (2005) Evidence for a relationship between genetic variants at the brain-derived neurotrophic factor (BDNF) locus and major depression. Biol Psychiatry 58: 307-314. (Pubitemid 41133624)
8. Angelucci F, Brene S, Mathe AA (2005) BDNF in schizophrenia, depression and corresponding animal models. Mol Psychiatry 10: 345-352.
9. Bath KG, Lee FS (2006) Variant BDNF (Val66Met) impact on brain structure and function. Cogn Affect Behav Neurosci 6: 79-85.
10. Duman RS (2004) Role of neurotrophic factors in the etiology and treatment of mood disorders. Neuromolecular Med 5: 11-25.
11. Martinowich K, Manji H, Lu B (2007) New insights into BDNF function in depression and anxiety. Nat Neurosci 10: 1089-1093. (Pubitemid 47339961)
12. Bueller JA, Aftab M, Sen S, Gomez-Hassan D, Burmeister M, et al. (2006) BDNF Val66Met allele is associated with reduced hippocampal volume in healthy subjects. Biol Psychiatry 59: 812-815.
13. Frodl T, Schule C, Schmitt G, Born C, Baghai T, et al. (2007) Association of the brain-derived neurotrophic factor Val66Met polymorphism with reduced hippocampal volumes in major depression. Arch Gen Psychiatry 64: 410-416. (Pubitemid 46556460)
14. Hajek T, Kopecek M, Hoschl C (2012) Reduced hippocampal volumes in healthy carriers of brain-derived neurotrophic factor Val66Met polymorphism: meta-analysis. World J Biol Psychiatry 13: 178-187.
15. Pezawas L, Verchinski BA, Mattay VS, Callicott JH, Kolachana BS, et al. (2004) The brain-derived neurotrophic factor val66met polymorphism and variation in human cortical morphology. J Neurosci 24: 10099-10102. (Pubitemid 39492034)
16. Sublette ME, Baca-Garcia E, Parsey RV, Oquendo MA, Rodrigues SM, et al. (2008) Effect of BDNF val66met polymorphism on age-related amygdala volume changes in healthy subjects. Prog Neuropsychopharmacol Biol Psychiatry 32: 1652-1655.
17. Mueller SC, Aouidad A, Gorodetsky E, Goldman D, Pine DS, et al. (2013) Gray matter volume in adolescent anxiety: an impact of the brain-derived neurotrophic factor Val(66)Met polymorphism? J Am Acad Child Adolesc Psychiatry 52: 184-195.
18. Montag C, Weber B, Fliessbach K, Elger C, Reuter M (2009) The BDNF Val66Met polymorphism impacts parahippocampal and amygdala volume in healthy humans: incremental support for a genetic risk factor for depression. Psychol Med 39: 1831-1839.
19. Gasic GP, Smoller JW, Perlis RH, Sun M, Lee S, et al. (2009) BDNF, relative preference, and reward circuitry responses to emotional communication. Am J Med Genet B Neuropsychiatr Genet 150B: 762-781.
20. Hariri AR, Goldberg TE, Mattay VS, Kolachana BS, Callicott JH, et al. (2003) Brain-derived neurotrophic factor val66met polymorphism affects human memory-related hippocampal activity and predicts memory performance. J Neurosci 23: 6690-6694. (Pubitemid 36951196)
21. Molendijk ML, van Tol MJ, Penninx BW, van der Wee NJ, Aleman A, et al. (2012) BDNF val66met affects hippocampal volume and emotion-related hippocampal memory activity. Transl Psychiatry 2: e74. doi: 10.1038/tp.2011.72.
22. Montag C, Reuter M, Newport B, Elger C, Weber B (2008) The BDNF Val66Met polymorphism affects amygdala activity in response to emotional stimuli: evidence from a genetic imaging study. Neuroimage 42: 1554-1559.
23. Mukherjee P, Whalley HC, McKirdy JW, McIntosh AM, Johnstone EC, et al. (2011) Effects of the BDNF Val66Met polymorphism on neural responses to facial emotion. Psychiatry Res 191: 182-188.
24. Outhred T, Das P, Dobson-Stone C, Griffiths K, Felmingham KL, et al. (2012) The functional epistasis of 5-HTTLPR and BDNF Val66Met on emotion processing: a preliminary study. Brain Behav 2: 778-788.
25. Van Oostrom I, Franke B, Rijpkema M, Gerritsen L, Arias-Vasquez A, et al. (2012) Interaction between BDNF Val66Met and childhood stressful life events is associated to affective memory bias in men but not women. Biol Psychol 89: 214-219.
26. Lau JY, Goldman D, Buzas B, Hodgkinson C, Leibenluft E, et al. (2010) BDNF gene polymorphism (Val66Met) predicts amygdala and anterior hippocampus responses to emotional faces in anxious and depressed adolescents. Neuroimage 53: 952-961.
27. Verhagen M, Van der Meij A, Van Deurzen PA, Janzing JG, Arias-Vasquez A, et al. (2010) Meta-analysis of the BDNF Val66Met polymorphism in major depressive disorder: effects of gender and ethnicity. Mol Psychiatry 15: 260-271.
28. Van Wingen G, Rijpkema M, Franke B, Van Eijndhoven P, Tendolkar I, et al. (2010) The brain-derived neurotrophic factor Val66Met polymorphism affects memory formation and retrieval of biologically salient stimuli. Neuroimage 50: 1212-1218.
29. Shalev I, Lerer E, Israel S, Uzefovsky F, Gritsenko I, et al. (2009) BDNF Val66Met polymorphism is associated with HPA axis reactivity to psychological stress characterized by genotype and gender interactions. Psychoneuroendocrinology 34: 382-388.
30. Van der Vorst H, Engels RC, Meeus W, Dekovic M, Van Leeuwe J (2005) The role of alcohol-specific socialization in adolescents' drinking behaviour. Addiction 100: 1464-1476. (Pubitemid 41442316)
31. Van Roekel E, Scholte RH, Verhagen M, Goossens L, Engels RC (2010) Loneliness in adolescence: gene x environment interactions involving the serotonin transporter gene. J Child Psychol Psychiatry 51: 747-754.
32. Marcoen A, Goossens L, Caes P (1987) Loneliness in pre- through late adolescence: Exploring the contributions of a multidimensional approach. J Youth Adolesc 16: 561-577. (Pubitemid 18034047)
33. Duncan TE, Duncan SC, Strycker LA (2006) An introduction to latent variable growth curve modeling: Concepts, issues, and applications, 2nd ed. Mahwah: NJ, Erlbaum.
34. Muthén LK, Muthén BO (1998-2007) Mplus User's Guide (5th ed). CA, Los Angeles: Muthén & Muthén.
35. Marcoen A, Goossens L (1993) Loneliness, attitude toward aloneness, and solitude: Age differences and developmental significance during adolescence. In: Jackson S, Rodriguez-Tome H, editors. Adolescence and its Social Worlds: Hove, UK, Erlbaum. 197-227.
36. Qualter P, Rotenberg K, Barrett L, Henzi P, Barlow A, et al. (2013) Investigating hypervigilance for social threat of lonely children. J Abnorm Child Psychol 41: 325-338.
37. Cacioppo JT, Norris CJ, Decety J, Monteleone G, Nusbaum H (2009) In the eye of the beholder: individual differences in perceived social isolation predict regional brain activation to social stimuli. J Cogn Neurosci 21: 83-92.
38. Rutter M, Moffitt TE, Caspi A (2006) Gene-environment interplay and psychopathology: multiple varieties but real effects. J Child Psychol Psychiatry 47: 226-261. (Pubitemid 43356058)
39. Lang UE, Hellweg R, Kalus P, Bajbouj M, Lenzen KP, et al. (2005) Association of a functional BDNF polymorphism and anxiety-related personality traits. Psychopharmacology (Berl) 180: 95-99. (Pubitemid 40897075)
40. Sen S, Nesse RM, Stoltenberg SF, Li S, Gleiberman L, et al. (2003) A BDNF coding variant is associated with the NEO personality inventory domain neuroticism, a risk factor for depression. Neuropsychopharmacology 28: 397-401.
41. Heinrich LM, Gullone E (2006) The clinical significance of loneliness: A literature review. Clin Psychol Rev 26: 695-718. (Pubitemid 44316874)
42. Meltser I, Tahera Y, Simpson E, Hultcrantz M, Charitidi K, et al. (2008) Estrogen receptor beta protects against acoustic trauma in mice. J Clin Invest 118: 1563-1570. (Pubitemid 351500449)
43. Doane LD, Adam EK (2010) Loneliness and cortisol: momentary, day-to-day, and trait associations. Psychoneuroendocrinology 35: 430-441.
44. Pressman SD, Cohen S, Miller GE, Barkin A, Rabin BS, et al. (2005) Loneliness, social network size, and immune response to influenza vaccination in college freshmen. Health Psychol 24: 297-306. (Pubitemid 40677201)
45. Weiss LA, Pan L, Abney M, Ober C (2006) The sex-specific genetic architecture of quantitative traits in humans. Nat Genet 38: 218-222. (Pubitemid 43177237)
46. Sasahara K, Shikimi H, Haraguchi S, Sakamoto H, Honda S, et al. (2007) Mode of action and functional significance of estrogen-inducing dendritic growth, spinogenesis, and synaptogenesis in the developing Purkinje cell. J Neurosci 27: 7408-7417. (Pubitemid 47071728)
47. Scharfman HE, Maclusky NJ (2005) Similarities between actions of estrogen and BDNF in the hippocampus: coincidence or clue? Trends Neurosci 28: 79-85. (Pubitemid 40178924)
48. Monteggia LM, Luikart B, Barrot M, Theobold D, Malkovska I, et al. (2007) Brain-derived neurotrophic factor conditional knockouts show gender differences in depression-related behaviors. Biol Psychiatry 61: 187-197. (Pubitemid 46072778)
49. Cahill L (2006) Why sex matters for neuroscience. Nat Rev Neurosci 7: 477-484.
50. Groves JO (2007) Is it time to reassess the BDNF hypothesis of depression? Mol Psychiatry 12: 1079-1088.
51. Karege F, Perret G, Bondolfi G, Schwald M, Bertschy G, et al. (2002) Decreased serum brain-derived neurotrophic factor levels in major depressed patients. Psychiatry Res 109: 143-148. (Pubitemid 34258493)
52. Cicchetti D, Rogosch FA (1996) Equifinality and multifinality in developmental psychopathology. Dev Psychopathol 8: 597-600.
53. De Geus E, Goldberg T, Boomsma DI, Posthuma D (2008) Imaging the genetics of brain structure and function. Biol Psychol 79: 1-8.
54. Lucht MJ, Barnow S, Sonnenfeld C, Rosenberger A, Grabe HJ, et al. (2009) Associations between the oxytocin receptor gene (OXTR) and affect, loneliness and intelligence in normal subjects. Progress in Neuropsychopharmacology and Biological Psychiatry 33: 860-866.
55. Van Roekel E, Verhagen M, Engels RCME, Goossens L, Scholte RHJ (2013) Oxytocin receptor gene (OXTR) in relation to loneliness in adolescence: Interactions with sex, parental support, and DRD2 and 5-HTTLPR genotypes. Psych Gen 23: 204-213.
56. Van Roekel E, Verhagen M, Scholte RH, Kleinjan M, Goossens L, et al. (2013) The oxytocin receptor gene (OXTR) in relation to state levels of loneliness in adolescence: evidence for micro-level gene-environment interactions. PLoS One 8: e77689. doi:10.1371/journal.pone.0077689.
57. Van Roekel E, Goossens L, Scholte RH, Engels RC, Verhagen M (2011) The dopamine D2 receptor gene, perceived parental support, and adolescent loneliness: longitudinal evidence for gene-environment interactions. J Child Psychol Psychiatry 52: 1044-1051.
58. Chou KL, Cacioppo JT, Kumari M, Song YQ (2013) Influence of Social Environment on Loneliness in Older Adults: Moderation by Polymorphism in the CRHR1. Am J Geriatr Psychiatry. doi: 10.1016/j.jagp.2012.11.002.
59. Dunn EC, Solovieff N, Lowe SR, Gallagher PJ, Chaponis J, et al. (2014) Interaction between genetic variants and exposure to Hurricane Katrina on post-traumatic stress and post-traumatic growth: A prospective analysis of low income adults. J Affect Disord 152-154: 243-249.
60. Unternaehrer E, Luers P, Mill J, Dempster E, Meyer AH, et al. (2012) Dynamic changes in DNA methylation of stress-associated genes (OXTR, BDNF) after acute psychosocial stress. Transl Psychiatry 2: e150. doi: 10.1038/tp.2012.77.
61. Gauderman WJ, Morrison JM (2006) QUANTO 1.1: A computer program for power and sample size calculations for genetic-epidemiology studies. http://hydrauscedu/gxe.
62. Wong MY, Day NE, Luan JA, Chan KP, Wareham NJ (2003) The detection of gene-environment interaction for continuous traits: should we deal with measurement error by bigger studies or better measurement? Int J Epidemiol 32: 51-57. (Pubitemid 36503473)
63. Muthén BO, Curran PJ (1997) General longitudinal modeling of individual differences in experimental designs: A latent variable framework for analysis and power estimation. Psychol Methods 2: 371-402. (Pubitemid 127453678)
64. Webster MJ, Weickert CS, Herman MM, Kleinman JE (2002) BDNF mRNA expression during postnatal development, maturation and aging of the human prefrontal cortex. Brain Res Dev Brain Res 139: 139-150. (Pubitemid 35453900)
65. Hilt LM, Sander LC, Nolen-Hoeksema S, Simen AA (2007) The BDNF Val66Met polymorphism predicts rumination and depression differently in young adolescent girls and their mothers. Neurosci Lett 429: 12-16. (Pubitemid 350116345)