Association between methylation of the glucocorticoid receptor gene, childhood maltreatment, and clinical severity in borderline personality disorder

Journal of Psychiatric Research

Volumn 57, Issue 1, 2014, Pages 34-40

  Martín Blanco, Ana ^a,b   Ferrer, Marc ^b,c   Soler, Joaquim ^a,b   Salazar, Juliana ^a   Vega, Daniel ^b,d   Andión, Oscar ^b,c   Sanchez Mora, Cristina ^e   Arranz, Maria Jesús ^a   Ribases, Marta ^e   Feliu Soler, Albert ^a,b   Pérez, Víctor ^a,b   Pascual, Juan Carlos ^a,b  

^a HOSPITAL DE LA SANTA CREU I SANT PAU   (Spain)

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^c HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^d Servei de Psiquiatria i Salut Mental   (Spain)

^e HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

Author keywords

Borderline personality disorder; Childhood trauma; Epigenetics; Genetics; Glucocorticoid receptor gene; Methylation

Indexed keywords

GLUCOCORTICOID RECEPTOR; NR3C1 PROTEIN, HUMAN; MESSENGER RNA;

ADULT; ARTICLE; AUTOMUTILATION; BORDERLINE STATE; CHILD ABUSE; CHILDHOOD INJURY; CHILDHOOD TRAUMA QUESTIONNAIRE; DISEASE SEVERITY; DNA METHYLATION; FEMALE; GENETIC ASSOCIATION; GENOTYPE ENVIRONMENT INTERACTION; GLUCOCORTICOID RECEPTOR GENE; HOSPITALIZATION; HUMAN; MAJOR CLINICAL STUDY; MALE; PHYSICAL ABUSE; PRIORITY JOURNAL; PROMOTER REGION; RECEPTOR GENE; SELF REPORT; STRUCTURED CLINICAL INTERVIEW FOR DSM DISORDERS; CHILD; GENETICS; PSYCHOLOGY; SEVERITY OF ILLNESS INDEX; YOUNG ADULT; CHILD HOSPITALIZATION; CHILD NEGLECT; CHILD SEXUAL ABUSE; CORRELATION ANALYSIS; CPG ISLAND; DNA EXTRACTION; EMOTIONAL ABUSE; SEMI STRUCTURED INTERVIEW; SEX DIFFERENCE;

ADULT; BORDERLINE PERSONALITY DISORDER; CHILD; CHILD ABUSE; DNA METHYLATION; FEMALE; GENE-ENVIRONMENT INTERACTION; HOSPITALIZATION; HUMANS; MALE; PROMOTER REGIONS, GENETIC; RECEPTORS, GLUCOCORTICOID; SELF-INJURIOUS BEHAVIOR; SEVERITY OF ILLNESS INDEX; YOUNG ADULT;

EID: 84905587278     PISSN: 00223956     EISSN: 18791379     Source Type: Journal    
DOI: 10.1016/j.jpsychires.2014.06.011     Document Type: Article

References (45)

1. Barrachina J., Soler J., Campins M.J., Tejero A., Pascual J.C., Alvarez E., et al. Validation of a Spanish version of the diagnostic interview for borderlines revised (DIB-R). Actas Esp Psiquiatr 2004, 32:293-298.
2. Beauchaine T.P., Klein D.N., Crowell S.E., Derbidge C., Gatzke-Kopp L. Multifinality in the development of personality disorders: a Biology × Sex × Environment interaction model of antisocial and borderline traits. Dev Psychopathol 2009, 21:735-770.
3. Bernstein D.P., Stein J.A., Newcomb M.D., Walker E., Pogge D., Ahluvalia T., et al. Development and validation of a brief screening version of the Childhood Trauma Questionnaire. Child Abuse Negl 2003, 27:169-190.
4. Carpenter L.L., Carvalho J.P., Tyrka A.R., Wier L.M., Mello A.F., Mello M.F., et al. Decreased adrenocorticotropic hormone and cortisol responses to stress in healthy adults reporting significant childhood maltreatment. Biol Psychiatry 2007, 62:1080-1087.
5. Carrasco J.L., Díaz-Marsá M., Pastrana J.I., Molina R., Brotons L., López-Ibor M.I., et al. Hypothalamic-pituitary-adrenal axis response in borderline personality disorder without post-traumatic features. Br J Psychiatry 2007, 190:357-358.
6. Crowell S.E., Beauchaine T.P., Linehan M.M. A biosocial developmental model of borderline personality: elaborating and extending Linehan's theory. Psychol Bull 2009, 135:495-510.
7. Dammann G., Teschler S., Haag T., Altmüller F., Tuczek F., Dammann R.H. Increased DNA methylation of neuropsychiatric genes occurs in borderline personality disorder. Epigenetics 2011, 6:1454-1462.
8. Davies M.N., Volta M., Pidsley R., Lunnon K., Dixit A., Lovestone S., et al. Functional annotation of the human brain methylome identifies tissue-specific epigenetic variation across brain and blood. Genome Biol 2012, 13:R43.
9. Freeman A.I., Munn H.L., Lyons V., Dammermann A., Seckl J.R., Chapman K.E. Glucocorticoid down-regulation of rat glucocorticoid receptor does not involve differential promoter regulation. J Endocrinol 2004, 183:365-374.
10. Gómez-Beneyto M., Villar M., Renovell M., Pérez F., Hernández M., Leal C., et al. The diagnosis of personality disorder with a modified version of the SCID-II in a Spanish clinical sample. J Personal Disord 1994, 8:104-110.
11. Heim C., Nemeroff C.B. The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol Psychiatry 2001, 50:200-204.
12. Hollenberg S.M., Weinberger C., Ong E.S., Cerelli G., Oro A., Lebo R., et al. Primary structure and expression of a functional human glucocorticoid receptor cDNA. Nature 1985-86, 318:635-641.
13. Hompes T., Izzi B., Gellens E., Morreels M., Fieuws S., Pexsters A., et al. Investigating the influence of maternal cortisol and emotional state during pregnancy on the DNA methylation status of the glucocorticoid receptor gene (NR3C1) promoter region in cord blood. J Psychiatr Res 2013, 47:880-891.
14. Jaenisch R., Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 2003, 33(Suppl.):245-254.
15. Labonte B., Yerko V., Gross J., Mechawar N., Meaney M.J., Szyf M., et al. Differential glucocorticoid receptor exon 1(B), 1(C), and 1(H) expression and methylation in suicide completers with a history of childhood abuse. Biol Psychiatry 2012, 72:41-48.
16. Lam L.L., Emberly E., Fraser H.B., Neumann S.M., Chen E., Miller G.E., et al. Factors underlying variable DNA methylation in a human community cohort. PNAS 2012, 109(Suppl. 2):17253-17260.
17. Linehan M.M. Cognitive-behavioral treatment for borderline personality disorder; the dialectics of effective treatment 1993, The Guilford Press, New York.
18. Martín-Blanco A., Soler J., Villalta L., Feliu-Soler A., Elices M., Pérez V., et al. Exploring the interaction between childhood maltreatment and temperamental traits on the severity of borderline personality disorder. Compr Psychiatry 2014, 55:311-318.
19. Masliah E., Dumaop W., Galasko D., Desplats P. Distinctive patterns of DNA methylation associated with Parkinson disease: identification of concordant epigenetic changes in brain and peripheral blood leukocytes. Epigenetics 2013, 8:1030-1038.
20. McCormick J.A., Lyons V., Jacobson M.D., Noble J., Diorio J., Nyirenda M., et al. 5'-heterogeneity of glucocorticoid receptor messenger RNA is tissue specific: differential regulation of variant transcripts by early-life events. Mol Endocrinol 2000, 14:506-517.
21. McGowan P.O., Meaney M.J., Szyf M. Diet and the epigenetic (re)programming of phenotypic differences in behavior. Brain Res 2008, 1237:12-24.
22. McGowan P.O., Sasaki A., D'Alessio A.C., Dymov S., Labonte B., Szyf M., et al. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci 2009, 12:342-348.
23. Meaney M.J., Ferguson-Smith A.C. Epigenetic regulation of the neural transcriptome: the meaning of the marks. Nat Neurosci 2010, 13:1313-1318.
24. Miller S.A., Dykes D.D., Polesky H. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 1989, 16:1215.
25. Mulligan C.J., D'Errico N.C., Stees J., Hughes D.A. Methylation changes at NR3C1 in newborns associate with maternal prenatal stress exposure and newborn birth weight. Epigenetics 2012, 7:853-857.
26. Murgatroyd C., Spengler D. Epigenetics of early child development. Front Psychiatry 2011, 2:16.
27. Nemeroff C.B. The preeminent role of early untoward experience on vulnerability to major psychiatric disorders: the nature-nurture controversy revisited and soon to be resolved. Mol Psychiatry 1999, 4:106-108.
28. Oberlander T.F., Weinberg J., Papsdorf M., Grunau R., Misri S., Devlin A.M. Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics 2008, 3:97-106.
29. Perroud N., Paoloni-Giacobino A., Prada P., Olié E., Salzmann A., Nicastro R., et al. Increased methylation of glucocorticoid receptor gene (NR3C1) in adults with a history of childhood maltreatment: a link with the severity and type of trauma. Transl Psychiatry 2011, 1:e59.
30. Perroud N., Dayer A., Piguet C., Nallet A., Favre S., Malafosse A., et al. Childhood maltreatment and methylation of the glucocorticoid receptor gene NR3C1 in bipolar disorder. Br J Psychiatry 2013, [in press].
31. Perroud N., Salzmann A., Prada P., Nicastro R., Hoeppli M.E., Furrer S., et al. Response to psychotherapy in borderline personality disorder and methylation status of the BDNF gene. Transl Psychiatry 2013, 3:e207.
32. Radtke K.M., Ruf M., Gunter H.M., Dohrmann K., Schauer M., Meyer A., et al. Transgenerational impact of intimate partner violence on methylation in the promoter of the glucocorticoid receptor. Transl Psychiatry 2011, 1:e21.
33. Terry M.B., Delgado-Cruzata L., Vin-Raviv N., Wu H.C., Santella R.M. DNA methylation in white blood cells: association with risk factors in epidemiologic studies. Epigenetics 2011, 6:828-837.
34. Turner J.D., Muller C.P. Structure of the glucocorticoid receptor (NR3C1) gene 5' untranslated region: identification, and tissue distribution of multiple new human exon 1. J Mol Endocrinol 2005, 35:283-292.
35. Turner J.D., Alt S.R., Cao L., Vernocchi S., Trifonova S., Battello N., et al. Transcriptional control of the glucocorticoid receptor: CpG islands, epigenetics and more. Biochem Pharmacol 2010, 80:1860-1868.
36. Tyrka A.R., Price L.H., Marsit C., Walters O.C., Carpenter L.L. Childhood adversity and epigenetic modulation of the leukocyte glucocorticoid receptor: preliminary findings in healthy adults. PLoS One 2012, 7:e30148.
37. van der Knaap L.J., Riese H., Hudziak J.J., Verbiest M.M., Verhulst F.C., Oldehinkel A.J., et al. Glucocorticoid receptor gene (NR3C1) methylation following stressful events between birth and adolescence. The TRAILS study. Transl Psychiatry 2014, 4:e381.
38. Weaver I.C., Cervoni N., Champagne F.A., D'Alessio A.C., Sharma S., Seckl J.R., et al. Epigenetic programming by maternal behavior. Nat Neurosci 2004, 7:847-854.
39. Widom C.S., Czaja S.J., Paris J. A prospective investigation of borderline personality disorder in abused and neglected children followed up into adulthood. J Personal Disord 2009, 23:433-446.
40. Wingenfeld K., Spitzer C., Rullkötter N., Löwe B. Borderline personality disorder: hypothalamus pituitary adrenal axis and findings from neuroimaging studies. Psychoneuroendocrinology 2010, 35:154-170.
41. Wu H.C., Delgado-Cruzata L., Flom J.D., Kappil M., Ferris J.S., Liao Y., et al. Global methylation profiles in DNA from different blood cell types. Epigenetics 2011, 6:76-85.
42. Yehuda R., Daskalakis N.P., Desarnaud F., Makotkine I., Lehrner A.L., Koch E., et al. Epigenetic biomarkers as predictors and correlates of symptom improvement following psychotherapy in combat veterans with PTSD. Front Psychiatry 2013, 4:118.
43. Zanarini M.C. Childhood experiences associated with the development of borderline personality disorder. Psychiatr Clin North Am 2000, 23:89-101.
44. Zanarini M.C., Frankenburg F.R. Pathways to the development of borderline personality disorder. J Personal Disord 1997, 11:93-104.
45. Zeilinger S., Kühnel B., Klopp N., Baurecht H., Kleinschmidt A., Gieger C., et al. Tobacco smoking leads to extensive genome-wide changes in DNA methylation. PLoS One 2013, 8:e63812.