An analysis of gene expression in PTSD implicates genes involved in the glucocorticoid receptor pathway and neural responses to stress

Psychoneuroendocrinology

Volumn 57, Issue , 2015, Pages 1-13

  Logue, Mark W ^a,b,c   Smith, Alicia K ^d   Baldwin, Clinton ^b   Wolf, Erika J ^a,b   Guffanti, Guia ^e   Ratanatharathorn, Andrew ^f   Stone, Annjanette ^g   Schichman, Steven A ^g   Humphries, Donald ^a   Binder, Elisabeth B ^d,h   Arloth, Janine ^h   Menke, Andreas ^h   Uddin, Monica ⁱ   Wildman, Derek ^i,j   Galea, Sandro ^f   Aiello, Allison E ^k   Koenen, Karestan C ^f   Miller, Mark W ^a,b  

^a VA BOSTON HEALTHCARE SYSTEM   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c BOSTON UNIVERSITY SCHOOL OF PUBLIC HEALTH   (United States)

^d EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e Och Spine at New York Presbyterian Hospitals   (United States)

^f Department of Medicine   (United States)

^g CENTRAL ARKANSAS VETERANS HEALTHCARE SYSTEM   (United States)

^h MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

ⁱ UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^j WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^k University of North Carolina at Chapel Hill   (United States)

more..

Author keywords

ATP6AP1L; DSCAM; Gene expression; Glucocorticoid responsive; PTSD; Whole blood

Indexed keywords

GLUCOCORTICOID RECEPTOR; TRANSCRIPTOME;

AMYGDALOID NUCLEUS; ARTICLE; ATP6AP1L GENE; BDNF GENE; BRAIN REGION; CONTROLLED STUDY; DISEASE SEVERITY; DSCAM GENE; GENE; GENE EXPRESSION; GENE FUNCTION; GENE TARGETING; HIPPOCAMPUS; HUMAN; MAJOR CLINICAL STUDY; NR3C1 GENE; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; TBC1D15 GENE; TXNRD1 GENE; ADULT; AMYGDALA; BLOOD; BRAIN; CASE CONTROL STUDY; GENETICS; MALE; PHYSIOLOGICAL STRESS; PHYSIOLOGY; UNITED STATES; VETERAN;

ADULT; AMYGDALA; BRAIN; CASE-CONTROL STUDIES; HUMANS; MALE; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, GLUCOCORTICOID; STRESS DISORDERS, POST-TRAUMATIC; STRESS, PHYSIOLOGICAL; TRANSCRIPTOME; UNITED STATES; VETERANS;

EID: 84929304551     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2015.03.016     Document Type: Article

References (54)

1. Andero R., Ressler K.J. Fear extinction and BDNF: translating animal models of PTSD to the clinic. Genes Brain Behav. 2012, 11:503-512.
2. Barbosa-Morais N.L., Dunning M.J., Samarajiwa S.A., Darot J.F., Ritchie M.E., Lynch A.G., Tavare S. A re-annotation pipeline for Illumina BeadArrays: improving the interpretation of gene expression data. Nucleic Acids Res. 2010, 38:e17.
3. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 1995, 57:289-300.
4. Blake D.D., Weathers F.W., Nagy L.M., Kaloupek D.G., Charney D.S., Keane T.M. The Clinician-Administered PTSD Scale-IV 1990, National Center for Posttraumatic Stress Disorder Behavioral Sciences Division, Boston, MA.
5. Blake D.D., Weathers F.W., Nagy L.M., Kaloupek D.G., Gusman F.D., Charney D.S., Keane T.M. The development of a clinician-administered PTSD scale. J. Trauma Stress 1995, 8:75-90.
6. Boccaccio I., Glatt-Deeley H., Watrin F., Roeckel N., Lalande M., Muscatelli F. The human MAGEL2 gene and its mouse homologue are paternally expressed and mapped to the Prader-Willi region. Hum. Mol. Genet. 1999, 8:2497-2505.
7. Boyle M.P., Kolber B.J., Vogt S.K., Wozniak D.F., Muglia L.J. Forebrain glucocorticoid receptors modulate anxiety-associated locomotor activation and adrenal responsiveness. J. Neurosci. 2006, 26:1971-1978.
8. Champagne F.A., Curley J.P. Epigenetic mechanisms mediating the long-term effects of maternal care on development. Neurosci. Biobehav. Rev. 2009, 33:593-600.
9. Choi J.D., Underkoffler L.A., Wood A.J., Collins J.N., Williams P.T., Golden J.A., Schuster E.F., Loomes K.M., Oakey R.J. A novel variant of Inpp5f is imprinted in brain, and its expression is correlated with differential methylation of an internal CpG island. Mol. Cell Biol. 2005, 25:5514-5522.
10. Daskalakis N.P., Cohen H., Cai G., Buxbaum J.D., Yehuda R. Expression profiling associates blood and brain glucocorticoid receptor signaling with trauma-related individual differences in both sexes. Proc. Natl. Acad Sci. U.S.A. 2014, 111:13529-13534.
11. Dell'Osso L., Carmassi C., Del Debbio A., Catena Dell'Osso M., Bianchi C., da Pozzo E., Origlia N., Domenici L., Massimetti G., Marazziti D., Piccinni A. Brain-derived neurotrophic factor plasma levels in patients suffering from post-traumatic stress disorder. Prog. Neuropsychopharmacol. Biol. Psychiatry 2009, 33:899-902.
12. Dunning, M., Lynch, A., Eldridge, M., illuminaHumanv4.db: Illumina HumanHT12v4 annotation data.(chip illuminaHumanv4). R package version 1.22.1.
13. Goldmann E., Aiello A., Uddin M., Delva J., Koenen K., Gant L.M., Galea S. Pervasive exposure to violence and posttraumatic stress disorder in a predominantly African American Urban Community: the Detroit Neighborhood Health Study. J Trauma Stress 2011, 24:747-751.
14. Guffanti G., Galea S., Yan L., Roberts A.L., Solovieff N., Aiello A.E., Smoller J.W., De Vivo I., Ranu H., Uddin M., Wildman D.E., Purcell S., Koenen K.C. Genome-wide association study implicates a novel RNA gene, the lincRNA AC068718.1, as a risk factor for post-traumatic stress disorder in women. Psychoneuroendocrinology 2013, 38:3029-3038.
15. Hennings J.M., Owashi T., Binder E.B., Horstmann S., Menke A., Kloiber S., Dose T., Wollweber B., Spieler D., Messer T., Lutz R., Kunzel H., Bierner T., Pollmacher T., Pfister H., Nickel T., Sonntag A., Uhr M., Ising M., Holsboer F., Lucae S. Clinical characteristics and treatment outcome in a representative sample of depressed inpatients-findings from the Munich Antidepressant Response Signature (MARS) project. J. Psychiatr. Res. 2009, 43:215-229.
16. Houseman E.A., Accomando W.P., Koestler D.C., Christensen B.C., Marsit C.J., Nelson H.H., Wiencke J.K., Kelsey K.T. DNA methylation arrays as surrogate measures of cell mixture distribution. BMC Bioinform. 2012, 13:86.
17. Kubany E.S., Haynes S.N., Leisen M.B., Owens J.A., Kaplan A.S., Watson S.B., Burns K. Development and preliminary validation of a brief broad-spectrum measure of trauma exposure: the Traumatic Life Events Questionnaire. Psychol. Assess. 2000, 12:210-224.
18. Lambert W.M., Xu C.F., Neubert T.A., Chao M.V., Garabedian M.J., Jeanneteau F.D. Brain-derived neurotrophic factor signaling rewrites the glucocorticoid transcriptome via glucocorticoid receptor phosphorylation. Mol. Cell. Biol. 2013, 33:3700-3714.
19. Logue M.W., Baldwin C., Guffanti G., Melista E., Wolf E.J., Reardon A.F., Uddin M., Wildman D., Galea S., Koenen K.C., Miller M.W. A genome-wide association study of post-traumatic stress disorder identifies the retinoid-related orphan receptor alpha (RORA) gene as a significant risk locus. Mol. Psychiatry 2013, 18:937-942.
20. Luedi P.P., Dietrich F.S., Weidman J.R., Bosko J.M., Jirtle R.L., Hartemink A.J. Computational and experimental identification of novel human imprinted genes. Genome Res. 2007, 17:1723-1730.
21. Matsuoka Y., Nishi D., Noguchi H., Kim Y., Hashimoto K. Longitudinal changes in serum brain-derived neurotrophic factor in accident survivors with posttraumatic stress disorder. Neuropsychobiology 2013, 68:44-50.
22. Mehta D., Gonik M., Klengel T., Rex-Haffner M., Menke A., Rubel J., Mercer K.B., Putz B., Bradley B., Holsboer F., Ressler K.J., Muller-Myhsok B., Binder E.B. Using polymorphisms in FKBP5 to define biologically distinct subtypes of posttraumatic stress disorder: evidence from endocrine and gene expression studies. Arch. Gen. Psychiatry 2011, 68:901-910.
23. Mehta D., Klengel T., Conneely K.N., Smith A.K., Altmann A., Pace T.W., Rex-Haffner M., Loeschner A., Gonik M., Mercer K.B., Bradley B., Muller-Myhsok B., Ressler K.J., Binder E.B. Childhood maltreatment is associated with distinct genomic and epigenetic profiles in posttraumatic stress disorder. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:8302-8307.
24. Menke A., Arloth J., Putz B., Weber P., Klengel T., Mehta D., Gonik M., Rex-Haffner M., Rubel J., Uhr M., Lucae S., Deussing J.M., Muller-Myhsok B., Holsboer F., Binder E.B. Dexamethasone stimulated gene expression in peripheral blood is a sensitive marker for glucocorticoid receptor resistance in depressed patients. Neuropsychopharmacology 2012, 37:1455-1464.
25. Miller M.W., Wolf E.J., Reardon A., Greene A., Ofrat S., McInerney S. Personality and the latent structure of PTSD comorbidity. J. Anxiety Disord. 2012, 26:599-607.
26. Miller M.W., Sadeh N. Traumatic stress, oxidative stress and post-traumatic stress disorder: neurodegeneration and the accelerated-aging hypothesis. Mol Psychiatry 2014, 19:1156-1162.
27. Molendijk M.L., Spinhoven P., Polak M., Bus B.A., Penninx B.W., Elzinga B.M. Serum BDNF concentrations as peripheral manifestations of depression: evidence from a systematic review and meta-analyses on 179 associations (N=9484). Mol. Psychiatry 2014, 19:791-800.
28. Mootha V.K., Lindgren C.M., Eriksson K.F., Subramanian A., Sihag S., Lehar J., Puigserver P., Carlsson E., Ridderstrale M., Laurila E., Houstis N., Daly M.J., Patterson N., Mesirov J.P., Golub T.R., Tamayo P., Spiegelman B., Lander E.S., Hirschhorn J.N., Altshuler D., Groop L.C. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 2003, 34:267-273.
29. Nakamura H. Thioredoxin and its related molecules: update 2005. Antioxid. Redox Signal. 2005, 7:823-828.
30. Pepin M.C., Pothier F., Barden N. Impaired type II glucocorticoid-receptor function in mice bearing antisense RNA transgene. Nature 1992, 355:725-728.
31. Perroud N., Paoloni-Giacobino A., Prada P., Olie E., Salzmann A., Nicastro R., Guillaume S., Mouthon D., Stouder C., Dieben K., Huguelet P., Courtet P., Malafosse A. Increased methylation of glucocorticoid receptor gene (NR3C1) in adults with a history of childhood maltreatment: a link with the severity and type of trauma. Trans. Psychiatry 2011, 1:e59.
32. Ressler K.J., Mercer K.B., Bradley B., Jovanovic T., Mahan A., Kerley K., Norrholm S.D., Kilaru V., Smith A.K., Myers A.J., Ramirez M., Engel A., Hammack S.E., Toufexis D., Braas K.M., Binder E.B., May V. Post-traumatic stress disorder is associated with PACAP and the PAC1 receptor. Nature 2011, 470:492-497.
33. Sarapas C., Cai G., Bierer L.M., Golier J.A., Galea S., Ising M., Rein T., Schmeidler J., Muller-Myhsok B., Uhr M., Holsboer F., Buxbaum J.D., Yehuda R. Genetic markers for PTSD risk and resilience among survivors of the World Trade Center attacks. Dis. Markers 2011, 30:101-110.
34. Schmucker D., Chen B. Dscam and DSCAM: complex genes in simple animals, complex animals yet simple genes. Genes Dev. 2009, 23:147-156.
35. Segman R.H., Shefi N., Goltser-Dubner T., Friedman N., Kaminski N., Shalev A.Y. Peripheral blood mononuclear cell gene expression profiles identify emergent post-traumatic stress disorder among trauma survivors. Mol. Psychiatry 2005, 10:500-513. (425).
36. Skelton K., Ressler K.J., Norrholm S.D., Jovanovic T., Bradley-Davino B. PTSD and gene variants: new pathways and new thinking. Neuropharmacology 2012, 62:628-637.
37. Smyth G.K. Limma: linear models for microarray data. Bioinformatics and Computational Biology Solutions using R and Bioconductor 2005, 397-420. Springer, New York, NY. R. Gentleman, V. Carey, S. Dudoit, R. Irizarry, W. Huber (Eds.).
38. Subramanian A., Tamayo P., Mootha V.K., Mukherjee S., Ebert B.L., Gillette M.A., Paulovich A., Pomeroy S.L., Golub T.R., Lander E.S., Mesirov J.P. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:15545-15550.
39. Supek F., Supekova L., Mandiyan S., Pan Y.C., Nelson H., Nelson N. A novel accessory subunit for vacuolar H(+)-ATPase from chromaffin granules. J. Biol. Chem. 1994, 269:24102-24106.
40. Tronche F., Kellendonk C., Kretz O., Gass P., Anlag K., Orban P.C., Bock R., Klein R., Schutz G. Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat. Genet. 1999, 23:99-103.
41. Tycko B., Morison I.M. Physiological functions of imprinted genes. J. Cell. Physiol. 2002, 192:245-258.
42. Uddin M., Aiello A.E., Wildman D.E., Koenen K.C., Pawelec G., de Los Santos R., Goldmann E., Galea S. Epigenetic and immune function profiles associated with posttraumatic stress disorder. Proc Natl Acad Sci U S A 2010, 107:9470-9475.
43. Uddin M., Galea S., Chang S.C., Aiello A.E., Wildman D.E., de los Santos R., Koenen K.C. Gene expression and methylation signatures of MAN2C1 are associated with PTSD. Dis. Markers 2011, 30:111-121.
44. Willer C.J., Li Y., Abecasis G.R. METAL: fast and efficient meta-analysis of genomewide association scans. Bioinformatics 2010, 26:2190-2191.
45. Wolf E.J., Miller M.W., Harrington K.M., Reardon A. Personality-based latent classes of posttraumatic psychopathology: personality disorders and the internalizing/externalizing model. J. Abnorm. Psychol. 2012, 121:256-262.
46. Xie P., Kranzler H.R., Yang C., Zhao H., Farrer L.A., Gelernter J. Genome-wide association study identifies new susceptibility loci for posttraumatic stress disorder. Biol. Psychiatry 2013, 74:656-663.
47. Yamakawa K., Huot Y.K., Haendelt M.A., Hubert R., Chen X.N., Lyons G.E., Korenberg J.R. DSCAM: a novel member of the immunoglobulin superfamily maps in a Down syndrome region and is involved in the development of the nervous system. Hum. Mol. Genet. 1998, 7:227-237.
48. Yehuda R., Cai G., Golier J.A., Sarapas C., Galea S., Ising M., Rein T., Schmeidler J., Muller-Myhsok B., Holsboer F., Buxbaum J.D. Gene expression patterns associated with posttraumatic stress disorder following exposure to the World Trade Center attacks. Biol. Psychiatry 2009, 66:708-711.
49. Yehuda R., Levengood R.A., Schmeidler J., Wilson S., Guo L.S., Gerber D. Increased pituitary activation following metyrapone administration in post-traumatic stress disorder. Psychoneuroendocrinology 1996, 21:1-16.
50. Yehuda R., Lowy M.T., Southwick S.M., Shaffer D., Giller E.L. Lymphocyte glucocorticoid receptor number in posttraumatic stress disorder. Am. J. Psychiatry 1991, 148:499-504.
51. Yehuda R., Southwick S.M., Krystal J.H., Bremner D., Charney D.S., Mason J.W. Enhanced suppression of cortisol following dexamethasone administration in posttraumatic stress disorder. Am. J. Psychiatry 1993, 150:83-86.
52. Yehuda R., Teicher M.H., Trestman R.L., Levengood R.A., Siever L.J. Cortisol regulation in posttraumatic stress disorder and major depression: a chronobiological analysis. Biol. Psychiatry 1996, 40:79-88.
53. Zhang X.Y., Chen da C., Xiu M.H., Yang F.D., Tan Y.L., He S., Kosten T.A., Kosten T.R. Thioredoxin, a novel oxidative stress marker and cognitive performance in chronic and medicated schizophrenia versus healthy controls. Schizophr. Res. 2013, 143:301-306.
54. Zieker J., Zieker D., Jatzko A., Dietzsch J., Nieselt K., Schmitt A., Bertsch T., Fassbender K., Spanagel R., Northoff H., Gebicke-Haerter P.J. Differential gene expression in peripheral blood of patients suffering from post-traumatic stress disorder. Mol. Psychiatry 2007, 12:116-118.