Neural Mechanism of a Sex-Specific Risk Variant for Posttraumatic Stress Disorder in the Type i Receptor of the Pituitary Adenylate Cyclase Activating Polypeptide

Biological Psychiatry

Volumn 78, Issue 12, 2015, Pages 840-847

  Pohlack, Sebastian T ^a   Nees, Frauke ^a   Ruttorf, Michaela ^a   Cacciaglia, Raffaele ^a   Winkelmann, Tobias ^a   Schad, Lothar R ^a   Witt, Stephanie H ^a   Rietschel, Marcella ^a   Flor, Herta ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

ADCYAP1R1; Amygdala; Fear conditioning; Functional magnetic resonance imaging; Hippocampus; PTSD

Indexed keywords

HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE RECEPTOR 1;

ALLELE; AROUSAL; ARTICLE; BLOOD OXYGENATION; BRAIN REGION; CALIFORNIA VERBAL LEARNING TEST; CONDITIONING; CULTURE FAIR INTELLIGENCE TEST; ELECTRODERMAL RESPONSE; FEAR; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENE FREQUENCY; GENETIC ASSOCIATION; GENETIC CODE; GENETIC VARIABILITY; GENOTYPE; HIPPOCAMPUS; HUMAN; INTELLIGENCE TEST; MALE; NEUROPSYCHOLOGICAL TEST; NORMAL HUMAN; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; SELF REPORT; SINGLE NUCLEOTIDE POLYMORPHISM; STATE DEPENDENT LEARNING; STRUCTURED CLINICAL INTERVIEW FOR DSM DISORDERS; VERBAL BEHAVIOR; AMYGDALA; ASSOCIATION; BRAIN MAPPING; CONDITIONED REFLEX; GENETICS; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; SEX DIFFERENCE;

AMYGDALA; BRAIN MAPPING; CONDITIONING, CLASSICAL; CUES; FEAR; FEMALE; GALVANIC SKIN RESPONSE; GENOTYPE; HIPPOCAMPUS; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; NEUROPSYCHOLOGICAL TESTS; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE, TYPE I; SEX FACTORS; STRESS DISORDERS, POST-TRAUMATIC;

EID: 84947494620     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2014.12.018     Document Type: Article

References (44)

1. C.P. McLean, A. Asnaani, B.T. Litz, and S.G. Hofmann Gender differences in anxiety disorders: Prevalence, course of illness, comorbidity and burden of illness J Psychiatr Res 45 2011 102 1035
2. M.B. Stein, K.L. Jang, S. Taylor, P.A. Vernon, and W.J. Livesley Genetic and environmental influences on trauma exposure and posttraumatic stress disorder symptoms: A twin study Am J Psychiatry 159 2002 1675 1681
3. S.D. Norrholm, and K.J. Ressler Genetics of anxiety and trauma-related disorders Neuroscience 164 2009 272 287
4. K.J. Ressler, K.B. Mercer, B. Bradley, T. Jovanovic, A. Mahan, K. Kerley, and et al. Post-traumatic stress disorder is associated with PACAP and the PAC1 receptor Nature 470 2011 492 497
5. N. Stroth, Y. Holighaus, D. Ait-Ali, and L.E. Eiden PACAP: A master regulator of neuroendocrine stress circuits and the cellular stress response Ann N Y Acad Sci 1220 2011 49 59
6. Y. Zhong Mediation of PACAP-like neuropeptide transmission by coactivation of Ras/Raf and cAMP signal transduction pathways in Drosophila Nature 375 1995 588 592
7. M. Sauvage, P. Brabet, F. Holsboer, J. Bockaert, and T. Steckler Mild deficits in mice lacking pituitary adenylate cyclase-activating polypeptide receptor type 1 (PAC1) performing on memory tasks Brain Res Mol Brain Res 84 2000 79 89
8. C.R. Brewin The nature and significance of memory disturbance in posttraumatic stress disorder Annu Rev Clin Psychol 7 2011 203 227
9. D. Vaudry, A. Falluel-Morel, S. Bourgault, M. Basille, D. Burel, O. Wurtz, and et al. Pituitary adenylate cyclase-activating polypeptide and its receptors: 20 years after the discovery Pharmacol Rev 61 2009 283 357
10. D.T. Acheson, J.E. Gresack, and V.B. Risbrough Hippocampal dysfunction effects on context memory: Possible etiology for posttraumatic stress disorder Neuropharmacology 62 2012 674 685
11. J.C. Pruessner, K. Dedovic, M. Pruessner, C. Lord, C. Buss, L. Collins, and et al. Stress regulation in the central nervous system: evidence from structural and functional neuroimaging studies in human populations - 2008 Curt Richter Award Winner Psychoneuroendocrinology 35 2010 179 191
12. S.T. Pohlack, F. Nees, M. Ruttorf, L.R. Schad, and H. Flor Activation of the ventral striatum during aversive contextual conditioning in humans Biol Psychol 91 2012 74 80
13. C. Otto, Y. Kovalchuk, D.P. Wolfer, P. Gass, M. Martin, W. Zuschratter, and et al. Impairment of mossy fiber long-term potentiation and associative learning in pituitary adenylate cyclase activating polypeptide type I receptor-deficient mice J Neurosci 21 2001 5520 5527
14. S.P. Orr, L.J. Metzger, N.B. Lasko, M.L. Macklin, T. Peri, and R.K. Pitman De novo conditioning in trauma-exposed individuals with and without posttraumatic stress disorder J Abnorm Psychol 109 2000 290 298
15. R. Yehuda, and J. LeDoux Response variation following trauma: a translational neuroscience approach to understanding PTSD Neuron 56 2007 19 32
16. C. Sehlmeyer, S. Schoning, P. Zwitserlood, B. Pfleiderer, T. Kircher, V. Arolt, and et al. Human fear conditioning and extinction in neuroimaging: A systematic review PLoS One 4 2009 e5865
17. S. Kuhn, and J. Gallinat Gray matter correlates of posttraumatic stress disorder: A quantitative meta-analysis Biol Psychiatry 73 2013 70 74
18. J.M. Hettema, P. Annas, M.C. Neale, K.S. Kendler, and M. Fredrikson A twin study of the genetics of fear conditioning Arch Gen Psychiatry 60 2003 702 708
19. I.M. Marks Fears, Phobias, and Rituals: Panic, Anxiety, and Their Disorders 1987 Oxford University Press New York
20. C. Grillon, and C.A. Morgan 3rd Fear-potentiated startle conditioning to explicit and contextual cues in Gulf War veterans with posttraumatic stress disorder J Abnorm Psychol 108 1999 134 142
21. I. Indovina, T.W. Robbins, A.O. Nunez-Elizalde, B.D. Dunn, and S.J. Bishop Fear-conditioning mechanisms associated with trait vulnerability to anxiety in humans Neuron 69 2011 563 571
22. A.L. Mahan, and K.J. Ressler Fear conditioning, synaptic plasticity and the amygdala: Implications for posttraumatic stress disorder Trends Neurosci 35 2012 24 35
23. R. Cacciaglia, F. Nees, S.T. Pohlack, M. Ruttorf, T. Winkelmann, S.H. Witt, and et al. A risk variant for alcoholism in the NMDA receptor affects amygdala activity during fear conditioning in humans Biol Psychol 94 2013 74 81
24. S.T. Pohlack, F. Nees, M. Ruttorf, S.H. Witt, V. Nieratschker, M. Rietschel, and et al. Risk variant for schizophrenia in the neurogranin gene impacts on hippocampus activation during contextual fear conditioning Mol Psychiatry 16 2011 1072 1073
25. H.-U. Wittchen, U. Wunderlich, S. Gruschwitz, and M. Zaudig SKID I. Strukturiertes Klinisches Interview für DSM-IV 1997 Hogrefe Göttingen
26. R.H. Weiss Grundintelligenztest Skala 2. CFT-20 (Culture Fair Intelligence Test) 4th ed. 1998 Hogrefe Göttingen
27. J. Ilmberger Deutsche Version des California Verbal Learning Test 1988 LMU Munich
28. L. Laux, P. Glanzmann, P. Schaffner, and C.D. Spielberger Das State-Trait-Angstinventar (STAI) 1981 Beltz-Testgesellschaft Weinheim
29. C. Grillon, J.M. Baas, B. Cornwell, and L. Johnson Context conditioning and behavioral avoidance in a virtual reality environment: Effect of predictability Biol Psychiatry 60 2006 752 759
30. M.E. Bouton Context, Ambiguity, and Classical Conditioning Current Directions in Psychological Science 3 1994 49 53
31. M.M. Bradley, and P.J. Lang Measuring emotion: The Self-Assessment Manikin and the Semantic Differential J Behav Ther Exp Psychiatry 25 1994 49 59
32. N. Tzourio-Mazoyer, B. Landeau, D. Papathanassiou, F. Crivello, O. Etard, N. Delcroix, and et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain Neuroimage 15 2002 273 289
33. E.J. Rose, and G. Donohoe Brain vs behavior: An effect size comparison of neuroimaging and cognitive studies of genetic risk for schizophrenia Schizophr Bull 39 2013 518 526
34. S. Lang, A. Kroll, S.J. Lipinski, M. Wessa, S. Ridder, C. Christmann, and et al. Context conditioning and extinction in humans: Differential contribution of the hippocampus, amygdala and prefrontal cortex Eur J Neurosci 29 2009 823 832
35. E.M. Glover, J.E. Phifer, D.F. Crain, S.D. Norrholm, M. Davis, B. Bradley, and et al. Tools for translational neuroscience: PTSD is associated with heightened fear responses using acoustic startle but not skin conductance measures Depress Anxiety 28 2011 1058 1066
36. L.M. Almli, K.B. Mercer, K. Kerley, H. Feng, B. Bradley, K.N. Conneely, and et al. ADCYAP1R1 genotype associates with post-traumatic stress symptoms in highly traumatized African-American females Am J Med Genet B Neuropsychiatr Genet 162B 2013 262 272
37. T. Jovanovic, S.D. Norrholm, J. Davis, K.B. Mercer, L. Almli, A. Nelson, and et al. PAC1 receptor (ADCYAP1R1) genotype is associated with dark-enhanced startle in children Mol Psychiatry 18 2013 742 743
38. S.C. Chang, P. Xie, R.F. Anton, I. De Vivo, L.A. Farrer, H.R. Kranzler, and et al. No association between ADCYAP1R1 and post-traumatic stress disorder in two independent samples Mol Psychiatry 17 2012 239 241
39. B.G. Dias, and K.J. Ressler PACAP and the PAC1 receptor in post-traumatic stress disorder Neuropsychopharmacology 38 2013 245 246
40. M. Uddin, S.C. Chang, C. Zhang, K. Ressler, K.B. Mercer, S. Galea, and et al. Adcyap1r1 genotype, posttraumatic stress disorder, and depression among women exposed to childhood maltreatment Depress Anxiety 30 2013 251 258
41. J.S. Stevens, L.M. Almli, N. Fani, D.A. Gutman, B. Bradley, S.D. Norrholm, and et al. PACAP receptor gene polymorphism impacts fear responses in the amygdala and hippocampus Proc Natl Acad Sci U S A 111 2014 3158 3163
42. L. Wang, C. Cao, R. Wang, Y. Qing, J. Zhang, and X.Y. Zhang PAC1 receptor (ADCYAP1R1) genotype is associated with PTSDs emotional numbing symptoms in Chinese earthquake survivors J Affect Disord 150 2013 156 159
43. C.J. Merz, K. Tabbert, J. Schweckendiek, T. Klucken, D. Vaitl, R. Stark, and et al. Neuronal correlates of extinction learning are modulated by sex hormones Soc Cogn Affect Neurosci 7 2012 819 830
44. D. Wagner, M. Heinrichs, and U. Ehlert Prevalence of symptoms of posttraumatic stress disorder in German professional firefighters Am J Psychiatry 155 1998 1727 1732