Stress-related disorders, pituitary adenylate cyclase-activating peptide (PACAP)ergic system, and sex differences

Dialogues in Clinical Neuroscience

Volumn 18, Issue 4, 2016, Pages 403-413

  Ramikie, Teniel S ^a   Ressler, Kerry J ^a  

^a MCLEAN HOSPITAL   (United States)

Author keywords

ADCYAP1; ADCYAP1R1; Amygdala; Anxiety; Estrogen; Fear; Fear conditioning; Genetic; PACAP; PTSD; Sex difference; Threat

Indexed keywords

HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE RECEPTOR 1; MESSENGER RNA; ADCYAP1 PROTEIN, HUMAN; BIOLOGICAL MARKER; ESTROGEN;

ARTICLE; ESTROGEN RESPONSIVE ELEMENT; ESTROGEN THERAPY; FEAR; GENE CONTROL; GENETIC RISK; GENETIC VARIABILITY; HUMAN; NEUROIMAGING; NONHUMAN; POSTTRAUMATIC STRESS DISORDER; PSYCHOTRAUMA; RISK FACTOR; SEX DIFFERENCE; SINGLE NUCLEOTIDE POLYMORPHISM; STRESS; ANIMAL; BLOOD; COPING BEHAVIOR; FEMALE; GENETIC POLYMORPHISM; GENETICS; GENOTYPE ENVIRONMENT INTERACTION; MALE; MEMORY; MENTAL STRESS; PATHOPHYSIOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SEXUAL DEVELOPMENT;

ADAPTATION, PSYCHOLOGICAL; ANIMALS; BIOMARKERS; ESTROGENS; FEAR; FEMALE; GENE-ENVIRONMENT INTERACTION; HUMANS; MALE; MEMORY; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; POLYMORPHISM, GENETIC; RECEPTORS, PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE, TYPE I; RISK FACTORS; SEX CHARACTERISTICS; SEX FACTORS; STRESS DISORDERS, POST-TRAUMATIC; STRESS, PHYSIOLOGICAL; STRESS, PSYCHOLOGICAL;

EID: 85012970325     PISSN: 12948322     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (100)

1. Bangasser DA, Valentino RJ. Sex differences in stress-related psychiatric disorders: neurobiological perspectives. Front Neuroendocrinol. 2014;35(3):303-319.
2. Breslau N, Davis GC, Peterson EL, Schultz L. Psychiatric sequelae of posttraumatic stress disorder in women. Arch Gen Psychiatry. 1997;54(1):81-87.
3. Alim TN, Graves E, Mellman TA, et al. Trauma exposure, posttraumatic stress disorder and depression in an African-American primary care population. J Natl Med Assoc. 2006;98(10):1630-1636.
4. Resnick HS, Kilpatrick DG, Dansky BS, Saunders BE, Best CL. Prevalence of civilian trauma and posttraumatic stress disorder in a representative national sample of women. J Consult Clin Psychol. 1993;61(6):984-991.
5. Pynoos RS, Frederick C, Nader K, et al. Life threat and posttraumatic stress in school-age children. Arch Gen Psychiatry. 1987;44(12):1057-1063.
6. Sartor CE, McCutcheon VV, Pommer NE, et al. Common genetic and environmental contributions to post-traumatic stress disorder and alcohol dependence in young women. Psychol Med. 2011;41(7):1497-1505.
7. Stein MB, Jang KL, Taylor S, Vernon PA, Livesley WJ. Genetic and environmental influences on trauma exposure and posttraumatic stress disorder symptoms: a twin study. Am J Psychiatry. 2002;159(10):1675-1681.
8. Dias BG, Ressler KJ. PACAP and the PAC1 receptor in post-traumatic stress disorder. Neuropsychopharmacology. 2013;38(1):245-246.
9. Vaudry D, Falluel-Morel A, Bourgault S, et al. Pituitary adenylate cyclase-activating polypeptide and its receptors: 20 years after the discovery. Pharmacol Rev. 2009;61(3):283-357.
10. Miyata A, Jiang L, Dahl RD, et al. Isolation of a neuropeptide corresponding to the N-terminal 27 residues of the pituitary adenylate cyclase activating polypeptide with 38 residues (PACAP38). Biochem Biophys Res Commun. 1990;170(2):643-648.
11. Arimura A, Somogyvari-Vigh A, Miyata A, Mizuno K, Coy DH, Kitada C. Tissue distribution of PACAP as determined by RIA: highly abundant in the rat brain and testes. Endocrinology. 1991;129(5):2787-2789.
12. Joo KM, Chung YH, Kim MK, et al. Distribution of vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide receptors (VPAC1, VPAC2, and PAC1 receptor) in the rat brain. J Comp Neurol. 2004;476(4):388-413.
13. Shivers BD, Gorcs TJ, Gottschall PE, Arimura A. Two high affinity binding sites for pituitary adenylate cyclase-activating polypeptide have different tissue distributions. Endocrinology. 1991;128(6):3055-3065.
14. Spengler D, Waeber C, Pantaloni C, et al. Differential signal transduction by five splice variants of the PACAP receptor. Nature. 1993;365(6442):170-175.
15. Ajpru S, McArthur AJ, Piggins HD, Sugden D. Identification of PAC1 receptor isoform mRNAs by real-time PCR in rat suprachiasmatic nucleus. Brain Res Mol Brain Res. 2002;105(1-2):29-37.
16. Pilzer I, Gozes I. VIP provides cellular protection through a specific splice variant of the PACAP receptor: a new neuroprotection target. Peptides. 2006;27(11):2867-2876.
17. Kondo T, Tominaga T, Ichikawa M, Iijima T. Differential alteration of hippocampal synaptic strength induced by pituitary adenylate cyclase activating polypeptide-38 (PACAP-38). Neurosci Lett. 1997;221(2-3):189-192.
18. Tye KM, Deisseroth K. Optogenetic investigation of neural circuits underlying brain disease in animal models. Nat Rev Neurosci. 2012;13(4):251-266.
19. Tye KM, Prakash R, Kim SY, et al. Amygdala circuitry mediating reversible and bidirectional control of anxiety. Nature. 2011;471(7338):358-362.
20. Ressler KJ, Mercer KB, Bradley B, et al. Post-traumatic stress disorder is associated with PACAP and the PAC1 receptor. Nature. 2011;470(7335):492-497.
21. Driscoll MD, Sathya G, Muyan M, Klinge CM, Hilf R, Bambara RA. Sequence requirements for estrogen receptor binding to estrogen response elements. J Biol Chem. 1998;273(45):29321-29330.
22. Heldring N, Pike A, Andersson S, et al. Estrogen receptors: how do they signal and what are their targets. Physiol Rev. 2007;87(3):905-931.
23. Klinge CM. Estrogen receptor interaction with estrogen response elements. Nucleic Acids Res. 2001;29(14):2905-2919.
24. Moore JP Jr, Burger LL, Dalkin AC, Winters SJ. Pituitary adenylate cyclase activating polypeptide messenger RNA in the paraventricular nucleus and anterior pituitary during the rat estrous cycle. Biol Reprod. 2005;73(3):491-499.
25. Fata JE, Chaudhary V, Khokha R. Cellular turnover in the mammary gland is correlated with systemic levels of progesterone and not 17β-estradiol during the estrous cycle. Biol Reproduction. 2001;65(3):680-688.
26. Hammack SE, May V. Pituitary adenylate cyclase activating polypeptide in stress-related disorders: data convergence from animal and human studies. Biol Psychiatry. 2015;78(3):167-177.
27. Missig G, Roman CW, Vizzard MA, Braas KM, Hammack SE, May V. Parabrachial nucleus (PBn) pituitary adenylate cyclase activating polypeptide (PACAP) signaling in the amygdala: implication for the sensory and behavioral effects of pain. Neuropharmacology. 2014;86:38-48.
28. Condro MC, Matynia A, Foster NN, et al. High-resolution characterization of a PACAP-EGFP transgenic mouse model for mapping PACAPexpressing neurons. J Comp Neurol. 2016 May 14. Epub ahead of print. doi:10.1002/cne.24035.
29. Goosens KA. Hippocampal regulation of aversive memories. Curr Opin Neurobiol. 2011;21(3):460-466.
30. Hammack SE, Cheung J, Rhodes KM, et al. Chronic stress increases pituitary adenylate cyclase-activating peptide (PACAP) and brain-derived neurotrophic factor (BDNF) mRNA expression in the bed nucleus of the stria terminalis (BNST): roles for PACAP in anxiety-like behavior. Psychoneuroendocrinology. 2009;34(6):833-843.
31. Tanida M, Shintani N, Morita Y, et al. Regulation of autonomic nerve activities by central pituitary adenylate cyclase-activating polypeptide. Regul Pept. 2010;161(1-3):73-80.
32. Agarwal A, Halvorson LM, Legradi G. Pituitary adenylate cyclaseactivating polypeptide (PACAP) mimics neuroendocrine and behavioral manifestations of stress: evidence for PKA-mediated expression of the corticotropin-releasing hormone (CRH) gene. Brain Res Mol Brain Res. 2005;138(1):45-57.
33. Dore R, Iemolo A, Smith KL, Wang X, Cottone P, Sabino V. CRF mediates the anxiogenic and anti-rewarding, but not the anorectic effects of PACAP. Neuropsychopharmacology. 2013;38(11):2160-2169.
34. Stroth N, Liu Y, Aguilera G, Eiden LE. Pituitary adenylate cyclase-activating polypeptide controls stimulus-transcription coupling in the hypothalamic-pituitary-adrenal axis to mediate sustained hormone secretion during stress. J Neuroendocrinol. 2011;23(10):944-955.
35. Roman CW, Lezak KR, Hartsock MJ, et al. PAC1 receptor antagonism in the bed nucleus of the stria terminalis (BNST) attenuates the endocrine and behavioral consequences of chronic stress. Psychoneuroendocrinology. 2014;47:151-165.
36. Lehmann ML, Mustafa T, Eiden AM, Herkenham M, Eiden LE. PACAPdeficient mice show attenuated corticosterone secretion and fail to develop depressive behavior during chronic social defeat stress. Psychoneuroendocrinology. 2013;38(5):702-715.
37. Mustafa T, Jiang SZ, Eiden AM, Weihe E, Thistlethwaite I, Eiden LE. Impact of PACAP and PAC1 receptor deficiency on the neurochemical and behavioral effects of acute and chronic restraint stress in male C57BL/6 mice. Stress. 2015;18(4):408-418.
38. Lezak KR, Roelke E, Harris OM, et al. Pituitary adenylate cyclase-activating polypeptide (PACAP) in the bed nucleus of the stria terminalis (BNST) increases corticosterone in male and female rats. Psychoneuroendocrinology. 2014;45:11-20.
39. Sabatinelli D, Fortune EE, Li Q, et al. Emotional perception: meta-analyses of face and natural scene processing. Neuroimage. 2011;54(3):2524-2533.
40. Phan KL, Wager TD, Taylor SF, Liberzon I. Functional neuroimaging studies of human emotions. CNS Spectr. 2004;9(4):258-266.
41. Phan KL, Taylor SF, Welsh RC, Ho SH, Britton JC, Liberzon I. Neural correlates of individual ratings of emotional salience: a trial-related fMRI study. Neuroimage. 2004;21(2):768-780.
42. Admon R, Lubin G, Rosenblatt JD, et al. Imbalanced neural responsivity to risk and reward indicates stress vulnerability in humans. Cereb Cortex. 2013;23(1):28-35.
43. Shvil E, Sullivan GM, Schafer S, et al. Sex differences in extinction recall in posttraumatic stress disorder: a pilot fMRI study. Neurobiol Learn Mem. 2014;113:101-108.
44. Morey LC, Benson KT. An investigation of adherence to diagnostic criteria, revisited: clinical diagnosis of the DSM-IV/DSM-5 section II personality disorders. J Pers Disord. 2016;30(1):130-144.
45. Morey M, Fernandez-Marmiesse A, Castineiras D, Fraga JM, Couce ML, Cocho JA. Corrigendum to "A glimpse into past, present, and future DNA sequencing" [Mol. Genet. Metab. 110 (2013) 3-24]. Mol Genet Metab. 2015;114(3):484.
46. Lissek S, Powers AS, McClure EB, et al. Classical fear conditioning in the anxiety disorders: a meta-analysis. Behav Res Ther. 2005;43(11):1391-1424.
47. Jovanovic T, Ely T, Fani N, et al. Reduced neural activation during an inhibition task is associated with impaired fear inhibition in a traumatized civilian sample. Cortex. 2013;49(7):1884-1891.
48. Jovanovic T, Norrholm SD, Blanding NQ, et al. Impaired fear inhibition is a biomarker of PTSD but not depression. Depress Anxiety. 2010;27(3):244-251.
49. Jovanovic T, Norrholm SD, Fennell JE, et al. Posttraumatic stress disorder may be associated with impaired fear inhibition: relation to symptom severity. Psychiatry Res. 2009;167(1-2):151-160.
50. Norrholm SD, Jovanovic T, Olin IW, et al. Fear extinction in traumatized civilians with posttraumatic stress disorder: relation to symptom severity. Biol Psychiatry. 2011;69(6):556-563.
51. Pitman RK, Rasmusson AM, Koenen KC, et al. Biological studies of post-traumatic stress disorder. Nat Rev Neurosci. 2012;13(11):769-787.
52. Graham BM, Milad MR. Blockade of estrogen by hormonal contraceptives impairs fear extinction in female rats and women. Biol Psychiatry. 2013;73(4):371-378.
53. Glover EM, Jovanovic T, Mercer KB, et al. Estrogen levels are associated with extinction deficits in women with posttraumatic stress disorder. Biol Psychiatry. 2012;72(1):19-24.
54. Rasmusson AM, Charney DS. Animal models of relevance to PTSD. Ann N Y Acad Sci. 1997;821:332-351.
55. Otto C, Kovalchuk Y, Wolfer DP, 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. 2001;21(15):5520-5527.
56. Cho JH, Deisseroth K, Bolshakov VY. Synaptic encoding of fear extinction in mPFC-amygdala circuits. Neuron. 2013;80(6):1491-1507.
57. Schmidt SD, Myskiw JC, Furini CR, Schmidt BE, Cavalcante LE, Izquierdo I. PACAP modulates the consolidation and extinction of the contextual fear conditioning through NMDA receptors. Neurobiol Learn Mem. 2015;118:120-124.
58. Meewisse ML, Reitsma JB, de Vries GJ, Gersons BP, Olff M. Cortisol and post-traumatic stress disorder in adults: systematic review and metaanalysis. Br J Psychiatry. 2007;191:387-392.
59. Stein MB, Jang KL, Livesley WJ. Heritability of social anxiety-related concerns and personality characteristics: a twin study. J Nerv Ment Dis. 2002;190(4):219-224.
60. Norrholm SD, Ressler KJ. Genetics of anxiety and trauma-related disorders. Neuroscience. 2009;164(1):272-287.
61. Hashimoto R, Hashimoto H, Shintani N, et al. Pituitary adenylate cyclase-activating polypeptide is associated with schizophrenia. Mol Psychiatry. 2007;12(11):1026-1032.
62. Aragam N, Wang KS, Pan Y. Genome-wide association analysis of gender differences in major depressive disorder in the Netherlands NESDA and NTR population-based samples. J Affect Disord. 2011;133(3):516-521.
63. Jovanovic T, Norrholm SD, Blanding NQ, et al. Fear potentiation is associated with hypothalamic-pituitary-adrenal axis function in PTSD. Psychoneuroendocrinology. 2010;35(6):846-857.
64. Kamkwalala A, Norrholm SD, Poole JM, et al. Dark-enhanced startle responses and heart rate variability in a traumatized civilian sample: putative sex-specific correlates of posttraumatic stress disorder. Psychosom Med. 2012;74(2):153-159.
65. Klinge CM. Estrogen receptor interaction with co-activators and corepressors. Steroids. 2000;65(5):227-251.
66. Jovanovic T, Norrholm SD, Davis J, et al. PAC1 receptor (ADCYAP1R1) genotype is associated with dark-enhanced startle in children. Mol Psychiatry. 2013;18(7):742-743.
67. Graham BM, Milad MR. Inhibition of estradiol synthesis impairs fear extinction in male rats. Learn Mem. 2014;21(7):347-350.
68. Handa RJ, Nunley KM, Lorens SA, Louie JP, McGivern RF, Bollnow MR. Androgen regulation of adrenocorticotropin and corticosterone secretion in the male rat following novelty and foot shock stressors. Physiol Behav. 1994;55(1):117-124.
69. McDermott CM, Liu D, Schrader LA. Role of gonadal hormones in anxiety and fear memory formation and inhibition in male mice. Physiol Behav. 2012;105(5):1168-1174.
70. Hodosy J, Zelmanova D, Majzunova M, et al. The anxiolytic effect of testosterone in the rat is mediated via the androgen receptor. Pharmacol Biochem Behav. 2012;102(2):191-195.
71. Cahill L, Uncapher M, Kilpatrick L, Alkire MT, Turner J. Sex-related hemispheric lateralization of amygdala function in emotionally influenced memory: an fMRI investigation. Learn Mem. 2004;11(3):261-266.
72. Zeidan MA, Igoe SA, Linnman C, et al. Estradiol modulates medial prefrontal cortex and amygdala activity during fear extinction in women and female rats. Biol Psychiatry. 2011;70(10):920-927.
73. Goldstein JM, Jerram M, Abbs B, Whitfield-Gabrieli S, Makris N. Sex differences in stress response circuitry activation dependent on female hormonal cycle. J Neurosci. 2010;30(2):431-438.
74. Breslau N, Davis GC, Andreski P, Peterson EL, Schultz LR. Sex differences in posttraumatic stress disorder. Arch Gen Psychiatry. 1997;54(11):1044-1048.
75. Seeman MV. Psychopathology in women and men: focus on female hormones. Am J Psychiatry. 1997;154(12):1641-1647.
76. Stevens JS, Almli LM, Fani N, et al. PACAP receptor gene polymorphism impacts fear responses in the amygdala and hippocampus. Proc Natl Acad Sci U S A. 2014;111(8):3158-3163.
77. Dannlowski U, Kugel H, Huber F, et al. Childhood maltreatment is associated with an automatic negative emotion processing bias in the amygdala. Hum Brain Mapp. 2013;34(11):2899-2909.
78. Cho JH, Zushida K, Shumyatsky GP, Carlezon WA Jr, Meloni EG, Bolshakov VY. Pituitary adenylate cyclase-activating polypeptide induces postsynaptically expressed potentiation in the intra-amygdala circuit. J Neurosci. 2012;32(41):14165-14177.
79. Yang K, Lei G, Jackson MF, Macdonald JF. The involvement of PACAP/VIP system in the synaptic transmission in the hippocampus. J Mol Neurosci. 2010;42(3):319-326.
80. Lindholm D, Skoglosa Y, Takei N. Developmental regulation of pituitary adenylate cyclase activating polypeptide (PACAP) and its receptor 1 in rat brain: function of PACAP as a neurotrophic factor. Ann N Y Acad Sci. 1998;865:189-196.
81. Stevens JS, Jovanovic T, Fani N, et al. Disrupted amygdala-prefrontal functional connectivity in civilian women with posttraumatic stress disorder. J Psychiatr Res. 2013;47(10):1469-1478.
82. Rauch SL, Whalen PJ, Shin LM, et al. Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder: a functional MRI study. Biol Psychiatry. 2000;47(9):769-776.
83. Pohlack ST, Nees F, Ruttorf M, et al. Neural mechanism of a sex-specific risk variant for posttraumatic stress disorder in the type i receptor of the pituitary adenylate cyclase activating polypeptide. Biol Psychiatry. 2015;78(12):840-847.
84. Panthong A, Kanjanapothi D, Taesotikul T, Phankummoon A, Panthong K, Reutrakul V. Anti-inflammatory activity of methanolic extracts from Ventilago harmandiana Pierre. J Ethnopharmacol. 2004;91(2-3):237-242.
85. Brewin CR. The nature and significance of memory disturbance in posttraumatic stress disorder. Annu Rev Clin Psychol. 2011;7:203-227.
86. Lyons MJ, Goldberg J, Eisen SA, et al. Do genes influence exposure to trauma? A twin study of combat. Am J Med Genet. 1993;48(1):22-27.
87. Herman JP. Neural control of chronic stress adaptation. Front Behav Neurosci. 2013;7:61.
88. Ohman A, Mineka S. Fears, phobias, and preparedness: toward an evolved module of fear and fear learning. Psychol Rev. 2001;108(3):483-522.
89. Joels M, Baram TZ. The neuro-symphony of stress. Nat Rev Neurosci. 2009;10(6):459-466.
90. Ursano RJ, Fullerton CS, Epstein RS, et al. Acute and chronic posttraumatic stress disorder in motor vehicle accident victims. Am J Psychiatry. 1999;156(4):589-595.
91. Walker JL, Carey PD, Mohr N, Stein DJ, Seedat S. Gender differences in the prevalence of childhood sexual abuse and in the development of pediatric PTSD. Arch Womens Ment Health. 2004;7(2):111-121.
92. Olff M, Langeland W, Draijer N, Gersons BP. Gender differences in posttraumatic stress disorder. Psychol Bull. 2007;133(2):183-204.
93. Marmar CR, Weiss DS, Schlenger WE, et al. Peritraumatic dissociation and posttraumatic stress in male Vietnam theater veterans. Am J Psychiatry. 1994;151(6):902-907.
94. Tsukiyama N, Saida Y, Kakuda M, et al. PACAP centrally mediates emotional stress-induced corticosterone responses in mice. Stress. 2011;14(4):368-375.
95. Hatanaka M, Tanida M, Shintani N, et al. Lack of light-induced elevation of renal sympathetic nerve activity and plasma corticosterone levels in PACAP-deficient mice. Neurosci Lett. 2008;444(2):153-156.
96. Young EA, Breslau N. Saliva cortisol in posttraumatic stress disorder: a community epidemiologic study. Biol Psychiatry. 2004;56(3):205-209.
97. Yehuda R, Southwick SM, Krystal JH, Bremner D, Charney DS, Mason JW. Enhanced suppression of cortisol following dexamethasone administration in posttraumatic stress disorder. Am J Psychiatry. 1993;150(1):83-86.
98. Brewin CR, Andrews B, Valentine JD. Meta-analysis of risk factors for posttraumatic stress disorder in trauma-exposed adults. J Consult Clinical Psychol. 2000;68(5):748-766.
99. Ozer EJ, Best SR, Lipsey TL, Weiss DS. Predictors of posttraumatic stress disorder and symptoms in adults: a meta-analysis. Psychol Bull. 2003;129(1):52-73.
100. Uddin M, Chang SC, Zhang C, et al. ADCYAP1R1 genotype, posttraumatic stress disorder, and depression among women exposed to childhood maltreatment. Depress Anxiety. 2013;30(3):251-258.