Forebrain-specific CRF overproduction during development is sufficient to induce enduring anxiety and startle abnormalities in adult mice

Neuropsychopharmacology

Volumn 39, Issue 6, 2014, Pages 1409-1419

  Toth, Mate ^a,b   Gresack, Jodi E ^a,c   Bangasser, Debra A ^d,e   Plona, Zach ^d   Valentino, Rita J ^d   Flandreau, Elizabeth I ^a   Mansuy, Isabelle M ^f   Merlo Pich, Emilio ^g   Geyer, Mark A ^a,b   Risbrough, Victoria B ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

^d CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^e TEMPLE UNIVERSITY   (United States)

^f University of Zurich Brain Research Institute   (Switzerland)

^g Novartis Pharma   (Switzerland)

Author keywords

anxiety; CRF overexpression; development; sex differences; startle

Indexed keywords

CORTICOSTERONE; CORTICOTROPIN RELEASING FACTOR;

ACOUSTIC REFLEX; ACOUSTIC STARTLE REFLEX; ADULTHOOD; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; AVOIDANCE BEHAVIOR; BASAL GANGLION; BEHAVIOR; BODY WEIGHT; BRAIN CORTEX; BRAIN DEVELOPMENT; CONDITIONING; CONTROLLED STUDY; CORPUS STRIATUM; EARLY LIFE STRESS; EXPLORATORY BEHAVIOR; FEAR; FEMALE; FOREBRAIN; HABITUATION; HIPPOCAMPUS; HORMONE RELEASE; HYPOTHALAMUS; LEARNING; LIFESPAN; LIGHT DARK CYCLE; LOCOMOTION; MALE; MESENCEPHALON; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PHENOTYPE; PONS; POSTNATAL DEVELOPMENT; PREPULSE INHIBITION; PRIORITY JOURNAL; SEPTUM PELLUCIDUM; SEX DIFFERENCE; SIGNAL TRANSDUCTION; STARTLE REFLEX; ANIMAL; C57BL MOUSE; DISEASE MODEL; GENETICS; GROWTH, DEVELOPMENT AND AGING; INHIBITION (PSYCHOLOGY); MENTAL STRESS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; SENSORY GATING; TRANSGENIC MOUSE;

ANIMALS; ANXIETY; AVOIDANCE LEARNING; CONDITIONING (PSYCHOLOGY); CORTICOTROPIN-RELEASING HORMONE; DISEASE MODELS, ANIMAL; EXPLORATORY BEHAVIOR; FEAR; FEMALE; HABITUATION, PSYCHOPHYSIOLOGIC; INHIBITION (PSYCHOLOGY); MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PROSENCEPHALON; REFLEX, STARTLE; SENSORY GATING; SEX FACTORS; STRESS, PSYCHOLOGICAL;

EID: 84900824696     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2013.336     Document Type: Article

References (49)

1. Adamec R, Fougere D, Risbrough V (2010). CRF receptor blockade prevents initiation and consolidation of stress effects on affect in the predator stress model of PTSD. Int J Neuropsychopharmacol 13: 747-757.
2. Avishai-Eliner S, Yi SJ, Baram TZ (1996). Developmental profile of messenger RNA for the corticotropin-releasing hormone receptor in the rat limbic system. Brain Res Dev Brain Res 91: 159-163. (Pubitemid 26069866)
3. Baker DG, West SA, Nicholson WE, Ekhator NN, Kasckow JW, Hill KK et al (1999). Serial CSF corticotropin-releasing hormone levels and adrenocortical activity in combat veterans with posttraumatic stress disorder. Am J Psychiatry 156: 585-588. (Pubitemid 29162980)
4. Baldwin HA, Rassnick S, Rivier J, Koob GF, Britton KT (1991). CRF antagonist reverses the "anxiogenic" response to ethanol withdrawal in the rat. Psychopharmacology 103: 227-232.
5. Bangasser DA, Curtis A, Reyes BA, Bethea TT, Parastatidis I, Ischiropoulos H et al (2010). Sex differences in corticotropinreleasing factor receptor signaling and trafficking: potential role in female vulnerability to stress-related psychopathology. Mol Psychiatry 15: 877, 896-904.
6. Bangasser DA, Reyes BA, Piel D, Garachh V, Zhang XY, Plona ZM et al (2013). Increased vulnerability of the brain norepinephrine system of females to corticotropin-releasing factor overexpression. Mol Psychiatry 18: 166-173.
7. Bradley RG, Binder EB, Epstein MP, Tang Y, Nair HP, Liu W et al (2008). Influence of child abuse on adult depression: moderation by the corticotropin-releasing hormone receptor gene. Arch Gen Psychiatry 65: 190-200. (Pubitemid 351214318)
8. Braff DL, Geyer MA, Swerdlow NR (2001). Human studies of prepulse inhibition of startle: normal subjects, patient groups, and pharmacological studies. Psychopharmacology 156: 234-258. (Pubitemid 32705488)
9. Bremner JD, Licinio J, Darnell A, Krystal JH, Owens MJ, Southwick SM et al (1997). Elevated CSF corticotropin-releasing factor concentrations in posttraumatic stress disorder. Am J Psychiatry 154: 624-629. (Pubitemid 27197594)
10. Carpenter LL, Tyrka AR, McDougle CJ, Malison RT, Owens MJ, Nemeroff CB et al (2004). Cerebrospinal fluid corticotropinreleasing factor and perceived early-life stress in depressed patients and healthy control subjects. Neuropsychopharmacology 29: 777-784. (Pubitemid 38402485)
11. Coplan JD, Andrews MW, Rosenblum LA, Owens MJ, Friedman S, Gorman JM et al (1996). Persistent elevations of cerebrospinal fluid concentrations of corticotropin-releasing factor in adult nonhuman primates exposed to early-life stressors: implications for the pathophysiology of mood and anxiety disorders. Proc Natl Acad Sci USA 93: 1619-1623.
12. Curtis AL, Bethea T, Valentino RJ (2006). Sexually dimorphic responses of the brain norepinephrine system to stress and corticotropin-releasing factor. Neuropsychopharmacology 31: 544-554. (Pubitemid 43276970)
13. Flandreau EI, Ressler KJ, Owens MJ, Nemeroff CB (2012). Chronic overexpression of corticotropin-releasing factor from the central amygdala produces HPA axis hyperactivity and behavioral anxiety associated with gene-expression changes in the hippocampus and paraventricular nucleus of the hypothalamus. Psychoneuroendocrinology 37: 27-38.
14. Gresack JE, Risbrough VB, Scott CN, Coste S, Stenzel-Poore M, Geyer MA et al (2010). Isolation rearing-induced deficits in contextual fear learning do not require CRF(2) receptors. Behav Brain Res 209: 80-84.
15. Groenink L, Dirks A, Verdouw PM, de Graaff M, Peeters BW, Millan MJ et al (2008). CRF1 not glucocorticoid receptors mediate prepulse inhibition deficits in mice overexpressing CRF. Biol Psychiatry 63: 360-368. (Pubitemid 351146650)
16. Groenink L, Pattij T, De Jongh R, Van der Gugten J, Oosting RS, Dirks A et al (2003). 5-HT1A receptor knockout mice and mice overexpressing corticotropin-releasing hormone in models of anxiety. Eur J Pharmacol 463: 185-197. (Pubitemid 36205080)
17. Heim C, Nemeroff CB (2001). The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol Psychiatry 49: 1023-1039. (Pubitemid 32595461)
18. Hubbard DT, Nakashima BR, Lee I, Takahashi LK (2007). Activation of basolateral amygdala corticotropin-releasing factor 1 receptors modulates the consolidation of contextual fear. Neuroscience 150: 818-828. (Pubitemid 350235791)
19. Ivy AS, Rex CS, Chen Y, Dube C, Maras PM, Grigoriadis DE et al (2010). Hippocampal dysfunction and cognitive impairments provoked by chronic early-life stress involve excessive activation of CRH receptors. J Neurosci 30: 13005-13015.
20. Kessler RC, McGonagle KA, Swartz M, Blazer DG, Nelson CB (1993). Sex and depression in the National Comorbidity Survey. I: lifetime prevalence, chronicity and recurrence. J Affect Disord 29: 85-96. (Pubitemid 23334116)
21. Kessler RC, McLaughlin KA, Green JG, Gruber MJ, Sampson NA, Zaslavsky AM et al (2010). Childhood adversities and adult psychopathology in the WHO World Mental Health Surveys. Br J Psychiatry 197: 378-385.
22. Koenen KC, Widom CS (2009). A prospective study of sex differences in the lifetime risk of posttraumatic stress disorder among abused and neglected children grown up. J Trauma Stress 22: 566-574.
23. Kolber BJ, Boyle MP, Wieczorek L, Kelley CL, Onwuzurike CC, Nettles SA et al (2010). Transient early-life forebrain corticotropin-releasing hormone elevation causes long-lasting anxiogenic and despair-like changes in mice. J Neuroscience 30: 2571-2581.
24. Korosi A, Veening JG, Kozicz T, Henckens M, Dederen J, Groenink L et al (2006). Distribution and expression of CRF receptor 1 and 2 mRNAs in the CRF over-expressing mouse brain. Brain Res 1072: 46-54. (Pubitemid 43255450)
25. Kozicz T, Korosi A, Korsman C, Tilburg-Ouwens D, Groenink L, Veening J et al (2004). Urocortin expression in the Edinger-Westphal nucleus is down-regulated in transgenic mice overexpressing neuronal corticotropin- releasing factor. Neuroscience 123: 589-594. (Pubitemid 38045397)
26. Ladd CO, Owens MJ, Nemeroff CB (1996). Persistent changes in corticotropin-releasing factor neuronal systems induced by maternal deprivation. Endocrinology 137: 1212-1218. (Pubitemid 26095233)
27. Lee R, Geracioti TD Jr., Kasckow JW, Coccaro EF (2005). Childhood trauma and personality disorder: positive correlation with adult CSF corticotropin-releasing factor concentrations. Am J Psychiatry 162: 995-997. (Pubitemid 40676215)
28. Ludewig S, Geyer MA, Ramseier M, Vollenweider FX, Rechsteiner E, Cattapan-Ludewig K (2005). Information-processing deficits and cognitive dysfunction in panic disorder. J Psychiatry Neurosci 30: 37-43. (Pubitemid 40289245)
29. Michalon A, Koshibu K, Baumgartel K, Spirig DH, Mansuy IM (2005). Inducible and neuron-specific gene expression in the adult mouse brain with the rtTA2S-M2 system. Genesis 43: 205-212. (Pubitemid 43117837)
30. Muller MB, Zimmermann S, Sillaber I, Hagemeyer TP, Deussing JM, Timpl P et al (2003). Limbic corticotropin-releasing hormone receptor 1 mediates anxiety-related behavior and hormonal adaptation to stress. Nat Neurosci 6: 1100-1107. (Pubitemid 37186203)
31. Paxinos G, Franklin KBJ (2004). The Mouse Brain in Stereotaxic Coordinates. compact 2nd edn. Academic Press: San Diego, Calif.; London, xxxi 100 pof platespp.
32. Plotsky PM, Thrivikraman KV, Nemeroff CB, Caldji C, Sharma S, Meaney MJ (2005). Long-term consequences of neonatal rearing on central corticotropin-releasing factor systems in adult male rat offspring. Neuropsychopharmacology 30: 2192-2204. (Pubitemid 41643970)
33. Radulovic J, Ruhmann A, Liepold T, Spiess J (1999). Modulation of learning and anxiety by corticotropin-releasing factor (CRF) and stress: differential roles of CRF receptors 1 and 2. J Neurosci 19: 5016-5025. (Pubitemid 29270136)
34. Rainnie DG, Bergeron R, Sajdyk TJ, Patil M, Gehlert DR, Shekhar A (2004). Corticotrophin releasing factor-induced synaptic plasticity in the amygdala translates stress into emotional disorders. J Neurosci 24: 3471-3479. (Pubitemid 38481103)
35. Refojo D, Schweizer M, Kuehne C, Ehrenberg S, Thoeringer C, Vogl AM et al (2011). Glutamatergic and dopaminergic neurons mediate anxiogenic and anxiolytic effects of CRHR1. Science 333: 1903-1907.
36. Regev L, Tsoory M, Gil S, Chen A (2012). Site-specific genetic manipulation of amygdala corticotropin-releasing factor reveals its imperative role in mediating behavioral response to challenge. Biol Psychiatry 71: 317-326.
37. Risbrough VB, Hauger RL, Pelleymounter MA, Geyer MA (2003). Role of corticotropin releasing factor (CRF) receptors 1 and 2 in CRF-potentiated acoustic startle in mice. Psychopharmacology 170: 178-187. (Pubitemid 37421529)
38. Risbrough VB, Hauger RL, Roberts AL, Vale WW, Geyer MA (2004). Corticotropin-releasing factor receptors CRF1 and CRF2 exert both additive and opposing influences on defensive startle behavior. J Neurosci 24: 6545-6552. (Pubitemid 38971703)
39. Risbrough VB, Masten VL, Caldwell S, Paulus MP, Low MJ, Geyer MA (2006a). Differential contributions of dopamine D1, D2, and D3 receptors to MDMA-induced effects on locomotor behavior patterns in mice. Neuropsychopharmacology 31: 2349-2358. (Pubitemid 44607051)
40. Risbrough VB, Stein MB (2006b). Role of corticotropin releasing factor in anxiety disorders: a translational research perspective. Horm Behav 50: 550-561. (Pubitemid 44307112)
41. Silberstein S, Vogl AM, Refojo D, Senin SA, Wurst W, Holsboer F et al (2009). Amygdaloid pERK1/2 in corticotropin-releasing hormone overexpressing mice under basal and acute stress conditions. Neuroscience 159: 610-617.
42. Smith GW, Aubry JM, Dellu F, Contarino A, Bilezikjian LM, Gold LH et al (1998). Corticotropin releasing factor receptor 1- deficient mice display decreased anxiety, impaired stress response, and aberrant neuroendocrine development. Neuron 20: 1093-1102. (Pubitemid 28293127)
43. Stenzel-Poore MP, Heinrichs SC, Rivest S, Koob GF, Vale WW (1994). Overproduction of corticotropin-releasing factor in transgenic mice: a genetic model of anxiogenic behavior. J Neurosci 14(5 Pt 1): 2579-2584. (Pubitemid 24140886)
44. Swanson LW, Sawchenko PE, Rivier J, Vale WW (1983). Organization of ovine corticotropin-releasing factor immunoreactive cells and fibers in the rat brain: an immunohistochemical study. Neuroendocrinology 36: 165-186. (Pubitemid 13138041)
45. Sztainberg Y, Kuperman Y, Justice N, Chen A (2011). An anxiolytic role for CRF receptor type 1 in the globus pallidus. J Neurosci 31: 17416-17424.
46. Timpl P, Spanagel R, Sillaber I, Kresse A, Reul JM, Stalla GK et al (1998). Impaired stress response and reduced anxiety in mice lacking a functional corticotropin-releasing hormone receptor 1. Nat Genet 19: 162-166. (Pubitemid 28248798)
47. Vicentini E, Arban R, Angelici O, Maraia G, Perico M, Mugnaini M et al (2009). Transient forebrain over-expression of CRF induces plasma corticosterone and mild behavioural changes in adult conditional CRF transgenic mice. Pharmacol Biochem Behav 93: 17-24.
48. Weathington JM, Cooke BM (2012). Corticotropin-releasing factor receptor binding in the amygdala changes across puberty in a sex-specific manner. Endocrinology 153: 5701-5705.
49. Zorrilla EP, Koob GF (2010). Progress in corticotropin-releasing factor-1 antagonist development. Drug Discov Today 15: 371-383.