Corticotropin releasing factor in neuroplasticity

Frontiers in Neuroendocrinology

Volumn 35, Issue 2, 2014, Pages 171-179

  Regev, Limor ^a   Baram, Tallie Z ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

CRF; Epigenetics; Hippocampus; Hypothalamus; Memory; Neuropeptide; Plasticity; Stress; Synapse

Indexed keywords

CORTICOTROPIN RELEASING FACTOR; CORTICOTROPIN RELEASING FACTOR RECEPTOR;

AUTOREGULATION; CELL POPULATION; CELL STRUCTURE; CELL SURVIVAL; CELLULAR STRESS RESPONSE; CELLULAR STRESS SIGNAL; COGNITION; EARLY LIFE STRESS; EMOTION; ENDOCRINE FUNCTION; HIPPOCAMPUS; HORMONE RELEASE; HUMAN; HYPOTHALAMUS; LEARNING; MEMORY; NERVE CELL PLASTICITY; NERVE FUNCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; ANIMAL; METABOLISM; NERVE CELL; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

ANIMALS; CORTICOTROPIN-RELEASING HORMONE; HUMANS; MEMORY; NEURONAL PLASTICITY; NEURONS; STRESS, PHYSIOLOGICAL;

EID: 84896105768     PISSN: 00913022     EISSN: 10956808     Source Type: Journal    
DOI: 10.1016/j.yfrne.2013.10.001     Document Type: Review

References (158)

1. Agnati L.F., Guidolin D., Guescini M., Genedani S., Fuxe K. Understanding wiring and volume transmission. Brain Res. Rev. 2010, 64:137-159.
2. Aguilera G. HPA axis responsiveness to stress: implications for healthy aging. Exp. Gerontol. 2011, 46:90-95.
3. Aguilera G., Liu Y. The molecular physiology of CRH neurons. Front. Neuroendocrinol. 2012, 33:67-84.
4. Aisa B., Tordera R., Lasheras B., Del Río J., Ramírez M.J. Cognitive impairment associated to HPA axis hyperactivity after maternal separation in rats. Psychoneuroendocrinology 2007, 32:256-266.
5. Aldenhoff J.B., Gruol D.L., Rivier J., Vale W., Siggins G.R. Corticotropin releasing factor decreases postburst hyperpolarizations and excites hippocampal neurons. Science 1983, 221:875-877.
6. Arborelius L., Owens M.J., Plotsky P.M., Nemeroff C.B. The role of corticotropin-releasing factor in depression and anxiety disorders. J. Endocrinol. 1999, 160:1-12.
7. Aubry J.M., Bartanusz V., Pagliusi S., Schulz P., Kiss J.Z. Expression of ionotropic glutamate receptor subunit mRNAs by paraventricular corticotropin-releasing factor (CRF) neurons. Neurosci. Lett. 1996, 205:95-98.
8. Avishai-Eliner S., Eghbal-Ahmadi M., Tabachnik E., Brunson K.L., Baram T.Z. Down-regulation of hypothalamic corticotropin-releasing hormone messenger ribonucleic acid (mRNA) precedes early-life experience-induced changes in hippocampal glucocorticoid receptor mRNA. Endocrinology 2001, 142:89-97.
9. Avishai-Eliner S., Gilles E.E., Eghbal-Ahmadi Y., Bar-El Y., Baram T.Z. Altered regulation of gene and protein expression of hypothalamic-pituitary-adrenal axis components in an immature rat model of chronic stress. J. Neuroendocrinol. 2001, 13:799-807.
10. Bale T.L., Vale W.W. CRF and CRF receptors: role in stress responsivity and other behaviors. Annu. Rev. Pharmacol. Toxicol. 2004, 44:525-557.
11. Bale T.L., Picetti R., Contarino A., Koob G.F., Vale W.W., Lee K.F. Mice deficient for both corticotropin-releasing factor receptor 1 (CRFR1) and CRFR2 have an impaired stress response and display sexually dichotomous anxiety-like behavior. J. Neurosci. 2002, 22:193-199.
12. Bale T.L., Baram T.Z., Brown A.S., Goldstein J.M., Insel T.R., McCarthy M.M., Nemeroff C.B., Reyes T.M., Simerly R.B., Susser E.S., Nestler E.J. Early life programming and neurodevelopmental disorders. Biol. Psychiatry 2010, 68:314-319.
13. Baram T.Z., Hatalski C.G. Neuropeptide-mediated excitability: a key triggering mechanism for seizure generation in the developing brain. Trends Neurosci. 1998, 21:471-476.
14. Baram T.Z., Davis E.P., Obenaus A., Sandman C.A., Small S.L., Solodkin A., Stern H. Fragmentation and unpredictability of early-life experience in mental disorders. Am. J. Psychiatry 2012, 169:907-915.
15. Behan D.P., Heinrichs S.C., Troncoso J.C., Liu X.J., Kawas C.H., Ling N., De Souza E.B. Displacement of corticotropin releasing factor from its binding protein as a possible treatment for Alzheimer's disease. Nature 1995, 378:284-287.
16. Behan D.P., De Souza E.B., Lowry P.J., Potter E., Sawchenko P., Vale W.W. Corticotropin releasing factor (CRF) binding protein: a novel regulator of CRF and related peptides. Front. Neuroendocrinol. 1995, 16:362-382.
17. Bittencourt J.C., Sawchenko P.E. Do centrally administered neuropeptides access cognate receptors? An analysis in the central corticotropin-releasing factor system. J. Neurosci. 2000, 20:1142-1156.
18. Blank T., Nijholt I., Eckart K., Spiess J. Priming of long-term potentiation in mouse hippocampus by corticotropin-releasing factor and acute stress: implications for hippocampus-dependent learning. J. Neurosci. 2002, 22:3788-3794.
19. Blank T., Nijholt I., Grammatopoulos D.K., Randeva H.S., Hillhouse E.W., Spiess J. Corticotropin-releasing factor receptors couple to multiple G-proteins to activate diverse intracellular signaling pathways in mouse hippocampus: role in neuronal excitability and associative learning. J. Neurosci. 2003, 23:700-707.
20. Bliss T.V., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993, 361:31-39.
21. Bonfiglio J.J., Inda C., Refojo D., Holsboer F., Arzt E., Silberstein S. The corticotropin-releasing hormone network and the hypothalamic-pituitary-adrenal axis: molecular and cellular mechanisms involved. Neuroendocrinology 2011, 94:12-20.
22. Boudaba C., Schrader L.A., Tasker J.G. Physiological evidence for local excitatory synaptic circuits in the rat hypothalamus. J. Neurophysiol. 1997, 77:3396-3400.
23. Bradley R.G., Binder E.B., Epstein M.P., Tang Y., Nair H.P., Liu W., Gillespie C.F., Berg T., Evces M., Newport D.J., Stowe Z.N., Heim C.M., Nemeroff C.B., Schwartz A., Cubells J.F., Ressler K.J. Influence of child abuse on adult depression: moderation by the corticotropin-releasing hormone receptor gene. Arch. Gen. Psychiatry 2008, 65:190-200.
24. Brown M.R., Fisher L.A., Spiess J., Rivier J., Rivier C., Vale W. Comparison of the biologic actions of corticotropin-releasing factor and sauvagine. Regul. Pept. 1982, 4:107-114.
25. Brunson K.L., Avishai-Eliner S., Hatalski C.G., Baram T.Z. Neurobiology of the stress response early in life: evolution of a concept and the role of corticotropin releasing hormone. Mol. Psychiatry 2001, 6:647-656.
26. Brunson K.L., Kramár E., Lin B., Chen Y., Colgin L.L., Yanagihara T.L., Lynch G., Baram T.Z. Mechanisms of late-onset cognitive decline after early life stress. J. Neurosci. 2005, 25:9328-9338.
27. Chang D., Yi S.J., Baram T.Z. Developmental profile of corticotropin releasing hormone messenger RNA in the rat inferior olive. Int. J. Dev. Neurosci. 1996, 14:69-76.
28. Chen Y., Bender R.A., Frotscher M., Baram T.Z. Novel and transient populations of corticotropin-releasing hormone-expressing neurons in developing hippocampus suggest unique functional roles: a quantitative spatiotemporal analysis. J. Neurosci. 2001, 21:7171-7181.
29. Chen Y., Hatalski C.G., Brunson K.L., Baram T.Z. Rapid phosphorylation of the CRE binding protein precedes stress-induced activation of the corticotropin releasing hormone gene in medial parvocellular hypothalamic neurons of the immature rat. Mol. Brain Res. 2001, 96:39-49.
30. Chen Y., Bender R.A., Brunson K.L., Pomper J.K., Grigoriadis D.E., Wurst W., Baram T.Z. Modulation of dendritic differentiation by corticotropin-releasing factor in the developing hippocampus. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:15782-15787.
31. Chen Y., Brunson K.L., Adelmann G., Bender R.A., Frotscher M., Baram T.Z. Hippocampal corticotropin releasing hormone: pre- and postsynaptic location and release by stress. Neuroscience 2004, 126:533-540.
32. Chen Y., Rex C.S., Rice C.J., Dubé C.M., Gall C.M., Lynch G., Baram T.Z. Correlated memory defects and hippocampal dendritic spine loss after acute stress involve corticotropin-releasing hormone signaling. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:13123-13128.
33. Chen J., Evans A.N., Liu Y., Honda M., Saavedra J.M., Aguilera G. Maternal deprivation in rats is associated with corticotrophin-releasing hormone (CRH) promoter hypomethylation and enhances CRH transcriptional responses to stress in adulthood. J. Neuroendocrinol. 2012, 24:1055-1064.
34. Chen Y., Andres A.L., Frotscher M., Baram T.Z. Tuning synaptic transmission in the hippocampus by stress: the CRH system. Front. Cell Neurosci. 2012, 6:13.
35. Chen Y., Kramár E.A., Chen L.Y., Babayan A.H., Andres A.L., Gall C.M., Lynch G., Baram T.Z. Impairment of synaptic plasticity by the stress mediator CRH involves selective destruction of thin dendritic spines via RhoA signaling. Mol. Psychiatry 2013, 18:485-496.
36. Christoffel D.J., Golden S.A., Russo S.J. Structural and synaptic plasticity in stress-related disorders. Rev. Neurosci. 2011, 22:535-549.
37. Contarino A., Dellu F., Koob G.F., Smith G.W., Lee K.F., Vale W., Gold L.H. Reduced anxiety-like and cognitive performance in mice lacking the corticotropin-releasing factor receptor 1. Brain Res. 1999, 835:1-9.
38. Cope J.L., Regev L., Chen Y., Korosi A., Rice C.J., Ji S., Rogge G.A., Wood M.A., Baram T.Z. Differential contribution of CBP:CREB binding to corticotropin-releasing hormone expression in the infant and adult hypothalamus. Stress 2013, 10.3109/10253890.2013.806907.
39. Coste S.C., Murray S.E., Stenzel-Poore M.P. Animal models of CRH excess and CRH receptor deficiency display altered adaptations to stress. Peptides 2001, 22:733-741.
40. Cullinan W.E. GABA(A) receptor subunit expression within hypophysiotropic CRH neurons: a dual hybridization histochemical study. J. Comp. Neurol. 2000, 419:344-351.
41. Dabrowska J., Hazra R., Ahern T.H., Guo J.D., McDonald A.J., Mascagni F., Muller J.F., Young L.J., Rainnie D.G. Neuroanatomical evidence for reciprocal regulation of the corticotrophin-releasing factor and oxytocin systems in the hypothalamus and the bed nucleus of the stria terminalis of the rat: Implications for balancing stress and affect. Psychoneuroendocrinology 2011, 36:1312-1326.
42. de Kloet E.R., Joëls M., Holsboer F. Stress and the brain: from adaptation to disease. Nat. Rev. Neurosci. 2005, 6:463-475.
43. De Souza E.B., Whitehouse P.J., Kuhar M.J., Price D.L., Vale W.W. Reciprocal changes in corticotropin-releasing factor (CRF)-like immunoreactivity and CRF receptors in cerebral cortex of Alzheimer's disease. Nature 1986, 319:593-595.
44. Dedovic K., Duchesne A., Andrews J., Engert V., Pruessner J.C. The brain and the stress axis: the neural correlates of cortisol regulation in response to stress. Neuroimage 2009, 47:864-871.
45. Dent G.W., Smith M.A., Levine S. Rapid induction of corticotropin-releasing hormone gene transcription in the paraventricular nucleus of the developing rat. Endocrinology 2000, 141:1593-1598.
46. Denver R.J. Neuroendocrinology of amphibian metamorphosis. Curr. Top Dev. Biol. 2013, 103:195-227.
47. Di S., Malcher-Lopes R., Halmos K.C., Tasker J.G. Nongenomic glucocorticoid inhibition via endocannabinoid release in the hypothalamus: a fast feedback mechanism. J. Neurosci. 2003, 23:4850-4857.
48. Dong H., Murphy K.M., Meng L., Montalvo-Ortiz J., Zeng Z., Kolber B.J., Zhang S., Muglia L.J., Csernansky J.G. Corticotrophin releasing factor accelerates neuropathology and cognitive decline in a mouse model of Alzheimer's disease. J. Alzheimers Dis. 2012, 28:579-592.
49. Elliott E., Ezra-Nevo G., Regev L., Neufeld-Cohen A., Chen A. Resilience to social stress coincides with functional DNA methylation of the Crf gene in adult mice. Nat. Neurosci. 2010, 13:1351-1353.
50. Fenoglio K.A., Brunson K.L., Avishai-Eliner S., Stone B.A., Kapadia B.J., Baram T.Z. Enduring, handling-evoked enhancement of hippocampal memory function and glucocorticoid receptor expression involves activation of the corticotropin-releasing factor type 1 receptor. Endocrinology 2005, 146:4090-4096.
51. Fenoglio K.A., Chen Y., Baram T.Z. Neuroplasticity of the hypothalamic-pituitary-adrenal axis early in life requires recurrent recruitment of stress-regulating brain regions. J. Neurosci. 2006, 26:2434-2442.
52. Fenoglio K.A., Brunson K.L., Baram T.Z. Hippocampal neuroplasticity induced by early-life stress: functional and molecular aspects. Front. Neuroendocrinol. 2006, 27:180-192.
53. Flandreau E.I., Ressler K.J., Owens M.J., Nemeroff C.B. 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 2012, 37:27-38.
54. Gallagher J.P., Orozco-Cabal L.F., Liu J., Shinnick-Gallagher P. Synaptic physiology of central CRH system. Eur. J. Pharmacol. 2008, 583:215-225.
55. Gallopin T., Geoffroy H., Rossier J., Lambolez B. Cortical sources of CRF, NKB, and CCK and their effects on pyramidal cells in the neocortex. Cereb. Cortex 2006, 16:1440-1452.
56. Gibbs D.M., Vale W. Presence of corticotropin releasing factor-like immunoreactivity in hypophysial portal blood. Endocrinology 1982, 111:1418-1420.
57. Ginsberg A.B., Campeau S., Day H.E., Spencer R.L. Acute glucocorticoid pretreatment suppresses stress-induced hypothalamic-pituitary-adrenal axis hormone secretion and expression of corticotropin-releasing hormone hnRNA but does not affect c-fos mRNA or Fos protein expression in the paraventricular nucleus of the hypothalamus. J. Neuroendocrinol. 2003, 15:1075-1083.
58. Groeneweg F.L., Karst H., de Kloet E.R., Joëls M. Rapid non-genomic effects of corticosteroids and their role in the central stress response. J. Endocrinol. 2011, 209:153-167.
59. Hatalski C.G., Guirguis C., Baram T.Z. Corticotropin releasing factor mRNA expression in the hypothalamic paraventricular nucleus and the central nucleus of the amygdala is modulated by repeated acute stress in the immature rat. J. Neuroendocrinol. 1998, 10:663-669.
60. Hollrigel G.S., Chen K., Baram T.Z., Soltesz I. The pro-convulsant actions of corticotropin-releasing hormone in the hippocampus of infant rats. Neuroscience 1998, 84:71-79.
61. Holmes K.D., Babwah A.V., Dale L.B., Poulter M.O., Ferguson S.S. Differential regulation of corticotropin releasing factor 1alpha receptor endocytosis and trafficking by beta-arrestins and Rab GTPases. J. Neurochem. 2006, 96:934-949.
62. Hung H.C., Chou C.K., Chiu T.H., Lee E.H. CRF increases protein phosphorylation and enhances retention performance in rats. Neuroreport 1992, 3:181-184.
63. Ivy A.S., Brunson K.L., Sandman C., Baram T.Z. Dysfunctional nurturing behavior in rat dams with limited access to nesting material: a clinically relevant model for early-life stress. Neuroscience 2008, 154:1132-1142.
64. Ivy A.S., Rex C.S., Chen Y., Dubé C., Maras P.M., Grigoriadis D.E., Gall C.M., Lynch G., Baram T.Z. Hippocampal dysfunction and cognitive impairments provoked by chronic early-life stress involve excessive activation of CRH receptors. J. Neurosci. 2010, 30:13005-13015.
65. Jankord R., Herman J.P. Limbic regulation of hypothalamo-pituitary-adrenocortical function during acute and chronic stress. Ann. N.Y. Acad. Sci. 2008, 1148:64-73.
66. Joëls M., Baram T.Z. The neuro-symphony of stress. Nat. Rev. Neurosci. 2009, 10:459-466.
67. Joëls M., Fernandez G., Roozendaal B. Stress and emotional memory: a matter of timing. Trends Cogn. Sci. 2011, 15:280-288.
68. Kaplan G.A., Turrell G., Lynch J.W., Everson S.A., Helkala E.L., Salonen J.T. Childhood socioeconomic position and cognitive function in adulthood. Int. J. Epidemiol. 2001, 30:256-263.
69. Karsten C.A., Baram T.Z. How does a neuron "know" to modulate its epigenetic machinery in response to early-life environment/experience?. Front. Psychiatry 2013, 4:89.
70. Kim J.J., Diamond D.M. The stressed hippocampus, synaptic plasticity and lost memories. Nat. Rev. Neurosci. 2002, 3:453-462.
71. Kiss J., Gorc T.J., Kuhn R., Knopfel T., Csaky A., Halasz B. Distribution of metabotropic glutamate receptor 1a in the rat hypothalamus: an immunocytochemical study using monoclonal and polyclonal antibody. Acta Biol. Hung. 1996, 47:221-237.
72. Korosi A., Baram T.Z. The pathways from mother's love to baby's future. Front. Behav. Neurosci. 2009, 3:27.
73. Korosi A., Shanabrough M., McClelland S., Liu Z.W., Borok E., Gao X.B., Horvath T.L., Baram T.Z. Early-life experience reduces excitation to stress-responsive hypothalamic neurons and reprograms the expression of corticotropin-releasing hormone. J. Neurosci. 2010, 30:703-713.
74. Kuzmiski J.B., Marty V., Baimoukhametova D.V., Bains J.S. Stress-induced priming of glutamate synapses unmasks associative short-term plasticity. Nat. Neurosci. 2010, 13:1257-1264.
75. Landgraf R., Neumann I.D. Vasopressin and oxytocin release within the brain: a dynamic concept of multiple and variable modes of neuropeptide communication. Front. Neuroendocrinol. 2004, 25:150-176.
76. Larson J., Lynch G. Induction of synaptic potentiation in hippocampus by patterned stimulation involves two events. Science 1986, 232:985-988.
77. Lee E.H., Lee C.P., Wang H.I., Lin W.R. Hippocampal CRF, NE, and NMDA system interactions in memory processing in the rat. Synapse 1993, 14:144-153.
78. Levine S. Maternal and environmental influences on the adrenocortical response to stress in weanling rats. Science 1967, 156:258-260.
79. Levy B.H., Tasker J.G. Synaptic regulation of the hypothalamic-pituitary-adrenal axis and its modulation by glucocorticoids and stress. Front. Cell. Neurosci. 2012, 6:24.
80. Lightman S.L. The neuroendocrinology of stress: a never ending story. J. Neuroendocrinol. 2008, 20:880-884.
81. Lister R., Mukamel E.A., Nery J.R., Urich M., Puddifoot C.A., Johnson N.D., Lucero J., Huang Y., Dwork A.J., Schultz M.D., Yu M., Tonti-Filippini J., Heyn H., Hu S., Wu J.C., Rao A., Esteller M., He C., Haghighi F.G., Sejnowski T.J., Behrens M.M., Ecker J.R. Global epigenomic reconfiguration during mammalian brain development. Science 2013, 341:1237905.
82. Liu Y., Aguilera G. Cyclic AMP inducible early repressor mediates the termination of corticotropin releasing hormone transcription in hypothalamic neurons. Cell. Mol. Neurobiol. 2009, 29:1275-1281.
83. Liu D., Diorio J., Tannenbaum B., Caldji C., Francis D., Freedman A., Sharma S., Pearson D., Plotsky P.M., Meaney M.J. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 1997, 277:1659-1662.
84. Liu D., Diorio J., Day J.C., Francis D.D., Meaney M.J. Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat. Neurosci. 2000, 3:799-806.
85. Liu Y., Poon V., Sanchez-Watts G., Watts A.G., Takemori H., Aguilera G. Salt-inducible kinase is involved in the regulation of corticotropin-releasing hormone transcription in hypothalamic neurons in rats. Endocrinology 2012, 153:223-233.
86. Lloyd R.B., Nemeroff C.B. The role of corticotropin-releasing hormone in the pathophysiology of depression: therapeutic implications. Curr. Top. Med. Chem. 2011, 11:609-617.
87. Lucassen P.J., Naninck E.F., van Goudoever J.B., Fitzsimons C., Joels M., Korosi A. Perinatal programming of adult hippocampal structure and function; emerging roles of stress, nutrition and epigenetics. Trends Neurosci. 2013, 10.1016/j.tins.2013.08.002.
88. Ma X.M., Levy A., Lightman S.L. Rapid changes in heteronuclear RNA for corticotrophin-releasing hormone and arginine vasopressin in response to acute stress. J. Endocrinol. 1997, 152:81-89.
89. Ma Y.L., Chen K.Y., Wei C.L., Lee E.H. Corticotropin-releasing factor enhances brain-derived neurotrophic factor gene expression to facilitate memory retention in rats. Chin. J. Physiol. 1999, 42:73-81.
90. Maras P.M., Baram T.Z. Sculpting the hippocampus from within: stress, spines, and CRH. Trends Neurosci. 2012, 35:315-324.
91. McClelland S., Korosi A., Cope J., Ivy A., Baram T.Z. Emerging roles of epigenetic mechanisms in the enduring effects of early-life stress and experience on learning and memory. Neurobiol. Learn. Mem. 2011, 96:79-88.
92. McEwen B.S. Stress and hippocampal plasticity. Annu. Rev. Neurosci. 1999, 22:105-122.
93. McEwen B.S. Brain on stress: how the social environment gets under the skin. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:17180-17185.
94. McEwen B.S., Gianaros P.J. Stress- and allostasis-induced brain plasticity. Annu. Rev. Med. 2011, 62:431-445.
95. McGill B.E., Bundle S.F., Yaylaoglu M.B., Carson J.P., Thaller C., Zoghbi H.Y. Enhanced anxiety and stress-induced corticosterone release are associated with increased Crh expression in a mouse model of Rett syndrome. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:18267-18272.
96. Meaney M.J., Viau V., Bhatnagar S., Betito K., Iny L.J., O'Donnell D., Mitchell J.B. Cellular mechanisms underlying the development and expression of individual differences in the hypothalamic-pituitary-adrenal stress response. J. Steroid Biochem. Mol. Biol. 1991, 39:265-274.
97. Merali Z., Kent P., Du L., Hrdina P., Palkovits M., Faludi G., Poulter M.O., Bédard T., Anisman H. Corticotropin-releasing hormone, arginine vasopressin, gastrin-releasing peptide, and neuromedin B alterations in stress-relevant brain regions of suicides and control subjects. Biol. Psychiatry 2006, 59:594-602.
98. Miklos I.H., Kovacs K.J. GABAergic innervation of corticotropin-releasing hormone (CRH)-secreting parvocellular neurons and its plasticity as demonstrated by quantitative immunoelectron microscopy. Neuroscience 2002, 113:581-592.
99. Mori N., Schoenherr C., Vandenbergh D.J., Anderson D.J. A common silencer element in the SCG10 and type II Na channel genes binds a factor present in nonneuronal cells but not in neuronal cells. Neuron 1992, 9:45-54.
100. Mueller B.R., Bale T.L. Sex-specific programming of offspring emotionality after stress early in pregnancy. J. Neurosci. 2008, 28:9055-9065.
101. Nederhof E., Schmidt M.V. Mismatch or cumulative stress: toward an integrated hypothesis of programming effects. Physiol. Behav. 2012, 106:691-700.
102. Nelson C.A., Zeanah C.H., Fox N.A., Marshall P.J., Smyke A.T., Guthrie D. Cognitive recovery in socially deprived young children: the Bucharest Early Intervention Project. Science 2007, 318:1937-1940.
103. Oakley R.H., Olivares-Reyes J.A., Hudson C.C., Flores-Vega F., Dautzenberg F.M., Hauger R.L. Carboxyl-terminal and intracellular loop sites for CRF1 receptor phosphorylation and beta-arrestin-2 recruitment: a mechanism regulating stress and anxiety responses. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 293:R209-222.
104. Osterlund C., Spencer R.L. Inhibitory effects of corticosterone in the hypothalamic paraventricular nucleus (PVN) on stress-induced adrenocorticotrophic hormone secretion and gene expression in the PVN and anterior pituitary. J. Neuroendocrinol. 2011, 23:1231-1240.
105. Pace T.W., Gaylord R.I., Jarvis E., Girotti M., Spencer R.L. Differential glucocorticoid effects on stress-induced gene expression in the paraventricular nucleus of the hypothalamus and ACTH secretion in the rat. Stress 2009, 12:400-411.
106. Palm K., Belluardo N., Metsis M., Timmusk T. Neuronal expression of zinc finger transcription factor REST/NRSF/XBR gene. J. Neurosci. 1998, 18:1280-1296.
107. Pawlak R., Rao B.S., Melchor J.P., Chattarji S., McEwen B., Strickland S. Tissue plasminogen activator and plasminogen mediate stress-induced decline of neuronal and cognitive functions in the mouse hippocampus. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:18201-18206.
108. Pinnock S.B., Herbert J. Corticosterone differentially modulates expression of corticotropin releasing factor and arginine vasopressin mRNA in the hypothalamic paraventricular nucleus following either acute or repeated restraint stress. Eur. J. Neurosci. 2001, 13:576-584.
109. Plotsky P.M., Meaney M.J. Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Brain Res. Mol. Brain Res. 1993, 18:195-200.
110. Punn A., Levine M.A., Grammatopoulos D.K. Identification of signaling molecules mediating corticotropin-releasing hormone-R1alpha-mitogen-activated protein kinase (MAPK) interactions: the critical role of phosphatidylinositol 3-kinase in regulating ERK1/2 but not p38 MAPK activation. Mol. Endocrinol. 2006, 20:3179-3195.
111. Raadsheer F.C., van Heerikhuize J.J., Lucassen P.J., Hoogendijk W.J., Tilders F.J., Swaab D.F. Corticotropin-releasing hormone mRNA levels in the paraventricular nucleus of patients with Alzheimer's disease and depression. Am. J. Psychiatry 1995, 152:1372-1376.
112. Radulovic J., Rühmann A., Liepold T., Spiess J. Modulation of learning and anxiety by corticotropin-releasing factor (CRF) and stress: differential roles of CRF receptors 1 and 2. J. Neurosci. 1999, 19:5016-5025.
113. Refojo D., Echenique C., Müller M.B., Reul J.M., Deussing J.M., Wurst W., Sillaber I., Paez-Pereda M., Holsboer F., Arzt E. Corticotropin-releasing hormone activates ERK1/2 MAPK in specific brain areas. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:6183-6188.
114. Refojo D., Schweizer M., Kuehne C., Ehrenberg S., Thoeringer C., Vogl A.M., Dedic N., Schumacher M., von Wolff G., Avrabos C., Touma C., Engblom D., Schütz G., Nave K.A., Eder M., Wotjak C.T., Sillaber I., Holsboer F., Wurst W., Deussing J.M. Glutamatergic and dopaminergic neurons mediate anxiogenic and anxiolytic effects of CRHR1. Science 2011, 333:1903-1907.
115. Regev L., Tsoory M., Gil S., Chen A. Site-specific genetic manipulation of amygdala corticotropin-releasing factor reveals its imperative role in mediating behavioral response to challenge. Biol. Psychiatry 2012, 71:317-326.
116. Reul J.M., Holsboer F. Corticotropin-releasing factor receptors 1 and 2 in anxiety and depression. Curr. Opin. Pharmacol. 2002, 2:23-33.
117. Reyes B.A., Valentino R.J., Van Bockstaele E.J. Stress-induced intracellular trafficking of corticotropin-releasing factor receptors in rat locus coeruleus neurons. Endocrinology 2008, 149:122-130.
118. Rice C.J., Sandman C.A., Lenjavi M.R., Baram T.Z. A novel mouse model for acute and long-lasting consequences of early life stress. Endocrinology 2008, 149:4892-4900.
119. Ritter S., Watts A.G., Dinh T.T., Sanchez-Watts G., Pedrow C. Immunotoxin lesion of hypothalamically projecting norepinephrine and epinephrine neurons differentially affects circadian and stressor-stimulated corticosterone secretion. Endocrinology 2003, 144:1357-1367.
120. Rivest S., Laflamme N., Nappi R.E. Immune challenge and immobilization stress induce transcription of the gene encoding the CRF receptor in selective nuclei of the rat hypothalamus. J. Neurosci. 1995, 15:2680-2695.
121. Rivier C., Rivier J., Vale W. Inhibition of adrenocorticotropic hormone secretion in the rat by immunoneutralization of corticotropin-releasing factor. Science 1982, 218:377-379.
122. Roozendaal B., Brunson K.L., Holloway B.L., McGaugh J.L., Baram T.Z. Involvement of stress-released corticotropin-releasing hormone in the basolateral amygdala in regulating memory consolidation. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:13908-13913.
123. Roozendaal B., Griffith Q.K., Buranday J., De Quervain D.J., McGaugh J.L. The hippocampus mediates glucocorticoid-induced impairment of spatial memory retrieval: dependence on the basolateral amygdala. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:1328-1333.
124. Roozendaal B., Hernandez A., Cabrera S.M., Hagewoud R., Malvaez M., Stefanko D.P., Haettig J., Wood M.A. Membrane-associated glucocorticoid activity is necessary for modulation of long-term memory via chromatin modification. J. Neurosci. 2010, 30:5037-5046.
125. Row B.W., Dohanich G.P. Post-training administration of corticotropin-releasing hormone (CRH) enhances retention of a spatial memory through a noradrenergic mechanism in male rats. Neurobiol. Learn. Mem. 2008, 89:370-378.
126. Sakanaka M., Shibasaki T., Lederis K. Corticotropin releasing factor-like immunoreactivity in the rat brain as revealed by a modified cobalt-glucose oxidase-diaminobenzidine method. J. Comp. Neurol. 1987, 260:256-298.
127. Schierloh A., Deussing J., Wurst W., Zieglgänsberger W., Rammes G. Corticotropin-releasing factor (CRF) receptor type 1-dependent modulation of synaptic plasticity. Neurosci. Lett. 2007, 416:82-86.
128. Seasholtz A.F., Burrows H.L., Karolyi I.J., Camper S.A. Mouse models of altered CRH-binding protein expression. Peptides 2001, 22:743-751.
129. Seth K.A., Majzoub J.A. Repressor element silencing transcription factor/neuron-restrictive silencing factor (REST/NRSF) can act as an enhancer as well as a repressor of corticotropin-releasing hormone gene transcription. J. Biol. Chem. 2001, 276:13917-13923.
130. Snyder K., Wang W.W., Han R., McFadden K., Valentino R.J. Corticotropin-releasing factor in the norepinephrine nucleus, locus coeruleus, facilitates behavioral flexibility. Neuropsychopharmacology 2012, 37:520-530.
131. Sterrenburg L., Gaszner B., Boerrigter J., Santbergen L., Bramini M., Elliott E., Chen A., Peeters B.W., Roubos E.W., Kozicz T. Chronic stress induces sex-specific alterations in methylation and expression of corticotropin-releasing factor gene in the rat. PLoS One 2011, 6:e28128.
132. Swanson L.W., Simmons D.M. Differential steroid hormone and neural influences on peptide mRNA levels in CRH cells of the paraventricular nucleus: a hybridization histochemical study in the rat. J. Comp. Neurol. 1989, 285:413-435.
133. Swanson L.W., Sawchenko P.E., Rivier J., Vale W.W. Organization of ovine corticotropin-releasing factor immunoreactive cells and fibers in the rat brain: an immunohistochemical study. Neuroendocrinology 1983, 36:165-186.
134. Swinny J.D., Valentino R.J. Corticotropin-releasing factor promotes growth of brain norepinephrine neuronal processes through Rho GTPase regulators of the actin cytoskeleton in rat. Eur. J. Neurosci. 2006, 24:2481-2490.
135. Szyf M., Bick J. DNA methylation: a mechanism for embedding early life experiences in the genome. Child Dev. 2013, 84:49-57.
136. Tanimura S.M., Watts A.G. Corticosterone can facilitate as well as inhibit corticotropin-releasing hormone gene expression in the rat hypothalamic paraventricular nucleus. Endocrinology 1998, 139:3830-3836.
137. Timmermans W., Xiong H., Hoogenraad C.C., Krugers H.J. Stress and excitatory synapses: from health to disease. Neuroscience 2013, 248:626-636.
138. Ulrich-Lai Y.M., Herman J.P. Neural regulation of endocrine and autonomic stress responses. Nat. Rev. Neurosci. 2009, 10:397-409.
139. Vale W., Spiess J., Rivier C., Rivier J. Characterization of a 41-residue ovine hypothalamic peptide that stimulates secretion of corticotropin and beta-endorphin. Science 1981, 213:1394-1397.
140. Vale W., Rivier C., Brown M.R., Spiess J., Koob G., Swanson L., Bilezikjian L., Bloom F., Rivier J. Chemical and biological characterization of corticotropin releasing factor. Recent Prog. Horm. Res. 1983, 39:245-270.
141. Valentino R.J., Van Bockstaele E. Convergent regulation of locus coeruleus activity as an adaptive response to stress. Eur. J. Pharmacol. 2008, 583:194-203.
142. Valentino R.J., Wehby R.G. Corticotropin-releasing factor: evidence for a neurotransmitter role in the locus coeruleus during hemodynamic stress. Neuroendocrinology 1988, 48:674-677.
143. Van Pett K., Viau V., Bittencourt J.C., Chan R.K., Li H.Y., Arias C., Prins G.S., Perrin M., Vale W., Sawchenko P.E. Distribution of mRNAs encoding CRF receptors in brain and pituitary of rat and mouse. J. Comp. Neurol. 2000, 428:191-212.
144. Wang H.L., Wayner M.J., Chai C.Y., Lee E.H. Corticotrophin-releasing factor produces a long-lasting enhancement of synaptic efficacy in the hippocampus. Eur. J. Neurosci. 1998, 10:3428-3437.
145. Wang H.L., Tsai L.Y., Lee E.H. Corticotropin-releasing factor produces a protein synthesis - dependent long-lasting potentiation in dentate gyrus neurons. J. Neurophysiol. 2000, 83:343-349.
146. Wang W., Dow K.E., Fraser D.D. Elevated corticotropin releasing hormone/corticotropin releasing hormone-R1 expression in postmortem brain obtained from children with generalized epilepsy. Ann. Neurol. 2001, 50:404-409.
147. 1 modulates early-life stress-programmed cognitive deficits. J. Neurosci. 2011, 31:13625-13634.
148. Wang X.D., Chen Y., Wolf M., Wagner K.V., Liebl C., Scharf S.H., Harbich D., Mayer B., Wurst W., Holsboer F., Deussing J.M., Baram T.Z., Müller M.B., Schmidt M.V. Forebrain CRHR1 deficiency attenuates chronic stress-induced cognitive deficits and dendritic remodeling. Neurobiol. Dis. 2011, 42:300-310.
149. Wang X.D., Su Y.A., Wagner K.V., Avrabos C., Scharf S.H., Hartmann J., Wolf M., Liebl C., Kühne C., Wurst W., Holsboer F., Eder M., Deussing J.M., Müller M.B., Schmidt M.V. Nectin-3 links CRHR1 signaling to stress-induced memory deficits and spine loss. Nat. Neurosci. 2013, 16:706-713.
150. Watts A.G. Glucocorticoid regulation of peptide genes in neuroendocrine CRH neurons: a complexity beyond negative feedback. Front. Neuroendocrinol. 2005, 26:109-130.
151. Weaver I.C., Champagne F.A., Brown S.E., Dymov S., Sharma S., Meaney M.J., Szyf M. Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life. J. Neurosci. 2005, 25:11045-11054.
152. Wilson R.S., Schneider J.A., Boyle P.A., Arnold S.E., Tang Y., Bennett D.A. Chronic distress and incidence of mild cognitive impairment. Neurology 2007, 68:2085-2092.
153. Wosiski-Kuhn M., Stranahan A.M. Opposing effects of positive and negative stress on hippocampal plasticity over the lifespan. Ageing Res. Rev. 2012, 11:399-403.
154. Yan X.X., Toth Z., Schultz L., Ribak C.E., Baram T.Z. Corticotropin-releasing hormone (CRH)-containing neurons in the immature rat hippocampal formation: light and electron microscopic features and colocalization with glutamate decarboxylase and parvalbumin. Hippocampus 1998, 8:231-243.
155. Yi S.J., Baram T.Z. Corticotropin-releasing hormone mediates the response to cold stress in the neonatal rat without compensatory enhancement of the peptide's gene expression. Endocrinology 1994, 135:2364-2368.
156. Ziegler D.R., Cullinan W.E., Herman J.P. Organization and regulation of paraventricular nucleus glutamate signaling systems: N-methyl-d-aspartate receptors. J. Comp. Neurol. 2005, 484:43-56.
157. Zoladz P.R., Diamond D.M. Linear and non-linear dose-response functions reveal a hormetic relationship between stress and learning. Dose Response 2008, 7:132-148.
158. Zoumakis E., Chrousos G.P. Corticotropin-releasing hormone receptor antagonists: an update. Endocr. Dev. 2010, 17:36-43.