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Reul JM, Collins A, Saliba RS, et al. Glucocorticoids, epigenetic control and stress resilience. Neurobiol Stress. 2014;1:44-59doi: 10.1016/j.ynstr.2014.10.001.
Reul, J. M., Collins, A., Saliba, R. S., Mifsud, K. R., Carter, S. D., Gutierrez-Mecinas, M., Qian, X., & Linthorst, A. C. (2015). Glucocorticoids, epigenetic control and stress resilience. Neurobiology of stress, 144-59. https://doi.org/10.1016/j.ynstr.2014.10.001
Reul, Johannes M H M, et al. "Glucocorticoids, epigenetic control and stress resilience." Neurobiology of stress vol. 1 (2015): 44-59. doi: https://doi.org/10.1016/j.ynstr.2014.10.001
Reul JM, Collins A, Saliba RS, Mifsud KR, Carter SD, Gutierrez-Mecinas M, Qian X, Linthorst AC. Glucocorticoids, epigenetic control and stress resilience. Neurobiol Stress. 2014 Oct 15;1:44-59. doi: 10.1016/j.ynstr.2014.10.001. eCollection 2015 Jan. PMID: 27589660; PMCID: PMC4721318.
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Neurobiol Stress. 2014 Oct 15;1:44-59. doi: 10.1016/j.ynstr.2014.10.001. eCollection 2015 Jan.

Glucocorticoids, epigenetic control and stress resilience.

Neurobiology of stress

Johannes M H M Reul, Andrew Collins, Richard S Saliba, Karen R Mifsud, Sylvia D Carter, Maria Gutierrez-Mecinas, Xiaoxiao Qian, Astrid C E Linthorst

Affiliations

  1. Neuro-Epigenetics Research Group, School of Clinical Sciences, University of Bristol, Dorothy Hodgkin Building, Whitson Street, Bristol BS1 3NY, United Kingdom.
  2. Neurobiology of Stress and Behaviour Research Group, School of Clinical Sciences, University of Bristol, Dorothy Hodgkin Building, Whitson Street, Bristol BS1 3NY, United Kingdom.

PMID: 27589660 PMCID: PMC4721318 DOI: 10.1016/j.ynstr.2014.10.001

Abstract

Glucocorticoid hormones play a pivotal role in the response to stressful challenges. The surge in glucocorticoid hormone secretion after stress needs to be tightly controlled with characteristics like peak height, curvature and duration depending on the nature and severity of the challenge. This is important as chronic hyper- or hypo-responses are detrimental to health due to increasing the risk for developing a stress-related mental disorder. Proper glucocorticoid responses to stress are critical for adaptation. Therefore, the tight control of baseline and stress-evoked glucocorticoid secretion are important constituents of an organism's resilience. Here, we address a number of mechanisms that illustrate the multitude and complexity of measures safeguarding the control of glucocorticoid function. These mechanisms include the control of mineralocorticoid (MR) and glucocorticoid receptor (GR) occupancy and concentration, the dynamic control of free glucocorticoid hormone availability by corticosteroid-binding globulin (CBG), and the control exerted by glucocorticoids at the signaling, epigenetic and genomic level on gene transcriptional responses to stress. We review the beneficial effects of regular exercise on HPA axis and sleep physiology, and cognitive and anxiety-related behavior. Furthermore, we describe that, possibly through changes in the GABAergic system, exercise reduces the impact of stress on a signaling pathway specifically in the dentate gyrus that is strongly implicated in the behavioral response to that stressor. These observations underline the impact of life style on stress resilience. Finally, we address how single nucleotide polymorphisms (SNPs) affecting glucocorticoid action can compromise stress resilience, which becomes most apparent under conditions of childhood abuse.

Keywords: CBG; Exercise; Glucocorticoid receptor; HPA axis; Mineralocorticoid receptor; PTSD

References

  1. Neurobiol Aging. 1988 May-Jun;9(3):253-60 - PubMed
  2. Physiol Behav. 1989 Aug;46(2):229-37 - PubMed
  3. J Steroid Biochem Mol Biol. 1991;40(4-6):685-8 - PubMed
  4. Biol Psychiatry. 2008 Jun 15;63(12):1103-10 - PubMed
  5. Child Dev. 2015 Jan-Feb;86(1):303-9 - PubMed
  6. Mol Endocrinol. 1989 Nov;3(11):1886-94 - PubMed
  7. Neuropsychobiology. 1985;14(1):5-12 - PubMed
  8. Neurobiol Learn Mem. 2010 Nov;94(4):530-7 - PubMed
  9. Endocr Rev. 1998 Jun;19(3):269-301 - PubMed
  10. Neuron. 2013 Feb 20;77(4):606-23 - PubMed
  11. Mol Cell Biol. 2006 Oct;26(19):7236-45 - PubMed
  12. Brain Res. 2008 Mar 14;1199:148-58 - PubMed
  13. Electroencephalogr Clin Neurophysiol. 1984 Apr;57(4):347-53 - PubMed
  14. Br J Psychiatry. 1994 Oct;165(4):457-65 - PubMed
  15. J Affect Disord. 2010 Sep;125(1-3):249-55 - PubMed
  16. Can J Psychiatry. 2013 Feb;58(2):76-83 - PubMed
  17. Am J Physiol. 1990 Nov;259(5 Pt 2):R998-1003 - PubMed
  18. Proc Natl Acad Sci U S A. 2012 Oct 16;109 Suppl 2:17180-5 - PubMed
  19. CNS Drug Rev. 2007 Winter;13(4):475-501 - PubMed
  20. Ann N Y Acad Sci. 2011 May;1226:14-33 - PubMed
  21. Neuroendocrinology. 2007;86(1):26-37 - PubMed
  22. Physiol Behav. 2012 Jul 16;106(5):691-700 - PubMed
  23. Dev Neurobiol. 2012 Jun;72(6):878-90 - PubMed
  24. Neuroscience. 1998 Jun;84(4):1025-39 - PubMed
  25. Hippocampus. 1993 Apr;3(2):183-92 - PubMed
  26. Epigenomics. 2013 Apr;5(2):109-12 - PubMed
  27. J Appl Physiol Respir Environ Exerc Physiol. 1979 Dec;47(6):1278-83 - PubMed
  28. Proc Natl Acad Sci U S A. 1999 Nov 9;96(23):13427-31 - PubMed
  29. Eur J Neurosci. 2002 Dec;16(12):2441-52 - PubMed
  30. Psychoneuroendocrinology. 1987;12(2):83-105 - PubMed
  31. Endocrinology. 2006 Jun;147(6):2909-15 - PubMed
  32. Br J Psychiatry. 1994 Oct;165(4):447-56 - PubMed
  33. Neurosci Biobehav Rev. 2001 Mar;25(2):117-42 - PubMed
  34. Psychoneuroendocrinology. 2008 Jul;33(6):693-710 - PubMed
  35. Endocrinology. 1985 Dec;117(6):2505-11 - PubMed
  36. Am J Psychiatry. 2010 Feb;167(2):190-7 - PubMed
  37. Front Psychiatry. 2014 Jan 22;5:5 - PubMed
  38. J Steroid Biochem Mol Biol. 1991;40(4-6):755-62 - PubMed
  39. Eur J Neurosci. 2005 Oct;22(7):1691-700 - PubMed
  40. Eur J Neurosci. 2003 May;17(10):2171-9 - PubMed
  41. Behav Neurosci. 1992 Feb;106(1):62-71 - PubMed
  42. Am J Psychiatry. 2001 Apr;158(4):575-81 - PubMed
  43. Brain Behav Immun. 2011 Oct;25(7):1305-15 - PubMed
  44. Endocr Rev. 1990 Feb;11(1):65-79 - PubMed
  45. Endocrinology. 1995 Jun;136(6):2678-88 - PubMed
  46. Brain Res. 1998 Mar 9;786(1-2):11-7 - PubMed
  47. Horm Behav. 2003 Jan;43(1):124-31 - PubMed
  48. J Psychiatr Res. 2012 Jan;46(1):72-9 - PubMed
  49. Transl Psychiatry. 2014 Apr 08;4:e381 - PubMed
  50. Pharmacol Biochem Behav. 2008 Aug;90(2):163-73 - PubMed
  51. Endocrinology. 2010 Feb;151(2):649-59 - PubMed
  52. Ann N Y Acad Sci. 2001 Mar;933:265-77 - PubMed
  53. Ageing Res Rev. 2005 May;4(2):141-94 - PubMed
  54. Trends Pharmacol Sci. 1998 Aug;19(8):317-21 - PubMed
  55. Epigenetics. 2009 Oct 1;4(7):434-9 - PubMed
  56. Int J Neuropsychopharmacol. 2010 Jun;13(5):649-60 - PubMed
  57. Arch Gen Psychiatry. 1988 Jun;45(6):577-9 - PubMed
  58. Proc Natl Acad Sci U S A. 2000 Dec 19;97(26):14742-7 - PubMed
  59. Endocrinology. 2012 Sep;153(9):4346-53 - PubMed
  60. J Neurosci. 2011 Oct 5;31(40):14436-49 - PubMed
  61. Science. 1987 Jul 17;237(4812):268-75 - PubMed
  62. JAMA. 2008 Mar 19;299(11):1291-305 - PubMed
  63. Physiol Behav. 2012 Jul 16;106(5):689-90 - PubMed
  64. Trends Neurosci. 1992 Jan;15(1):25-30 - PubMed
  65. Neuroendocrinology. 1988 Feb;47(2):109-15 - PubMed
  66. Lancet. 1983 Jul 9;2(8341):98-9 - PubMed
  67. Cochrane Database Syst Rev. 2013 Sep 12;(9):CD004366 - PubMed
  68. Curr Opin Pharmacol. 2002 Feb;2(1):23-33 - PubMed
  69. Dis Markers. 2011;30(2-3):101-10 - PubMed
  70. Eur J Pharmacol. 1983 Aug 19;92(1-2):99-103 - PubMed
  71. Neuron. 1994 Dec;13(6):1457-62 - PubMed
  72. Psychol Bull. 2009 Nov;135(6):885-908 - PubMed
  73. Endocrinology. 2009 Sep;150(9):4170-9 - PubMed
  74. J Psychosom Res. 1989;33(5):537-47 - PubMed
  75. J Psychopharmacol. 2010 May;24(5):745-56 - PubMed
  76. Biol Psychiatry. 1995 Sep 15;38(6):391-403 - PubMed
  77. Depress Anxiety. 1996-1997;4(3):100-10 - PubMed
  78. J Psychosom Res. 1993 Sep;37(6):565-74 - PubMed
  79. Curr Opin Pharmacol. 2011 Aug;11(4):332-7 - PubMed
  80. Acta Physiol (Oxf). 2014 Jan;210(1):46-57 - PubMed
  81. J Steroid Biochem Mol Biol. 1991;40(1-3):63-9 - PubMed
  82. Eur J Pharmacol. 1985 Sep 24;115(2-3):211-7 - PubMed
  83. Behav Brain Res. 2004 Dec 6;155(2):197-206 - PubMed
  84. Endocrinology. 1993 Jan;132(1):161-8 - PubMed
  85. Behav Neurosci. 1991 Dec;105(6):798-803 - PubMed
  86. Proc Natl Acad Sci U S A. 2001 Oct 23;98(22):12790-5 - PubMed
  87. Am J Psychiatry. 2011 Oct;168(10):1107-16 - PubMed
  88. Psychoneuroendocrinology. 2010 Nov;35(10):1454-61 - PubMed
  89. Arch Gen Psychiatry. 2009 Mar;66(3):305-11 - PubMed
  90. Brain Res. 1993 Mar 5;605(1):18-24 - PubMed
  91. Science. 1984 Dec 14;226(4680):1342-4 - PubMed
  92. BMC Med Genomics. 2014 Mar 11;7:13 - PubMed
  93. Exp Neurol. 2012 Jan;233(1):3-11 - PubMed
  94. Mol Cell. 2006 Nov 3;24(3):367-81 - PubMed
  95. PLoS One. 2009;4(1):e4330 - PubMed
  96. JAMA. 2014 Jun 18;311(23):2432-3 - PubMed
  97. Endocrinology. 2003 Jul;144(7):3012-23 - PubMed
  98. J Neurochem. 2007 May;101(3):815-28 - PubMed
  99. Stress. 2014 Sep;17(5):445-50 - PubMed
  100. Endocrinology. 1990 Aug;127(2):900-6 - PubMed
  101. Endocrinology. 1993 Jul;133(1):312-20 - PubMed
  102. Eur J Neurosci. 1997 Apr;9(4):637-42 - PubMed
  103. J Endocrinol. 1987 Dec;115(3):459-67 - PubMed
  104. J Neurosci. 2011 May 11;31(19):7111-21 - PubMed
  105. J Neurosci. 2007 Nov 14;27(46):12732-42 - PubMed
  106. Neuropharmacology. 2014 May;80:115-32 - PubMed
  107. Endocrinology. 1988 Feb;122(2):444-9 - PubMed
  108. Brain Res. 2009 Oct 13;1293:91-100 - PubMed
  109. J Steroid Biochem. 1986 Jan;24(1):269-72 - PubMed
  110. Stress. 2008 Mar;11(2):88-100 - PubMed
  111. J Affect Disord. 2010 Nov;126(3):411-4 - PubMed
  112. Behav Neurosci. 2008 Apr;122(2):282-92 - PubMed
  113. Prog Neurobiol. 2006 May;79(1):1-48 - PubMed
  114. Eur J Appl Physiol. 2001 Jun;84(6):521-6 - PubMed
  115. Endocrinol Jpn. 1987 Apr;34(2):213-20 - PubMed
  116. Arch Gen Psychiatry. 2011 Sep;68(9):901-10 - PubMed
  117. Neuropsychopharmacology. 2010 Jul;35(8):1684-92 - PubMed
  118. Mol Endocrinol. 2010 Mar;24(3):511-25 - PubMed
  119. Nat Neurosci. 2004 Aug;7(8):847-54 - PubMed
  120. J Biol Chem. 1990 Dec 25;265(36):22067-70 - PubMed
  121. Eur J Neurosci. 2008 May;27(10):2701-13 - PubMed
  122. Trends Neurosci. 1997 Feb;20(2):78-84 - PubMed
  123. Dev Psychopathol. 2012 Nov;24(4):1417-25 - PubMed
  124. Nat Neurosci. 2003 Oct;6(10):1100-7 - PubMed
  125. JAMA. 2000 Aug 2;284(5):592-7 - PubMed
  126. Br J Psychiatry. 2010 Nov;197(5):378-85 - PubMed
  127. Endocr Rev. 1984 Winter;5(1):25-44 - PubMed
  128. Mol Psychiatry. 2009 Mar;14(3):261-8 - PubMed
  129. Endocrinology. 2011 Oct;152(10):3738-48 - PubMed
  130. Eur J Pharmacol. 2000 Sep 29;405(1-3):235-49 - PubMed
  131. Eur J Neurosci. 2002 Mar;15(6):1048-60 - PubMed
  132. Nat Rev Neurosci. 2005 Jun;6(6):463-75 - PubMed
  133. Psychoneuroendocrinology. 2007 Aug;32 Suppl 1:S21-5 - PubMed
  134. Curr Opin Pharmacol. 2011 Aug;11(4):326-31 - PubMed
  135. Neurosci Biobehav Rev. 1992 Winter;16(4):525-34 - PubMed
  136. Front Neuroendocrinol. 2003 Jul;24(3):151-80 - PubMed
  137. Mol Cell Endocrinol. 2012 Mar 24;350(2):299-309 - PubMed
  138. Arch Gen Psychiatry. 2012 Jul;69(7):722-31 - PubMed
  139. Endocrinology. 1990 Aug;127(2):907-15 - PubMed
  140. Hippocampus. 1994 Jun;4(3):374-91 - PubMed
  141. Endocrinology. 2008 Jul;149(7):3244-53 - PubMed
  142. J Neurosci. 1995 Apr;15(4):2920-34 - PubMed
  143. Nat Neurosci. 2009 Mar;12(3):342-8 - PubMed
  144. Mol Cell. 2000 Jun;5(6):905-15 - PubMed
  145. Prog Neuropsychopharmacol Biol Psychiatry. 2011 Jan 15;35(1):252-6 - PubMed
  146. Depress Anxiety. 2001;14(1):19-28 - PubMed
  147. Horm Metab Res. 1992 Nov;24(11):511-5 - PubMed
  148. Neuropsychopharmacology. 2011 Sep;36(10):1982-91 - PubMed
  149. J Neurosci Res. 1988 Sep;21(1):88-94 - PubMed
  150. J Psychiatr Res. 2014 Apr;51:93-9 - PubMed
  151. Clin Psychol Rev. 2001 Feb;21(1):33-61 - PubMed
  152. Eur Neuropsychopharmacol. 2014 Jun;24(6):907-18 - PubMed
  153. Neuroendocrinology. 1994 Nov;60(5):509-19 - PubMed
  154. J Neurophysiol. 1997 Mar;77(3):1624-9 - PubMed
  155. Eur J Neurosci. 2008 Jul;28(2):389-98 - PubMed
  156. Genes Dev. 2000 Dec 1;14(23):3003-13 - PubMed
  157. BMJ. 2012 Jun 06;344:e2758 - PubMed
  158. Endocrine. 2005 Dec;28(3):325-32 - PubMed
  159. Psychoneuroendocrinology. 2009 Dec;34 Suppl 1:S186-95 - PubMed
  160. Genes Brain Behav. 2014 Jan;13(1):25-37 - PubMed
  161. Nat Genet. 2004 Dec;36(12):1319-25 - PubMed
  162. J Neuroendocrinol. 2009 Feb;21(2):132-40 - PubMed
  163. J Neurosci. 1997 Jun 1;17(11):4448-60 - PubMed
  164. Steroids. 2014 Dec;92:62-73 - PubMed
  165. J Neurosci. 1989 Sep;9(9):3072-82 - PubMed
  166. Endocrinology. 1985 Nov;117(5):1803-12 - PubMed
  167. Proc Natl Acad Sci U S A. 2011 Aug 16;108(33):13806-11 - PubMed
  168. Nature. 1985 Dec 19-1986 Jan 1;318(6047):635-41 - PubMed
  169. Endocrinology. 1994 Aug;135(2):520-32 - PubMed
  170. Cell. 2000 Oct 13;103(2):263-71 - PubMed
  171. J Neurosci. 2001 Jul 1;21(13):4822-9 - PubMed

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