Knockdown of steroid receptors in the central nucleus of the amygdala induces heightened pain behaviors in the rat

Neuropharmacology

Volumn 93, Issue , 2015, Pages 116-123

  Johnson, Anthony C ^a   Greenwood Van Meerveld, Beverley ^a,b  

^a UNIVERSITY OF OKLAHOMA HEALTH SCIENCES CENTER   (United States)

^b UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

Author keywords

Amygdala; Glucocorticoid receptor; Mineralocorticoid receptor; Nociception; Oligodeoxynucleotide; Rat

Indexed keywords

ANTISENSE OLIGODEOXYNUCLEOTIDE; CHOLESTEROL; CORTICOSTERONE; CORTICOTROPIN RELEASING FACTOR; GLUCOCORTICOID RECEPTOR; MINERALOCORTICOID RECEPTOR; MINERALOCORTICOID;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CENTRAL NUCLEUS (AMYGDALA); COLON DILATATION; CONTROLLED STUDY; GENE SILENCING; MALE; MOTOR PERFORMANCE; NOCICEPTION; NONHUMAN; PAIN; PROTEIN EXPRESSION; RAT; VISCERAL PAIN; ADVERSE EFFECTS; ANALYSIS OF VARIANCE; ANIMAL; DEFICIENCY; DRUG EFFECTS; FISCHER 344 RAT; GENETICS; METABOLISM; PHYSIOLOGY; STIMULATION;

ANALYSIS OF VARIANCE; ANIMALS; CENTRAL AMYGDALOID NUCLEUS; CHOLESTEROL; CORTICOSTERONE; MALE; MINERALOCORTICOIDS; NOCICEPTION; OLIGODEOXYRIBONUCLEOTIDES, ANTISENSE; PAIN; PHYSICAL STIMULATION; RATS; RATS, INBRED F344; RECEPTORS, GLUCOCORTICOID; RECEPTORS, MINERALOCORTICOID; VISCERAL PAIN;

EID: 84922697870     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2015.01.018     Document Type: Article

References (68)

1. C. Anacker, K.J. O'Donnell, and M.J. Meaney Early life adversity and the epigenetic programming of hypothalamic-pituitary-adrenal function Dialogues Clin. Neurosci. 16 2014 321 333
2. S.M. Berman, B.D. Naliboff, B. Suyenobu, J.S. Labus, J. Stains, G. Ohning, L. Kilpatrick, J.A. Bueller, K. Ruby, J. Jarcho, and E.A. Mayer Reduced brainstem inhibition during anticipated pelvic visceral pain correlates with enhanced brain response to the visceral stimulus in women with irritable bowel syndrome J. Neurosci.: off. J. Soc. Neurosci. 28 2008 349 359
3. S. Bhatnagar, and M. Dallman Neuroanatomical basis for facilitation of hypothalamic-pituitary-adrenal responses to a novel stressor after chronic stress Neuroscience 84 1998 1025 1039
4. B. Bonaz, M. Baciu, E. Papillon, R. Bost, N. Gueddah, J.F. Le Bas, J. Fournet, and C. Segebarth Central processing of rectal pain in patients with irritable bowel syndrome: an fMRI study Am. J. Gastroenterol. 97 2002 654 661
5. M. Burgmer, M. Gaubitz, C. Konrad, M. Wrenger, S. Hilgart, G. Heuft, and B. Pfleiderer Decreased gray matter volumes in the cingulo-frontal cortex and the amygdala in patients with fibromyalgia Psychosom. Med. 71 2009 566 573
6. L. Chang, S. Sundaresh, J. Elliott, P.A. Anton, P. Baldi, A. Licudine, M. Mayer, T. Vuong, M. Hirano, B.D. Naliboff, V.Z. Ameen, and E.A. Mayer Dysregulation of the hypothalamic-pituitary-adrenal (HPA) axis in irritable bowel syndrome Neurogastroenterol. Motil.: off. J. Eur. Gastrointest. Motil. Soc. 21 2009 149 159
7. R.S. Choung, and G.R. Locke 3rd Epidemiology of IBS Gastroenterol. Clin. N. Am. 40 2011 1 10
8. I. Cifre, C. Sitges, D. Fraiman, M.A. Munoz, P. Balenzuela, A. Gonzalez-Roldan, M. Martinez-Jauand, N. Birbaumer, D.R. Chialvo, and P. Montoya Disrupted functional connectivity of the pain network in fibromyalgia Psychosom. Med. 74 2012 55 62
9. E.R. De Kloet, and J.M. Reul Feedback action and tonic influence of corticosteroids on brain function: a concept arising from the heterogeneity of brain receptor systems Psychoneuroendocrinology 12 1987 83 105
10. T.G. Dinan, E.M. Quigley, S.M. Ahmed, P. Scully, S. O'Brien, L. O'Mahony, S. O'Mahony, F. Shanahan, and P.W. Keeling Hypothalamic-pituitary-gut axis dysregulation in irritable bowel syndrome: plasma cytokines as a potential biomarker? Gastroenterology 130 2006 304 311
11. F. Dong, W. Xie, J.A. Strong, and J.M. Zhang Mineralocorticoid receptor blocker eplerenone reduces pain behaviors in vivo and decreases excitability in small-diameter sensory neurons from local inflamed dorsal root ganglia in vitro Anesthesiology 117 2012 1102 1112
12. S. Elsenbruch, C. Rosenberger, U. Bingel, M. Forsting, M. Schedlowski, and E.R. Gizewski Patients with irritable bowel syndrome have altered emotional modulation of neural responses to visceral stimuli Gastroenterology 139 2010 1310 1319
13. M. Engelmann, R. Landgraf, P. Lorscher, C. Conzelmann, J.C. Probst, F. Holsboer, and J.M. Reul Downregulation of brain mineralocorticoid and glucocorticoid receptor by antisense oligodeoxynucleotide treatment fails to alter spatial navigation in rats Eur. J. Pharmacol. 361 1998 17 26
14. L.F. Ferrari, E. Levine, and J.D. Levine Independent contributions of alcohol and stress axis hormones to painful peripheral neuropathy Neuroscience 228 2013 409 417
15. Y. Fu, and V. Neugebauer Differential mechanisms of CRF1 and CRF2 receptor functions in the amygdala in pain-related synaptic facilitation and behavior J. Neurosci.: off. J. Soc. Neurosci. 28 2008 3861 3876
16. A. Geiss, N. Rohleder, and F. Anton Evidence for an association between an enhanced reactivity of interleukin-6 levels and reduced glucocorticoid sensitivity in patients with fibromyalgia Psychoneuroendocrinology 37 2012 671 684
17. T.S. Gray Amygdaloid CRF pathways. Role in autonomic, neuroendocrine, and behavioral responses to stress Ann. N. Y. Acad. Sci. 697 1993 53 60
18. T.S. Gray, and E.W. Bingaman The amygdala: corticotropin-releasing factor, steroids, and stress Crit. Rev. Neurobiol. 10 1996 155 168
19. B. Greenwood-Van Meerveld, M. Gibson, W. Gunter, J. Shepard, R. Foreman, and D. Myers Stereotaxic delivery of corticosterone to the amygdala modulates colonic sensitivity in rats Brain Res. 893 2001 135 142
20. X. Gu, L. Peng, D. Yang, Q. Ma, Y. Zheng, C. Liu, B. Zhu, L. Song, X. Sun, and Z. Ma The respective and interaction effects of spinal GRs and MRs on radicular pain induced by chronic compression of the dorsal root ganglion in the rat Brain Res. 1396 2011 88 95
21. F. Han, J. Ding, and Y. Shi Expression of amygdala mineralocorticoid receptor and glucocorticoid receptor in the single-prolonged stress rats BMC Neurosci. 15 2014 77
22. S. Hong, G. Zheng, and J.W. Wiley Epigenetic regulation of genes that modulate chronic stress-induced visceral pain in the peripheral nervous system Gastroenterology 148 1 2015 148 157.e7
23. P. Hu, J. Liu, J. Zhao, X.R. Qi, C.C. Qi, P.J. Lucassen, and J.N. Zhou All-trans retinoic acid-induced hypothalamus-pituitary-adrenal hyperactivity involves glucocorticoid receptor dysregulation Transl. Psychiatry 3 2013 e336
24. K.B. Jensen, R. Loitoile, E. Kosek, F. Petzke, S. Carville, P. Fransson, H. Marcus, S.C. Williams, E. Choy, Y. Mainguy, O. Vitton, R.H. Gracely, R. Gollub, M. Ingvar, and J. Kong Patients with fibromyalgia display less functional connectivity in the brain's pain inhibitory network Mol. Pain 8 2012 32
25. G. Ji, Y. Fu, K.A. Ruppert, and V. Neugebauer Pain-related anxiety-like behavior requires CRF1 receptors in the amygdala Mol. Pain 3 2007 13
26. G. Ji, and V. Neugebauer Differential effects of CRF1 and CRF2 receptor antagonists on pain-related sensitization of neurons in the central nucleus of the amygdala J. Neurophysiol. 97 2007 3893 3904
27. G. Ji, and V. Neugebauer Pro- and anti-nociceptive effects of corticotropin-releasing factor (CRF) in central amygdala neurons are mediated through different receptors J. Neurophysiol. 99 2008 1201 1212
28. M. Joels, and T.Z. Baram The neuro-symphony of stress Nat. Rev. Neurosci. 10 2009 459 466
29. A.C. Johnson, L. Tran, J. Schulkin, and B. Greenwood-Van Meerveld Importance of stress receptor-mediated mechanisms in the amygdala on visceral pain perception in an intrinsically anxious rat Neurogastroenterol. Motil.: off. J. Eur. Gastrointest. Motil. Soc. 24 2012 479 486 e219
30. J.Y. Kim, S.H. Kim, J. Seo, S.H. Kim, S.W. Han, E.J. Nam, S.K. Kim, H.J. Lee, S.J. Lee, Y.T. Kim, and Y. Chang Increased power spectral density in resting-state pain-related brain networks in fibromyalgia Pain 154 2013 1792 1797
31. K.J. Livak, and T.D. Schmittgen Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method Methods 25 2001 402 408
32. G.F. Longstreth, W.G. Thompson, W.D. Chey, L.A. Houghton, F. Mearin, and R.C. Spiller Functional bowel disorders Gastroenterology 130 2006 1480 1491
33. S.J. Lupien, B.S. McEwen, M.R. Gunnar, and C. Heim Effects of stress throughout the lifespan on the brain, behaviour and cognition Nat. Rev. Neurosci. 10 2009 434 445
34. J.A. Macedo, J. Hesse, J.D. Turner, J. Meyer, D.H. Hellhammer, and C.P. Muller Glucocorticoid sensitivity in fibromyalgia patients: decreased expression of corticosteroid receptors and glucocorticoid-induced leucine zipper Psychoneuroendocrinology 33 2008 799 809
35. S. Makino, P.W. Gold, and J. Schulkin Corticosterone effects on corticotropin-releasing hormone mRNA in the central nucleus of the amygdala and the parvocellular region of the paraventricular nucleus of the hypothalamus Brain Res. 640 1994 105 112
36. P.O. McGowan Epigenomic mechanisms of early adversity and HPA dysfunction: considerations for PTSD research Front. Psychiatry 4 2013 110
37. S.A. McLean, D.A. Williams, P.K. Stein, R.E. Harris, A.K. Lyden, G. Whalen, K.M. Park, I. Liberzon, A. Sen, R.H. Gracely, J.N. Baraniuk, and D.J. Clauw Cerebrospinal fluid corticotropin-releasing factor concentration is associated with pain but not fatigue symptoms in patients with fibromyalgia Neuropsychopharmacol.: off. Publ. Am. Coll. Neuropsychopharmacol. 31 2006 2776 2782
38. B. Myers, K. Dittmeyer, and B. Greenwood-Van Meerveld Involvement of amygdaloid corticosterone in altered visceral and somatic sensation Behav. Brain Res. 181 2007 163 167
39. B. Myers, and B. Greenwood-Van Meerveld Corticosteroid receptor-mediated mechanisms in the amygdala regulate anxiety and colonic sensitivity Am. J. Physiol. Gastrointest. Liver Physiol. 292 2007 G1622 G1629
40. B. Myers, and B. Greenwood-Van Meerveld Divergent effects of amygdala glucocorticoid and mineralocorticoid receptors in the regulation of visceral and somatic pain Am. J. Physiol. Gastrointest. Liver Physiol. 298 2010 G295 G303
41. B. Myers, and B. Greenwood-Van Meerveld Elevated corticosterone in the amygdala leads to persistent increases in anxiety-like behavior and pain sensitivity Behav. Brain Res. 214 2010 465 469
42. B.D. Naliboff, S. Berman, L. Chang, S.W. Derbyshire, B. Suyenobu, B.A. Vogt, M. Mandelkern, and E.A. Mayer Sex-related differences in IBS patients: central processing of visceral stimuli Gastroenterology 124 2003 1738 1747
43. G. Paxinos, and C. Watson The Rat Brain in Stereotaxic Coordinates 2007 Academic Press/Elsevier Amsterdam; Boston
44. J.M. Reul Making memories of stressful events: a journey along epigenetic, gene transcription, and signaling pathways Front. Psychiatry 5 2014 5
45. J.M. Reul, and E.R. de Kloet Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation Endocrinology 117 1985 2505 2511
46. J.M.H.M. Reul, A. Collins, R.S. Saliba, K.R. Mifsud, S.D. Carter, M. Gutierrez-Mecinas, X. Qian, and A.C.E. Linthorst Glucocorticoids, epigenetic control and stress resilience Neurobiol. Stress 1 2015 44 59
47. W. Riedel, U. Schlapp, S. Leck, P. Netter, and G. Neeck Blunted ACTH and cortisol responses to systemic injection of corticotropin-releasing hormone (CRH) in fibromyalgia: role of somatostatin and CRH-binding protein Ann. N. Y. Acad. Sci. 966 2002 483 490
48. A. Riedl, M. Schmidtmann, A. Stengel, M. Goebel, A.S. Wisser, B.F. Klapp, and H. Monnikes Somatic comorbidities of irritable bowel syndrome: a systematic analysis J. Psychosom. Res. 64 2008 573 582
49. R.R. Sakai, B.S. McEwen, S.J. Fluharty, and L.Y. Ma The amygdala: site of genomic and nongenomic arousal of aldosterone-induced sodium intake Kidney Int. 57 2000 1337 1345
50. R.M. Sapolsky, B.S. McEwen, and T.C. Rainbow Quantitative autoradiography of [3H]corticosterone receptors in rat brain Brain Res. 271 1983 331 334
51. J. Schmid, N. Theysohn, F. Gass, S. Benson, C. Gramsch, M. Forsting, E.R. Gizewski, and S. Elsenbruch Neural mechanisms mediating positive and negative treatment expectations in visceral pain: a functional magnetic resonance imaging study on placebo and nocebo effects in healthy volunteers Pain 154 2013 2372 2380
52. J. Schulkin, P.W. Gold, and B.S. McEwen Induction of corticotropin-releasing hormone gene expression by glucocorticoids: implication for understanding the states of fear and anxiety and allostatic load Psychoneuroendocrinology 23 1998 219 243
53. D.A. Seminowicz, J.S. Labus, J.A. Bueller, K. Tillisch, B.D. Naliboff, M.C. Bushnell, and E.A. Mayer Regional gray matter density changes in brains of patients with irritable bowel syndrome Gastroenterology 139 2010 48 57 e42
54. J.D. Shepard, K.W. Barron, and D.A. Myers Corticosterone delivery to the amygdala increases corticotropin-releasing factor mRNA in the central amygdaloid nucleus and anxiety-like behavior Brain Res. 861 2000 288 295
55. J.D. Shepard, K.W. Barron, and D.A. Myers Stereotaxic localization of corticosterone to the amygdala enhances hypothalamo-pituitary-adrenal responses to behavioral stress Brain Res. 963 2003 203 213
56. J.D. Shepard, J. Schulkin, and D.A. Myers Chronically elevated corticosterone in the amygdala increases corticotropin releasing factor mRNA in the dorsolateral bed nucleus of stria terminalis following duress Behav. Brain Res. 174 2006 193 196
57. A.M. Stankiewicz, A.H. Swiergiel, and P. Lisowski Epigenetics of stress adaptations in the brain Brain Res. Bull. 98 2013 76 92
58. L.W. Swanson, and G.D. Petrovich What is the amygdala? Trends Neurosci. 21 1998 323 331
59. K. Tillisch, E.A. Mayer, and J.S. Labus Quantitative meta-analysis identifies brain regions activated during rectal distension in irritable bowel syndrome Gastroenterology 140 2011 91 100
60. L. Tran, A. Chaloner, A.H. Sawalha, and B. Greenwood Van-Meerveld Importance of epigenetic mechanisms in visceral pain induced by chronic water avoidance stress Psychoneuroendocrinology 38 2013 898 906
61. L. Tran, and B. Greenwood-Van Meerveld Altered expression of glucocorticoid receptor and corticotropin-releasing factor in the central amygdala in response to elevated corticosterone Behav. Brain Res. 234 2012 380 385
62. L. Tran, J. Schulkin, and B. Greenwood-Van Meerveld Importance of CRF receptor-mediated mechanisms of the bed nucleus of the stria terminalis in the processing of anxiety and pain Neuropsychopharmacol.: off. Publ. Am. Coll. Neuropsychopharmacol. 39 11 2014 2633 2645
63. L. Tran, J. Schulkin, C.O. Ligon, and B. Greenwood Van-Meerveld Epigenetic modulation of chronic anxiety and pain by histone deacetylation Mol. Psychiatry 2014 10.1038/mp.2014.122
64. L. Tran, B. Wiskur, and B. Greenwood-Van Meerveld The role of the anteriolateral bed nucleus of the stria terminalis in stress-induced nociception Am. J. Physiol. Gastrointest. Liver Physiol. 302 2012 G1301 G1309
65. J. Vandesompele, K. De Preter, F. Pattyn, B. Poppe, N. Van Roy, A. De Paepe, and F. Speleman Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes Genome Biol. 3 2002 RESEARCH0034
66. S. Wang, G. Lim, Q. Zeng, B. Sung, Y. Ai, G. Guo, L. Yang, and J. Mao Expression of central glucocorticoid receptors after peripheral nerve injury contributes to neuropathic pain behaviors in rats J. Neurosci.: off. J. Soc. Neurosci. 24 2004 8595 8605
67. S. Wang, G. Lim, Q. Zeng, B. Sung, L. Yang, and J. Mao Central glucocorticoid receptors modulate the expression and function of spinal NMDA receptors after peripheral nerve injury J. Neurosci.: off. J. Soc. Neurosci. 25 2005 488 495
68. C.H. Wilder-Smith, D. Schindler, K. Lovblad, S.M. Redmond, and A. Nirkko Brain functional magnetic resonance imaging of rectal pain and activation of endogenous inhibitory mechanisms in irritable bowel syndrome patient subgroups and healthy controls Gut 53 2004 1595 1601