The realization of the brain-gut interactions with corticotropin-releasing factor and glucocorticoids

Current Neuropharmacology

Volumn 14, Issue 8, 2016, Pages 876-881

  Filaretova, Ludmila ^a   Bagaeva, Tatiana ^a  

^a PAVLOV INSTITUTE OF PHYSIOLOGY   (Russian Federation)

Author keywords

Brain gut axis; Corticotropin releasing factor; Gastric injury; Gastric mucosa; Gastroprotection; Glucocorticoids; Hypothalamic pituitary adrenocortical axis; Stress

Indexed keywords

CORTICOTROPIN; CORTICOTROPIN RELEASING FACTOR; GLUCOCORTICOID;

BRAIN GUT AXIS; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; NERVOUS SYSTEM; NONHUMAN; REVIEW; STOMACH PROTECTION; STOMACH ULCER; STRESS; ANIMAL; BRAIN; GASTROINTESTINAL TRACT; MENTAL STRESS; METABOLISM;

ANIMALS; BRAIN; CORTICOTROPIN-RELEASING HORMONE; GASTROINTESTINAL TRACT; GLUCOCORTICOIDS; HUMANS; STRESS, PSYCHOLOGICAL;

EID: 85010297646     PISSN: 1570159X     EISSN: 18756190     Source Type: Journal    
DOI: 10.2174/1570159X14666160614094234     Document Type: Review

References (71)

1. Bonaz, B.L.; Bernstein, C.N. Brain-gut interactions in inflammatory bowel disease. Gastroenterology, 2013, 144(1), 36-49. [http://dx.doi.org/10.1053/j.gastro.2012.10.003] [PMID: 23063970]
2. Filaretova, L. The hypothalamic-pituitary-adrenocortical system: Hormonal brain-gut interaction and gastroprotection. Auton. Neurosci., 2006, 125(1-2), 86-93. [http://dx.doi.org/10.1016/j.autneu.2006.01.005] [PMID: 16481222]
3. Holzer, P.; Farzi, A. Neuropeptides and the microbiota-gut-brain axis. Adv. Exp. Med. Biol., 2014, 817, 195-219. [http://dx.doi.org/10.1007/978-1-4939-0897-4_9] [PMID: 24997035]
4. Taché, Y.; Million, M. Role of corticotropin-releasing factor signaling in stress-related alterations of colonic motility and hyperalgesia. J. Neurogastroenterol. Motil., 2015, 21(1), 8-24. [http://dx.doi.org/10.5056/jnm14162] [PMID: 25611064]
5. Wood, J.D. The first nobel prize for integrated systems physiology: Ivan Petrovich Pavlov, 1904. Physiology (Bethesda), 2004, 19, 326-330. [http://dx.doi.org/10.1152/physiol.00034.2004] [PMID: 15546849]
6. Pavlov, I.P. Lectures on the Work of the Digestive Glands; Griffin: London, 1902.
7. Taché, Y.; Adelson, D.; Yang, H. TRH/TRH-R1 receptor signaling in the brain medulla as a pathway of vagally mediated gut responses during the cephalic phase. Curr. Pharm. Des., 2014, 20(16), 2725-2730. [http://dx.doi.org/10.2174/13816128113199990578] [PMID: 23886382]
8. Smith, G.P. Pavlov and integrative physiology. Am. J. Physiol. Regul. Integr. Comp. Physiol., 2000, 279(3), R743-R755. [PMID: 10956230]
9. Holtmann, G.; Talley, N.J. The stomach-brain axis. Best Pract. Res. Clin. Gastroenterol., 2014, 28(6), 967-979. [http://dx.doi.org/10.1016/j.bpg.2014.10.001] [PMID: 25439064]
10. Burokas, A.; Moloney, R.D.; Dinan, T.G.; Cryan, J.F. Microbiota regulation of the Mammalian gut-brain axis. Adv. Appl. Microbiol., 2015, 91, 1-62. [http://dx.doi.org/10.1016/bs.aambs.2015.02.001] [PMID: 25911232]
11. Saulnier, D.M.; Ringel, Y.; Heyman, M.B.; Foster, J.A.; Bercik, P.; Shulman, R.J.; Versalovic, J.; Verdu, E.F.; Dinan, T.G.; Hecht, G.; Guarner, F. The intestinal microbiome, probiotics and prebiotics in neurogastroenterology. Gut Microbes, 2013, 4(1), 17-27. [http://dx.doi.org/10.4161/gmic.22973] [PMID: 23202796]
12. Moloney, R.D.; Desbonnet, L.; Clarke, G.; Dinan, T.G.; Cryan, J.F. The microbiome: stress, health and disease. Mamm. Genome, 2014, 25(1-2), 49-74. [http://dx.doi.org/10.1007/s00335-013-9488-5] [PMID: 24281320]
13. Gunion, M.W.; Kauffman, G.L., Jr; Taché, Y. Intrahypothalamic corticotropin-releasing factor elevates gastric bicarbonate and inhibits stress ulcers in rats. Am. J. Physiol., 1990, 258(1 Pt 1), G152-G157. [PMID: 2301576]
14. Gunion, M.W.; Taché, Y. Intrahypothalamic microinfusion of corticotropin-releasing factor inhibits gastric acid secretion but increases secretion volume in rats. Brain Res., 1987, 411(1), 156-161. [http://dx.doi.org/10.1016/0006-8993(87)90693-7] [PMID: 3496936]
15. Konturek, P.C.; Brzozowski, T.; Konturek, S.J. Stress and the gut: pathophysiology, clinical consequences, diagnostic approach and treatment options. J. Physiol. Pharmacol., 2011, 62(6), 591-599. [PMID: 22314561]
16. Selye, H. A syndrome produced by diverse nocuous agents. Nature, 1936, 138, 32. [http://dx.doi.org/10.1038/138032a0]
17. Cannon, W.B. Bodily changes in pain, hunger, fear and rage, 2nd ed; Charles T. Branford Co.: Boston, 1953.
18. Szabo, S. Hans Selye and the development of the stress concept. Special reference to gastroduodenal ulcerogenesis. Ann. N. Y. Acad. Sci., 1998, 851, 19-27. [http://dx.doi.org/10.1111/j.1749-6632.1998.tb08972.x] [PMID: 9668601]
19. Szabó, S. Hans Selye 70 years later: steroids, stress ulcers & H. Pylori. Ideggyogy. Sz., 2014, 67(3-4), 91-94. [PMID: 26118247]
20. Szabo, S.; Tache, Y.; Somogyi, A. The legacy of Hans Selye and the origins of stress research: a retrospective 75 years after his landmark brief "letter" to the editor# of nature. Stress, 2012, 15(5), 472-478. [http://dx.doi.org/10.3109/10253890.2012.710919] [PMID: 22845714]
21. Hernandez, D.E.; Glavin, G.B. Neurobiology of stress ulcers; New York Academy of Sciences: New York, 1990.
22. Selye, H. The Story of the Adaption Syndrome; ACTA INC; Medical Publisher: Montreal, 1952.
23. Stengel, A.; Taché, Y. Corticotropin-releasing factor signaling and visceral response to stress. Exp. Biol. Med. (Maywood), 2010, 235(10), 1168-1178. [http://dx.doi.org/10.1258/ebm.2010.009347] [PMID: 20881321]
24. Selye, H. The Stress of Life; McGraw-Hill Book Co.: New York, 1956.
25. 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(4514), 1394-1397. [http://dx.doi.org/10.1126/science.6267699] [PMID: 6267699]
26. Selye, H. In Vivo. The case for supramolecular biology presented in six informal, illustrated lectures; Liveright: New York, 1967.
27. Murphy, H.M.; Wideman, C.H.; Brown, T.S. Plasma corticosterone levels and ulcer formation in rats with hippocampal lesions. Neuroendocrinology, 1979, 28(2), 123-130. [http://dx.doi.org/10.1159/000122852] [PMID: 431775]
28. Weiss, J.M. Effects of punishing the coping response (conflict) on stress pathology in rats. J. Comp. Physiol. Psychol., 1971, 77(1), 14-21. [http://dx.doi.org/10.1037/h0031582] [PMID: 5166074]
29. Black, H.E. The effects of steroids upon the gastrointestinal tract. Toxicol. Pathol., 1988, 16(2), 213-222. [http://dx.doi.org/10.1177/019262338801600214] [PMID: 3055231]
30. Bonfils, S.; Hardouin, J-P.; Rossi, G.; Richier, G.; Lambling, A. Les ulceration gastriques provoquees chez le rat blanc par la cortisone et la delta-cortisone. Arch. mal. app. digest., 1957, 46, 385-399.
31. Gray, S.J. The effect of steroids on the gastrointestinal tract. Am. J. Gastroenterol., 1958, 30(3), 266-268. [PMID: 13571202]
32. Gray, S.J. Stress and gastrointestinal tract. Am. J. Gastroenterol., 1964, 41, 243-247. [PMID: 14134420]
33. Gray, S.J.; Benson, J.A., Jr; Reifenstein, R.W. Chronic stress and peptic ulcer. I. Effect of corticotropin (ACTH) and cortisone on gastric secretion. J. Am. Med. Assoc., 1951, 147(16), 1529-1537. [http://dx.doi.org/10.1001/jama.1951.03670330021007] [PMID: 14873720]
34. Gray, S.J.; Benson, J.A., Jr; Spiro, H.M.; Reifenstein, R.W. Effects of ACTH and cortisone upon the stomach: its significance in the normal and in peptic ulcer. Gastroenterology, 1951, 19(4), 658-673. [PMID: 14897066]
35. Gray, S.J.; Ramsey, C.; Reifenstein, R.W.; Benson, J.A., Jr The significance of hormonal factors in the pathogenesis of peptic ulcer. Gastroenterology, 1953, 25(2), 156-172. [PMID: 13107915]
36. Messer, J.; Reitman, D.; Sacks, H.S.; Smith, H., Jr; Chalmers, T.C. Association of adrenocorticosteroid therapy and peptic-ulcer disease. N. Engl. J. Med., 1983, 309(1), 21-24. [http://dx.doi.org/10.1056/NEJM198307073090105] [PMID: 6343871]
37. Robert, A.; Northam, J.I.; Nezamis, J.E.; Phillips, J.P. Exertion ulcers in the rat. Am. J. Dig. Dis., 1970, 15(5), 497-507. [http://dx.doi.org/10.1007/BF02283881] [PMID: 5309628]
38. Sandweiss, D.J. Effects of adrenocorticotropic hormone (ACTH) and of cortisone on peptic ulcer. I. Clinical review. Gastroenterology, 1954, 27(5), 604-616. [PMID: 13210598]
39. Weusten, B.L.; Jacobs, J.W.; Bijlsma, J.W. Corticosteroid pulse therapy in active rheumatoid arthritis. Semin. Arthritis Rheum., 1993, 23(3), 183-192. [http://dx.doi.org/10.1016/S0049-0172(05)80039-3] [PMID: 8122121]
40. Brodie, D.A.; Hanson, H.M. A study of the factors involved in the production of gastric ulcers by the restraint technique. Gastroenterology, 1960, 38, 353-360. [PMID: 13804627]
41. Hernandez, D.E.; Adcock, J.W.; Nemeroff, C.B.; Prange, A.J., Jr The role of the adrenal gland in cytoprotection against stressinduced gastric ulcers in rats. J. Neurosci. Res., 1984, 11(2), 193-201. [http://dx.doi.org/10.1002/jnr.490110209] [PMID: 6708137]
42. Murison, R.; Overmier, J.B.; Hellhammer, D.H.; Carmona, M. Hypothalamo-pituitary-adrenal manipulations and stress ulcerations in rats. Psychoneuroendocrinology, 1989, 14(5), 331-338. [http://dx.doi.org/10.1016/0306-4530(89)90002-4] [PMID: 2813656]
43. Perretti, M.; Mugridge, K.G.; Wallace, J.L.; Parénte, L. Reduction of aspirin-induced gastric damage in rats by interleukin-1 beta: possible involvement of endogenous corticosteroids. J. Pharmacol. Exp. Ther., 1992, 261(3), 1238-1247. [PMID: 1602386]
44. Szabo, S.; Gallagher, G.T.; Horner, H.C.; Frankel, P.W.; Underwood, R.H.; Konturek, S.J.; Brzozowski, T.; Trier, J.S. Role of the adrenal cortex in gastric mucosal protection by prostaglandins, sulfhydryls, and cimetidine in the rat. Gastroenterology, 1983, 85(6), 1384-1390. [PMID: 6605275]
45. Munck, A.; Guyre, P.M.; Holbrook, N.J. Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocr. Rev., 1984, 5(1), 25-44. [http://dx.doi.org/10.1210/edrv-5-1-25] [PMID: 6368214]
46. Filaretova, L.P. The dependence of the formation of stress stomach ulcers on the function of hypothalamo-hypophyseal-adrenocorticalsystem. Sechenov Physiol. J., 1990, 78, 1594-1600.
47. Filaretova, L. Glucocorticoids are gastroprotective under physiologic conditions. Ther. Adv. Chronic Dis., 2011, 2(5), 333-342. [http://dx.doi.org/10.1177/2040622311412420] [PMID: 23251759]
48. Filaretova, L.P.; Filaretov, A.A.; Makara, G.B. Corticosterone increase inhibits stress-induced gastric erosions in rats. Am. J. Physiol., 1998, 274(6 Pt 1), G1024-G1030. [PMID: 9696701]
49. Filaretova, L.; Bagaeva, T.; Podvigina, T.; Makara, G. Various ulcerogenic stimuli are potentiated by glucocorticoid deficiency in rats. J. Physiol. Paris, 2001, 95(1-6), 59-65. [http://dx.doi.org/10.1016/S0928-4257(01)00069-9] [PMID: 11595419]
50. Filaretova, L.P.; Bagaeva, T.R.; Amagase, K.; Takeuchi, K. Contribution of glucocorticoids to protective influence of preconditioning mild stress against stress-induced gastric erosions. Ann. N. Y. Acad. Sci., 2008, 1148, 209-212. [http://dx.doi.org/10.1196/annals.1410.005] [PMID: 19120111]
51. Filaretova, L.; Morozova, O.; Laszlo, F.; Morschl, E.; Zelena, D. Does chronic stress enhance the risk of diseases? Endocr. Regul., 2013, 47(4), 177-188. [http://dx.doi.org/10.4149/endo_2013_04_177] [PMID: 24156706]
52. Guth, P.H. Current concepts in gastric microcirculatory pathophysiology. Yale J. Biol. Med., 1992, 65(6), 677-688. [PMID: 1341071]
53. Filaretova, L.; Maltcev, N.; Bogdanov, A.; Levkovich, Y. Role of gastric microcirculation in the gastroprotection by glucocorticoids released during water-restraint stress in rats. Chin. J. Physiol., 1999, 42(3), 145-152. [PMID: 10707888]
54. Filaretova, L.P.; Podvigina, T.T.; Bagaeva, T.R.; Tanaka, A.; Takeuchi, K. Mechanisms underlying the gastroprotective action of glucocorticoids released in response to ulcerogenic stress factors. Ann. N. Y. Acad. Sci., 2004, 1018, 288-292. [http://dx.doi.org/10.1196/annals.1296.034] [PMID: 15240380]
55. Lu, N.Z.; Cidlowski, J.A. Translational regulatory mechanisms generate N-terminal glucocorticoid receptor isoforms with unique transcriptional target genes. Mol. Cell, 2005, 18(3), 331-342. [http://dx.doi.org/10.1016/j.molcel.2005.03.025] [PMID: 15866175]
56. Kanemasa, H.; Ozawa, H.; Konishi, H.; Ito, T.; Nishi, M.; Mitsufuji, S.; Kodama, T.; Hattori, T.; Kawata, M. Distribution of glucocorticoid receptor immunoreactivity in gastric mucosa of normal and adrenalectomized rats. Dig. Dis. Sci., 1999, 44(10), 2081-2087. [http://dx.doi.org/10.1023/A: 1026686705421] [PMID: 10548361]
57. Heitzer, M.D.; Wolf, I.M.; Sanchez, E.R.; Witchel, S.F.; DeFranco, D.B. Glucocorticoid receptor physiology. Rev. Endocr. Metab. Disord., 2007, 8(4), 321-330. [http://dx.doi.org/10.1007/s11154-007-9059-8] [PMID: 18049904]
58. Moguilewsky, M.; Philibert, D. RU 38486: potent antiglucocorticoid activity correlated with strong binding to the cytosolic glucocorticoid receptor followed by an impaired activation. J. Steroid Biochem., 1984, 20(1), 271-276. [http://dx.doi.org/10.1016/0022-4731(84)90216-4] [PMID: 6708512]
59. Tempel, D.L.; McEwen, B.S.; Leibowitz, S.F. Adrenal steroid receptors in the PVN: studies with steroid antagonists in relation to macronutrient intake. Neuroendocrinology, 1993, 57(6), 1106-1113. [http://dx.doi.org/10.1159/000126477] [PMID: 8232767]
60. Alexandrová, M. Stress induced tyrosine aminotransferase activity via glucocorticoid receptor. Horm. Metab. Res., 1994, 26(2), 97-99. [http://dx.doi.org/10.1055/s-2007-1000781] [PMID: 7911118]
61. Rivier, C.L.; Grigoriadis, D.E.; Rivier, J.E. Role of corticotropinreleasing factor receptors type 1 and 2 in modulating the rat adrenocorticotropin response to stressors. Endocrinology, 2003, 144(6), 2396-2403. [http://dx.doi.org/10.1210/en.2002-0117] [PMID: 12746300]
62. Taché, Y.; Brunnhuber, S. From Hans Selye’s discovery of biological stress to the identification of corticotropin-releasing factor signaling pathways: implication in stress-related functional bowel diseases. Ann. N. Y. Acad. Sci., 2008, 1148, 29-41. [http://dx.doi.org/10.1196/annals.1410.007] [PMID: 19120089]
63. Kawakubo, K.; Taché, Y. Protective effect of endogenous CRF on restraint-induced gastric lesions in rats. Gastroenterology, 1999, 116, A210.
64. Ray, A.; Henke, P.G.; Gulati, K.; Sen, P. The amygdaloid complex, corticotropin releasing factor and stress-induced gastric ulcerogenesis in rats. Brain Res., 1993, 624(1-2), 286-290. [http://dx.doi.org/10.1016/0006-8993(93)90089-6] [PMID: 8252401]
65. Wang, L.; Cardin, S.; Martínez, V.; Taché, Y. Intracerebroventricular CRF inhibits cold restraint-induced c-fos expression in the dorsal motor nucleus of the vagus and gastric erosions in rats. Brain Res., 1996, 736(1-2), 44-53. [http://dx.doi.org/10.1016/0006-8993(96)00726-3] [PMID: 8930307]
66. Bakke, H.K.; Bogsnes, A.; Murison, R. Studies on the interaction between ICV effects of CRF and CNS noradrenaline depletion. Physiol. Behav., 1990, 47(6), 1253-1260. [http://dx.doi.org/10.1016/0031-9384(90)90379-I] [PMID: 2168567]
67. Shibasaki, T.; Yamauchi, N.; Hotta, M.; Masuda, A.; Oono, H.; Wakabayashi, I.; Ling, N.; Demura, H. Brain corticotropinreleasing factor acts as inhibitor of stress-induced gastric erosion in rats. Life Sci., 1990, 47(11), 925-932. [http://dx.doi.org/10.1016/0024-3205(90)90539-4] [PMID: 2215074]
68. Mikics, E.; Kruk, M.R.; Haller, J. Genomic and non-genomic effects of glucocorticoids on aggressive behavior in male rats. Psychoneuroendocrinology, 2004, 29(5), 618-635. [http://dx.doi.org/10.1016/S0306-4530(03)00090-8] [PMID: 15041085]
69. Filaretova, L.; Bagaeva, T.; Morozova, O. Stress and the stomach: corticotropin-releasing factor may protect the gastric mucosa in stress through involvement of glucocorticoids. Cell. Mol. Neurobiol., 2012, 32(5), 829-836. [http://dx.doi.org/10.1007/s10571-012-9800-z] [PMID: 22290156]
70. Filaretova, L.; Podvigina, T.; Bagaeva, T.; Morozova, O. From gastroprotective to ulcerogenic effects of glucocorticoids: role of long-term glucocorticoid action. Curr. Pharm. Des., 2014, 20(7), 1045-1050. [http://dx.doi.org/10.2174/13816128113199990419] [PMID: 23782149]
71. Pellissier, S.; Dantzer, C.; Mondillon, L.; Trocme, C.; Gauchez, A.S.; Ducros, V.; Mathieu, N.; Toussaint, B.; Fournier, A.; Canini, F.; Bonaz, B. Relationship between vagal tone, cortisol, TNFalpha, epinephrine and negative affects in Crohn’s disease and irritable bowel syndrome. PLoS One, 2014, 9(9), e105328.