Altered neuro-endocrine-immune pathways in the irritable bowel syndrome: The top-down and the bottom-up model

Journal of Gastroenterology

Volumn 47, Issue 11, 2012, Pages 1177-1185

  Stasi, Cristina ^a   Rosselli, Massimo ^a   Bellini, Massimo ^b   Laffi, Giacomo ^a   Milani, Stefano ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

^b UNIVERSITY OF PISA   (Italy)

Author keywords

Corticotropin releasing hormone; Exteroreceptive stress; Interoceptive stress; Mast cells; Stress

Indexed keywords

ADRENALIN; BETA ENDORPHIN; CALCITONIN GENE RELATED PEPTIDE; CORTICOTROPIN; CORTICOTROPIN RELEASING FACTOR; HYDROCORTISONE; INTERLEUKIN 1BETA; INTERLEUKIN 6; NEUROKININ A; NEUROPEPTIDE Y; NORADRENALIN; PROOPIOMELANOCORTIN; SEROTONIN; SUBSTANCE P; TACHYKININ RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

ANXIETY DISORDER; CENTRAL NERVOUS SYSTEM; CHRONIC STRESS; DEPRESSION; DISEASE ASSOCIATION; DISEASE COURSE; GASTROINTESTINAL MOTILITY; HORMONE RELEASE; HUMAN; HYPOTHALAMUS HYPOPHYSIS SYSTEM; IMMUNE RESPONSE; INTESTINE INNERVATION; IRRITABLE COLON; MENTAL DISEASE; MENTAL STRESS; MOTOR DYSFUNCTION; NEUROENDOCRINE DISEASE; NEUROIMAGING; PATHOGENESIS; PATHOPHYSIOLOGY; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSYCHOTHERAPY; REMISSION; REVIEW; SYMPATHETIC INNERVATION; VAGUS NERVE STIMULATION; VISCERAL PAIN;

ANIMALS; CENTRAL NERVOUS SYSTEM; ENTERIC NERVOUS SYSTEM; HUMANS; IRRITABLE BOWEL SYNDROME; MENTAL DISORDERS; NERVOUS SYSTEM DISEASES; NEUROIMAGING; STRESS, PSYCHOLOGICAL;

EID: 84872276280     PISSN: 09441174     EISSN: 14355922     Source Type: Journal    
DOI: 10.1007/s00535-012-0627-7     Document Type: Review

References (78)

1. Mayer EA. The neurobiology of stress and gastrointestinal disease. Gut. 2000;47:861-9.
2. Straub RH, Herfarth H, Falk W, Andus T, Schölmerich J. Uncoupling of the sympathetic nervous system and the hypothalamic- pituitary-adrenal axis in inflammatory bowel disease? J Neuroimmunol. 2002;126:116-25.
3. Stasi C, Orlandelli E. Role of the brain-gut axis in the pathophysiology of Crohn's disease. Dig Dis. 2008;26:156-66.
4. Drossman DA. The functional gastrointestinal disorders and the Rome II process. Gut. 1999;45:1-5.
5. Drossman DA. The functional gastrointestinal disorders and the Rome III process. Gastroenterology. 2006;130:1377-90.
6. Lovallo WR, Thomas TL. Stress hormones in psychophysiological research: emotional, behavioral, and cognitive implications. In: Cacioppo JT, Tassinary LG, Berntson GG, editors. Handbook of psychophysiology. Cambridge: Cambridge University Press; 2000. p. 342-67.
7. Lea R, Whorwell PJ. New insights into the psychosocial aspects of irritable bowel syndrome. Curr Gastroenterol Rep. 2003;5: 343-50.
8. Lydiard RB, Fossey MD, Marsh W, Ballenger JC. Prevalence of psychiatric disorders in patients with irritable bowel syndrome. Psychosomatics. 1993;34:229-34.
9. Thijssen AY, Jonkers DM, Leue C, van der Veek PP, Vidakovic- Vukic M, van Rood YR, et al. Dysfunctional cognitions, anxiety and depression in irritable bowel syndrome. J Clin Gastroenterol. 2010;44:e236-41.
10. Delvaux M, Denis P, Allemand H. Sexual abuse is more frequently reported by IBS patients than by patients with organic digestive diseases or controls. Results of a multicentre inquiry. French Club of Digestive Motility. Eur J Gastroenterol Hepatol. 1997;9:345-52.
11. Bennett EJ, Tennant CC, Piesse C, Badcock CA, Kellow JE. Level of chronic life stress predicts clinical outcome in irritable bowel syndrome. Gut. 1998;43:256-61.
12. O'Mahony SM, Hyland NP, Dinan TG, Cryan JF. Maternal separation as a model of brain-gut axis dysfunction. Psychopharmacology (Berl). 2011;214:71-88.
13. Irwin C, Falsetti SA, Lydiard RB, Ballenger JC, Brock CD, Brener W. Comorbidity of posttraumatic stress disorder and irritable bowel syndrome. J Clin Psychiatry. 1996;57:576-8.
14. Prior A, Colgan SM, Whorwell PJ. Changes in rectal sensitivity after hypnotherapy with irritable bowel syndrome. Gut. 1990;31: 896-8.
15. Poitras P, Riberdy Poitras M, Boivin M, Verrier P. Evolution of visceral sensitivity in patients with irritable bowel syndrome. Dig Dis Sci. 2002;47:914-20.
16. Houghton LA, Calvert EL, Jackson NA, Cooper P, Whorwell PJ. Visceral sensation and emotion: a study using hypnosis. Gut. 2002;51:701-4.
17. Mulak A, Bonaz B. Irritable bowel syndrome: a model of the brain-gut interactions. Med Sci Monit. 2004;10:RA55-62.
18. Silverman DH, Munakata JA, Ennes H, Mandelkern MA, Hoh CK, Mayer EA. Regional cerebral activity in normal and pathological perception of visceral pain. Gastroenterology. 1997;112: 64-72.
19. Drossman DA, Ringel Y, Vogt BA, Leserman J, Lin W, Smith JK, et al. Alterations of brain activity associated with resolution of emotional distress and pain in a case of severe irritable bowel syndrome. Gastroenterology. 2003;124:754-61.
20. Mertz H, Morgan V, Tanner G, Pichens D, Price R, Shyr Y, et al. Regional cerebral activation in irritable bowel syndrome and control subjects with painful and nonpainful rectal distention. Gastroenterology. 2000;118:842-8.
21. Baciu MV, Bonaz BL, Papillon E, Bost RA, Le Bas JF, Fournet J, et al. Central processing of rectal pain: a functional MR imaging study. Am J Neuroradiol. 1999;20:1920-4.
22. Bonaz B, Baciu M, Papillon E, Bost R, Gueddah N, Le Bas JF, et al. Central processing of rectal pain in patients with irritable bowel syndrome: an fMRI study. Am J Gastroenterol. 2002;97: 654-61.
23. Sternberg EM, Chrousos GP, Wilder RL, Gold PW. The stress response and the regulation of inflammatory disease. Ann Intern Med. 1992;117:854-66.
24. Gue M, Tekamp A, Tabis N, Junien JL, Buéno L. Cholecystokinin blockade of emotional stress- and CRF-induced colonic motor alterations in rats: role of the amygdala. Brain Res. 1994;658:232-8.
25. Sajdyk TJ, Shekhar A, Gehlert DR. Interactions between NPY and CRF in the amygdala to regulate emotionality. Neuropeptides. 2004;38:225-34.
26. Swanson LW, Sawchenko PE, Rivier J, Vale WW. Organization of ovine corticotropin-releasing factor immunoreactive cells and fibers in the rat brain: an immunohistochemical study. Neuroendocrinology. 1983;36:165-86.
27. Taché Y, Monnikes H, Bonaz B, Rivier J. Role of CRF in stressrelated alterations of gastric and colonic motor function. Ann NY Acad Sci. 1993;697:233-43.
28. Taché Y, Martinez V, Million M, Rivier J. Corticotropinreleasing factor and the brain-gut motor response to stress. Can J Gastroenterol. 1999;13:18A-25A.
29. Smith GW, Aubry JM, Dellu F, Contarino A, Bilezikjian LM, Gold LH, et al. Corticotropin releasing factor receptor 1-deficient mice display decreased anxiety, impaired stress response, and aberrant neuroendocrine development. Neuron. 1998;20:1093-102.
30. Timpl P, Spanagel R, Sillaber I, Kresse A, Reul JM, Stalla GK, et al. Impaired stress response and reduced anxiety in mice lacking a functional corticotropin-releasing hormone receptor. Nat Genet. 1998;19:162-6.
31. Cole MA, Kalman BA, Pace TW, Topczewski F, Lowrey MJ, Spencer RL. Selective blockade of the mineralocorticoid receptor impairs hypothalamic-pituitary-adrenal axis expression of habituation. J Neuroendocrinol. 2000;12:1034-42.
32. Munakata J, Mayer EA, Chang L, Schmulson M, Liu M, Tougas G, et al. Autonomic and neuroendocrine responses to recto-sigmoid stimulation. Gastroenterology. 1998;114:A808.
33. Heitkemper M, Jarrett M, Cain K, Shaver J, Bond E, Woods NF, et al. Increased urine catecholamines and cortisol in women with irritable bowel syndrome. Am J Gastroenterol. 1996;91:906-13.
34. Heim C, Newport DJ, Bonsall R, Miller AH, Nemeroff CB. Altered pituitary-adrenal axis responses to provocative challenge tests in adult survivors of childhood abuse. Am J Psychiatry. 2001;158:575-81.
35. Heim C, Ehlert U, Hellhammer DH. The potential role of hypocortisolism in the pathophysiology of stress-related bodily disorders. Psychoneuroendocrinology. 2000;25:1-35.
36. Stratakis CA, Chrousos GP. Neuroendocrinology and pathophysiology of the stress system. Ann N Y Acad Sci. 1995;771: 1-18.
37. Spiller RC, Jenkis D, Thornley JP, Hebden JM, Wright T, Skinner M, et al. Increased rectal mucosal enteroendocrine cells, T lymphocytes, and increased gut permeability following acute Campylobacter enteritis and in post-dysenteric irritable bowel syndrome. Gut. 2000;47:804-11.
38. Creed F. The relationship between psychosocial parameters and outcome in the irritable bowel syndrome. Am J Med. 1999;107: 74-80.
39. Gwee KA, Leong YL, Graham C, McKendrick MW, Collins SM, Walters SJ, et al. The role of psychological and biological factors in postinfective gut dysfunction. Gut. 1999;44:400-6.
40. Aggarwal A, Cutts TF, Abell AL, Cardoso S, Familoni B, Bremer J, et al. Predominant symptoms in irritable bowel syndrome correlate with specific autonomic nervous system abnormalities. Gastroenterology. 1994;106:945-50.
41. Tougas G. The autonomic nervous system in functional bowel disorders. Gut. 2000;47:iv78-80.
42. Heitkemper M, Jarret M, Cain KC, Burr R, Levy RL, Feld A, et al. Autonomic nervous system in women with irritable bowel syndrome. Dig Dis Sci. 2001;46:1276-84.
43. Elsenbruch S, Orr WC. Diarrhea and constipation-predominant IBS patients in postprandrial autonomic and cortisol responses. Am J Gastroenterol. 2001;96:460-6.
44. Azpiroz F. Hypersensitivity in functional gastrointestinal disorders. Gut. 2002;51:i25-8.
45. Gupta V, Sheffield D, Verne GN. Evidence for autonomic dysregulation in irritable bowel syndrome. Dig Dis Sci. 2002;47: 1716-22.
46. Chang L, Berman S, Mayer EA, Suyenobu B, Derbyshire S, Naliboff B, et al. Brain responses to visceral and somatic stimuli in patients with irritable bowel syndrome with and without fibromyalgia. Am J Gastroenterol. 2003;98:1354-61.
47. Jarret ME, Burr RL, Cain KC, Hertig V, Weisman P, Heitkemper MM. Anxiety and depression are related to autonomic nervous system function in women with irritable bowel syndrome. Dig Dis Sci. 2003;48:386-94.
48. Isgar B, Harman M, Kaye MD, Whorwel PJ. Symptoms of irritable bowel syndrome in ulcerative colitis in remission. Gut. 1983;24:190-2.
49. Park JH, Rhee PL, Kim HS, Lee JH, Kim YH, Kim JJ, et al. Mucosal mast cell counts correlate with visceral hypersensitivity in patients with diarrhea predominant irritable bowel syndrome. Gut. 2000;47:804-11.
50. Church MK, Lowman MA, Robinson C, Holgate ST, Benyon RC. Interaction of neuropeptides with human mast cells. Int Arch Allergy Appl Immunol. 1989;88:70-8.
51. Arzubiaga C, Morrow J, Roberts LJ, Biaggioni I. Neuropeptide Y, a putative cotransmitter in noradrenergic neurons, induces mast cell degranulation but not prostaglandin D2 release. J Allergy Clin Immunol. 1991;87:88-93.
52. Gui XY. Mast cells: a possible link between psychological stress, enteric infection, food allergy and gut hypersensitivity in the irritable bowel syndrome. J Gastroenterol Hepatol. 1998;13:980-9.
53. Elenkov IJ, Wilder RL, Chrousos GP, Vizi ES. The sympathetic nerve-an integrative interface between two supersystems: the brain and the immune system. Pharmacol Rev. 2000;52:595-638.
54. Gershon MD. Serotonin and its implication for the management of irritable bowel syndrome. Rev Gastroenterol Disord. 2003;3: S25-34.
55. Mertz H. Role of the brain and sensory pathways in gastrointestinal sensory disorders in humans. Gastroenterology. 2002;51:i29-33.
56. Mayer EA, Naliboff BD, Chang L. Basic pathophysiologic mechanisms in irritable bowel syndrome. Dig Dis. 2001;19:212-8.
57. Kim DY, Camilleri M. Serotonin: a mediator of the brain-gut connection. Am J Gastroenterol. 2000;95:2698-709.
58. Kim HJ, Camilleri M, Carlson PJ, Cremonini F, Ferber I, Stephens D, et al. Association of distinct α2 adrenoceptor and serotonin transporter polymorphisms with constipation and somatic symptoms in functional gastrointestinal disorders. Gut. 2004;53:829-37.
59. Whitehead WE, Engel BT, Schuster MM. Irritable bowel syndrome: physiological and psychological differences between diarrhea-predominant and constipation-predominant patients. Dig Dis Sci. 1980;25:404-13.
60. Simrén M, Abrahamsson H, Bjornsson ES. An exaggerated sensory component of the gastrocolonic response in patients with irritable bowel syndrome. Gut. 2001;48:20-7.
61. Slater BJ, Plusa SM, Smith AN, Varma JS. Rectal hypersensitivity in the irritable bowel syndrome. Int J Colorectal Dis. 1997;12:29-32.
62. Harraf F, Schmulson M, Saba L, Varma JS. Subtypes of constipation predominant irritable bowel syndrome based on rectal perception. Gut. 1998;43:388-94.
63. Steens J, Van Der Schaar PJ, Penning C, Brussee J, Masclee AA. Compliance, tone and sensitivity of the rectum in different subtypes of irritable bowel syndrome. Neurogastroenterol Motil. 2002;14:241-7.
64. Tam FSF, Hiller K, Bunce K. Investigation of the 5-HT receptor type involved in inhibition of spontaneous activity of human colonic circular muscle. Br J Pharmacol. 1992;106:25P.
65. Evangelista S. Involvement of tachykinins in intestinal inflammation. Curr Pharm Des. 2001;7:19-30.
66. Holzer P, Holzer-Petsche U. Tachykinins in the gut. Part II. Roles in neural excitation, secretion and inflammation. Pharmacol Ther. 1997;73:219-63.
67. Holzer P, Holzer-Petsche U. Tachykinins in the gut. Part I. Expression, release and motor function. Pharmacol Ther. 1997; 73:173-217.
68. Leng YX, Wei YY, Chen H, Zhou SP, Yang YL, Duan LP. Alteration of cholinergic and peptidergic neurotransmitters in rat ileum induced by acute stress following transient intestinal infection is mast cell dependent. Chin Med J. 2010;123:227-33.
69. Stead RH, Tomioka M, Quinonez G, Simon GT, Felten SY, Bienenstock J. Intestinal mucosal mast cells in normal and nematode-infected rat intestines are in intimate contact with peptidergic nerves. Proc Natl Acad Sci USA. 1987;84:2975-9.
70. Palsson OS, Morteau O, Bozymski EM, Woosley JT, Sartor RB, Davies MJ, et al. Elevated vasoactive intestinal peptide concentrations in patients with irritable bowel syndrome. Dig Dis Sci. 2004;49:1236-43.
71. Salio C, Lossi L, Ferrini F, Merighi A. Neuropeptides as synaptic transmitters. Cell Tissue Res. 2006;326:583-98.
72. Farhadi A, Fields JZ, Keshavarzian A. Mucosal mast cells are pivotal elements in inflammatory bowel disease that connect the dots: stress, intestinal hyperpermeability and inflammation. World J Gastroenterol. 2007;13:3027-30.
73. Barbara G, Stanghellini V, De Giorgio R, Cremon C, Cottrell GS, Santini D, et al. Activated mast cells in proximity to colonic nerves correlate with abdominal pain in irritable bowel syndrome. Gastroenterology. 2004;126:693-702.
74. Rodríguez-Fandiño O, Hernández-Ruiz J, Schmulson M. From cytokines to Toll-like receptors and beyond-current knowledge and future research needs in irritable bowel syndrome. J Neurogastroenterol Motil. 2010;16:363-73.
75. Liebregts T, Adam B, Bredack C, Röth A, Heinzel S, Lester S, et al. Immune activation in patients with irritable bowel syndrome. Gastroenterology. 2007;132:913-20.
76. Dinan TG, Quigley EM, Ahmed SM, Scully P, O'Brien S, O'Mahony L, et al. Hypothalamic-pituitary-gut axis dysregulation in irritable bowel syndrome: plasma cytokines as a potential biomarker? Gastroenterology. 2006;130:304-11.
77. Wood JD. Neuropathophysiology of irritable bowel syndrome. J Clin Gastroenterol. 2002;35:S11-22.
78. Stasi C, Zignego AL, Laffi G, Rosselli M. The liver-cytokine- brain circuit in interferon-based treatment of patients with chronic viral hepatitis. J Viral Hepatitis. 2011;18:525-32.