The role of the sympathetic nervous system in intestinal inflammation

Gut

Volumn 55, Issue 11, 2006, Pages 1640-1649

  Straub, R H ^a   Wiest, R ^a   Strauch, U G ^a   Harle P ^a   Scholmerich J ^a  

^a UNIVERSITY HOSPITAL REGENSBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE; ADRENERGIC RECEPTOR; NERVE GROWTH FACTOR; NEUROTRANSMITTER; NORADRENALIN; SUBSTANCE P;

ADRENERGIC SYSTEM; APOPTOSIS; CELL INFILTRATION; CELL MIGRATION; CELL TYPE; ENTERITIS; HUMAN; IMMUNE FUNCTION TEST; IMMUNE RESPONSE; IMMUNOMODULATION; INFLAMMATION; INNATE IMMUNITY; INTESTINE INNERVATION; INTESTINE MOTILITY; INTESTINE MUCOSA; INTESTINE SECRETION; INTESTINE WALL; NEUROPHYSIOLOGY; PEPTIDERGIC NERVOUS SYSTEM; PRIORITY JOURNAL; REVIEW; RHEUMATOID ARTHRITIS; SYMPATHETIC NERVE;

GASTROENTERITIS; HUMANS; INTESTINES; NEUROTRANSMITTER AGENTS; SYMPATHETIC NERVOUS SYSTEM;

EID: 33750347509     PISSN: 00175749     EISSN: None     Source Type: Journal    
DOI: 10.1136/gut.2006.091322     Document Type: Review

References (113)

1. Selye H, Fortier C. Adaptive reactions to stress. Res Publ Assoc Res Nerv Ment Dis 1949;29:3-18.
2. Levine JD, Goetzl EJ, Basbaum AI. Contribution of the nervous system to the pathophysiology of rheumatoid arthritis and other polyarthritides. Rheum Dis Clin North Am 1987;13:369-83.
3. Levine JD, Coderre TJ, Helms C, et al. Beta 2-adrenergic mechanisms in experimental arthritis. Proc Natl Acad Sci U S A 1988;85:4553-6.
4. Dhabhar FS, McEwen BS. Bidirectional effects of stress and glucocorticoid hormones on immune function: possible explanations for paradoxical observations. In: Ader R, Felten DL, Cohen N, eds. Psychoneuroimmunology. San Diego: Academic Press, 2001:301-38.
5. Johnson HM, Archer DL, Torres BA. Cyclic GMP as the second messenger in helper cell requirement for gamma-interferon production. J Immunol 1982;129:2570-2.
6. Novogrodsky A, Patya M, Rubin AL, et al. Agents that increase cellular cAMP inhibit production of interleukin-2, but not its activity. Biochem Biophys Res Commun 1983;114:93-8.
7. Renz H, Gong JH, Schmidt A, et al. Release of tumor necrosis factor-alpha from macrophages. Enhancement and suppression are dose-dependently regulated by prostaglandin E2 and cyclic nucleotides. J Immunol 1988;141:2388-93.
8. Snijdewint FG, Kalinski P, Wierenga EA, et al. Prostaglandin E2 differentially modulates cytokine secretion profiles of human T helper lymphocytes. J Immunol 1993;150:5321-9.
9. Elenkov IJ, Papanicolaou DA, Wilder RL, et al. Modulatory effects of glucocorticoids and catecholamines on human interleukin-12 and interleukin-10 production: clinical implications. Proc Assoc Am Physicians 1996;108:374-81.
10. Coderre TJ, Chan AK, Helms C, et al. Increasing sympathetic nerve terminal-dependent plasma extravasation correlates with decreased arthritic joint injury in rats. Neuroscience 1991;40:185-9.
11. Lorton D, Lubahn C, Klein N, et al. Dual role for noradrenergic innervation of lymphoid tissue and arthritic joints in adjuvant-induced arthritis. Brain Behav Immun 1999;13:315-34.
12. Härle P, Mobius D, Carr DJ, et al. An opposing time-dependent immune-modulating effect of the sympathetic nervous system conferred by altering the cytokine profile in the local lymph nodes and spleen of mice with type II collagen-induced arthritis. Arthritis Rheum 2005;52:1305-13.
13. Bähr M, Frotscher M. Duus' Neurologisch-topische Diagnostik. Suttgart: Thieme, 2003.
14. Besedovsky HO, Del Rey A. Immune-neuro-endocrine interactions. Endocr Rev 1996;17:64-102.
15. Bluthe RM, Walter V, Parnet P, et al. Lipopolysaccharide induces sickness behaviour in rats by a vagal mediated mechanism. C R Acad Sci III 1994;317:499-503.
16. Watkins LR, Goehler LE, Relton JK, et al. Blockade of interleukin-1 induced hyperthermia by subdiaphragmatic vagotomy: evidence for vagal mediation of immune-brain communication. Neurosci Lett 1995;183:27-31.
17. Furness JB, Costa M. Morphology and distribution of intrinsic adrenergic neurones in me proximal colon or the guinea-pig. Z Zellforsch Mikrosk Anat 1971;120:346-63.
18. Jacobowitz D. Histochemical studies of the autonomic innervation of the gut. J Pharmacol Exp Ther 1965;149:358-64.
19. Llewellyn-Smith IJ, Furness JB, O'Brien PE, et al. Noradrenergic nerves in human small intestine. Distribution and ultrastructure. Gastroenterology 1984;87:513-29.
20. Capurso L, Friedmann CA, Parks AG. Adrenergic fibres in the human intestine. Gut 1968;9:678-82.
21. Furness JB. The origin and distribution of adrenergic nerve fibres in the guinea-pig colon. Histochemie 1970;21:295-306.
22. Felten DL, Felten SY, Carlson SL, et al. Noradrenergic and peptidergic innervation of lymphoid tissue. J Immunol 1985;135:755-65s.
23. Goyal RK, Hirano I. Mechanisms of disease: the enteric nervous system. N Engl J Med 1996;334:1106-15.
24. Frieling T, Becker K, Schemann M. The role of the enteric nervous system for gastrointestinal functions. Z Gastroenterol 1997;35(suppl 2):14-19.
25. Geboes K, Collins S. Structural abnormalities of the nervous system in Crohn's disease and ulcerative colitis. Neurogastroenterol Motil 1998;10:189-202.
26. Powis DA, Bunn SJ. Neurotransmitter release and its modulation. Cambridge: Cambridge University Press, 1995.
27. Lundberg JM, Rudehill A, Sollevi A, et al. Co-release of neuropeptide Y and noradrenaline from pig spleen in vivo: Importance of subcellular storage, nerve impulse frequency and pattern, feedback regulation and resupply by axonal transport. Neuroscience 1989;28:475-86.
28. Straub RH. Complexity of the bi-directional neuroimmune junction in the spleen. Trends Pharmacol Sci 2004;25:640-6.
29. Straub RH, Schaller T, Miller LE, et al. Neuropeptide Y cotransmission with norepinephrine in the sympathetic nerve-macrophage interplay. J Neurochem 2000;75:2464-71.
30. Oikarinen J, Hamalainen L, Oikarinen A. Modulation of glucocorticoid receptor activity by cyclic nucleotides and its implications on the regulation of human skin fibroblast growth and protein synthesis. Biochim Biophys Acta 1984;799:158-65.
31. Gruol DJ, Campbell NF, Bourgeois S. Cyclic AMP-dependent protein kinase promotes glucocorticoid receptor function. J Biol Chem 1986;261:4909-14.
32. Nakada MT, Stadel JM, Poksay KS, et al. Glucocorticoid regulation of beta-adrenergic receptors in 3T3-L1 preadipocytes. Mol Pharmacol 1987;31:377-84.
33. Dong Y, Aronsson M, Gustafsson JA, et al. The mechanism of cAMP-induced glucocorticoid receptor expression. Correlation to cellular glucocorticoid response. J Biol Chem 1989;264:13679-83.
34. DiBattista JA, Martel-Pelletier J, Cloutier JM, et al. Modulation of glucocorticoid receptor expression in human articular chondrocytes by cAMP and prostaglandins. J Rheumatol Suppl 1991;27:102-5.
35. Kom SH, Wouters EF, Wesseling G, et al. Interaction between glucocorticoids and beta2-agonists: alpha and beta glucocorticoid-receptor mRNA expression in human Bronchial epithelial cells. Biochem Pharmacol 1998;56:1561-9.
36. Eickelberg O, Roth M, Lorx R, et al. Ligand-independent activation of the glucocorticoid receptor by beta2-adrenergic receptor agonists in primary human lung fibrobfasts and vascular smooth muscle cells. J Biol Chem 1999;274:1005-10.
37. Schmidt P, Holsboer F, Spengler D. Beta(2)-adrenergic receptors potentiates glucocorticoid receptor transactivation via G protein betagamma-subunits and the phosphoinositide 3-kinase pathway. Mol Endocrinol 2001;15:553-64.
38. Straub RH, Günzler C, Miller LE, et al. Anti-inflammatory cooperativity of corticosteroids and norepinephrine in rheumatoid arthritis synovial tissue in vivo and in vitro. FASEB J 2002;16:993-1000.
39. Straub RH, Mayer M, Kreutz M, et al. Neurotransmitters of the sympathetic nerve terminal are powerful chemoattractants for monocytes. J Leukoc Biol 2000;67:553-8.
40. Schedlowski M, Hosch W, Oberbeck R, et al. Catecholamines modulate human NK cell circulation and function via spleen-independent beta 2-adrenergic mechanisms. J Immunol 1996;156:93-9.
41. Rose FR, Hirschhorn R, Weissmann G, et al. Adenosine promotes neutrophil chemotaxis. J Exp Med 1988;167:1186-94.
42. Kavelaars A, van de Pol M, Zijlstra J, et al. Beta 2-adrenergic activation enhances interleukin-8 production by human monocytes. J Neuroimmunol 1997;77:211-16.
43. Vlisidou I, Lyte M, van Diemen PM, et al. The neuroendocrine stress hormone norepinephrine augments Escherichia coli O157:H7-induced enteritis and adherence in a bovine ligated ileal loop model of infection. Infect Immun 2004;72:5446-51.
44. Toft P, Svendsen P, Tonnesen E, et al. Redistribution of lymphocytes after major surgical stress. Acta Anaesthesiol Scand 1993;37:245-9.
45. Gonzalez-Ariki S. Husband AJ. The role of sympathetic innervation of the gut in regulating mucosal immune responses. Brain Behav Immun 1998;12:53-63.
46. Adolphs J, Schmidt DK, Mousa SA, et al. Thoracic epidural anesthesia attenuates hemorrhage-induced impairment of intestinal perfusion in rats. Anesthesiology 2003;99:685-92.
47. Maestroni GJ. Dendritic cell migration controlled by alpha 1b-adrenergic receptors. J Immunol 2000;165:6743-7.
48. Josefeson E, Bergquist J, Ekman R, et al. Catecholomines are synthesized by mouse lymphocytes and regulate function of these cells by induction of apoptosis. Immunology 1996;88:140-6.
49. Bergquist J, Josefsson E, Tarkowski A, et al. Measurements of catecholamine-mediated apoptosis of immunocompetent cells by capillary electrophoresis. Electrophoresis 1997;18:1760-6.
50. Communal C, Singh K, Pimentel DR, et al. Norepinephrine stimulates apoptosis in adult rat ventricular myocytes by activation of the beta-adrenergic pathway. Circulation 1998;98:1329-34.
51. Dincer HE, Gangopadhyay N, Wang R, et al. Norepinephrine induces alveolar epithelial apoptosis mediated by alpha-, beta-, and angoitensin receptor activation. Am J Physiol Lung Cell Mol Physiol 2001;281:L624-30.
52. Del Rey A, Kabiersch A, Petzoldt S, et al. Sympathetic abnormalities during autoimmune processes: potential relevance of noradrenaline-induced apoptosis. Ann N V Acad Sci 2003;992:158-67.
53. Fu YC, Chi CS, Yin SC, et al. Norepinephrine induces apoptosis in neonatal rat endothelial cells via down-regulation of Bcl-2 and activation of beta-adrenergic and caspase-2 pathways. Cardiovasc Res 2004;61:143-51.
54. Marra S, Burnett M, Hoffman-Goetz L. Intravenous catecholamine administration affects mouse intestinal lymphocyte number and apoptosis. J Neuroimmunol 2005;158:76-85.
55. Elenkov IJ, Wilder RL, Chrousos GP, et al. The sympathetic nervous system-an integrative interface between two supersystems: the brain and the immune system. Pharmacol Rev 2000;52:595-638.
56. Farmer P, Pugin J. Beta-adrenergic agonists exert their "anti-inflammatory" effects in monocytic cells through lhe IkappaB/NF-kappaB pathway. Am J Physiol Lung Cell Mol Physiol 2000;279:L675-82.
57. Spengler RN, Allen RM, Remick DG, et al. Stimulation of alpha-adrenergic receptor augments the production of macrophage-derived tumor necrosis factor. J Immunol 1990;145:1430-4.
58. Weatherby KE, Zwilling BS, Lafuse WP. Resistance of macrophages to Mycobacterium avium is induced by alpha2-adrenergic stimulation. Infect Immun 2003;71:22-9.
59. Straub RH, Pongratz G, Günzler C, et al. Immunoregulation of IL-6 secretion by endogenous and exogenous adenosine and by exogenous purinergic agonists in splenic tissue slices. J Neuroimmunol 2002;125:73-81.
60. Kohm AP, Sanders VM. Norepinephrine: a messenger from the brain to the immune system. Immunol Today 2000;21:539-42.
61. Cobelens PM, Kavelaars A, Vroon A, et al. The beta 2-adrenergic agonist salbutamol potentiates oral induction of tolerance, suppressing adjuvant arthritis and antigen-specific immunity. J Immunol 2002;169:5028-35.
62. Staub RH, Pongratz G, Weidler C, et al. Ablation of the sympathetic nervous system decreases gram-negative and increases gram-positive bacterial dissemination: key rotes for tumor necrosis factor/phagocytes and interleukin-4/lymphocytes. J Infect Dis 2005;192:560-72.
63. Rantapää-Dahlqvist S, de Jong BA, Berglin E, et al. Antibodies against cyclic citrullinated peptide and IgA rheumatoid factor predict the development of rheumatoid arthritis. Arthritis Rheum 2003;48:2741-9.
64. Nielen MM, van Schaardenburg D, Reesink HW, et al. Specific autoantibodies precede the symptoms of rheumatoid arthritis: a study of serial measurements in blood donors. Arthritis Rheum 2004;50:380-6.
65. Miller LE, Jüsten HP, Schölmerich J, et al. The loss of sympathetic nerve fibers in the synovial tissue of patients with rheumatoid arthritis is accompanied by increased norepinephrine release from synovial macrophages. FASEB J 2000;14:2097-107.
66. Weidler C, Holzer C, Harbuz M, et al. Low density of sympathetic nerve fibres and increased density of brain derived neurotropnic factor positive cells in RA synovium. Ann Rheum Dis 2005;64:13-20.
67. Mei Q, Mundinger TO, Lernmark A, et al. Early, selective, and marked loss of sympathetic nerves from the islets of BioBreeder diabetic rats. Diabetes 2002;51:2997-3002.
68. Dvorak AM, Silen W. Differentiation between Crohn's disease and other inflammatory conditions by electron microscopy. Ann Surg 1985;201:53-63.
69. Polignano FM, Caradonna P, Maiorano E, et al. Recurrence of acute colonic pseudo-obstruction in selective adrenergic dysautonomia associated with infectious toxoplasmosis. Scand J Gastroenterol 1997;32:89-94.
70. Belai A, Boulos PB, Robson T, et al. Neurochemical coding in the small intestine of patients with Crohn's disease. Gut 1997;40:767-74.
71. Staub RH, Stebner K, Harte P, et al. Key role of the sympathetic microenvironment for the interplay of tumour necrosis factor and interleukin 6 in normal but not in inflamed mouse colon mucosa. Gut 2005;54:1098-106.
72. Geboes K. Immunopathological studies of the small intestinal intramural nervous system and of intramural vessels in Crohn's disease. Verh K Acad Geneeskd Belg 1993;55:267-301.
73. Reinshagen M, von Boyen G, Adler G, et al. Role of neurotrophins in inflammation of the gut. Curr Opin Investig Drugs 2002;3:565-8.
74. Giger RJ, Urquhart ER, Gillespie SK, et al. Neuropilin-2 is a receptor for semaphorin IV: insight into the structural basis of receptor function and specificity. Neuron 1998;21:1079-92.
75. Chen H, He Z, Bogri A, et al. Semaphorin-neurapilin interactions underlying sympathetic axon responses to class III semaphorins. Neuron 1998;21:1283-90.
76. Chen H, He Z, Tessier-Lavigne M. Axon guidance mechanisms: semaphorins as simultaneous repellents and anti-repellents. Nat Neurosci 1998;1:436-9.
77. Miller LE, Weidler C, Falk W, et al. Increased prevalence of semaphorin 3C, a repellent of sympathetic nerve fibers, in the synovial tissue of patients with rheumatoid arthritis. Arthritis Rheum 2004;50:1156-63.
78. Kyosola K, Penttila O, Salaspuro M. Rectal mucosal adrenergic innervation and enterochromaffin cells in ulcerative colitis and irritable colon. Scand J Gastroenterol 1977;12:363-7.
79. Magro F, Vieira-Coelho MA, Fraga S, et al. Impaired synthesis or cellular storage of norepinephrine, dopamine, and 5-hydroxytryptamine in human inflammatory bowel disease. Dig Dis Sci 2002;47:216-24.
80. Magro F, Fraga S, Ribeiro T, et al. Decreased availability of intestinal dopamine in transmural colitis may relate to inhibitory effects of interferon-gamma upon L-DOPA uptake. Acta Physiol Scand 2004;180:379-86.
81. Swain MG, Blennerhassett PA, Collins SM. Impaired sympathetic nerve function in the inflamed rat intestine. Gastroenterology 1991;100:675-82.
82. Elenkov IJ, Kovacs K, Duda E, et al. Presynaptic inhibitory effect of TNF-alpha on the release of noradrenaline in isolated median eminence. J Neuroimmunol 1992;41:117-20.
83. Rühl A, Hurst S, Collins SM. Synergism between interleukins 1 beta and 6 on noradrenergic nerves in rat myenteric plexus. Gostroenterotogy 1994;1077:993-1001.
84. Rühl A, Collins SM. Role of nitric oxide in norepinephrine release from myenteric plexus in vitro and in Trichinella spiralis-infected rats. Neurogastroenterol Motil 1997;9:33-9.
85. Blandizzi C, Fornai M, Colucci R, et al. Altered prejundional modulation of intestinal cholinergic and noradrenergic pathways by alpha2-adrenoceptors in the presence of experimental colitis. Br J Pharmacol 2003;139:309-20.
86. Xio Y, Hu HZ, Liu S, et al. Clostridium difficile toxin A excites enteric neurones and suppresses sympathetic neurotransmission in the guinea pig. Gut 2000;46:481-6.
87. Xio Y, Hu HZ, Liu S, et al. IL-1 beta and IL-6 excite neurons and suppress nicotinic and noradrenergic neurotransmission in guinea pig enteric nervous system. J Clin Invest 1999;103:1309-16.
88. Bartho L. Adrenergic responses of the guinea-pig ileum: inhibition by prostaglandins and potentiation by non-steroid anti-inflammatory drugs (NSAIDs). Arch Int Pharmacodyn Ther 1978;235:238-47.
89. Penttila O, Kyosola K, Klinge E, et al. Studies of rectal mucosal catecholamines in ulcerative colitis. Ann Clin Res 1975;7:32-6.
90. Tornblom H, Lindberg G, Nyberg B, et al. Full-thickness biopsy of the jejunum reveals inflammation and enteric neuropathy in irritable bowel syndrome. Gastroenterology 2002;123:1972-9.
91. Ohlsson B, Fork FT, Veress B, et al. Coexistent chronic idiopathic intestinal pseudo obstruction and inflammatory bowel disease. Gut 2005;54:729-30.
92. Spiller RC, Jenkins D, Thornley JP, 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.
93. Baerwald C, Graefe C, von Wiehert P, et al. Decreased density of beta-adrenergic receptors on peripheral blood mononuclear cells in patients with rheumatoid arthritis. J Rheumatol 1992;19:204-10.
94. Wahle M, Kolker S, Krause A, et al. Impaired calecholaminergic signalling of B lymphocytes in patients with chronic rheumatic diseases. Ann Rheum Dis 2001;60:505-10.
95. Heijnen CJ, Rouppe vd V, Wulffraat N, et al. Functional alpha 1-adrenergic receptors on leukocytes of patients with poryarticular juvenile rheumatoid arthritis. J Neuroimmunol 1996;71:223-6.
96. Straub RH, Härle P. Sympathetic neurotransmitters in joint inflammation. Rheum Dis Clin North Am 2005;31:43-59.
97. van dec Vliet A, van der Poel KI, Bast A. Intestinal smooth muscle dysfunction after intraperitoneal injection of zymosan in the rat: are oxygen radicals involved? Gut 1992;33:336-41.
98. Martinolle JP, More J, Dubech N, et al. Inverse regulation of alpha- and beta-adrenoceptors during trinitrobenzenesulfonic acid (TNB)-induced inflammation in guinea-pig small intestine. Life Sci 1993;52:1499-508.
99. Cowles VE, Ryan RP, Sarna SK. Interaction between blood flow and motility in normal and inflamed ileum. Neurogastroenterol Motil 1999;11:409-20.
100. Green BT, Lyte M, Kulkarni-Narla A, et al. Neuromodulation of enteropathogen internalization in Peyer's patches from porcine jejunum. J Neuroimmunol 2003;141:74-82.
101. Konttinen YT, Kemppinen P, Segerberg M, et al. Peripheral and spinal neural mechanisms in arthritis, with particular reference to treatment of inflammation and pain. Arthritis Rheum 1994;37:965-82.
102. Leden I, Eriksson A, Lilja B, et al. Autonomic nerve function in rheumatoid arthritis of varying severity. Scand J Rheumatol 1983;12:166-70.
103. Kuis W, Jong-de Vos V, Sinnema G, et al. The autonomic nervous system and the immune system in juvenile rheumatoid arthritis. Brain Behav Immun 1996;10:387-98.
104. Perry F, Heller PH, Kamiya J, et al. Altered autonomic function in patients with arthritis or with chronic myofascial pain. Pain 1989;39:77-84.
105. Dekkers JC. Psychophysiological responsiveness in recently diagnosed patients with rheumatoid arthritis (Thesis). Dordrecht: Drukkerij Dekkers, 2000.
106. Glück T, Oertel M, Reber T, et al. Altered function of the hypothalamic stress axes in patients with moderately active systemic lupus erytnematosus. I. The hypothalamus-autonomic nervous system axis. J Rheumatol 2000;27:903-10.
107. Straub RH, Herfarth H, Falk W, et al. Uncoupling of the sympatnetic nervous system and the hypothalamic-pituitary-adrenal axis in inflammatory bowel disease? J Neuroimmunol 2002;126:116-25.
108. Wolfe F, Mitchell DM, Sibley JT, et al. The mortality of rheumatoid arthritis. Arthritis Rheum 1994;37:481-94.
109. Straub RH, Schölmerich J, Cutolo M. The multiple facets of premature aging in rheumatoid arthritis. Arthritis Rheum 2003;48:2713-21.
110. Crofford LJ, Kalogeras KT, Mastorakos G, et al. Circadian relationships between interleukin (IL)-6 and hypothalamic-pituitary-adrenal axis hormones: failure of IL-6 to cause sustained hypercortisolism in patients with early untreated rheumatoid arthritis. J Clin Endocrinol Metab 1997;82:1279-83.
111. Cutolo M, Foppiani L, Prete C, et al. Hypothalamic-pituitary- adrenocortical axis function in premenopausal women with rheumatoid arthritis not treated with glucocorticoids. J Rheumatol 1999;26:282-8.
112. Straub RH, Vogl D, Gross V, et al. Association of humoral markers of inflammation and dehydroepiandrosterone sulfate or cortisol serum levels in patients with chronic inflammatory bowel disease. Am J Gastroenterol 1998;93:2197-202.
113. Straub RH, Besedovsky HO. Integrated evolutionary, immunological, and neuroendocrine framework for the pathogenesis of chronic disabling inflammatory diseases. FASEB J 2003;17:2176-83.