Clinical and experimental evidence of sympathetic neural dysfunction during inflammatory bowel disease

Clinical and Experimental Pharmacology and Physiology

Volumn 36, Issue 10, 2009, Pages 1026-1033

  Boissé, Lysa ^a,b   Chisholm, Susan P ^c   Lukewich, Mark K ^c   Lomax, Alan E ^b,c,d  

^a Division of Neurology

^b Departments of Medicine   (Canada)

^c QUEEN S UNIVERSITY   (Canada)

^d KINGSTON GENERAL HOSPITAL   (Canada)

Author keywords

Calcium current; Electrophysiology; Inflammation; Inflammatory bowel diseases; Sympathetic neurotransmission

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM CHANNEL N TYPE; NEUROPEPTIDE Y; NEUROTRANSMITTER; NORADRENALIN; PURINE;

ADRENERGIC SYSTEM; ADRENERGIC TRANSMISSION; CALCIUM CURRENT; CROHN DISEASE; DEMYELINATING NEUROPATHY; ENTERITIS; HUMAN; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; INTESTINE INNERVATION; MUSCLE CELL; NERVE CELL; NEUROPHYSIOLOGY; NEUROTRANSMITTER RELEASE; NONHUMAN; PATHOGENESIS; REVIEW; SENSORY NERVE; SYMPATHETIC NERVE; ULCERATIVE COLITIS; VARICOSIS;

ANIMALS; AUTONOMIC NERVOUS SYSTEM DISEASES; DISEASE MODELS, ANIMAL; HUMANS; INFLAMMATION; INFLAMMATORY BOWEL DISEASES; INTESTINES; MODELS, BIOLOGICAL; SYMPATHETIC NERVOUS SYSTEM;

EID: 72449205192     PISSN: 03051870     EISSN: 14401681     Source Type: Journal    
DOI: 10.1111/j.1440-1681.2009.05242.x     Document Type: Review

References (92)

1. Xie J, Itzkowitz SH. Cancer in inflammatory bowel disease. World J. Gastroenterol. 2008; 14: 378-389
2. Xavier RJ, Podolsky DK. Unravelling the pathogenesis of inflammatory bowel disease. Nature 2007; 448:427-434 (Pubitemid 47123518)
3. Strober W, Fuss I,Mannon P. The fundamental basis of inflammatory bowel disease. J. Clin. Invest. 2007; 117: 514-521 (Pubitemid 46348505)
4. Tracey KJ. The inflammatory reflex. Nature 2002; 420: 853-859
5. Lomax AE,Linden DR, Mawe GM, Sharkey KA. Effects of gastrointestinal inflammation on enteroendocrine cells and enteric neural reflex, circuits. Auton. Neurosa, 2006; 127:250-257
6. Beyak MJ, Vanner S. Inflammation-induced hyperexcitability of nociceptive gastrointestinal DRG neurones. The role of voltage-gated ion channels. Neurogastroenterol. Motil. 2005; 17:175-186 (Pubitemid 40476677)
7. Geboes K, Collins S. Structural, abnormalities of the nervous system in Crohn's disease and ulcerative colitis. Neurogastroenterol. Motil. 1998; 10: 189-202. (Pubitemid 28286846)
8. Vasina V, Barbara G, Talamonti L et al. Enteric neuroplasticity evoked by inflammation. Auton. Neurosa. 2006; 127: 264-272
9. Collins SM. The immunomodulation of enteric neuromuscular function: Implications for motility and inflammatory disorders. Gastroenterology 1996; 111: 1683-1699
10. Bai A, Lu N, Guo Y, Chen J, Liu Z. Modulation of inflammatory response via alpha2-adrenoceptor blockade in acute murine colitis. Clin. Exp. Immunol. 2009; 156: 353-362
11. Rosas-Ballina M, Ochani M, Parrish WR et al. Splenic nerve is required for cholinergic antiinflammatory pathway control of TNF in endotoxemia. Proc. Natl Acad. Sci. USA 2008; 105:11008-11013
12. Kuratani K, Kodama H, Yamaguchi I. Enhancement of gastric mucosal, blood flow by beta-3 adrenergic agonists prevents indomethacin induced antral ulcer in the rat. J. Pharmacol. Exp. Ther. 1994; 270:559-565 (Pubitemid 24271366)
13. Borovikova LV, Ivanova S, Zhang M. et al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 2000; 405: 458-462 (Pubitemid 30367422)
14. The FO, Boeckxstaens GE, Snoek SA et al. Activation of the cholinergic anti-inflammatory pathway ameliorates postoperative ileus in mice. Gastroenterology 2007; 133: 1219-1228
15. Ghia JE, Blennerhassett P, Collins SM, Impaired parasympathetic function increases susceptibility to inflammatory bowel disease in a mouse model of depression. J. Clin. Invest. 2008; 118:2209-2218 (Pubitemid 351872339)
16. Straub RH, Grum. F, Strauch UG et al. Anti-inflammatory role of sympathetic nerves in chronic intestinal inflammation. Gut 2008; 57: 911-921, (Pubitemid 351919525)
17. Hughes P, Brierly S, Blackshaw LA. Post inflammatory modification of colonic afferent mechanosensitivity. Clin. Exp. Pharmacol. Physiol. 2009; 36: 1034-1040
18. Bron R, Furness JB. The rhythm of digestion: Keeping time in the gastrointestinal tract. Clin. Exp. Pharmacol. Physiol. 2009; 36: 1041-1048
19. Szurszewski JH, Miller SM. Physiology of prevertebral, ganglia. In: Johnson LR (ed.). Physiology of the Gastrointestinal Tract. Raven Press, New York. 1994; 795-877.
20. Furness JB, Clerc N, Vogalis F, Stebbing MJ. The enteric nervous system and its extrinsic connections. In: Yamada T (ed.). Textbook of Gastroenterology. Lippincot Williams, Baltimore. 2003; 12-34.
21. Miolan JP, Niel JP. The mammalian, sympathetic prevertebral ganglia: Integrative properties and role in the nervous control of digestive tract motility. J. Auton. Nerv. Syst. 1996; 58:125-138
22. Lomax AE. Anti-inflammatory effects of beta3-adrenoceptors: The burgeoning field of neurogastroimmunology. Neurogastroenterol. Motil. 2008; 20: 967-970
23. Burnstock G. Physiology and pathophysiology of purinergic neurotransmission. Physiol. Rev. 2007; 87: 659-797.
24. Neshat S, Devries M, Barajas-Espinosa AR, Skeith L, Chisholm SP, Lomax AE. Loss of purinergic vascular regulation in the colon during colitis is associated with upregulation of CD39. Am. J. Physiol. Gastrointest Liver Physiol. 2009; 296: G399-405.
25. 2+ current underlies the reduction in. noradrenaline release during colitis. Am. J. Physiol, Gastrointest. Liver Physiol, 2009; 296: G1077-84.
26. 2+ current in postganglionic sympathetic neurons. J. Physiol. 2009; 587:2623-2634
27. Blandizzi C. Enteric alpha-2 adrenoceptors: Pathophysiological implications in functional and inflammatory bowel disorders. Neurochem. Int. 2007; 51: 282-288 (Pubitemid 47374317)
28. Lam RS, App EM, Nahirney D et al. Regulation of Cl secretion by α-adrenergic receptors in mouse colonic epithelium. J. Physiol. 2003; 548:475-484
29. Lomax. AE, O'Reilly M, Neshat S, Vanner SJ. Sympathetic vasoconstrictor regulation of mouse colonic submucosal arterioles is altered in experimental colitis. J. Physiol. 2007; 583: 71.9-30 (Pubitemid 47343501)
30. Zhang L, Jensen RT, Maton PN. Characterization, of beta-adrenoreceptors on smooth muscle cells from guinea pig stomach. Am. J. Physiol. 1990; 259: G436-42. (Pubitemid 20317853)
31. Zhao A, Bossone C, Pineiro-Carrero V, Shea-Donohue T. Colitisinduced alterations in adrenergic control of circular smooth, muscle in vitro in rats. J. Pharmacol. Exp. Ther. 2001; 299: 768-774
32. Feiten. DL, Ackerman KD, Wiegand SJ, Feiten SY. Noradrenergic sympathetic innervation, of the spleen. I. Nerve fibers associate with lymphocytes and macrophages in specific compartments of the splenic white pulp. J. Neurosci. Reí. 1987; 18: 28-36. (Pubitemid 18101344)
33. Feiten SY, Feiten DL, Bellinger DL, Olschowka JA. Noradrenergic and peptidergic innervation of lymphoid organs. Chem. Immunol. 1992; 52: 25-48.
34. Madden KS, Sanders VM, Feiten DL. Catecholamine influences and sympathetic neural modulation of immune responsiveness. Annu. Rev. Pharmacol. Toxicol. 1995;35:417-448
35. Flierl MA, Rittirsch D, Nadeau BA et al. Phagocyte-derived catechol amines enhance acute inflammatory injury. Nature 2007; 449: 721-725 (Pubitemid 47552095)
36. 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.
37. Khan. MM, Sansoni P, Silverman ED, Engleman EG, Melmon KL. Beta-adrenergic receptors on human suppressor, helper, and cytolytic lymphocytes. Biochem. Pharmacol. 1986; 35:1137-1142 (Pubitemid 16075531)
38. Sanders V.M., Baker RA, Ramer-Quinn DS, Kasprowicz DJ, Fuchs BA, Street NE. Differential expression of the beta2-adrenergic receptor by Th1 and Th2 clones: Implications for cytokine production and B cell help. J. Immunol. 1997; 158:4200-4210
39. Kuratani K, Kodama H, Yamaguchi I. The differential roles of sympathetic nerve activity in the pathogenesis of antral and corpus lesions induced by indomethacin in rats. J. Pharmacol. Exp. Ther. 1994; 271:695-702. (Pubitemid 24377752)
40. Straub RH, Stebner K, Harte P, Kees F, Falk W, Scholmerich J. 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. Gui 2005; 54: 1098-1106 (Pubitemid 41025901)
41. McCafferty DM, Wallace JL, Sharkey KA, Effects of chemical sympathectomy and sensory nerve ablation on experimental colitis in the rat. Am. J. Physiol. 1997; 272: G272-80.
42. Saunders PR, Miceli P, Vallance BA et al. Noradrenergic and cholinergic neural pathways mediate stress-induced reactivation of colitis in the rat. Auton. Neurosa. 2006; 124: 56-68. (Pubitemid 43297858)
43. Straub RH, Wiest R, Strauch UG, Harte P, Scholmerich. J. The role of the sympathetic nervous system, in intestinal inflammation. Gut 2006; 55: 1640-1649 (Pubitemid 44629216)
44. Elenkov IJ, Hasko G, Kovacs KJ, Vizi ES. Modulation of lipopolysaccharide-induced tumor necrosis factor-alpha production by selective alpha- and beta-adrenergic drugs in mice. J. Neuroimmunol. 1995; 61: 123-131
45. Selmeczy Z, Szelenyi J, Vizi. ES. Intact noradrenaline transporter is needed for the sympathetic fine-tuning of cytokine balance. Eur. J. Pharmacol. 2003; 469: 175-181 (Pubitemid 36629564)
46. Szelenyi. J, Vizi ES. The catecholamine cytokine balance: Interaction between the brain, and the immune system. Ann. N. Y. Acad. Sci. 2007; 1113: 311-324 (Pubitemid 350015022)
47. Vasina V, bu-Gharbieh E, Barbara G et al. The beta3-adrenoceptor agonist SR58611A ameliorates experimental colitis in rats. Neurogastroenterol. Motil. 2008; 20: 1030-1041
48. Jacobson K, McHugh K, Collins SM. Experimental colitis alters myenteric nerve function at inflamed and noninflamed sites in the rat. Gastroenterology 1995; 109: 7.18-22.
49. Jacobson K, McHugh K, Collins SM. The mechanism of altered neural function in a rat model of acute colitis. Gastroenterology 1997; 112: 156-162 (Pubitemid 27008997)
50. Swain. MG, Blennerhassett PA, Collins SM. Impaired sympathetic nerve function, in the inflamed rat intestine. Gastroenterology 1991; 100: 675-682
51. Blandizzi C, Fornai M, Colucci R et al. Altered prejunctional modulation of intestinal cholinergic and noradrenergic pathways by alpha2adrenoceptors in the presence of experimental colitis. Br. J. Pharmacol. 2003; 139: 309-320 (Pubitemid 36760363)
52. Klein CM. Evaluation and management of autonomic nervous system disorders. Semin. Neurol. 2008; 28:195-204.
53. Gondim FA, Brannagan TH III, Sander HW, Chin. RL, Latov N. Peripheral neuropathy in. patients with inflammatory bowel, disease. Brain 2005; 128: 867-879 (Pubitemid 40516923)
54. Thaisetthawatkul P, Collazo-Clavell ML, Sarr MG, Norell JE, Dyck PJ. A controlled study of peripheral neuropathy after bariatric surgery. Neurology 2004; 63:1462-1470 (Pubitemid 39426282)
55. Navarro F, Hanauer SB. Treatment of inflammatory bowel disease: Safety and tolerability issues. Am. J. Gastroenterol. 2003; 98 (Suppl): S 18-23. (Pubitemid 38044603)
56. Scheid R, Teich N. Neurologic manifestations of ulcerative colitis. Eur. J. Neurol. 2007; 14:483-493
57. Lindgren S, Luja B, Rosen. I, Sundkvist G. Disturbed autonomic nerve function in patients with Crohn's disease. Scand. J. Gastroenterol. 1991; 26: 361-366
58. Lindgren. S, Stewenius J, Sjolund K, Lilja B, Sundkvist G. Autonomic vagal nerve dysfunction in patients with ulcerative colitis. Scand. J. Gastroenterol. 1993; 28: 638-642 (Pubitemid 23192697)
59. Ohlsson B, Sundkvist G, Lindgren S. Subclinical sympathetic neuropathy appears early in the course of Crohn's disease. BMC Gastroenterol. 2007; 7: 33.
60. Ohlsson B, Veress B, Lindgren S, Sundkvist G. Enteric ganglioneuritis and abnormal interstitial cells of Cajal: Features of inflammatory bowel disease. Inflamm. Bowel Dis. 2007; 13: 721-726 (Pubitemid 46909986)
61. Ganguli SC, Kamath MV, Redmond K et al. A comparison of autonomic function in patients with inflammatory bowel disease and in healthy controls. Neurogastroenterol. Motil. 2007; 19: 961-967 (Pubitemid 350198319)
62. Maule S, Pierangeli G, Cevoli S et al. Sympathetic hyperactivity in patients with ulcerative colitis. Clin. Auton. Res. 2007; 17: 21.7-20 (Pubitemid 47358563)
63. Straub RH, Antoniou E, Zeuner M, Gross V, Scholmerich J, Andus T. Association of autonomic nervous hyperreflexia and systemic inflammation in patients with. Crohn's disease and ulcerative colitis. J. Neuroimmunol. 1.997; 80: 149-157
64. Mouzas IA, Pallis AG, Kochiadakis GE et al. Autonomic imbalance during the day in patients with inflammatory bowel disease in remission. Evidence from spectral analysis of heart rate variability over 24 hours. Dig. Liver Dis. 2002; 34: 775-780
65. Lechin F, van der Dijs B, Insausti CL et al Treatment of ulcerative colitis with Clonidine. J. Clin. Pharmacol. 1985; 25: 219-226
66. Furlan. R, Ardizzone S, Palazzolo L et al. Sympathetic overactivity in active ulcerative colitis: Effects of Clonidine. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2006; 290: R224-32.
67. Beitzke M, Poster P, Fortin J, Škrabal F. Autonomie dysfunction and hemodynamics in vitamin B12 deficiency. Auton. Neumsci. 2002; 97:45-54. (Pubitemid 34234860)
68. Hobson-Webb LD, Roach ES, Donofrio PD. Metronidazole: Newly recognized cause of autonomic neuropathy. J. Child Neurol. 2006; 21: 429-431
69. Natah SS, Mouihate A, Pittman QJ, Sharkey KA. Disruption of the blood-brain barrier during TNBS colitis. Neurogastroenterol. Motil. 2005; 17:433-446 (Pubitemid 40768916)
70. Hathaway CA, Appleyard CB, Percy WH, Williams JL. Experimental colitis increases blood-brain barrier permeability in rabbits. Am. J. Physiol 1999; 276: G1174-80.
71. Hart PE, Gould SR, MacSweeney JE, Clifton A, Schon F. Brain whitematter lesions in inflammatory bowel disease. Lancet 1998; 351: 1558. (Pubitemid 28230897)
72. Lomax AE, Mawe GM, Sharkey KA. Synaptic facilitation and enhanced neuronal excitability in the submucosal plexus during experimental colitis in guinea-pig. J. Physiol. 2005; 564: 863-875
73. Lomax AE, Fernandez E, Sharkey KA. Plasticity of the enteric nervous , system during intestinal inflammation. Neurogastroenterol. Motil. 2005; 17:4-15. (Pubitemid 40204006)
74. Lomax AE, O'Hara JR, Hyland NP, Mawe GM, Sharkey KA. Persistent alterations to enteric neural signaling in the guinea pig colon following the resolution, of colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 2007; 292: G482-91.
75. O'Hara JR, Lomax AE, Mawe GM, Sharkey KA. Ileitis alters neuronal and enteroendocrine signalling in guinea pig distal colon. Gut 2007; 56: 186-194
76. Linden DR, Sharkey KA, Mawe GM. Enhanced excitability of myenteric AH neurones in. the inflamed guinea-pig distal colon. J. Physiol. 2003;547:589-601.
77. Linden DR, Chen JX, Gershon MD, Sharkey KA, Mawe GM. Serotonin availability is increased in mucosa of guinea pigs with TNBS-induced colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 2003; 285: G207-16.
78. + currents in mouse colonic dorsal root ganglia neurons and their role in colitis-induced hyperexcitability. Am. J. Physiol. Gastrointest. Liver Physiol. 2004; 287: G845-55.
79. Moore BA, Stewart TM, Hill C, Vanner SJ. TNBS ileitis evokes hyperexcitability and changes in ionic membrane properties of nociceptive DRG neurons. Am. J. Physiol. Gastrointest. Liver Physiol. 2002; 282: G1045-51. (Pubitemid 34651611)
80. Stewart T, Beyak MJ, Vanner S. Ileitis modulates potassium and sodium currents in guinea pig dorsal root ganglia sensory neurons. J. Physiol. 2003; 552: 797-807. (Pubitemid 37428421)
81. Dong XX, Thacker M, Pontell L, Furness JB, Nurgali K. Effects of intestinal inflammation on specific subgroups of guinea-pig celiac ganglion neurons. Neurosci. Lett. 2008; 444: 231-235
82. Nurgali. K, Nguyen TV, Matsuyama H, Thacker M, Robbins HL, Furness JB. Phenotypic changes of morphologically identified guinea-pig myenteric neurons following intestinal inflammation. J. Physiol. 2007; 583: 593-609. (Pubitemid 47351107)
83. 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; 47:216-224 (Pubitemid 34075041)
84. Catterall WA, Few AP. Calcium channel regulation and presynaptic plasticity. Neuron 2008; 59: 882-901.
85. Baker DM, Sanier RM, Blaggan AS. Morphometric studies on the microvasculature of pre- and paravertebral sympathetic ganglia in the adult and aged rat by light and electron microscopy. J. Neurocytol. 1989; 18: 647-660
86. Chau YP, Lu KS. Investigation of the blood-ganglion barrier properties in rat sympathetic ganglia by using lanthanum, ion and horseradish, per\oxidase as tracers. Acta Anat 1995; 153:135-144
87. Birch D, Knight GE, Boulos PB, Bumstock G. Analysis of innervation of human mesenteric vessels in. non-inflamed and inflamed bowel: A confocal and functional study. Neurogastroenterol. Motil 2008; 20: 660-670 (Pubitemid 351678621)
88. Belai A, Boulos PB, Robson T, Bumstock G. Neurochemical coding in the small intestine of patients with Crohn's disease. Gut 1.997; 40: 767-774
89. Nance DM, Sanders VM. Autonomic innervation and regulation of the immune system. (1987-2007). Brain Behav. Immun. 2007; 21: 736-745
90. Lundgren O. Microcirculation of the gastrointestinal tract, and pancreas. In: Renkin E, Michel CC (eds). Handbook of Physiology. The Cardiovascular System. Microcirculation. American Physiological Society, Bethesda, MD. 1984; 799-863.
91. Vanner S Surprenant A. Neural reflexes controlling intestinal microcirculation, Am. J. Physiol. 1996; 271: G223-30.
92. Hatoum OA, Miura H, Binion DG. The vascular contribution in the pathogenesis of inflammatory bowel disease. Am. J. Physiol. Heart Circ. Physiol. 2003; 285: H1791-6. (Pubitemid 37305919)