Effects of inflammation on the innervation of the colon

Toxicologic Pathology

Volumn 42, Issue 1, 2014, Pages 111-117

  Moynes, Derek M ^a   Lucas, Graydon H ^a   Beyak, Michael J ^a   Lomax, Alan E ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

animal models; cellular pathology; digestive system; inflammation; nervous system.

Indexed keywords

ADRENERGIC SYSTEM; ARTICLE; COLITIS; DEFECATION HABIT; GASTROINTESTINAL TRACT; HUMAN; INFLAMMATION; INTESTINE INNERVATION; MOTOR SYSTEM; NONHUMAN; PAIN; PRIORITY JOURNAL; SENSORY NERVE; SYMPATHETIC INNERVATION;

ANIMAL MODELS; CELLULAR PATHOLOGY; DIGESTIVE SYSTEM; INFLAMMATION; NERVOUS SYSTEM.;

ANIMALS; COLON; DISEASE MODELS, ANIMAL; HUMANS; INFLAMMATION; INFLAMMATORY BOWEL DISEASES; NEURONS;

EID: 84892705541     PISSN: 01926233     EISSN: 15331601     Source Type: Journal    
DOI: 10.1177/0192623313505929     Document Type: Article

References (101)

1. Antonioli L., Fornai M., Colucci R., Ghisu N., Tuccori M., Awwad O., Bin A., Zoppellaro C., Castagliuolo I., Gaion R. M., Giron M. C., Blandizzi C.. Control of enteric neuromuscular functions by purinergic A(3) receptors in normal rat distal colon and experimental bowel inflammation. Br J Pharmacol. 2010 ; 161: 856-71
2. Asfaha S., Bell C. J., Wallace J. L., Macnaughton W. K.. Prolonged colonic epithelial hyporesponsiveness after colitis: Role of inducible nitric oxide synthase. Am J Physiol. 1999 ; 276: G703-10
3. Belai A., Boulos P. B., Robson T., Burnstock G.. Neurochemical coding in the small intestine of patients with Crohn's disease. Gut. 1997 ; 40: 767-74
4. Bernardini N., Segnani C., Ippolito C., De Giorgio R., Colucci R., Faussone-Pellegrini M. S., Chiarugi M., Campani D., Castagna M., Mattii L., Blandizzi C., Dolfi A.. Immunohistochemical analysis of myenteric ganglia and interstitial cells of Cajal in ulcerative colitis. J Cell Mol Med. 2012 ; 16: 318-27
5. Bertrand P. P., Kunze W. A., Furness J. B., Bornstein J. C.. The terminals of myenteric intrinsic primary afferent neurons of the guinea-pig ileum are excited by 5-hydroxytryptamine acting at 5-hydroxytryptamine-3 receptors. Neuroscience. 2000 ; 101: 459-69
6. Beyak M. J., Ramji N., Krol K. M., Kawaja M. D., Vanner S. J.. Two TTX-resistant Na+ 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
7. Birch D., Knight G. E., Boulos P. B., Burnstock G.. Analysis of innervation of human mesenteric vessels in non-inflamed and inflamed bowel - A confocal and functional study. Neurogastroenterol Motil. 2008 ; 20: 660-70
8. Blandizzi C.. Enteric alpha-2 adrenoceptors: Pathophysiological implications in functional and inflammatory bowel disorders. Neurochem Int. 2007 ; 51: 282-88
9. Blandizzi C., Fornai M., Colucci R., Baschiera F., Barbara G., De Giorgio R., De Ponti F., Breschi M. C., Del Tacca M.. Altered prejunctional modulation of intestinal cholinergic and noradrenergic pathways by alpha2-adrenoceptors in the presence of experimental colitis. Br J Pharmacol. 2003 ; 139: 309-20
10. Bornstein J. C., Furness J. B., Kunze W. A.. Electrophysiological characterization of myenteric neurons: How do classification schemes relate?. J Auton Nerv Syst. 1994 ; 48: 1-15
11. Boyer L., Ghoreishi M., Templeman V., Vallance B. A., Buchan A. M., Jevon G., Jacobson K.. Myenteric plexus injury and apoptosis in experimental colitis. Auton Neurosci. 2005 ; 117: 41-53
12. Brierley S. M., Jones R. C., Gebhart G. F., Blackshaw L. A.. Splanchnic and pelvic mechanosensory afferents signal different qualities of colonic stimuli in mice. Gastroenterology. 2004 ; 127: 166-78
13. Brookes S. J.. Classes of enteric nerve cells in the guinea-pig small intestine. Anat Rec. 2001 ; 262: 58-70
14. Brookes S. J., Spencer N. J., Costa M., Zagorodnyuk V. P.. Extrinsic primary afferent signalling in the gut. Nat Rev Gastroenterol Hepatol. 2013 ; 10: 286-96
15. Brunsden A. M., Brookes S. J., Bardhan K. D., Grundy D.. Mechanisms underlying mechanosensitivity of mesenteric afferent fibers to vascular flow. Am J Physiol Gastrointest Liver Physiol. 2007 ; 293: G422-28
16. Coldwell J. R., Phillis B. D., Sutherland K., Howarth G. S., Blackshaw L. A.. Increased responsiveness of rat colonic splanchnic afferents to 5-HT after inflammation and recovery. J Physiol. 2007 ; 579: 203-13
17. Collins S. M., Hurst S. M., Main C., Stanley E., Khan I., Blennerhassett P., Swain M.. Effect of inflammation of enteric nerves. Cytokine-induced changes in neurotransmitter content and release. Ann N Y Acad Sci. 1992 ; 664: 415-24
18. Crivellato E., Soldano F., Travan L.. A light and electron microscopic quantitative analysis of nerve-immune cell contacts in the gut-associated lymphoid tissue of the mouse colon. J Submicr Cytol Pathol. 2002 ; 34: 55-66
19. Defaweux V., Dorban G., Demonceau C., Piret J., Jolois O., Thellin O., Thielen C., Heinen E., Antoine N.. Interfaces between dendritic cells, other immune cells, and nerve fibres in mouse Peyer's patches: Potential sites for neuroinvasion in prion diseases. Microsc Res Tech. 2005 ; 66: 1-9
20. De Schepper H. U., De Man J. G., Ruyssers N. E., Deiteren A., Van Nassauw L., Timmermans J. P., Martinet W., Herman A. G., Pelckmans P. A., De Winter B. Y.. TRPV1 receptor signaling mediates afferent nerve sensitization during colitis-induced motility disorders in rats. Am J Physiol Gastrointest Liver Physiol. 2008 ; 294: G245-53
21. Dong X. X., Thacker M., Pontell L., Furness J. B., Nurgali K.. Effects of intestinal inflammation on specific subgroups of guinea-pig celiac ganglion neurons. Neurosci Lett. 2008 ; 444: 231-35
22. Dvorak A. M., Osage J. E., Monahan R. A., Dickersin G. R.. Crohn's disease: Transmission electron microscopic studies. III. Target tissues. Proliferation of and injury to smooth muscle and the autonomic nervous system. Hum Pathol. 1980 ; 11: 620-34
23. Dvorak A. M., Silen W.. Differentiation between Crohn's disease and other inflammatory conditions by electron microscopy. Ann Surg. 1985 ; 201: 53-63
24. Elenkov I. J., Wilder R. L., Chrousos G. P., Vizi E. S.. The sympathetic nerve - An integrative interface between two supersystems: The brain and the immune system. Pharmacol Rev. 2000 ; 52: 595-638
25. Evans R. J., Surprenant A.. Vasoconstriction of guinea-pig submucosal arterioles following sympathetic nerve stimulation is mediated by the release of ATP. Br J Pharmacol. 1992 ; 106: 242-49
26. Feng B., La J. H., Tanaka T., Schwartz E. S., McMurray T. P., Gebhart G. F.. Altered colorectal afferent function associated with TNBS-induced visceral hypersensitivity in mice. Am J Physiol Gastrointest Liver Physiol. 2012 ; 303: G817-24
27. Furlan R., Ardizzone S., Palazzolo L., Rimoldi A., Perego F., Barbic F., Bevilacqua M., Vago L., Bianchi P. G., Malliani A.. Sympathetic overactivity in active ulcerative colitis: Effects of clonidine. Am J Physiol Regul Integr Comp Physiol. 2006 ; 290: R224-32
28. Furness J. B. The Enteric Nervous System. Cambridge, MA: Blackwell Publishing ; 2006 :
29. Furness J. B.. The enteric nervous system and neurogastroenterology. Nat Rev Gastroenterol Hepatol. 2012 ; 9: 286-94
30. Furness J. B., Clerc N., Vogalis F., Stebbing M. J. Textbook of Gastroenterology. Yamada T. Alpers D. H., ed. Riverwoods, IL: Lippincot Williams ; 2003: 12-34.
31. Furness J. B., Jones C., Nurgali K., Clerc N.. Intrinsic primary afferent neurons and nerve circuits within the intestine. Prog Neurobiol. 2004 ; 72: 143-64
32. Ganguli S. C., Kamath M. V., Redmond K., Chen Y., Irvine E. J., Collins S. M., Tougas G.. A comparison of autonomic function in patients with inflammatory bowel disease and in healthy controls. Neurogastroenterol Motil. 2007 ; 19: 961-67
33. Geboes K., Collins S.. Structural abnormalities of the nervous system in Crohn's disease and ulcerative colitis. Neurogastroenterol Motil. 1998 ; 10: 189-202
34. Gershon MD, Kirchgessner AL, Wade PR Physiology of the Gastrointestinal Tract. Johnson LR Alpers DH Jacobson ED Walsh ED, ed. New York: Raven Press ; 381-422.
35. Gibbs G. F., Drummond P. D., Finch P. M., Phillips J. K.. Unravelling the pathophysiology of complex regional pain syndrome: Focus on sympathetically maintained pain. Clin Exp Pharmacol Physiol. 2008 ; 35: 717-24
36. Grundy D.. Signalling the state of the digestive tract. Auton Neurosci. 2006 ; 125: 76-80
37. Gulbransen B. D., Bashashati M., Hirota S. A., Gui X., Roberts J. A., MacDonald J. A., Muruve D. A., McKay D. M., Beck P. L., Mawe G. M., Thompson R. J., Sharkey K. A.. Activation of neuronal P2X7 receptor-pannexin-1 mediates death of enteric neurons during colitis. Nat Med. 2012 ; 18: 600-4
38. Harrington A. M., Brierley S. M., Isaacs N., Hughes P. A., Castro J., Blackshaw L. A.. Sprouting of colonic afferent central terminals and increased spinal mitogen-activated protein kinase expression in a mouse model of chronic visceral hypersensitivity. J Comp Neurol. 2012 ; 520: 2241-55
39. Hatoum O. A., Binion D. G., Otterson M. F., Gutterman D. D.. Acquired microvascular dysfunction in inflammatory bowel disease: Loss of nitric oxide-mediated vasodilation. Gastroenterology. 2003 ; 125: 58-69
40. Hirst G. D., Johnson S. M., van Helden D. F.. The slow calcium-dependent potassium current in a myenteric neurone of the guinea-pig ileum. J Physiol. 1985 ; 361: 315-37
41. Hirst G. D., McKirdy H. C.. Presynaptic inhibition at mammalian peripheral synapse?. Nature. 1974 ; 250: 430-31
42. Hons I. M., Storr M. A., Mackie K., Lutz B., Pittman Q. J., Mawe G. M., Sharkey K. A.. Plasticity of mouse enteric synapses mediated through endocannabinoid and purinergic signaling. Neurogastroenterol Motil. 2012 ; 24: e113-24
43. Hughes P. A., Brierley S. M., Martin C. M., Brookes S. J., Linden D. R., Blackshaw L. A.. Post-inflammatory colonic afferent sensitisation: Different subtypes, different pathways and different time courses. Gut. 2009 ; 58: 1333-41
44. Huizinga J. D., Lammers W. J.. Gut peristalsis is governed by a multitude of cooperating mechanisms. Am J Physiol Gastrointest Liver Physiol. 2009 ; 296: G1-8
45. Izzo A. A., Camilleri M.. Emerging role of cannabinoids in gastrointestinal and liver diseases: Basic and clinical aspects. Gut. 2008 ; 57: 1140-55
46. Izzo A. A., Camilleri M.. Cannabinoids in intestinal inflammation and cancer. Pharmacol Res. 2009 ; 60: 117-25
47. Izzo A. A., Sharkey K. A.. Cannabinoids and the gut: New developments and emerging concepts. Pharmacol Therapeut. 2010 ; 126: 21-38
48. Jacobson K., McHugh K., Collins S. M.. Experimental colitis alters myenteric nerve function at inflamed and noninflamed sites in the rat. Gastroenterology. 1995 ; 109: 718-22
49. Janig W.. Integration of gut function by sympathetic reflexes. Bailliere Clin Gastroenterol. 1988 ; 2: 45-62
50. Krauter E. M., Strong D. S., Brooks E. M., Linden D. R., Sharkey K. A., Mawe G. M.. Changes in colonic motility and the electrophysiological properties of myenteric neurons persist following recovery from trinitrobenzene sulfonic acid colitis in the guinea pig. Neurogastroenterol Motil. 2007 ; 19: 990-1000
51. Kyosola K., Penttila O., Salaspuro M.. Rectal mucosal adrenergic innervation and enterochromaffin cells in ulcerative colitis and irritable colon. Scand J Gastroenterol. 1977 ; 12: 363-67
52. La J. H., Gebhart G. F.. Colitis decreases mechanosensitive K2P channel expression and function in mouse colon sensory neurons. Am J Physiol Gastrointest Liver Physiology. 2011 ; 301: G165-74
53. Linden D. R., Couvrette J. M., Ciolino A., McQuoid C., Blaszyk H., Sharkey K. A., Mawe G. M.. Indiscriminate loss of myenteric neurones in the TNBS-inflamed guinea-pig distal colon. Neurogastroenterol Motil. 2005 ; 17: 751-60
54. Linden D. R., Sharkey K. A., Ho W., Mawe G. M.. Cyclooxygenase-2 contributes to dysmotility and enhanced excitability of myenteric AH neurones in the inflamed guinea pig distal colon. J Physiol. 2004 ; 557: 191-205
55. Linden D. R., Sharkey K. A., Mawe G. M.. Enhanced excitability of myenteric AH neurones in the inflamed guinea-pig distal colon. J Physiol. 2003 ; 547: 589-601
56. Lomax A. E., Fernandez E., Sharkey K. A.. Plasticity of the enteric nervous system during intestinal inflammation. Neurogastroenterol Motil. 2005 ; 17: 4-15
57. Lomax A. E., Linden D. R., Mawe G. M., Sharkey K. A.. Effects of gastrointestinal inflammation on enteroendocrine cells and enteric neural reflex circuits. Auton Neurosci. 2006 ; 126-127: 250-57
58. Lomax A. E., Mawe G. M., Sharkey K. A.. Synaptic facilitation and enhanced neuronal excitability in the submucosal plexus during experimental colitis in guinea-pig. J Physiol. 2005 ; 564: 863-75
59. Lomax A. E., O'Hara J. R., Hyland N. P., Mawe G. M., Sharkey K. A.. 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
60. Lomax A. E., O'Reilly M., Neshat S., Vanner S. J.. Sympathetic vasoconstrictor regulation of mouse colonic submucosal arterioles is altered in experimental colitis. J Physiol. 2007 ; 583: 719-30
61. Lomax A. E., Sharkey K. A., Furness J. B.. The participation of the sympathetic innervation of the gastrointestinal tract in disease states. Neurogastroenterol Motil. 2010 ; 22: 7-18
62. Lomax A. E., Zhang J. Y., Furness J. B.. Origins of cholinergic inputs to the cell bodies of intestinofugal neurons in the guinea pig distal colon. J Comp Neurol. 2000 ; 416: 451-60
63. Lourenssen S., Wells R. W., Blennerhassett M. G.. Differential responses of intrinsic and extrinsic innervation of smooth muscle cells in rat colitis. Exp Neurol. 2005 ; 195: 497-507
64. Lundgren O. Handbook of Physiology. The Cardiovascular System. Microcirculation. Renkin E. M. C. C., ed. Bethesda, MD: American Physiological Society ; 1984: 799-863.
65. Lynn P. A., Blackshaw L. A. In vitro recordings of afferent fibres with receptive fields in the serosa, muscle and mucosa of rat colon. J Physiol. 1999 ; 518 (Pt 1). 271-82
66. Lynn P. A., Brookes S. J.. Function and morphology correlates of rectal nerve mechanoreceptors innervating the guinea pig internal anal sphincter. Neurogastroenterol Motil. 2011 ; 23: 88-95
67. Lynn P., Zagorodnyuk V., Hennig G., Costa M., Brookes S.. Mechanical activation of rectal intraganglionic laminar endings in the guinea pig distal gut. J Physiol. 2005 ; 564: 589-601
68. Magro F., Vieira-Coelho M. A., Fraga S., Serrao M. P., Veloso F. T., Ribeiro T., Soares-da-Silva P.. Impaired synthesis or cellular storage of norepinephrine, dopamine, and 5-hydroxytryptamine in human inflammatory bowel disease. Dig Dis Sci. 2002 ; 47: 216-24
69. Manning B. P., Sharkey K. A., Mawe G. M.. Effects of PGE2 in guinea pig colonic myenteric ganglia. Am J Physiol Gastrointest Liver Physiol. 2002 ; 283: G1388-97
70. Matsumoto K., Lo M. W., Hosoya T., Tashima K., Takayama H., Murayama T., Horie S.. Experimental colitis alters expression of 5-HT receptors and transient receptor potential vanilloid 1 leading to visceral hypersensitivity in mice. Lab Invest. 2012 ; 92: 769-82
71. Maule S., Pierangeli G., Cevoli S., Grimaldi D., Gionchetti P., Barbara G., Rizzello F., Stanghellini V., Corinaldesi R., Campieri M., Cortelli P.. Sympathetic hyperactivity in patients with ulcerative colitis. Clin Auton Res. 2007 ; 17: 217-20
72. Mawe G. M., Strong D. S., Sharkey K. A.. Plasticity of enteric nerve functions in the inflamed and postinflamed gut. Neurogastroenterol Motil. 2009 ; 21: 481-91
73. Mazumdar S., Das K. M.. Immunocytochemical localization of vasoactive intestinal peptide and substance P in the colon from normal subjects and patients with inflammatory bowel disease. Am J Gastroenterol. 1992 ; 87: 176-81
74. McCafferty D. M., Wallace J. L., Sharkey K. A.. Effects of chemical sympathectomy and sensory nerve ablation on experimental colitis in the rat. Am J Physiol. 1997 ; 272: G272-80
75. Mori M., Stokes K. Y., Vowinkel T., Watanabe N., Elrod J. W., Harris N. R., Lefer D. J., Hibi T., Granger D. N.. Colonic blood flow responses in experimental colitis: Time course and underlying mechanisms. Am J Physiol Gastrointest Liver Physiol. 2005 ; 289: G1024-29
76. Motagally M. A., Lukewich M. K., Chisholm S. P., Neshat S., Lomax A. E.. Tumour necrosis factor alpha activates nuclear factor kappaB signalling to reduce N-type voltage-gated Ca2+ current in postganglionic sympathetic neurons. J Physiol. 2009 ; 587: 2623-34
77. Motagally M. A., Neshat S., Lomax A. E.. Inhibition of sympathetic N-type voltage-gated Ca2+ current underlies the reduction in norepinephrine release during colitis. Am J Physiol Gastrointest Liver Physiol. 2009 ; 296: G1077-84
78. Neshat S., Devries M., Barajas-Espinosa A. R., Skeith L., Chisholm S. P., Lomax A. E.. Loss of purinergic vascular regulation in the colon during colitis is associated with upregulation of CD39. Am J Physiol Gastrointest Liver Physiol. 2009 ; 296: G399-05
79. Neunlist M., Aubert P., Toquet C., Oreshkova T., Barouk J., Lehur P. A., Schemann M., Galmiche J. P.. Changes in chemical coding of myenteric neurones in ulcerative colitis. Gut. 2003 ; 52: 84-90
80. Nurgali K., Qu Z., Hunne B., Thacker M., Pontell L., Furness J. B.. Morphological and functional changes in guinea-pig neurons projecting to the ileal mucosa at early stages after inflammatory damage. J Physiol. 2011 ; 589: 325-39
81. Roberts J. A., Lukewich M. K., Sharkey K. A., Furness J. B., Mawe G. M., Lomax A. E.. The roles of purinergic signaling during gastrointestinal inflammation. Curr Opin Pharmacol. 2012 ; 12: 659-66
82. Sanders K. M.. G protein-coupled receptors in gastrointestinal physiology. IV. Neural regulation of gastrointestinal smooth muscle. Am J Physiol. 1998 ; 275: G1-7
83. Sanders V. M.. The beta2-adrenergic receptor on T and B lymphocytes: Do we understand it yet?. Brain Behav Immun. 2012 ; 26: 195-200
84. Sanders K. M., Koh S. D., Ro S., Ward S. M.. Regulation of gastrointestinal motility - Insights from smooth muscle biology. Nat Rev Gastroenterol Hepatol. 2012 ; 9: 633-45
85. Sanovic S., Lamb D. P., Blennerhassett M. G.. Damage to the enteric nervous system in experimental colitis. Am J Pathol. 1999 ; 155: 1051-57
86. Sharma P., Makharia G. K., Ahuja V., Dwivedi S. N., Deepak K. K.. Autonomic dysfunctions in patients with inflammatory bowel disease in clinical remission. Dig Dis Sci. 2009 ; 54: 853-61
87. Sjovall H., Redfors S., Hallback D. A., Eklund S., Jodal M., Lundgren O.. The effect of splanchnic nerve stimulation on blood flow distribution, villous tissue osmolality and fluid and electrolyte transport in the small intestine of the cat. Acta Physiologica Scandinavica. 1983a ; 117: 359-65
88. Sjovall H., Redfors S., Jodal M., Lundgren O.. On the mode of action of the sympathetic fibres on intestinal fluid transport: Evidence for the existence of a glucose-stimulated secretory nervous pathway in the intestinal wall. Acta physiologica Scandinavica. 1983b ; 119: 39-48
89. Stewart T., Beyak M. J., Vanner S.. Ileitis modulates potassium and sodium currents in guinea pig dorsal root ganglia sensory neurons. J Physiol. 2003 ; 552: 797-807
90. Straub R. H., Grum F., Strauch U., Capellino S., Bataille F., Bleich A., Falk W., Scholmerich J., Obermeier F.. Anti-inflammatory role of sympathetic nerves in chronic intestinal inflammation. Gut. 2008 ; 57: 911-21
91. Straub R. H., Wiest R., Strauch U. G., Harle P., Scholmerich J.. The role of the sympathetic nervous system in intestinal inflammation. Gut. 2006 ; 55: 1640-49
92. Swain M. G., Blennerhassett P. A., Collins S. M.. Impaired sympathetic nerve function in the inflamed rat intestine. Gastroenterology. 1991 ; 100: 675-82
93. Szurszewski J. H., Ermilov L. G., Miller S. M. Prevertebral ganglia and intestinofugal afferent neurones. Gut. 2002 ; 51 (Suppl 1). i6-10
94. Szurszewski J. H., Miller S. M. Physiology of the Gastrointestinal Tract. Johnson L. R., ed. New York, NY: Raven press ; 1994: 795-877.
95. Vanner S., Macnaughton W. K. Submucosal secretomotor and vasodilator reflexes. Neurogastroenterol Motil. 2004 ; 16 (Suppl 1). 39-43
96. Vanner S., Surprenant A.. Neural reflexes controlling intestinal microcirculation. Am J Physiol. 1996 ; 271: G223-30
97. Vento P., Kiviluoto T., Keranen U., Jarvinen H. J., Kivilaakso E., Soinila S.. Quantitative comparison of growth-associated protein-43 and substance P in ulcerative colitis. J Histochem Cytochem. 2001 ; 49: 749-58
98. Vogalis F., Furness J. B., Kunze W. A.. Afterhyperpolarization current in myenteric neurons of the guinea pig duodenum. J Neurophysiol. 2001 ; 85: 1941-51
99. Wood J. D., Alpers D. H., Andrews P. L. Fundamentals of neurogastroenterology. Gut. 1999 ; 45 (Suppl 2). II6-16
100. Wynn G., Ma B., Ruan H. Z., Burnstock G.. Purinergic component of mechanosensory transduction is increased in a rat model of colitis. Am J Physiol Gastrointest Liver Physiol. 2004 ; 287: G647-57
101. Xia C. M., Colomb D. G., Akbarali H. I., Qiao L. Y.. Prolonged sympathetic innervation of sensory neurons in rat thoracolumbar dorsal root ganglia during chronic colitis. Neurogastroenterol Motil. 2011 ; 23: 801 - e339