Involvement of interleukin-17A-induced hypercontractility of intestinal smooth muscle cells in persistent gut motor dysfunction

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Akiho, Hirotada ^a,b   Tokita, Yohei ^c   Nakamura, Kazuhiko ^a   Satoh, Kazuko ^c   Nishiyama, Mitsue ^c   Tsuchiya, Naoko ^c   Tsuchiya, Kazuaki ^c   Ohbuchi, Katsuya ^c   Iwakura, Yoichiro ^d,e   Ihara, Eikichi ^a   Takayanagi, Ryoichi ^a   Yamamoto, Masahiro ^c  

^a KYUSHU UNIVERSITY   (Japan)

^b KITAKYUSHU MUNICIPAL MEDICAL CENTER   (Japan)

^c TSUMURA AND CO   (Japan)

^d TOKYO UNIVERSITY OF SCIENCE   (Japan)

^e JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

I KAPPA B ZETA; INTERLEUKIN 17; MITOGEN ACTIVATED PROTEIN KINASE P38; MYOSIN LIGHT CHAIN 2; RGS4 PROTEIN; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; I KAPPA B KINASE; IL17A PROTEIN, MOUSE; IL1B PROTEIN, MOUSE; INTERLEUKIN 1BETA; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; MYOSIN; RGS PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CONTROLLED STUDY; DOWN REGULATION; ENTERITIS; ENZYME ACTIVATION; GASTROINTESTINAL MOTILITY DISORDER; GASTROINTESTINAL TRANSIT; HUMAN; HUMAN CELL; IN VITRO STUDY; INTESTINAL DYSMOTILITY; INTESTINE MUSCLE; MOUSE; NONHUMAN; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; DISEASE MODEL; GASTROINTESTINAL MOTILITY; GENETICS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY;

ANIMALS; DISEASE MODELS, ANIMAL; ENTERITIS; ENZYME ACTIVATION; GASTROINTESTINAL MOTILITY; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; HUMANS; I-KAPPA B KINASE; INTERLEUKIN-17; INTERLEUKIN-1BETA; MAP KINASE KINASE 4; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MYOSINS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RGS PROTEINS;

EID: 84900385526     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0092960     Document Type: Article

References (61)

1. Brand S (2009) Crohn's disease: Th1, Th17 or both? The change of a paradigm: new immunological and genetic insights implicate Th17 cells in the pathogenesis of Crohn's disease. Gut 58: 1152-1167.
2. Anderson CA, Massey DC, Barrett JC, Prescott NJ, Tremelling M, et al. (2009) Investigation of Crohn's disease risk loci in ulcerative colitis further defines their molecular relationship. Gastroenterology 136: 523-529 e523.
3. Khan WI, Collins SM (2006) Gut motor function: immunological control in enteric infection and inflammation. Clin Exp Immunol 143: 389-397.
4. Facco M, Brun P, Baesso I, Costantini M, Rizzetto C, et al. (2008) T cells in the myenteric plexus of achalasia patients show a skewed TCR repertoire and react to HSV-1 antigens. Am J Gastroenterol 103: 1598-1609.
5. Frasko R, Maruna P, Gurlich R, Trca S (2008) Transcutaneous electrogastrography in patients with ileus. Relations to interleukin-1beta, interleukin-6, procalcitonin and C-reactive protein. Eur Surg Res 41: 197-202.
6. Grover M, Herfarth H, Drossman DA (2009) The functional-organic dichotomy: postinfectious irritable bowel syndrome and inflammatory bowel disease-irritable bowel syndrome. Clin Gastroenterol Hepatol 7: 48-53.
7. El-Salhy M (2012) Irritable bowel syndrome: diagnosis and pathogenesis. World J Gastroenterol 18: 5151-5163.
8. Akiho H, Deng Y, Blennerhassett P, Kanbayashi H, Collins SM (2005) Mechanisms underlying the maintenance of muscle hypercontractility in a model of postinfective gut dysfunction. Gastroenterology 129: 131-141. (Pubitemid 41002050)
9. Akiho H, Blennerhassett P, Deng Y, Collins SM (2002) Role of IL-4, IL-13, and STAT6 in inflammation-induced hypercontractility of murine smooth muscle cells. Am J Physiol Gastrointest Liver Physiol 282: G226-232. (Pubitemid 34651678)
10. Khan WI, Vallance BA, Blennerhassett PA, Deng Y, Verdu EF, et al. (2001) Critical role for signal transducer and activator of transcription factor 6 in mediating intestinal muscle hypercontractility and worm expulsion in Trichinella spiralis-infected mice. Infect Immun 69: 838-844. (Pubitemid 32109547)
11. Kobayashi T, Okamoto S, Hisamatsu T, Kamada N, Chinen H, et al. (2008) IL23 differentially regulates the Th1/Th17 balance in ulcerative colitis and Crohn's disease. Gut 57: 1682-1689.
12. Ohama T, Hori M, Momotani E, Iwakura Y, Guo F, et al. (2007) Intestinal inflammation downregulates smooth muscle CPI-17 through induction of TNF-alpha and causes motility disorders. Am J Physiol Gastrointest Liver Physiol 292: G1429-1438. (Pubitemid 47084664)
13. Schwarz NT, Kalff JC, Turler A, Speidel N, Grandis JR, et al. (2004) Selective jejunal manipulation causes postoperative pan-enteric inflammation and dysmotility. Gastroenterology 126: 159-169. (Pubitemid 38040733)
14. Kinoshita K, Sato K, Hori M, Ozaki H, Karaki H (2003) Decrease in activity of smooth muscle L-type Ca2+ channels and its reversal by NF-kappaB inhibitors in Crohn's colitis model. Am J Physiol Gastrointest Liver Physiol 285: G483-493. (Pubitemid 37021808)
15. Nakae S, Komiyama Y, Nambu A, Sudo K, Iwase M, et al. (2002) Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 17: 375-387. (Pubitemid 35279557)
16. de Backer O, Blanckaert B, Leybaert L, Lefebvre RA (2008) A novel method for the evaluation of intestinal transit and contractility in mice using fluorescence imaging and spatiotemporal motility mapping. Neurogastroenterol Motil 20: 700-707. (Pubitemid 351678614)
17. Yanai T, Kobayashi H, Yamataka A, Lane GJ, Miyano T, et al. (2004) Acetylcholine-related bowel dysmotility in homozygous mutant NCX/HOX11L.1-deficient (NCX-/-) mice-evidence that acetylcholine is implicated in causing intestinal neuronal dysplasia. J Pediatr Surg 39: 927-930. (Pubitemid 38833784)
18. Mizutani T, Akiho H, Khan WI, Murao H, Ogino H, et al. (2010) Persistent gut motor dysfunction in a murine model of T-cell-induced enteropathy. Neurogastroenterol Motil 22: 196-203, e165.
19. Miura N, Yamamoto M, Fukutake M, Ohtake N, Iizuka S, et al. (2005) Anti-CD3 induces bi-phasic apoptosis in murine intestinal epithelial cells: possible involvement of the Fas/Fas ligand system in different T cell compartments. Int Immunol 17: 513-522. (Pubitemid 41417848)
20. Merger M, Viney JL, Borojevic R, Steele-Norwood D, Zhou P, et al. (2002) Defining the roles of perforin, Fas/FasL, and tumour necrosis factor alpha in T cell induced mucosal damage in the mouse intestine. Gut 51: 155-163. (Pubitemid 34791439)
21. Kim HR, Appel S, Vetterkind S, Gangopadhyay SS, Morgan KG (2008) Smooth muscle signalling pathways in health and disease. J Cell Mol Med 12: 2165-2180.
22. Hu W, Mahavadi S, Li F, Murthy KS (2007) Upregulation of RGS4 and downregulation of CPI-17 mediate inhibition of colonic muscle contraction by interleukin-1beta. Am J Physiol Cell Physiol 293: C1991-2000. (Pubitemid 350258450)
23. Tovey SC, Willars GB (2004) Single-cell imaging of intracellular Ca2+ and phospholipase C activity reveals that RGS 2, 3, and 4 differentially regulate signaling via the Galphaq/11-linked muscarinic M3 receptor. Mol Pharmacol 66: 1453-1464. (Pubitemid 39564772)
24. Roy AA, Lemberg KE, Chidiac P (2003) Recruitment of RGS2 and RGS4 to the plasma membrane by G proteins and receptors reflects functional interactions. Mol Pharmacol 64: 587-593. (Pubitemid 37048561)
25. Hu W, Li F, Mahavadi S, Murthy KS (2008) Interleukin-1beta up-regulates RGS4 through the canonical IKK2/IkappaBalpha/NF-kappaB pathway in rabbit colonic smooth muscle. Biochem J 412: 35-43.
26. Gujral N, Freeman HJ, Thomson AB (2013) Celiac disease: prevalence, diagnosis, pathogenesis and treatment. World J Gastroenterol 18: 6036-6059.
27. Tursi A (2004) Gastrointestinal motility disturbances in celiac disease. J Clin Gastroenterol 38: 642-645.
28. Bassotti G, Villanacci V, Mazzocchi A, Mariano M, Incardona P, et al. (2008) Antroduodenojejunal motor activity in untreated and treated celiac disease patients. J Gastroenterol Hepatol 23: e23-28. (Pubitemid 352019400)
29. Ciaccio EJ, Tennyson CA, Bhagat G, Lewis SK, Green PH (2012) Quantitative estimates of motility from videocapsule endoscopy are useful to discern celiac patients from controls. Dig Dis Sci 57: 2936-2943.
30. Cullmann JL, Bickelhaupt S, Froehlich JM, Szucs-Farkas Z, Tutuian R, et al. (2013) MR imaging in Crohn's disease: correlation of MR motility measurement with histopathology in the terminal ileum. Neurogastroenterol Motil 25: 749-e577.
31. Bickelhaupt S, Pazahr S, Chuck N, Blume I, Froehlich JM, et al. (2013) Crohn's disease: small bowel motility impairment correlates with inflammatory-related markers C-reactive protein and calprotectin. Neurogastroenterol Motil 25: 467-473.
32. Menys A, Helbren E, Makanyanga J, Emmanuel A, Forbes A, et al. (2013) Small bowel strictures in Crohn's disease: a quantitative investigation of intestinal motility using MR enterography. Neurogastroenterol Motil 25: 967-e775.
33. De Schepper HU, De Man JG, Moreels TG, Pelckmans PA, De Winter BY (2008) Review article: gastrointestinal sensory and motor disturbances in inflammatory bowel disease - clinical relevance and pathophysiological mechanisms. Aliment Pharmacol Ther 27: 621-637. (Pubitemid 351406302)
34. Liebregts T, Adam B, Bredack C, Roth A, Heinzel S, et al. (2007) Immune activation in patients with irritable bowel syndrome. Gastroenterology 132: 913-920. (Pubitemid 46440872)
35. Al-Khatib K, Lin HC (2009) Immune activation and gut microbes in irritable bowel syndrome. Gut Liver 3: 14-19.
36. Dunlop SP, Jenkins D, Neal KR, Spiller RC (2003) Relative importance of enterochromaffin cell hyperplasia, anxiety, and depression in postinfectious IBS. Gastroenterology 125: 1651-1659. (Pubitemid 37500429)
37. Spiller RC, Jenkins D, Thornley JP, Hebden JM, Wright T, et al. (2000) Increased rectal mucosal enteroendocrine cells, T lymphocytes, and increased gut permeability following acute Campylobacter enteritis and in post-dysenteric irritable bowel syndrome. Gut 47: 804-811.
38. Cremon C, Gargano L, Morselli-Labate AM, Santini D, Cogliandro RF, et al. (2009) Mucosal immune activation in irritable bowel syndrome: gender-dependence and association with digestive symptoms. Am J Gastroenterol 104: 392-400.
39. Cann PA, Read NW, Brown C, Hobson N, Holdsworth CD (1983) Irritable bowel syndrome: relationship of disorders in the transit of a single solid meal to symptom patterns. Gut 24: 405-411. (Pubitemid 13089484)
40. Gwee KA, Leong YL, Graham C, McKendrick MW, Collins SM, et al. (1999) The role of psychological and biological factors in postinfective gut dysfunction. Gut 44: 400-406. (Pubitemid 29119338)
41. Sadik R, Bjornsson E, Simren M (2010) The relationship between symptoms, body mass index, gastrointestinal transit and stool frequency in patients with irritable bowel syndrome. Eur J Gastroenterol Hepatol 22: 102-108.
42. Camilleri M, Katzka DA (2012) Irritable bowel syndrome: methods, mechanisms, and pathophysiology. Genetic epidemiology and pharmacogenetics in irritable bowel syndrome. Am J Physiol Gastrointest Liver Physiol 302: G1075-1084.
43. Fernandez S, Molina IJ, Romero P, Gonzalez R, Pena J, et al. (2011) Characterization of gliadin-specific Th17 cells from the mucosa of celiac disease patients. Am J Gastroenterol 106: 528-538.
44. Monteleone I, Sarra M, Del Vecchio Blanco G, Paoluzi OA, Franze E, et al. (2010) Characterization of IL-17A-producing cells in celiac disease mucosa. J Immunol 184: 2211-2218.
45. Castellanos-Rubio A, Santin I, Irastorza I, Castano L, Carlos Vitoria J, et al. (2009) TH17 (and TH1) signatures of intestinal biopsies of CD patients in response to gliadin. Autoimmunity 42: 69-73.
46. Raza A, Yousaf W, Giannella R, Shata MT (2012) Th17 cells: interactions with predisposing factors in the immunopathogenesis of inflammatory bowel disease. Expert Rev Clin Immunol 8: 161-168.
47. Ortega C, Fernandez S, Estevez OA, Aguado R, Molina IJ, et al. (2013) IL-17 producing T cells in celiac disease: angels or devils? Int Rev Immunol 32: 534-543.
48. Geremia A, Jewell DP (2012) The IL-23/IL-17 pathway in inflammatory bowel disease. Expert Rev Gastroenterol Hepatol 6: 223-237.
49. Hundorfean G, Neurath MF, Mudter J (2012) Functional relevance of T helper 17 (Th17) cells and the IL-17 cytokine family in inflammatory bowel disease. Inflamm Bowel Dis 18: 180-186.
50. Hueber W, Sands BE, Lewitzky S, Vandemeulebroecke M, Reinisch W, et al. (2012) Secukinumab, a human anti-IL-17A monoclonal antibody, for moderate to severe Crohn's disease: unexpected results of a randomised, double-blind placebo-controlled trial. Gut 61: 1693-1700.
51. Patel DD, Lee DM, Kolbinger F, Antoni C (2013) Effect of IL-17A blockade with secukinumab in autoimmune diseases. Ann Rheum Dis 72 Suppl 2: ii116-123.
52. Esplugues E, Huber S, Gagliani N, Hauser AE, Town T, et al. (2011) Control of TH17 cells occurs in the small intestine. Nature 475: 514-518.
53. Kudo M, Melton AC, Chen C, Engler MB, Huang KE, et al. (2012) IL-17A produced by alphabeta T cells drives airway hyper-responsiveness in mice and enhances mouse and human airway smooth muscle contraction. Nat Med 18: 547-554.
54. Aube AC, Blottiere HM, Scarpignato C, Cherbut C, Roze C, et al. (1996) Inhibition of acetylcholine induced intestinal motility by interleukin 1 beta in the rat. Gut 39: 470-474. (Pubitemid 26338540)
55. Ohama T, Hori M, Sato K, Ozaki H, Karaki H (2003) Chronic treatment with interleukin-1beta attenuates contractions by decreasing the activities of CPI-17 and MYPT-1 in intestinal smooth muscle. J Biol Chem 278: 48794-48804. (Pubitemid 41079522)
56. Reynolds AM, Holmes MD, Scicchitano R (2000) Cytokines enhance airway smooth muscle contractility in response to acetylcholine and neurokinin A. Respirology 5: 153-160. (Pubitemid 30434963)
57. Wu ZX, Satterfield BE, Fedan JS, Dey RD (2002) Interleukin-1beta-induced airway hyperresponsiveness enhances substance P in intrinsic neurons of ferret airway. Am J Physiol Lung Cell Mol Physiol 283: L909-917. (Pubitemid 35204882)
58. Amrani Y, Lazaar AL, Panettieri RA Jr (1999) Up-regulation of ICAM-1 by cytokines in human tracheal smooth muscle cells involves an NF-kappa B-dependent signaling pathway that is only partially sensitive to dexamethasone. J Immunol 163: 2128-2134. (Pubitemid 29382219)
59. Shan X, Hu A, Veler H, Fatma S, Grunstein JS, et al. (2006) Regulation of Toll-like receptor 4-induced proasthmatic changes in airway smooth muscle function by opposing actions of ERK1/2 and p38 MAPK signaling. Am J Physiol Lung Cell Mol Physiol 291: L324-333. (Pubitemid 44343706)
60. Hu W, Li F, Mahavadi S, Murthy KS (2009) Upregulation of RGS4 expression by IL-1beta in colonic smooth muscle is enhanced by ERK1/2 and p38 MAPK and inhibited by the PI3K/Akt/GSK3beta pathway. Am J Physiol Cell Physiol 296: C1310-1320.
61. Zhang Y, Li F, Liu S, Wang H, Mahavadi S, et al. (2012) MEKK1-MKK4-JNK-AP1 pathway negatively regulates Rgs4 expression in colonic smooth muscle cells. PLoS One 7: e35646.