Intestinal inflammation downregulates smooth muscle CPI-17 through induction of TNF-α and causes motility disorders

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 292, Issue 5, 2007, Pages

  Ohama, Takashi ^a   Hori, Masatoshi ^a   Momotani, Eiichi ^b   Iwakura, Yoichiro ^c   Guo, Fengling ^d   Kishi, Hiroko ^d   Kobayashi, Sei ^d   Ozaki, Hiroshi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b NATIONAL INSTITUTE OF ANIMAL HEALTH   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d YAMAGUCHI UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Smooth muscle contraction; Tumor necrosis factor

Indexed keywords

BETA ESCIN; CALCIUM ION; CARBACHOL; CHOLINERGIC RECEPTOR STIMULATING AGENT; CPI 17 PROTEIN; CYTOKINE; GUANOSINE TRIPHOSPHATE; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; NITROBENZENE DERIVATIVE; PHOSPHOPROTEIN PHOSPHATASE INHIBITOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ESCIN; MUSCLE PROTEIN; PHOSPHOPROTEIN; PPP1R14A PROTEIN, MOUSE; PPP1R14A PROTEIN, RAT; TRINITROBENZENESULFONIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ILEITIS; ILEUM; IN VIVO STUDY; INTESTINAL DYSMOTILITY; INTESTINE MUSCLE; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REGULATORY MECHANISM; SENSITIZATION; SMOOTH MUSCLE CONTRACTION; SMOOTH MUSCLE FIBER; WILD TYPE; ANIMAL; BIOSYNTHESIS; CHEMICALLY INDUCED DISORDER; DISEASE MODEL; ENTEROPATHY; GASTROINTESTINAL MOTILITY; PHYSIOLOGY; SMOOTH MUSCLE;

ANIMALS; CARBACHOL; DISEASE MODELS, ANIMAL; DOWN-REGULATION; ESCIN; GASTROINTESTINAL MOTILITY; ILEITIS; INTERLEUKIN-1BETA; INTESTINAL DISEASES; MALE; MICE; MUSCLE PROTEINS; MUSCLE, SMOOTH; PHOSPHOPROTEINS; RATS; TRINITROBENZENESULFONIC ACID; TUMOR NECROSIS FACTOR-ALPHA;

EID: 34347373914     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00315.2006     Document Type: Article

References (42)

1. Akbarali HI, Pothoulakis C, Castagliuolo I. Altered ion channel activity in murine colonic smooth muscle myocytes in an experimental colitis model. Biochem Biophys Res Commun 275: 637-642, 2000.
2. Akiho H, Blennerhassett P, Deng Y, Collins SM. 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-G232, 2002.
3. Akiho H, Deng Y, Blennerhassett P, Kanbayashi H, Collins SM. Mechanisms underlying the maintenance of muscle hypercontractility in a model of postinfective gut dysfunction. Gastroenterology 129: 131-141, 2005.
4. Blennerhassett MG, Vignjevic P, Vermillion DL, Collins SM. Inflammation causes hyperplasia and hypertrophy in smooth muscle of rat small intestine. Am J Physiol Gastrointest Liver Physiol 262: G1041-G1046, 1992.
5. Cobrin GM, Abreu MT. Defects in mucosal immunity leading to Crohn's disease. Immunol Rev 206: 277-295, 2005.
6. Collins SM. The immunomodulation of enteric neuromuscular function: implications for motility and inflammatory disorders. Gastroenterology 111: 1683-1699, 1996.
7. Eto M, Kitazawa T, Brautigan DL. Phosphoprotein inhibitor CPI-17 specificity depends on allosteric regulation of protein phosphatase-1 by regulatory subunits. Proc Natl Acad Sci USA 101: 8888-8893, 2004.
8. Eto M, Ohmori T, Suzuki M, Furuya K, Morita F. A novel protein phosphatase-1 inhibitory protein potentiated by protein kinase C. Isolation from porcine aorta media and characterization. J Biochem (Tokyo) 118: 1104-1107, 1995.
9. Eto M, Senba S, Morita F, Yazawa M. Molecular cloning of a novel phosphorylation-dependent inhibitory protein of protein phosphatase-1 (CPI17) in smooth muscle: its specific localization in smooth muscle. FEBS Lett 410: 356-360, 1997.
10. 2+ sensitization of skinned muscle of guinea pig vas deferens. J Pharmacol Exp Ther 274: 555-561, 1995.
11. Hamaguchi T, Ito M, Feng J, Seko T, Koyama M, Machida H, Takase K, Amano M, Kaibuchi K, Hartshorne DJ, Nakano T. Phosphorylation of CPI-17, an inhibitor of myosin phosphatase, by protein kinase N. Biochem Biophys Res Commun 274: 825-830, 2000.
12. Hierholzer C, Kalff JC, Billiar TR, Bauer AJ, Tweardy DJ, Harbrecht BG. Induced nitric oxide promotes intestinal inflammation following hemorrhagic shock. Am J Physiol Gastrointest Liver Physiol 286: G225-G233, 2004.
13. Hirata K, Kikuchi A, Sasaki T, Kuroda S, Kaibuchi K, Matsuura Y, Seki H, Saida K, Takai Y. Involvement of rho p21 in the GTP-enhanced calcium ion sensitivity of smooth muscle contraction. J Biol Chem 267: 8719-8722, 1992.
14. Horai R, Asano M, Sudo K, Kanuka H, Suzuki M, Nishihara M, Takahashi M, Iwakura Y. Production of mice deficient in genes for interleukin (IL)-1α, IL-1β, IL-1α/β, and IL-1 receptor antagonist shows that IL-1β is crucial in turpentine-induced fever development and glucocorticoid secretion. J Exp Med 187: 1463-1475, 1998.
15. + channels in experimental colitis. Am J Physiol Gastrointest Liver Physiol 287: G274-G285, 2004.
16. Kalff JC, Schraut WH, Simmons RL, Bauer AJ. Surgical manipulation of the gut elicits an intestinal muscularis inflammatory response resulting in postsurgical ileus. Ann Surg 228: 652-663, 1998.
17. Kaneko H, Yamada H, Mizuno S, Udagawa T, Kazumi Y, Sekikawa K, Sugawara I. Role of tumor necrosis factor-α in Mycobacterium induced granuloma formation in tumor necrosis factor-α-deficient mice. Lab Invest 79: 379-386, 1999.
18. 2+ channel isoforms in murine colon: effect of inflammation. Pflügers Arch 449: 288-297, 2004.
19. Kinoshita K, Hori M, Fujisawa M, Sato K, Ohama T, Momotani E, Ozaki H. Role of TNF-α in muscularis inflammation and motility disorder in a TNBS-induced colitis model: clues from TNF-α-deficient mice. Neurogastroenterol Motil 18: 578-588, 2006.
20. 2+ channels and its reversal by NF-κB inhibitors in Crohn's colitis model. Am J Physiol Gastrointest Liver Physiol 285: G483-G493, 2003.
21. Kitazawa T, Eto M, Woodsome TP, Brautigan DL. Agonists trigger G protein-mediated activation of the CPI-17 inhibitor phosphoprotein of myosin light chain phosphatase to enhance vascular smooth muscle contractility. J Biol Chem 275: 9897-9900, 2000.
22. 2+ sensitization in rabbit smooth muscle. J Physiol 546: 879-889, 2003.
23. Kiyosue M, Fujisawa M, Kinoshita K, Hori M, Ozaki H. Different susceptibilities of spontaneous rhythmicity and myogenic contractility to intestinal muscularis inflammation in the hapten-induced colitis. Neurogastroenterol Motil 18: 1019-1030, 2006.
24. 2+ release in smooth muscle. Physiological role of inositol 1,4,5-trisphosphate in pharmacomechanical coupling. J Biol Chem 264: 17997-18004, 1989.
25. Koyama M, Ito M, Feng J, Seko T, Shiraki K, Takase K, Hartshorne DJ, Nakano T. Phosphorylation of CPI-17, an inhibitory phosphoprotein of smooth muscle myosin phosphatase, by Rho-kinase. FEBS Lett 475: 197-200, 2000.
26. Koyluoglu G, Kaya T, Bagcivan I, Yildiz T. Effect of L-NAME on decreased ileal muscle contractility induced by peritonitis in rats. J Pediatr Surg 37: 901-905, 2002.
27. Liu X, Rusch NJ, Striessnig J, Sarna SK. Down-regulation of L-type calcium channels in inflamed circular smooth muscle cells of the canine colon. Gastroenterology 120: 480-489, 2001.
28. MacDonald JA, Eto M, Borman MA, Brautigan DL, Haystead TA. Dual Ser and Thr phosphorylation of CPI-17, an inhibitor of myosin phosphatase, by MYPT-associated kinase. FEBS Lett 493: 91-94, 2001.
29. Mawe GM, Collins SM, Shea-Donohue T. Changes in enteric neural circuitry and smooth muscle in the inflamed and infected gut. Neurogastroenterol Motil 16, Suppl 1: 133-136, 2004.
30. Moreels TG, De Man JG, Dick JM, Nieuwendijk RJ, De Winter BY, Lefebvre RA, Herman AG, Pelckmans PA. Effect of TNBS-induced morphological changes on pharmacological contractility of the rat ileum. Eur J Pharmacol 423: 211-222, 2001.
31. Neurath MF, Fuss I, Kelsall BL, Stuber E, Strober W. Antibodies to interleukin 12 abrogate established experimental colitis in mice. J Exp Med 182: 1281-1290, 1995.
32. Ohama T, Hori M, Sato K, Ozaki H, Karaki H. Chronic treatment with interleukin-1β attenuates contractions by decreasing the activities of CPI-17 and MYPT-1 in intestinal smooth muscle. J Biol Chem 278: 48794-48804, 2003.
33. Pazdrak K, Shi XZ, Sarna SK. TNFα suppresses human colonic circular smooth muscle cell contractility by SP1- and NF-κB-mediated induction of ICAM-1. Gastroenterology 127: 1096-1109, 2004.
34. Salinthone S, Singer CA, Gerthoffer WT. Inflammatory gene expression by human colonic smooth muscle cells. Am J Physiol Gastrointest Liver Physiol 287: G627-G637, 2004.
35. Schwarz NT, Kalff JC, Turler A, Speidel N, Grandis JR, Billiar TR, Bauer AJ. Selective jejunal manipulation causes postoperative panenteric inflammation and dysmotility. Gastroenterology 126: 159-169, 2004.
36. Shi XZ, Pazdrak K, Saada N, Dai B, Palade P, Sarna SK. Negative transcriptional regulation of human colonic smooth muscle Cav1.2 channels by p50 and p65 subunits of nuclear factor-κB. Gastroenterology 129: 1518-1532, 2005.
37. Shi XZ, Sarna SK. G protein-mediated dysfunction of excitation-contraction coupling in ileal inflammation. Am J Physiol Gastrointest Liver Physiol 286: G899-G905, 2004.
38. Shi XZ, Sarna SK. Transcriptional regulation of inflammatory mediators secreted by human colonic circular smooth muscle cells. Am J Physiol Gastrointest Liver Physiol 289: G274-G284, 2005.
39. 2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase. Physiol Rev 83: 1325-1358, 2003.
40. Suzuki T, Won KJ, Horiguchi K, Kinoshita K, Hori M, Torihashi S, Momotani E, Itoh K, Hirayama K, Ward SM, Sanders KM, Ozaki H. Muscularis inflammation and the loss of interstitial cells of Cajal in the endothelin ETB receptor null rat. Am J Physiol Gastrointest Liver Physiol 287: G638-G646, 2004.
41. Vermillion DL, Collins SM. Increased responsiveness of jejunal longitudinal muscle in Trichinella-infected rats. Am J Physiol Gastrointest Liver Physiol 254: G124-G129, 1988.
42. Won KJ, Suzuki T, Hori M, Ozaki H. Motility disorder in experimentally obstructed intestine: relationship between muscularis inflammation and disruption of the ICC network. Neurogastroenterol Motil 18: 53-61, 2006.