Loss of guanylyl cyclase C (GCC) Signaling leads to dysfunctional intestinal barrier

PLoS ONE

Volumn 6, Issue 1, 2011, Pages

  Han, Xiaonan ^a   Mann, Elizabeth ^a   Gilbert, Shila ^a   Guan, Yanfang ^b   Steinbrecher, Kris A ^a   Montrose, Marshall H ^b   Cohen, Mitchell B ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b UNIVERSITY OF CINCINNATI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLAUDIN 2; GAMMA INTERFERON; GUANYLATE CYCLASE C; JUNCTIONAL ADHESION MOLECULE A; LIPOPOLYSACCHARIDE; MEMBRANE RECEPTOR; MYOSIN II; MYOSIN LIGHT CHAIN KINASE; STAT1 PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UROGUANYLIN; ATRIAL NATRIURETIC FACTOR RECEPTOR; ENTEROTOXIN RECEPTOR; MLCK PEPTIDE; PEPTIDE; RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE PERMEABILITY; CELL STRAIN CACO 2; CELL STRAIN HT29; CONTROLLED STUDY; INTESTINE BARRIER; INTESTINE EPITHELIUM CELL; INTESTINE FUNCTION; INTESTINE INJURY; INTESTINE MUCOSA; INTESTINE MUCOSA PERMEABILITY; MONOLAYER CULTURE; MOUSE; NONHUMAN; PERMEABILITY BARRIER; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; ANIMAL; CELL CULTURE; ENZYMOLOGY; INTESTINE; METABOLISM; MOUSE MUTANT; PATHOPHYSIOLOGY; PERMEABILITY; TIGHT JUNCTION;

MUS;

ANIMALS; CELLS, CULTURED; INTESTINAL MUCOSA; INTESTINES; MICE; MICE, KNOCKOUT; PEPTIDES; PERMEABILITY; RECEPTORS, GUANYLATE CYCLASE-COUPLED; RECEPTORS, PEPTIDE; SIGNAL TRANSDUCTION; TIGHT JUNCTIONS;

EID: 79551650331     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0016139     Document Type: Article

References (62)

1. Li P, Lin JE, Marszlowicz GP, Valentino MA, Chang C, et al. (2009) GCC signaling in colorectal cancer: Is colorectal cancer a paracrine deficiency syndrome? Drug News Perspect 22: 313-318.
2. Lin JE, Li P, Pitari GM, Schulz S, Waldman SA (2009) Guanylyl cyclase C in colorectal cancer: susceptibility gene and potential therapeutic target. Future Oncol 5: 509-522.
3. Lorenz JN, Nieman M, Sabo J, Sanford LP, Hawkins JA, et al. (2003) Uroguanylin knockout mice have increased blood pressure and impaired natriuretic response to enteral NaCl load. J Clin Invest 112: 1244-1254.
4. Schulz S, Green CK, Yuen PS, Garbers DL (1990) Guanylyl cyclase is a heatstable enterotoxin receptor. Cell 63: 941-948.
5. Zhang W, Mannan I, Schulz S, Parkinson SJ, Alekseev AE, et al. (1999) Interruption of transmembrane signaling as a novel antisecretory strategy to treat enterotoxigenic diarrhea. Faseb J 13: 913-922.
6. Li P, Lin JE, Chervoneva I, Schulz S, Waldman SA, et al. (2007) Homeostatic control of the crypt-villus axis by the bacterial enterotoxin receptor guanylyl cyclase C restricts the proliferating compartment in intestine. Am J Pathol 171: 1847-1858.
7. Li P, Schulz S, Bombonati A, Palazzo JP, Hyslop TM, et al. (2007) Guanylyl cyclase C suppresses intestinal tumorigenesis by restricting proliferation and maintaining genomic integrity. Gastroenterology 133: 599-607.
8. Carrithers SL, Barber MT, Biswas S, Parkinson SJ, Park PK, et al. (1996) Guanylyl cyclase C is a selective marker for metastatic colorectal tumors in human extraintestinal tissues. Proc Natl Acad Sci U S A 93: 14827-14832.
9. Lin JE, Li P, Snook AE, Schulz S, Dasgupta A, et al. (2010) The Hormone Receptor GUCY2C Suppresses Intestinal Tumor Formation by Inhibiting AKT Signaling. Gastroenterology.
10. Basu N, Bhandari R, Natarajan VT, Visweswariah SS (2009) Cross talk between receptor guanylyl cyclase C and c-src tyrosine kinase regulates colon cancer cell cytostasis. Mol Cell Biol 29: 5277-5289.
11. Garin-Laflam MP, Steinbrecher KA, Rudolph JA, Mao J, Cohen MB (2009) Activation of guanylate cyclase C signaling pathway protects intestinal epithelial cells from acute radiation-induced apoptosis. Am J Physiol Gastrointest Liver Physiol 296: G740-749.
12. Matter K, Balda MS (2003) Signalling to and from tight junctions. Nat Rev Mol Cell Biol 4: 225-236.
13. Mitic LL, Anderson JM (1998) Molecular architecture of tight junctions. Annu Rev Physiol 60: 121-142.
14. Ebnet K, Suzuki A, Ohno S, Vestweber D (2004) Junctional adhesion molecules (JAMs): more molecules with dual functions? J Cell Sci 117: 19-29.
15. Fanning AS, Anderson JM (2009) Zonula occludens-1 and -2 are cytosolic scaffolds that regulate the assembly of cellular junctions. Ann N Y Acad Sci 1165: 113-120.
16. Blair SA, Kane SV, Clayburgh DR, Turner JR (2006) Epithelial myosin light chain kinase expression and activity are upregulated in inflammatory bowel disease. Lab Invest 86: 191-201.
17. Wang F, Graham WV, Wang Y, Witkowski ED, Schwarz BT, et al. (2005) Interferon-gamma and tumor necrosis factor-alpha synergize to induce intestinal epithelial barrier dysfunction by up-regulating myosin light chain kinase expression. Am J Pathol 166: 409-419.
18. Wang F, Schwarz BT, Graham WV, Wang Y, Su L, et al. (2006) IFN-gammainduced TNFR2 expression is required for TNF-dependent intestinal epithelial barrier dysfunction. Gastroenterology 131: 1153-1163.
19. Mazzarella G, MacDonald TT, Salvati VM, Mulligan P, Pasquale L, et al. (2003) Constitutive activation of the signal transducer and activator of transcription pathway in celiac disease lesions. Am J Pathol 162: 1845-1855.
20. Moriez R, Salvador-Cartier C, Theodorou V, Fioramonti J, Eutamene H, et al. (2005) Myosin light chain kinase is involved in lipopolysaccharide-induced disruption of colonic epithelial barrier and bacterial translocation in rats. Am J Pathol 167: 1071-1079.
21. Clayburgh DR, Barrett TA, Tang Y, Meddings JB, Van Eldik LJ, et al. (2005) Epithelial myosin light chain kinase-dependent barrier dysfunction mediates T cell activation-induced diarrhea in vivo. J Clin Invest 115: 2702-2715.
22. Swenson ES, Mann EA, Jump ML, Witte DP, Giannella RA (1996) The guanylin/STa receptor is expressed in crypts and apical epithelium throughout the mouse intestine. Biochem Biophys Res Commun 225: 1009-1014.
23. Qian X, Prabhakar S, Nandi A, Visweswariah SS, Goy MF (2000) Expression of GC-C, a receptor-guanylate cyclase, and its endogenous ligands uroguanylin and guanylin along the rostrocaudal axis of the intestine. Endocrinology 141: 3210-3224.
24. Han X, Fink MP, Yang R, Delude RL (2004) Increased iNOS activity is essential for intestinal epithelial tight junction dysfunction in endotoxemic mice. Shock 21: 261-270.
25. Turner JR (2009) Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 9: 799-809.
26. Mudter J, Weigmann B, Bartsch B, Kiesslich R, Strand D, et al. (2005) Activation pattern of signal transducers and activators of transcription (STAT) factors in inflammatory bowel diseases. Am J Gastroenterol 100: 64-72.
27. Schwarz BT, Wang F, Shen L, Clayburgh DR, Su L, et al. (2007) LIGHT signals directly to intestinal epithelia to cause barrier dysfunction via cytoskeletal and endocytic mechanisms. Gastroenterology 132: 2383-2394.
28. Mann EA, Jump ML, Wu J, Yee E, Giannella RA (1997) Mice lacking the guanylyl cyclase C receptor are resistant to STa-induced intestinal secretion. Biochem Biophys Res Commun 239: 463-466.
29. Yu QH, Yang Q (2009) Diversity of tight junctions (TJs) between gastrointestinal epithelial cells and their function in maintaining the mucosal barrier. Cell Biol Int 33: 78-82.
30. Lubbe WJ, Zuzga DS, Zhou Z, Fu W, Pelta-Heller J, et al. (2009) Guanylyl cyclase C prevents colon cancer metastasis by regulating tumor epithelial cell matrix metalloproteinase-9. Cancer Res 69: 3529-3536.
31. Michl P, Barth C, Buchholz M, Lerch MM, Rolke M, et al. (2003) Claudin-4 expression decreases invasiveness and metastatic potential of pancreatic cancer. Cancer Res 63: 6265-6271.
32. Song X, Li X, Tang Y, Chen H, Wong B, et al. (2008) Expression of claudin-2 in the multistage process of gastric carcinogenesis. Histol Histopathol 23: 673-682.
33. Gonzalez-Mariscal L, Lechuga S, Garay E (2007) Role of tight junctions in cell proliferation and cancer. Prog Histochem Cytochem 42: 1-57.
34. Buccigrossi V, Armellino C, Ruberto E, Vittoria Barone M, De Marco G, et al. (2010) Polar effects on ion transport and cell proliferation induced by GC-C ligands in intestinal epithelial cells. Pediatr Res.
35. Cohen MB, Witte DP, Hawkins JA, Currie MG (1995) Immunohistochemical localization of guanylin in the rat small intestine and colon. Biochem Biophys Res Commun 209: 803-808.
36. Wisner DM, Harris LR, 3rd, Green CL, Poritz LS (2008) Opposing regulation of the tight junction protein claudin-2 by interferon-gamma and interleukin-4. J Surg Res 144: 1-7.
37. Utech M, Ivanov AI, Samarin SN, Bruewer M, Turner JR, et al. (2005) Mechanism of IFN-gamma-induced endocytosis of tight junction proteins: myosin II-dependent vacuolarization of the apical plasma membrane. Mol Biol Cell 16: 5040-5052.
38. Ceponis PJ, McKay DM, Ching JC, Pereira P, Sherman PM (2003) Enterohemorrhagic Escherichia coli O157:H7 disrupts Stat1-mediated gamma interferon signal transduction in epithelial cells. Infect Immun 71: 1396-1404.
39. Hassan SW, Doody KM, Hardy S, Uetani N, Cournoyer D, et al. (2010) Increased susceptibility to dextran sulfate sodium induced colitis in the T cell protein tyrosine phosphatase heterozygous mouse. PLoS One 5: e8868.
40. Su L, Shen L, Clayburgh DR, Nalle SC, Sullivan EA, et al. (2009) Targeted epithelial tight junction dysfunction causes immune activation and contributes to development of experimental colitis. Gastroenterology 136: 551-563.
41. Ye D, Ma I, Ma TY (2006) Molecular mechanism of tumor necrosis factor-alpha modulation of intestinal epithelial tight junction barrier. Am J Physiol Gastrointest Liver Physiol 290: G496-504.
42. Bazzoni G, Dejana E (2004) Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis. Physiol Rev 84: 869-901.
43. Laukoetter MG, Nava P, Lee WY, Severson EA, Capaldo CT, et al. (2007) JAM-A regulates permeability and inflammation in the intestine in vivo. J Exp Med 204: 3067-3076.
44. Olson TS, Reuter BK, Scott KG, Morris MA, Wang XM, et al. (2006) The primary defect in experimental ileitis originates from a nonhematopoietic source. J Exp Med 203: 541-552.
45. Amasheh S, Meiri N, Gitter AH, Schoneberg T, Mankertz J, et al. (2002) Claudin-2 expression induces cation-selective channels in tight junctions of epithelial cells. J Cell Sci 115: 4969-4976.
46. Zeissig S, Burgel N, Gunzel D, Richter J, Mankertz J, et al. (2007) Changes in expression and distribution of claudin 2, 5 and 8 lead to discontinuous tight junctions and barrier dysfunction in active Crohn's disease. Gut 56: 61-72.
47. Blikslager AT, Moeser AJ, Gookin JL, Jones SL, Odle J (2007) Restoration of barrier function in injured intestinal mucosa. Physiol Rev 87: 545-564.
48. Dunlop SP, Hebden J, Campbell E, Naesdal J, Olbe L, et al. (2006) Abnormal intestinal permeability in subgroups of diarrhea-predominant irritable bowel syndromes. Am J Gastroenterol 101: 1288-1294.
49. Strober W, Fuss I, Mannon P (2007) The fundamental basis of inflammatory bowel disease. J Clin Invest 117: 514-521.
50. Eutamene H, Bradesi S, Larauche M, Theodorou V, Beaufrand C, et al. (2009) Guanylate cyclase C-mediated antinociceptive effects of linaclotide in rodent models of visceral pain. Neurogastroenterol Motil.
51. Johnston JM, Kurtz CB, Drossman DA, Lembo AJ, Jeglinski BI, et al. (2009) Pilot study on the effect of linaclotide in patients with chronic constipation. Am J Gastroenterol 104: 125-132.
52. Han X, Ren X, Jurickova I, Groschwitz K, Pasternak BA, et al. (2009) Regulation of intestinal barrier function by signal transducer and activator of transcription 5b. Gut 58: 49-58.
53. Guan Y, Worrell RT, Pritts TA, Montrose MH (2009) Intestinal ischemiareperfusion injury: reversible and irreversible damage imaged in vivo. Am J Physiol Gastrointest Liver Physiol 297: G187-196.
54. Marchiando AM, Shen L, Graham WV, Weber CR, Schwarz BT, et al. (2010) Caveolin-1-dependent occludin endocytosis is required for TNF-induced tight junction regulation in vivo. J Cell Biol 189: 111-126.
55. Han X, Sosnowska D, Bonkowski EL, Denson LA (2005) Growth hormone inhibits signal transducer and activator of transcription 3 activation and reduces disease activity in murine colitis. Gastroenterology 129: 185-203.
56. Han X, Osuntokun B, Benight N, Loesch K, Frank SJ, et al. (2006) Signal transducer and activator of transcription 5b promotes mucosal tolerance in pediatric Crohn's disease and murine colitis. Am J Pathol 169: 1999-2013.
57. Leclercq IA, Field J, Farrell GC (2003) Leptin-specific mechanisms for impaired liver regeneration in ob/ob mice after toxic injury. Gastroenterology 124: 1451-1464.
58. Shivakumar P, Campbell KM, Sabla GE, Miethke A, Tiao G, et al. (2004) Obstruction of extrahepatic bile ducts by lymphocytes is regulated by IFNgamma in experimental biliary atresia. J Clin Invest 114: 322-329.
59. Han X, Fink MP, Delude RL (2003) Proinflammatory cytokines cause NO*- dependent and -independent changes in expression and localization of tight junction proteins in intestinal epithelial cells. Shock 19: 229-237.
60. Han X, Uchiyama T, Sappington PL, Yaguchi A, Yang R, et al. (2003) NAD+ ameliorates inflammation-induced epithelial barrier dysfunction in cultured enterocytes and mouse ileal mucosa. J Pharmacol Exp Ther 307: 443-449.
61. Drudy D, O'Donoghue DP, Baird A, Fenelon L, O'Farrelly C (2001) Flow cytometric analysis of Clostridium difficile adherence to human intestinal epithelial cells. J Med Microbiol 50: 526-534.
62. Han X, Gilbert S, Groschwitz K, Hogan S, Jurickova I, et al. (2010) Loss of GM-CSF signalling in non-haematopoietic cells increases NSAID ileal injury. Gut 59: 1066-1078.