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Review

Pharmacology and clinical potential of guanylyl cyclase C agonists in the treatment of ulcerative colitis

Pages 351-360 | Published online: 19 Apr 2013

References

  • Langan RC Gotsch PB Krafczyk MA Skillinge DD Ulcerative colitis: diagnosis and treatment Am Fam Physician 2007 76 9 1323 1330 18019875
  • Lakatos PL Recent trends in the epidemiology of inflammatory bowel diseases: up or down? World J Gastroenterol 2006 12 38 6102 6108 17036379
  • Blumberg RS Strober W Prospects for research in inflammatory bowel disease JAMA 2001 285 5 643 647 11176874
  • Podolsky DK Inflammatory bowel disease N Engl J Med 2002 347 6 417 429 12167685
  • Xavier RJ Podolsky DK Unravelling the pathogenesis of inflammatory bowel disease Nature 2007 448 7152 427 434 17653185
  • Sartor RB Mechanisms of disease: pathogenesis of Crohn’s disease and ulcerative colitis Nat Clin Pract Gastroenterol Hepatol 2006 3 7 390 407 16819502
  • Guerrant RL Hughes JM Chang B Robertson DC Murad F Activation of intestinal guanylate cyclase by heat-stable enterotoxin of Escherichia coli: studies of tissue specificity, potential receptors, and intermediates J Infect Dis 1980 142 2 220 228 6106030
  • Forte LR Guanylin regulatory peptides: structures, biological activities mediated by cyclic GMP and pathobiology Regul Pept 1999 81 1–3 25 39 10395405
  • Harris LA Crowell MD Linaclotide, a new direction in the treatment of irritable bowel syndrome and chronic constipation Curr Opin Mol Ther 2007 9 4 403 410 17694454
  • synergypharma.com [homepage on the Internet] New York, NY Synergy Pharmaceuticals, Inc. 2013 Available from: http://www.synergypharma.com Accessed January 14, 2013
  • Guarino A Cohen MB Giannella RA Small and large intestinal guanylate cyclase activity in children: effect of age and stimulation by Escherichia coli heat-stable enterotoxin Pediatr Res 1987 21 6 551 555 2885801
  • Waldman SA O’Hanley P Falkow S Schoolnik G Murad F A simple, sensitive, and specific assay for the heat-stable enterotoxin of Escherichia coli J Infect Dis 1984 149 1 83 89 6141207
  • Han X Mann E Gilbert S Loss of guanylyl cyclase C (GCC) signaling leads to dysfunctional intestinal barrier PLoS One 2011 6 1 e16139 21305056
  • Lin JE Snook AE Li P GUCY2C opposes systemic genotoxic tumorigenesis by regulating AKT-dependent intestinal barrier integrity PLoS One 2012 7 2 e31686 22384056
  • Schulz S Green CK Yuen PS Garbers DL Guanylyl cyclase is a heat-stable enterotoxin receptor Cell 1990 63 5 941 948 1701694
  • Schmitt CK Meysick KC O’Brien AD Bacterial toxins: friends or foes? Emerg Infect Dis 1999 5 2 224 234 10221874
  • Lucas KA Pitari GM Kazerounian S Guanylyl cyclases and signaling by cyclic GMP Pharmacol Rev 2000 52 3 375 414 10977868
  • Mann EA Jump ML Wu J Yee E Giannella RA Mice lacking the guanylyl cyclase C receptor are resistant to STa-induced intestinal secretion Biochem Biophys Res Commun 1997 239 2 463 466 9344852
  • Schulz S Lopez MJ Kuhn M Garbers DL Disruption of the guanylyl cyclase-C gene leads to a paradoxical phenotype of viable but heat-stable enterotoxin-resistant mice J Clin Invest 1997 100 6 1590 1595 9294128
  • Pawlowski SW Warren CA Guerrant R Diagnosis and treatment of acute or persistent diarrhea Gastroenterology 2009 136 6 1874 1886 19457416
  • Pitari GM Zingman LV Hodgson DM Bacterial enterotoxins are associated with resistance to colon cancer Proc Natl Acad Sci U S A 2003 100 5 2695 2699 12594332
  • Shailubhai K Yu HH Karunanandaa K Uroguanylin treatment suppresses polyp formation in the Apc(Min/+) mouse and induces apoptosis in human colon adenocarcinoma cells via cyclic GMP Cancer Res 2000 60 18 5151 5157 11016642
  • Pitari GM Di Guglielmo MD Park J Schulz S Waldman SA Guanylyl cyclase C agonists regulate progression through the cell cycle of human colon carcinoma cells Proc Natl Acad Sci U S A 2001 98 14 7846 7851 11438734
  • Currie MG Fok KF Kato J Guanylin: an endogenous activator of intestinal guanylate cyclase Proc Natl Acad Sci U S A 1992 89 3 947 951 1346555
  • Hamra FK Forte LR Eber SL Uroguanylin: structure and activity of a second endogenous peptide that stimulates intestinal guanylate cyclase Proc Natl Acad Sci U S A 1993 90 22 10464 10468 7902563
  • Kita T Smith CE Fok KF Characterization of human uroguanylin: a member of the guanylin peptide family Am J Physiol 1994 266 2 Pt 2 F342 F348 8141334
  • Kuhn M Molecular physiology of natriuretic peptide signalling Basic Res Cardiol 2004 99 2 76 82 14963665
  • Cohen MB Hawkins JA Witte DP Guanylin mRNA expression in human intestine and colorectal adenocarcinoma Lab Invest 1998 78 1 101 108 9461126
  • Hamra FK Eber SL Chin DT Currie MG Forte LR Regulation of intestinal uroguanylin/guanylin receptor-mediated responses by mucosal acidity Proc Natl Acad Sci U S A 1997 94 6 2705 2710 9122260
  • Cohen MB Witte DP Hawkins JA Currie MG Immunohistochemical localization of guanylin in the rat small intestine and colon Biochem Biophys Res Commun 1995 209 3 803 808 7733972
  • Whitaker TL Witte DP Scott MC Cohen MB Uroguanylin and guanylin: distinct but overlapping patterns of messenger RNA expression in mouse intestine Gastroenterology 1997 113 3 1000 1006 9287995
  • Scheving LA Jin WH Circadian regulation of uroguanylin and guanylin in the rat intestine Am J Physiol 1999 277 6 Pt 1 C1177 C1183 10600769
  • Steinbrecher KA Rudolph JA Luo G Cohen MB Coordinate upregulation of guanylin and uroguanylin expression by hypertonicity in HT29-18-N2 cells Am J Physiol 2002 283 6 C1729 C1737
  • Blanchard RK Cousins RJ Upregulation of rat intestinal uroguanylin mRNA by dietary zinc restriction Am J Physiol 1997 272 5 Pt 1 G972 G978 9176203
  • Li Z Knowles JW Goyeau D Low salt intake down-regulates the guanylin signaling pathway in rat distal colon Gastroenterology 1996 111 6 1714 1721 8942754
  • Pitari GM Li P Lin JE The paracrine hormone hypothesis of colorectal cancer Clin Pharmacol Ther 2007 82 4 441 447 17687268
  • Steinbrecher KA Tuohy TM Heppner Goss K Expression of guanylin is downregulated in mouse and human intestinal adenomas Biochem Biophys Res Commun 2000 273 1 225 230 10873591
  • Notterman DA Alon U Sierk AJ Levine AJ Transcriptional gene expression profiles of colorectal adenoma, adenocarcinoma, and normal tissue examined by oligonucleotide arrays Cancer Res 2001 61 7 3124 3130 11306497
  • Busby RW Kessler MM Bartolini WP Pharmacologic properties, metabolism, and disposition of linaclotide, a novel therapeutic peptide approved for the treatment of irritable bowel syndrome with constipation and chronic idiopathic constipation J Pharmacol Exp Ther 2013 344 1 196 206 23090647
  • Rao S Lembo AJ Shiff SJ A 12-week, randomized, controlled trial with a 4-week randomized withdrawal period to evaluate the efficacy and safety of linaclotide in irritable bowel syndrome with constipation Am J Gastroenterol 2012 107 11 1714 1724 22986440
  • Andresen V Camilleri M Busciglio IA Effect of 5 days linaclotide on transit and bowel function in females with constipation-predominant irritable bowel syndrome Gastroenterology 2007 133 3 761 768 17854590
  • Chey WD Lembo AJ Lavins BJ Linaclotide for irritable bowel syndrome with constipation: a 26-week, randomized, double-blind, placebo-controlled trial to evaluate efficacy and safety Am J Gastroenterol 2012 107 11 1702 1712 22986437
  • Krause WJ Cullingford GL Freeman RH Distribution of heat-stable enterotoxin/guanylin receptors in the intestinal tract of man and other mammals J Anat 1994 184 Pt 2 407 417 8014132
  • Krause WJ Freeman RH Eber SL Hamra FK Currie MG Forte LR Guanylyl cyclase receptors and guanylin-like peptides in reptilian intestine Gen Comp Endocrinol 1997 107 2 229 239 9245531
  • Krause WJ Freeman RH Eber SL Distribution of Escherichia coli heat-stable enterotoxin/guanylin/uroguanylin receptors in the avian intestinal tract Acta Anat 1995 153 3 210 219 8984830
  • Gong R Ding C Hu J Role for the membrane receptor guanylyl cyclase-C in attention deficiency and hyperactive behavior Science 2011 333 6049 1642 1646 21835979
  • Valentino MA Lin JE Snook AE A uroguanylin-GUCY2C endocrine axis regulates feeding in mice J Clin Invest 2011 121 9 3578 3588 21865642
  • Bryan NS Bian K Murad F Discovery of the nitric oxide signaling pathway and targets for drug development Front Biosci 2009 14 1 18 19273051
  • Pfeifer A Ruth P Dostmann W Sausbier M Klatt P Hofmann F Structure and function of cGMP-dependent protein kinases Rev Physiol Biochem Pharmacol 1999 135 105 149 9932482
  • Vaandrager AB Bot AG De Jonge HR Guanosine 3′,5′-cyclic monophosphate-dependent protein kinase II mediates heat-stable enterotoxin-provoked chloride secretion in rat intestine Gastroenterology 1997 112 2 437 443 9024297
  • Chao AC de Sauvage FJ Dong YJ Wagner JA Goeddel DV Gardner P Activation of intestinal CFTR Cl− channel by heat-stable enterotoxin and guanylin via cAMP-dependent protein kinase EMBO J 1994 13 5 1065 1072 7510634
  • Vaandrager AB Bot AG Ruth P Pfeifer A Hofmann F De Jonge HR Differential role of cyclic GMP-dependent protein kinase II in ion transport in murine small intestine and colon Gastroenterology 2000 118 1 108 114 10611159
  • Zuzga DS Pelta-Heller J Li P Bombonati A Waldman SA Pitari GM Phosphorylation of vasodilator-stimulated phosphoprotein Ser239 suppresses filopodia and invadopodia in colon cancer Int J Cancer 2012 130 11 2539 2548 21702043
  • Deguchi A Soh JW Li H Pamukcu R Thompson WJ Weinstein IB Vasodilator-stimulated phosphoprotein (VASP) phosphorylation provides a biomarker for the action of exisulind and related agents that activate protein kinase G Mol Cancer Ther 2002 1 10 803 809 12492113
  • Benz PM Blume C Seifert S Differential VASP phosphorylation controls remodeling of the actin cytoskeleton J Cell Sci 2009 122 Pt 21 3954 3965 19825941
  • Lindsay SL Ramsey S Aitchison M Renne T Evans TJ Modulation of lamellipodial structure and dynamics by NO-dependent phosphorylation of VASP Ser239 J Cell Sci 2007 120 Pt 17 3011 3021 17684063
  • Biel M Zong X Ludwig A Sautter A Hofmann F Structure and function of cyclic nucleotide-gated channels Rev Physiol Biochem Pharmacol 1999 135 151 171 9932483
  • Pitari GM Lin JE Shah FJ Enterotoxin preconditioning restores calcium-sensing receptor-mediated cytostasis in colon cancer cells Carcinogenesis 2008 29 8 1601 1607 18566015
  • Pitari GM Baksh RI Harris DM Li P Kazerounian S Waldman SA Interruption of homologous desensitization in cyclic guanosine 3′,5′-monophosphate signaling restores colon cancer cytostasis by bacterial enterotoxins Cancer Res 2005 65 23 11129 11135 16322263
  • Moens E Veldhoen M Epithelial barrier biology: good fences make good neighbours Immunology 2012 135 1 1 8 22044254
  • Potten CS Booth C Pritchard DM The intestinal epithelial stem cell: the mucosal governor Int J Exp Pathol 1997 78 4 219 243 9505935
  • Sanders DS Mucosal integrity and barrier function in the pathogenesis of early lesions in Crohn’s disease J Clin Pathol 2005 58 6 568 572 15917403
  • Steinbrecher KA Wowk SA Rudolph JA Witte DP Cohen MB Targeted inactivation of the mouse guanylin gene results in altered dynamics of colonic epithelial proliferation Am J Pathol 2002 161 6 2169 2178 12466132
  • Li P Lin JE Chervoneva I Schulz S Waldman SA Pitari GM Homeostatic regulation of the crypt-to-villus axis by the bacterial enterotoxin receptor guanylyl cyclase C restricts the proliferating compartment in intestine Am J Pathol 2007 171 6 1847 1858 17974601
  • Li P Schulz S Bombonati A Guanylyl cyclase C suppresses intestinal tumorigenesis by restricting proliferation and maintaining genomic integrity Gastroenterology 2007 133 2 599 607 17681179
  • Lin JE Li P Snook AE The hormone receptor GUCY2C suppresses intestinal tumor formation by inhibiting AKT signaling Gastroenterology 2010 138 1 241 254 19737566
  • Heazlewood CK Cook MC Eri R Aberrant mucin assembly in mice causes endoplasmic reticulum stress and spontaneous inflammation resembling ulcerative colitis PLoS Med 2008 5 3 e54 18318598
  • Kim YS Ho SB Intestinal goblet cells and mucins in health and disease: recent insights and progress Curr Gastroenterol Rep 2010 12 5 319 330 20703838
  • Bachmann O Seidler U News from the end of the gut – how the highly segmental pattern of colonic HCO(3)(−) transport relates to absorptive function and mucosal integrity Biol Pharm Bull 2011 34 6 794 802 21628874
  • Sandle GI Higgs N Crowe P Marsh MN Venkatesan S Peters TJ Cellular basis for defective electrolyte transport in inflamed human colon Gastroenterology 1990 99 1 97 105 2344946
  • Wojciak-Stothard B Torondel B Zhao L Renne T Leiper JM Modulation of Rac1 activity by ADMA/DDAH regulates pulmonary endothelial barrier function Mol Biol Cell 2009 20 1 33 42 18923147
  • Schlegel N Waschke J Vasodilator-stimulated phosphoprotein: crucial for activation of Rac1 in endothelial barrier maintenance Cardiovasc Res 2010 87 1 1 3 20308204
  • Ivanov AI McCall IC Parkos CA Nusrat A Role for actin filament turnover and a myosin II motor in cytoskeleton-driven disassembly of the epithelial apical junctional complex Mol Biol Cell 2004 15 6 2639 2651 15047870
  • Sturm A Dignass AU Epithelial restitution and wound healing in inflammatory bowel disease World J Gastroenterol 2008 14 3 348 353 18200658
  • Keyashian K Annunziata ML Sakuraba A Hanauer S Management of inflammatory bowel disease: past, present and future Expert Rev Clin Immunol 2012 8 4 303 305 22607175
  • Meier J Sturm A Current treatment of ulcerative colitis World J Gastroenterol 2011 17 27 3204 3212 21912469
  • Jenkins HR Inflammatory bowel disease Arch Dis Child 2001 85 5 435 437 11668114
  • Loftus EVJr Delgado DJ Friedman HS Sandborn WJ Colectomy and the incidence of postsurgical complications among ulcerative colitis patients with private health insurance in the United States Am J Gastroenterol 2008 103 7 1737 1745 18564126
  • Waljee A Waljee J Morris AM Higgins PD Threefold increased risk of infertility: a meta-analysis of infertility after ileal pouch anal anastomosis in ulcerative colitis Gut 2006 55 11 1575 1580 16772310
  • Turner JR Intestinal mucosal barrier function in health and disease Nat Rev Immunol 2009 9 11 799 809 19855405
  • Fasano A Zonulin and its regulation of intestinal barrier function: the biological door to inflammation, autoimmunity, and cancer Physiol Rev 2011 91 1 151 175 21248165
  • Wu F Dassopoulos T Cope L Genome-wide gene expression differences in Crohn’s disease and ulcerative colitis from endoscopic pinch biopsies: insights into distinctive pathogenesis Inflamm Bowel Dis 2007 13 7 807 821 17262812
  • Fiskerstrand T Arshad N Haukanes BI Familial diarrhea syndrome caused by an activating GUCY2C mutation N Engl J Med 2012 366 17 1586 1595 22436048
  • Okhuysen PC Jiang ZD Carlin L Forbes C DuPont HL Post-diarrhea chronic intestinal symptoms and irritable bowel syndrome in North American travelers to Mexico Am J Gastroenterol 2004 99 9 1774 1778 15330917
  • Cuppoletti J Blikslager AT Chakrabarti J Nighot PK Malinowska DH Contrasting effects of linaclotide and lubiprostone on restitution of epithelial cell barrier properties and cellular homeostasis after exposure to cell stressors BMC Pharmacol 2012 12 1 3 22553939
  • Steinbrecher KA Harmel-Laws E Garin-Laflam MP Murine guanylate cyclase C regulates colonic injury and inflammation J Immunol 2011 186 12 7205 7214 21555532