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Structure and function of the heat-stable enterotoxin receptor/guanylyl cyclase C

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Book cover Guanylate Cyclase

Part of the book series: Developments in Molecular and Cellular Biochemistry ((DMCB,volume 36))

Abstract

Guanylyl cyclase C (GC-C) was found to function as the principal receptor for heat-stable enterotoxins (STa), major causative factors in E. co/i-induced secretory diarrhea. GC-C is enriched in intestinal epithelium, but was also detected in other epithelial tissues. The enzyme belongs to the family of receptor guanylyl cyclases, and consists of an extracellular receptor domain, a single transmembrane domain, a kinase homology domain, and a catalytic domain. GC-C is modified by N-linked glycosylation and, at least in the small intestine, by proteolysis, resulting in a STa receptor that is coupled non-covalently to the intracellular domain. So far two endogenous ligands of mammalian GC-C have been identified i.e. the small cysteine-rich peptides guanylin and uroguanylin. The guanylins are released in an auto-or paracrine fashion into the intestinal lumen but may also function as endocrine hormones in gut-kidney communication and as regulators of ion transport in extra-intestinal epithelia. They are thought to activate GC-C by inducing a conformational change in the extracellular portion of the homotrimeric GC-C complex, which allows two of the three intracellular catalytic domains to dimerize and form two active catalytic clefts. In the intestine, activation of GC-C results in a dual action: stimulation of Cl and HCO3 secretion, through the opening of apical CFTR Cl channels; and inhibition of Na absorption, through blockade of an apical Na/H exchanger. The principal effector of the GC-C effect on ion transport is cGMP dependent protein kinase type II, which together with GC-C and the ion transporters, may form a supramolecular complex at the apical border of epithelial cells. (Mol Cell Biochem 230: 73–83, 2002)

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References

  1. Field M, Graf LH Jr, Laird WJ, Smith PL: Heat-stable enterotoxin of Escherichia colt: In vitro effects on guanylate cyclase activity, cyclic GMP concentration and ion transport. Proc Natl Acad Sci USA 75: 2800–2804, 1978

    Article  CAS  PubMed  Google Scholar 

  2. Hughes JM, Murad F, Chang B, Guerrant RL: Role of cyclic GMP in the action of heat-stable enterotoxin of Escherichia colt. Nature 271: 755–756,1978

    Article  CAS  PubMed  Google Scholar 

  3. De Jonge HR: The localization of guanylate cyclase in rat small intestinal epithelium. FEBS Lett 53: 237–242, 1975

    Article  PubMed  Google Scholar 

  4. Field M, Rao MC, Chang EB: Intestinal electrolyte transport and diarrheal disease. N Engl J Med 321: 800–806,800–806,1989

    Article  CAS  PubMed  Google Scholar 

  5. Kuno T, Kamisaki Y, Waldman SA, Gariepy J, Schoolnik G, Murad F: Characterization of the receptor for heat-stable enterotoxin from Escherichia colt in rat intestine. J Biol Chem 261: 1470–1476, 1986

    CAS  PubMed  Google Scholar 

  6. Waldman SA, Kuno T., Kamisaki Y, Chang LY, Gariepy J, O’Hanley P, Schoolnik G, Murad F: Intestinal receptor for heat-stable enterotoxin of Escherichia colt is tightly coupled to a novel form of particulate guanylate cyclase. Infect Immun 51: 320–326, 1986

    CAS  PubMed  Google Scholar 

  7. Ivens K, Gazzano H, O’Hanley P, Waldman SA: Heterogeneity of intestinal receptors for Escherichia colt heat-stable enterotoxin. Infect Immun 58: 1817–1820, 1990

    CAS  PubMed  Google Scholar 

  8. Thompson MR, Giannella RA: Different crosslinking agents identify distinctly different putative Escherichia colt heat-stable enterotoxin rat intestinal cell receptor proteins. J Recept Res 10: 97–117, 1990

    CAS  PubMed  Google Scholar 

  9. Schulz S, Green CK, Yuen PST, Garbers DL. Guanylyl cyclase is a heat-stable enterotoxin receptor. Cell 63: 941–948, 1990

    Article  CAS  PubMed  Google Scholar 

  10. de Sauvage FJ, Horuk R, Bennett G, Quan C, Burnier JP, Goeddel DV: Characterization of the recombinant human receptor for Escherichia colt heat-stable enterotoxin. J Biol Chem 267: 6479–6482, 1992

    PubMed  Google Scholar 

  11. Vaandrager AB, Schulz S, De Jonge HR, Garbers DL: Guanylyl cyclase-C is an N-linked glycoprotein receptor that accounts for multiple heat-stable enterotoxin binding proteins in the intestine. J Biol Chem 268: 2174–2179, 1993

    CAS  PubMed  Google Scholar 

  12. Vaandrager AB, van der Wiel E, Hom ML, Luthjens LH, De Jonge HR: Heat-stable enterotoxin receptor/guanylyl cyclase C is an oligomer consisting of functionally distinct subunits, which are non-covalently linked in the intestine. J Biol Chem 269: 16409–16415,1994

    CAS  PubMed  Google Scholar 

  13. 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 100: 1590–1595,1997

    Article  CAS  PubMed  Google Scholar 

  14. 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 239: 463–466, 1997

    Article  CAS  PubMed  Google Scholar 

  15. Charney AN, Egnor RW, Alexander-Chacko JT, Zaharia V, Mann EA, Giannella RA: Effect of E. colt heat-stable enterotoxin on colonic transport in guanylyl cyclase C receptor-deficient mice. Am J Physiol 280: G216–G221,2001

    Google Scholar 

  16. Currie MG, Fok KF, Kato J, Moore RJ, Hamra FK, Duffin KL, Smith CE: Guanylin: An endogenous activator of intestinal guanylate cyclase. Proc Natl Acad Sci USA 89: 947–951,1992

    Article  CAS  PubMed  Google Scholar 

  17. Forte LR, Currie MG: Guanylin: A peptide regulator of epithelial transport. FASEB J 9: 643–650, 1995

    CAS  PubMed  Google Scholar 

  18. Forte LR: Guanylin regulatory peptides: Structures, biological activities mediated by cyclic GMP and pathobiology. Reg Pep 81: 2539, 1999

    Google Scholar 

  19. Lucas KA, Pitari GM, Kazerounian S, Ruiz-Stewart 1, Park J, Schulz S, Chepenik KP, Waldman SA: Guanylyl cyclases and signaling by cyclic GMP. Pharmacol Rev 52: 375–414, 2000

    CAS  PubMed  Google Scholar 

  20. Pearlman JM, Prawer SP, Barber MT, Parkinson SJ, Schulz S, Park J, Zook M, Waldman SA: A splice variant of the transcript for guanylyl cyclase C is expressed in human colon and colorectal cancer cells. Dig Dis Sci 45: 298–305, 2000

    Article  CAS  PubMed  Google Scholar 

  21. Swenson ES, Mann EA, Jump ML, Giannella RA: Hepatocyte nuclear factor-4 regulates intestinal expression of the guanylin/heat-stable toxin receptor. Am J Physiol 276: G728–G736, 1999

    CAS  PubMed  Google Scholar 

  22. Park J, Schulz S, Waldman SA: Intestine-specific activity of the human guanylyl cyclase C promoter is regulated by Cdx2. Gastroenterology 119: 89–96, 2000

    Article  CAS  PubMed  Google Scholar 

  23. De Sauvage FJ, Camerato TR, Goeddel DV: Primary structure and functional expression of the human receptor for Escherichia coli heat-stable enterotoxin. J Biol Chem 266: 17912–17918, 1991

    CAS  Google Scholar 

  24. Singh S, Singh G, Heim JM, Gerzer R: Isolation and expression of a guanylate cyclase-coupled heat stable enterotoxin receptor cDNA from a human colonic cell line. Biochem Biophys Res Commun 179: 1455–1463,1991

    Article  CAS  PubMed  Google Scholar 

  25. Wada A, Hirayama T, Kitao S, Fujisawa J, Hidaka Y, Shimonishi Y: Pig intestinal membrane-bound receptor (guanylyl cyclase) for heat-stable enterotoxin: cDNA Cloning, functional expression, and characterization. Microbiol Immunol 38: 535–541, 1994

    CAS  PubMed  Google Scholar 

  26. London RM, Eber SL, Visweswariah SS, Krause WJ, Forte LR: Structure and activity of OK-GC: A kidney receptor guanylate cyclase activated by guanylin peptides. Am J Physiol 276: F882–F889, 1999

    CAS  PubMed  Google Scholar 

  27. Mantoku T, Muramatsu R, Nakauchi M, Yamagami S, Kusakabe T, Suzuki N: Sequence analysis of cDNA and genomic DNA, and mRNA expression of the medaka fish homolog of mammalian guanylyl cyclaseC. J Biochem (Tokyo) 125: 476–486, 1999

    Article  CAS  Google Scholar 

  28. Comrie MM, Cutler CP, Cramb G: Cloning and expression of guanylin from the European eel (Anguilla anguilla). Biochem Biophys Res Commun 281: 1078–1085, 2001

    Article  CAS  PubMed  Google Scholar 

  29. 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 107: 229–239, 1997

    Article  CAS  PubMed  Google Scholar 

  30. Garbers DL: The guanylyl cyclase receptors. Methods 19: 477–484, 1999

    Article  CAS  PubMed  Google Scholar 

  31. Nandi A, Mathew R, Visweswariah SS: Expression of the extracellular domain of the human heat-stable enterotoxin receptor in Escherichia coli and generation of neutralizing antibodies. Prot Exp Pur 8: 151–159, 1996

    Article  CAS  Google Scholar 

  32. Hasegawa M, Kawano Y, Matsumoto Y, Hidaka Y, Fujii J, Taniguchi N, Wada A, Hirayama T, Shimonishi Y: Expression and characterization of the extracellular domain of guanylyl cyclase C from a baculovirus and Sf21 insect cells. Prot Exp Pur 15: 271–281, 1999

    Article  Google Scholar 

  33. Hasegawa M, Hidaka Y, Matsumoto Y, Sanni T, Shimonishi Y: Determination of the binding site on the extracellular domain of guanylyl cyclase C to heat-stable enterotoxin. J Biol Chem 274: 31713–31718, 1999

    Article  CAS  PubMed  Google Scholar 

  34. Wada A, Hirayama T, Kitaura H, Fujisawa J, Hasegawa M, Hidaka Y, Shimonishi Y: Identification of ligand recognition sites in heat-stable enterotoxin receptor, membrane-associated guanylyl cyclase C by site-directed mutational analysis. Infect Immun 64: 5144–5150, 1996

    CAS  PubMed  Google Scholar 

  35. Hasegawa M, Hidaka Y, Wada A, Hirayama T, Shimonishi Y: The relevance of N-linked glycosylation to the binding of a ligand to guanylate cyclase C. Eur J Biochem 263: 338–346, 1999

    Article  CAS  PubMed  Google Scholar 

  36. Scheving LA, Chong KM: Differential processing of guanylyl cyclase C along villus-crypt axis of rat small intestine. Am J Physiol 272: C1995–02004, 1997

    CAS  PubMed  Google Scholar 

  37. Rudner XL, Mandal KK, DeSauvage FJ, Kindman LA, AlmenoffJS: Regulation of cell signaling by the cytoplasmic domains of the heat-stable enterotoxin receptor: Identification of autoinhibitory and activating motifs. Proc Natl Acad Sci USA 92: 5169–5173, 1995

    Article  CAS  PubMed  Google Scholar 

  38. Deshmane SP, Parkinson SJ, Crupper SS, Robertson DC, Schulz S, Waldman SA: Cytoplasmic domains mediate the ligand-induced affinity shift of guanylyl cyclase C. Biochemistry 36: 12921–12929, 1997

    Article  CAS  PubMed  Google Scholar 

  39. Potter LR, Hunter T: Guanylyl cyclase-linked natriuretic peptide receptors: Structure and regulation. J Biol Chem 276: 6057–6060, 2001

    Article  CAS  PubMed  Google Scholar 

  40. Katwa LC, Parker CD, Dybing JK, White AA: Nucleotide regulation of heat-stable enterotoxin receptor binding and of guanylate cyclase activation. Biochem J 283: 727–735, 1992

    CAS  PubMed  Google Scholar 

  41. Gazzano H, Wu HI, Waldman SA: Activation of particulate guanylate cyclase by Escherichia coli heat-stable enterotoxin is regulated by adenine nucleotides. Infect Immun 59: 1552–1557, 1991

    CAS  PubMed  Google Scholar 

  42. Vaandrager AB, van der Wiel E, de Jonge HR: Heat-stable enterotoxin activation of immunopurified guanylyl cyclase C. Modulation by adenine nucleotides. J Biol Chem 268: 19598–19603, 1993

    CAS  PubMed  Google Scholar 

  43. Parkinson SJ, Carrithers SL, Waldman SA: Opposing adenine nucleotide-dependent pathways regulate guanylyl cyclase C in rat intestine. J Biol Chem 269: 22683–22690, 1994

    CAS  PubMed  Google Scholar 

  44. Tucker CL, Hurley JH, Miller TR, Hurley JB: Two amino acid substitutions convert a guanylyl cyclase, RetGC-1, into an adenylyl cyclase. Proc Natl Acad Sci USA 95: 5993–5997, 1998

    Article  CAS  PubMed  Google Scholar 

  45. Hurley JH: The adenylyl and guanylyl cyclase superfamily. Curr Opin Struct Biol 8: 770–777, 1998

    Article  CAS  PubMed  Google Scholar 

  46. De Jonge HR: Properties of guanylate cyclase and levels of cyclic GMP in rat small intestinal villous and crypt cells. FEBS Lett 55: 143–152, 1975

    Article  PubMed  Google Scholar 

  47. Vijayachandra K, Guruprasad M, Bhandari R, Manjunath UH, Somesh BP, Srinivasan N, Suguna K, Visweswariah SS: Biochemical characterization of the intracellular domain of the human guanylyl cyclase C receptor provides evidence for a catalytically active homotrimer. Biochemistry 39: 16075–16083, 2000

    Article  CAS  PubMed  Google Scholar 

  48. Wada A, Hasegawa M, Matsumoto K, Niidome T, Kawano Y, Hidaka Y, Padilla PI, Kurazono H, Shimonishi Y, Hirayama T: The significance of Ser1029 of the heat-stable enterotoxin receptor (STaR): Relation of STa-mediated guanylyl cyclase activation and signaling by phorbol myristate acetate. FEBS Lett 384: 75–77, 1996

    Article  CAS  PubMed  Google Scholar 

  49. Crane JK, Shanks KL: Phosphorylation and activation of the intestinal guanylyl cyclase receptor for Escherichia coli heat-stable toxin by protein kinase C. Mol Cell Biochem 165: 111–120, 1996

    Article  CAS  PubMed  Google Scholar 

  50. Urbanski R, Carrithers SL, Waldman SA: Internalization of E. coli ST mediated by guanylyl cyclase C in T84 human colon carcinoma cells. Biochim Biophys Acta 1245: 29–36, 1995

    Article  PubMed  Google Scholar 

  51. Rudner XL, Nicchitta C, AlmenoffJS: Biogenesis, cellular localization, and functional activation of the heat-stable enterotoxin receptor (guanylyl cyclase C). Biochemistry 35: 10680–10686, 1996

    Article  CAS  PubMed  Google Scholar 

  52. Hirayama T, Wada A, Iwata N, Takasaki S, Shimonishi Y, Takeda Y: Glycoprotein receptors for a heat-stable enterotoxin (STh) produced by enterotoxigenic Escherichia coli. Infect Immun 60: 4213–4220, 1992

    CAS  PubMed  Google Scholar 

  53. Scheving LA, Russell WE, Chong KM: Structure, glycosylation, and localization of rat intestinal guanylyl cyclase C: Modulation by fasting. Am J Physiol 271: G959–G968, 1996

    CAS  PubMed  Google Scholar 

  54. Weikel CS, Spann CL, Chambers CP, Crane JK, Linden J, Hewlett EL: Phorbol esters enhance the cyclic GMP response of T84 cells to the heat-stable enterotoxin of Escherichia coli (STa). Infect Immun 58: 1402–1407, 1990

    CAS  PubMed  Google Scholar 

  55. Cohen MB, Jensen NJ, Hawkins JA, Mann EA, Thompson MR, Lentze MJ, Giannella RA: Receptors for Escherichia coli heat stable enterotoxin in human intestine and in a human intestinal cell line (Caco-2). J Cell Physiol 156: 138–144, 1993

    Article  CAS  PubMed  Google Scholar 

  56. Visweswariah SS, Ramachandran V, Ramamohan S, Das G, Ramachandran J: Characterization and partial purification of the human receptor for the heat-stable enterotoxin. Eur J Biochem 219: 727–736, 1994

    Article  CAS  PubMed  Google Scholar 

  57. Forte LR, Eber SL, Fan X, London RM, Wang Y, Rowland LM, Chin DT, Freeman RH, Krause WJ: Lymphoguanylin: Cloning and characterization of a unique member of the guanylin peptide family. Endocrinology 140: 1800–1806, 1999

    Article  CAS  PubMed  Google Scholar 

  58. Magert HJ, Reinecke M, David I, Raab HR, Adermann K, Zucht HD, Hill O, Hess R, Forssmann WG: Uroguanylin: Gene structure, expression, processing as a peptide hormone, and co-storage with somatostatin in gastrointestinal D-cells. Reg Pep 73: 165–176, 1998

    Article  Google Scholar 

  59. Whitaker TL, Steinbrecher KA, Copeland NG, Gilbert DJ, Jenkins NA, Cohen MB: The uroguanylin gene (Gucalb) is linked to guanylin (Guca2) on mouse chromosome 4. Genomics 45: 348–354, 1997

    Article  CAS  PubMed  Google Scholar 

  60. Miyazato M, Nakazato M, Matsukura S, Kangawa K, Matsuo H: Genomic structure and chromosomal localization of human uroguanylin. Genomics 43: 359–365, 1997

    Article  CAS  PubMed  Google Scholar 

  61. Greenberg RN, Hill M, Crytzer J, Krause WJ, Eber SL, Hamra FK, Forte LR: Comparison of effects of uroguanylin, guanylin, and Escherichia coli heat-stable enterotoxin STa in mouse intestine and kidney: Evidence that uroguanylin is an intestinal natriuretic hormone. J Invest Med 45: 276–282, 1997

    CAS  Google Scholar 

  62. Leda H, Naruse S, Kitagawa M, Ishiguro H, Hayakawa T: Effects of guanylin and uroguanylin on rat jejunal fluid and electrolyte transport: Comparison with heat-stable enterotoxin. Reg Pep 79: 165–171, 1999

    Article  Google Scholar 

  63. 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 USA 94: 2705–2710, 1997

    Article  CAS  PubMed  Google Scholar 

  64. Crane MR, Hugues M, O’Hanley PD, Waldman SA: Identification of two affinity states of low affinity receptors for Escherichia coli heat-stable enterotoxin: Correlation of occupation of lower affinity state with guanylate cyclase activation. Mol Pharmacol 41: 1073–1080, 1992

    CAS  PubMed  Google Scholar 

  65. Deshmane SP, Carrithers SL, Parkinson SJ, Crupper SS, Robertson DC, Waldman SA: Rat guanylyl cyclase C expressed in COS-7 cells exhibits multiple affinities for Escherichia coli heat-stable enterotoxin. Biochemistry 34: 9095–9102, 1995

    Article  CAS  PubMed  Google Scholar 

  66. Bakre MM, Ghanekar Y, Visweswariah SS: Homologous desensitization of the human guanylate cyclase C receptor. Cell-specific regulation of catalytic activity. Eur J Biochem 267: 179–187, 2000

    Article  CAS  PubMed  Google Scholar 

  67. Bakre MM, Visweswariah SS: Dual regulation of heat-stable enterotoxin-mediated cGMP accumulation in T84 cells by receptor desensitization and increased phosphodiesterase activity. FEBS Lett 408: 345–349, 1997

    Article  CAS  PubMed  Google Scholar 

  68. Tesmer JJ, Sunahara RK, Johnson RA, Gosselin G, Gilman AG, Sprang SR: Two-metal-ion catalysis in adenylyl cyclase. Science 285: 756–760, 1999

    Article  CAS  PubMed  Google Scholar 

  69. De Jonge HR, Bot AGM, Vaandrager AB: Mechanism of action of E. coli heat-stable enterotoxin. Zentralbl Bakteriol Mikrobiol Hyg Abt 1(suppl. 15): 335–340, 1986

    Google Scholar 

  70. elDeib MM, Parker CD, White AA: Regulation of intestinal mucosa guanylate cyclase by heroin, heme and protoporphyrin IX. Biochim Biophys Acta 928: 83–91, 1987

    Article  CAS  PubMed  Google Scholar 

  71. Parkinson SJ, Waldman SA: An intracellular adenine nucleotide binding site inhibits guanyly cyclase C by a guanine nucleotide-dependent mechanism. Biochemistry 35: 3213–3221, 1996

    Article  CAS  PubMed  Google Scholar 

  72. Parkinson SJ, Alekseev AE, Gomez LA, Wagner F, Terzic A, Waldman SA: Interruption of Escherichia coli heat-stable enterotoxin-induced guanylyl cyclase signaling and associated chloride current in human intestinal cells by 2-chloroadenosine. J Biol Chem 272: 754–758,1997

    Article  CAS  PubMed  Google Scholar 

  73. Zhang W, Mannan I, Schulz S, Parkinson SJ, Alekseev AE, Gomez LA, Terzic A, Waldman SA: Interruption of transmembrane signaling as a novel antisecretory strategy to treat enterotoxigenic diarrhea. FASEB J 13: 913–922, 1999

    CAS  PubMed  Google Scholar 

  74. Greenberg RN, Dunn JA, Guerrant RL: Reduction of the secretory response to Escherichia coli heat-stable enterotoxin by thiol and disulfide compounds. Infect Immun 41: 174–180, 1983

    CAS  PubMed  Google Scholar 

  75. ElDeib MM, Dove CR, Parker CD, Veum TL, Zinn GM, White AA: Reversal of the biological activity reducing of Escherichia coli heat-stable enterotoxin by disulfide-agents. Infect Immun 51: 24–30, 1986

    CAS  PubMed  Google Scholar 

  76. Cohen MB, Mann EA, Lau C, Henning SJ, Giannella RA: A gradient in expression of the Escherichia coli heat-stable enterotoxin receptor exists along the villus-to-crypt axis of rat small intestine. Biochem Biophys Res Commun 186: 483–490, 1992

    Article  CAS  PubMed  Google Scholar 

  77. Li Z, Goy MF: Peptide-regulated guanylate cyclase pathways in rat colon: In situ localization of GCA, GCC, and guanylin mRNA. Am J Physiol 265: G394–G402, 1993

    CAS  PubMed  Google Scholar 

  78. Lewis LG, Witte DP, Laney DW, Currie MG, Cohen MB: Guanylin mRNA is expressed in villous enterocytes of the rat small intestine and superficial epithelia of the rat colon. Biochem Biophys Res Commun 196: 553–560, 1993

    Article  CAS  PubMed  Google Scholar 

  79. Vaandrager AB, De Jonge HR: Effect of cGMP on intestinal transport. Adv Pharmacol 26: 253–283, 1994

    Article  CAS  PubMed  Google Scholar 

  80. Krause WJ, Cullingford GL, Freeman RH, Eber SL, Richardson KC, Fok KF, Currie MG, Forte LR: Distribution of heat-stable enterotoxin/ guanylin receptors in the intestinal tract of man and other mammals. J Anat 184: 407–417, 1994

    CAS  PubMed  Google Scholar 

  81. Cohen MB, Witte DP, Hawkins JA, Currie MG: Immunohistochemical localization of guanylin in the rat small intestine and colon. Biochem Biophys Res Commun 209: 803–808, 1995

    Article  CAS  PubMed  Google Scholar 

  82. London RM, Krause WJ, Fan X, Eber SL, Forte LR: Signal transduction pathways via guanylin and uroguanylin in stomach and intestine. Am J Physiol 273: G93–G105, 1997

    CAS  PubMed  Google Scholar 

  83. Qian X, Prabhakar S, Nandi A, Visweswariah SS, Goy MF: Expression of GC-C, a receptor-guanylate cyclase, and its endogenous ligands uroguanylin and guanylin along the rostrocaudal axis of the intestine. Endocrinology 141: 3210–24, 2000

    Article  CAS  PubMed  Google Scholar 

  84. Carrithers SL, Barber MT, Biswas S, Parkinson SJ, Park PK, Goldstein SD, Waldman SA: Guanylyl cyclase C is a selective marker for metastatic colorectal tumors in human extraintestinal tissues. Proc Natl Acad Sci USA 93: 14827–14832, 1996

    Article  CAS  PubMed  Google Scholar 

  85. Schulz S, Chrisman TD, Garbers DL: Cloning and expression of guanylin. Its existence in various mammalian tissues. J Biol Chem 267: 16019–16021, 1992

    CAS  PubMed  Google Scholar 

  86. Carrithers SL, Taylor B, Cai WY, Johnson BR, Ott CE, Greenberg RN, Jackson BA: Guanylyl cyclase-C receptor mRNA distribution along the rat nephron. Reg Pep 95: 65–74, 2000

    Article  CAS  Google Scholar 

  87. Cetin Y, Kulaksiz H, Redecker P, Bargsten G, Adermann K, Grube D, Forssmann WG: Bronchiolar nonciliated secretory (Clara) cells: Source of guanylin in the mammalian lung. Proc Natl Acad Sci USA 92: 5925–5959, 1995

    Article  Google Scholar 

  88. Rambotti MG, Giambanco I, Spreca A: Ultracytochemical detection of guanylate cyclase C activity in alimentary tract and associated glands of the rat. Influence of pH, ATP and the ions Mg“ and Mn’. Histochem J 32: 231–238, 2000

    Article  CAS  PubMed  Google Scholar 

  89. John M, Wiedenmann B, Kruhoffer M, Adermann K, Ankorina-Stark I, Schlatter E, Ahnert-Hilger G, Forssmann WG, Kuhn M: Guanylin stimulates regulated secretion from human neuroendocrine pancreatic cells. Gastroenterology 114: 791–797, 1998

    Article  CAS  PubMed  Google Scholar 

  90. D’Este L, Kulaksiz H, Rausch U, Vaccaro R, Wenger T, Tokunaga Y, Renda TG, Cetin Y: Expression of guanylin in `pars tuberalis-specific cells’ and gonadotrophs of rat adenohypophysis. Proc Natl Acad Sci USA 97: 1131–1136, 2000

    Article  PubMed  Google Scholar 

  91. Reinecke M, David I, Loffing-Cueni D, Ablinger P, Cetin Y, Kuhn M, Forssmann: Localization, expression, and characterization of guanylin in the rat adrenal medulla. Histochem Cell Biol 106: 367–374, 1996

    Article  CAS  PubMed  Google Scholar 

  92. Laney DW Jr, Bezerra JA, Kosiba JL, Degen SJ, Cohen MB: Upregulation of Escherichia coli heat-stable enterotoxin receptor in regenerating rat liver. Am J Physiol 266: G899–G906, 1994

    PubMed  Google Scholar 

  93. Scheving LA, Russell WE: Guanylyl cyclase C is up-regulated by nonparenchymal cells and hepatocytes in regenerating rat liver. Cancer Res 56: 5186–5191, 1996

    CAS  PubMed  Google Scholar 

  94. Fan X, Wang Y, London RM, Eber SL, Krause WJ, Freeman RH, Forte LR: Signaling pathways for guanylin and uroguanylin in the digestive, renal, central nervous, reproductive, and lymphoid systems. Endocrinology 138: 4636–4648, 1997

    Article  CAS  PubMed  Google Scholar 

  95. Forte LR, London RM, Freeman RH, Krause WJ: Guanylin peptides: Renal actions mediated by cyclic GMP. Am J Physiol 278: F180–F191, 2000

    CAS  Google Scholar 

  96. Fawcus K, Gorton VJ, Lucas ML, McEwan GT: Stimulation of three distinct guanylate cyclases induces mucosal surface alkalinisation in rat small intestine in vitro. Comp Biochem Physiol A Physiol 118: 291–295, 1997

    Article  CAS  PubMed  Google Scholar 

  97. Joo NS, London RM, Kim HD, Forte LR, Clarke LL: Regulation of intestinal Cl and HCO3 secretion by uroguanylin. Am J Physiol 274: G633–Q644, 1998

    CAS  PubMed  Google Scholar 

  98. Guba M, Kuhn M, Forssmann WG, Classen M, Gregor M, Seidler U: Guanylin strongly stimulates rat duodenal HCO3 secretion: Proposed mechanism and comparison with other secretagogues. Gastroenterology 111: 1558–1568, 1996

    Article  CAS  PubMed  Google Scholar 

  99. Shailubhai K, Yu HH, Karunanandaa K, Wang JY, Eber SL, Wang Y, Joo NS, Kim HD, Miedema BW, Abbas SZ, Boddupalli SS, Currie MG, Forte LR: Uroguanylin treatment suppresses polyp formation in the Apc(Min/+) mouse and induces apoptosis in human colon adenocarcinoma cells via cyclic GMP. Cancer Res 60: 5151–5157, 2000

    CAS  PubMed  Google Scholar 

  100. Li Z, Knowles JW, Goyeau D, Prabhakar S, Short DB, Perkins AG, Goy MF: Low salt intake down-regulates the guanylin signaling pathway in rat distal colon. Gastroenterology 111: 1714–1721, 1996

    Article  CAS  PubMed  Google Scholar 

  101. Moro F, Levenez F, Nemoz-Gaillard E, Pellissier S, Plaisancie P, Cuber JC: Release of guanylin immunoreactivity from the isolated vascularly perfused rat colon. Endocrinology 141: 2594–2599, 2000

    Article  CAS  PubMed  Google Scholar 

  102. Martin S, Adermann K, Forssmann WG, Kuhn M: Regulated, side-directed secretion of proguanylin from isolated rat colonic mucosa. Endocrinology 140: 5022–5029, 1999

    Article  CAS  PubMed  Google Scholar 

  103. Scheving LA, Jin WH: Circadian regulation of uroguanylin and guanylin in the rat intestine. Am J Physiol 277: C 1177-C1183, 1999

    CAS  PubMed  Google Scholar 

  104. 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. EMBOJ 13: 1065–1072, 1994

    CAS  Google Scholar 

  105. Tien XY, Brasitus TA, Kaetzel MA, Dedman JR, Nelson DJ: Activation of the cystic fibrosis transmembrane conductance regulator by cGMP in the human colonic cancer cell line, Caco-2. J Biol Chem 269: 51–54, 1994

    CAS  PubMed  Google Scholar 

  106. Cuthbert AW, Hickman ME, MacVinish U, Evans MJ, Colledge WH, Ratcliff R, Seale PW, Humphrey PP: Chloride secretion in response to guanylin in colonic epithelial from normal and transgenic cystic fibrosis mice. Br J Pharmacol 112: 31–36, 1994

    Article  CAS  PubMed  Google Scholar 

  107. Lohmann SM, Vaandrager AB, Smolenski A, Walter U, De Jonge HR. Distinct and specific functions of cGMP-dependent protein kinases. Trends Biochem Sci 22: 307–312, 1997

    Article  CAS  PubMed  Google Scholar 

  108. Seidler U, Blumenstein I, Kretz A, Viellard-Baron D, Rossmann H, Colledge WH, Evans M, Ratcliff R, Gregor M: A functional CFTR protein is required for mouse intestinal cAMP-, cGMP- and Ca“- dependent HCO3 secretion. J Physiol (Lond) 505: 411–423, 1997

    Article  CAS  Google Scholar 

  109. Hoogerwerf WA, Tsao SC, Devuyst O, Levine SA, Yun CH, Yip JW, Cohen ME, Wilson PD, Lazenby AJ, Tse CM, Donowitz M. NHE2 and NHE3 are human and rabbit intestinal brush-border proteins. Am J Physiol 270: G29–G41, 1996

    CAS  PubMed  Google Scholar 

  110. Schultheis PJ, Clarke LL, Meneton P, Miller ML, Soleimani M, Gawenis LR, Riddle TM, Duffy JJ, Doetschman T, Wang T, Giebisch G, Aronson PS, Lorenz JN, Shull G: Renal and intestinal absorptive defects in mice lacking the NHE3 Na’/H’ exchanger. Nat Genet 19: 282–285, 1998

    Article  CAS  PubMed  Google Scholar 

  111. Kere J, Lohi H, Hoglund P: Congenital chloride diarrhea. Am J Physiol 276: G7–G13, 1999

    CAS  PubMed  Google Scholar 

  112. Yun CH, Oh S, Zizak M, Steplock D, Tsao S, Tse CM, Weinman EJ, Donowitz M: cAMP-mediated inhibition of the epithelial brush border Na’/H’ exchanger, NHE3, requires an associated regulatory protein. Proc Natl Acad Sci USA 94: 3010–3015, 1997

    Article  CAS  PubMed  Google Scholar 

  113. Kurashima K, Yu FH, Cabado AG, Szabo EZ, Grinstein S, Orlowski J: Identification of sites required for down-regulation of Na’/H’ exchanger NHE3 activity by cAMP-dependent protein kinase phosphorylation-dependent and -independent mechanisms. J Biol Chem 272: 28672–28679, 1997

    Article  CAS  PubMed  Google Scholar 

  114. Vaandrager AB, Bot AG, De Jonge HR: Guanosine 3’,5’-cyclic monophosphate-dependent protein kinase Il mediates heat-stable enterotoxinprovoked chloride secretion in rat intestine. Gastroenterology 112: 437–443,1997

    Article  CAS  PubMed  Google Scholar 

  115. Pfeifer A, Aszodi A, Seidler U, Ruth P, Hofmann F, Fassler R: Intestinal secretory defects and dwarfism in mice lacking cGMPdependent protein kinase 11. Science 274: 2082–2086, 1996

    Article  CAS  PubMed  Google Scholar 

  116. 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 118: 108–114, 2000

    Article  CAS  PubMed  Google Scholar 

  117. Vaandrager AB, Smolenski A, Tilly BC, Houtsmuller AB, Ehlert EM, Bot AG, Edixhoven M, Boomaars WE, Lohmann SM, de Jonge HR: Membrane targeting of cGMP-dependent protein kinase is required for cystic fibrosis transmembrane conductance regulator C1- channel activation. Proc Natl Acad Sci USA 95: 1466–1471, 1998

    Article  CAS  PubMed  Google Scholar 

  118. Kleizen B, Braakman I, de Jonge HR: Regulated trafficking of the CFTR chloride channel. Eur J Cell Biol 79: 544–556, 2000

    Article  CAS  PubMed  Google Scholar 

  119. Korschen HG, Beyermann M, Muller F, Heck M, Vantler M, Koch KW, Kellner R, Wolfrum U, Bode C, Hofmann KP, Kaupp UB: Interaction of glutamic-acid-rich proteins with the cGMP signalling pathway in rod photoreceptors. Nature 400: 761–766, 1999

    Article  CAS  PubMed  Google Scholar 

  120. Forte LR, Thorne PK, Eber SL, Krause WJ, Freeman RH, Francis SH, Corbin JD: Stimulation of intestinal Cl-transport by heat-stable enterotoxin: Activation of cAMP-dependent protein kinase by cGMP. Am J Physiol 263: C607–C6115, 1992

    CAS  PubMed  Google Scholar 

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  1. Department of Biochemistry and Cell Biology, Faculty of Veterinary Medicine, Utrecht University, Utrecht, Netherlands

    Arie B. Vaandrager

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  1. Arie B. Vaandrager
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  1. The Unit of Regulatory and Molecular Biology Departments of Cell Biology and Ophthalmology SOM and NJMS, University of Medicine and Dentistry of New Jersey, Stratford, NJ, USA

    Rameshwar K. Sharma

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Vaandrager, A.B. (2002). Structure and function of the heat-stable enterotoxin receptor/guanylyl cyclase C. In: Sharma, R.K. (eds) Guanylate Cyclase. Developments in Molecular and Cellular Biochemistry, vol 36. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-0927-1_5

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  • DOI: https://doi.org/10.1007/978-1-4615-0927-1_5

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