About this Journal Submit a Manuscript Table of Contents
ISRN Nephrology
Volume 2013 (2013), Article ID 813648, 17 pages
http://dx.doi.org/10.5402/2013/813648
Review Article

Current Understanding of Guanylin Peptides Actions

Department of Physiology, School of Medicine, University of Zagreb, Salata 3, 10000 Zagreb, Croatia

Received 4 February 2013; Accepted 26 February 2013

Academic Editors: L. Espinosa, A. H. Tzamaloukas, and G.-P. Zhou

Copyright © 2013 Aleksandra Sindic. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. J. Lennane, W. S. Peart, R. M. Carey, and J. Shaw, “A comparison of natriuresis after oral and intravenous sodium loading in sodium depleted rabbits: evidence for a gastrointestinal or portal monitor of sodium intake,” Clinical Science and Molecular Medicine, vol. 49, no. 5, pp. 433–436, 1975. View at Scopus
  2. T. Kita, K. Kitamura, J. Sakata, and T. Eto, “Marked increase of guanylin secretion in response to salt loading in the rat small intestine,” American Journal of Physiology, vol. 277, no. 5, pp. G960–G966, 1999. View at Scopus
  3. Z. Li, J. W. Knowles, D. Goyeau et al., “Low salt intake down-regulates the guanylin signaling pathway in rat distal colon,” Gastroenterology, vol. 111, no. 6, pp. 1714–1721, 1996. View at Scopus
  4. R. N. Greenberg, M. Hill, J. Crytzer et al., “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,” Journal of Investigative Medicine, vol. 45, no. 5, pp. 276–283, 1997. View at Scopus
  5. S. L. Carrithers, C. E. Ott, M. J. Hill et al., “Guanylin and uroguanylin induce natriuresis in mice lacking guanylyl cyclase-C receptor,” Kidney International, vol. 65, no. 1, pp. 40–53, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. M. C. Fonteles, R. N. Greenberg, H. S. A. Monteiro, M. G. Currie, and L. R. Forte, “Natriuretic and kaliuretic activities of guanylin and uroguanylin in the isolated perfused rat kidney,” American Journal of Physiology, vol. 275, no. 2, pp. F191–F197, 1998. View at Scopus
  7. M. G. Currie, K. F. Fok, J. Kato et al., “Guanylin: an endogenous activator of intestinal guanylate cyclase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 3, pp. 947–951, 1992. View at Scopus
  8. F. K. Hamra, L. R. Forte, S. L. Eber et al., “Uroguanylin: structure and activity of a second endogenous peptide that stimulates intestinal guanylate cyclase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 22, pp. 10464–10468, 1993. View at Publisher · View at Google Scholar · View at Scopus
  9. L. R. Forte, S. L. Eber, X. Fan et al., “Lymphoguanylin: cloning and characterization of a unique member of the guanylin peptide family,” Endocrinology, vol. 140, no. 4, pp. 1800–1806, 1999. View at Scopus
  10. S. Yuge, K. Inoue, S. Hyodo, and Y. Takei, “A novel guanylin family (guanylin, uroguanylin, and renoguanylin) in eels: possible osmoregulatory hormones in intestine and kidney,” Journal of Biological Chemistry, vol. 278, no. 25, pp. 22726–22733, 2003. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Schulz, “Targeted gene disruption in the development of mouse models to elucidate the role of receptor guanylyl cyclase signaling pathways in physiological function,” Methods, vol. 19, no. 4, pp. 551–558, 1999. View at Publisher · View at Google Scholar · View at Scopus
  12. O. Hill, M. Kuhn, H. D. Zucht et al., “Analysis of the human guanylin gene and the processing and cellular localization of the peptide,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 6, pp. 2046–2050, 1995. View at Publisher · View at Google Scholar · View at Scopus
  13. H. J. Mägert, M. Reinecke, I. David et al., “Uroguanylin: gene structure, expression, processing as a peptide hormone, and co-storage with somatostatin in gastrointestinal D-cells,” Regulatory Peptides, vol. 73, no. 3, pp. 165–176, 1998. View at Publisher · View at Google Scholar · View at Scopus
  14. F. J. de Sauvage, S. Keshav, W. J. Kuang, N. Gillett, W. Henzel, and D. V. Goeddel, “Precursor structure, expression, and tissue distribution of human guanylin,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 19, pp. 9089–9093, 1992. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Miyazato, M. Nakazato, S. Matsukura, K. Kangawa, and H. Matsuo, “Uroguanylin gene expression in the alimentary tract and extra-gastrointestinal tissues,” FEBS Letters, vol. 398, no. 2-3, pp. 170–174, 1996. View at Publisher · View at Google Scholar · View at Scopus
  16. T. Kita, C. E. Smith, K. F. Fok et al., “Characterization of human uroguanylin: a member of the guanylin peptide family,” American Journal of Physiology, vol. 266, no. 2, pp. F342–F348, 1994. View at Scopus
  17. R. Hess, M. Kuhn, P. Schulz-Knappe et al., “GCAP-II: isolation and characterization of the circulating form of human uroguanylin,” FEBS Letters, vol. 374, no. 1, pp. 34–38, 1995. View at Publisher · View at Google Scholar · View at Scopus
  18. T. L. Whitaker, D. P. Witte, M. C. Scott, and M. B. Cohen, “Uroguanylin and guanylin: distinct but overlapping patterns of messenger RNA expression in mouse intestine,” Gastroenterology, vol. 113, no. 3, pp. 1000–1006, 1997. View at Publisher · View at Google Scholar · View at Scopus
  19. F. K. Hamra, S. L. Eber, D. T. Chin, M. G. Currie, and L. R. Forte, “Regulation of intestinal uroguanylin/guanylin receptor-mediated responses by mucosal acidity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 6, pp. 2705–2710, 1997. View at Publisher · View at Google Scholar · View at Scopus
  20. R. Potthast, E. Ehler, L. A. Scheving, A. Sindic, E. Schlatter, and M. Kuhn, “High salt intake increases uroguanylin expression in mouse kidney,” Endocrinology, vol. 142, no. 7, pp. 3087–3097, 2001. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Sindiće, C. Basoglu, A. Çerçi et al., “Guanylin, uroguanylin, and heat-stable euterotoxin activate guanylate cyclase C and/or a pertussis toxin-sensitive G protein in human proximal tubule cells,” Journal of Biological Chemistry, vol. 277, no. 20, pp. 17758–17764, 2002. View at Publisher · View at Google Scholar · View at Scopus
  22. K. Nokihara, V. Wray, E. Ando, S. Naruse, and T. Hayakawa, “Synthesis, solution structure, binding activity, and cGMP activation of human guanylin and its disulfide isomer,” Regulatory Peptides, vol. 70, no. 2-3, pp. 111–120, 1997. View at Publisher · View at Google Scholar · View at Scopus
  23. S. Schulz, C. K. Green, P. S. T. Yuen, and D. L. Garbers, “Guanylyl cyclase is a heat-stable enterotoxin receptor,” Cell, vol. 63, no. 5, pp. 941–948, 1990. View at Publisher · View at Google Scholar · View at Scopus
  24. M. Field, L. H. Graf, W. J. Laird, and P. L. Smith, “Heat-stable enterotoxin of Escherichia coli: in vitro effects on guanylate cyclase activity, cyclic GMP concentration, and ion transport in small intestine,” Proceedings of the National Academy of Sciences of the United States of America, vol. 75, no. 6, pp. 2800–2804, 1978. View at Scopus
  25. J. M. Hughes, F. Murad, B. Chang, and R. L. Guerrant, “Role of cyclic GMP in the action of heat-stable enterotoxin of Escherichia coli,” Nature, vol. 271, no. 5647, pp. 755–756, 1978. View at Scopus
  26. M. Kuhn, M. Raida, K. Adermann et al., “The circulating bioactive form of human guanylin is a high molecular weight peptide (10.3 kDa),” FEBS Letters, vol. 318, no. 2, pp. 205–209, 1993. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Nakazato, H. Yamaguchi, K. Shiomi et al., “Identification of 10-kDa proguanylin as a major guanylin molecule in human intestine and plasma and its increase in renal insufficiency,” Biochemical and Biophysical Research Communications, vol. 205, no. 3, pp. 1966–1975, 1994. View at Publisher · View at Google Scholar · View at Scopus
  28. H. J. Mägert, O. Hill, H. D. Zucht et al., “Porcine guanylin and uroguanylin: cDNA sequences, deduced amino acid sequences, and biological activity of the chemically synthesized peptides,” Biochemical and Biophysical Research Communications, vol. 259, no. 1, pp. 141–148, 1999. View at Publisher · View at Google Scholar · View at Scopus
  29. H. Kinoshita, S. Fujimoto, M. Nakazato et al., “Urine and plasma levels of uroguanylin and its molecular forms in renal diseases,” Kidney International, vol. 52, no. 4, pp. 1028–1034, 1997. View at Scopus
  30. M. Nakazato, H. Yamaguchi, H. Kinoshita et al., “Identification of biologically active and inactive human uroguanylins in plasma and urine and their increases in renal insufficiency,” Biochemical and Biophysical Research Communications, vol. 220, no. 3, pp. 586–593, 1996. View at Publisher · View at Google Scholar · View at Scopus
  31. N. G. Moss, R. C. Fellner, X. Qian et al., “Uroguanylin, an intestinal natriuretic peptide, is delivered to the kidney as an unprocessed propeptide,” Endocrinology, vol. 149, no. 9, pp. 4486–4498, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. X. Qian, N. G. Moss, R. C. Fellner, and M. F. Goy, “Circulating prouroguanylin is processed to its active natriuretic form exclusively within the renal tubules,” Endocrinology, vol. 149, no. 9, pp. 4499–4509, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. F. K. Hamra, X. Fan, W. J. Krause et al., “Prouroguanylin and proguanylin: purification from colon, structure, and modulation of bioactivity by proteases,” Endocrinology, vol. 137, no. 1, pp. 257–265, 1996. View at Publisher · View at Google Scholar · View at Scopus
  34. F. K. Hamra, W. J. Krause, S. L. Eber et al., “Opossum colonic mucosa contains uroguanylin and guanylin peptides,” American Journal of Physiology, vol. 270, no. 4, pp. G708–G716, 1996. View at Scopus
  35. M. Arao, T. Yamaguchi, T. Sugimoto, M. Fukase, and K. Chihara, “Characterization of a chymotrypsin-like hydrolytic activity in the opossum kidney cell,” Biochemistry and Cell Biology, vol. 72, no. 3-4, pp. 157–162, 1994. View at Scopus
  36. M. Miyazato, M. Nakazato, H. Yamaguchi et al., “Cloning and characterization of a cDNA encoding a precursor for human uroguanylin,” Biochemical and Biophysical Research Communications, vol. 219, no. 2, pp. 644–648, 1996. View at Publisher · View at Google Scholar · View at Scopus
  37. Z. Li, A. G. Perkins, M. F. Peters, M. J. Campa, and M. F. Goy, “Purification, cDNA sequence, and tissue distribution of rat uroguanylin,” Regulatory Peptides, vol. 68, no. 1, pp. 45–56, 1997. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Nakazato, H. Yamaguchi, Y. Date et al., “Tissue distribution, cellular source, and structural analysis of rat immunoreactive uroguanylin,” Endocrinology, vol. 139, no. 12, pp. 5247–5254, 1998. View at Scopus
  39. H. Kinoshita, M. Nakazato, H. Yamaguchi, S. Matsukura, S. Fujimoto, and T. Eto, “Increased plasma guanylin levels in patients with impaired renal function,” Clinical Nephrology, vol. 47, no. 1, pp. 28–32, 1997. View at Scopus
  40. H. Kinoshita, S. Fujimoto, H. Fukae et al., “Plasma and urine levels of uroguanylin, a new natriuretic peptide, in nephrotic syndrome,” Nephron, vol. 81, no. 2, pp. 160–164, 1999. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Martin, K. Adermann, W. G. Forssmann, and M. Kuhn, “Regulated, side-directed secretion of proguanylin from isolated rat colonic mucosa,” Endocrinology, vol. 140, no. 11, pp. 5022–5029, 1999. View at Scopus
  42. F. Moro, F. Levenez, E. Nemoz-Gaillard, S. Pellissier, P. Plaisancie, and J. C. Cuber, “Release of guanylin immunoreactivity from the isolated vascularly perfused rat colon,” Endocrinology, vol. 141, no. 7, pp. 2594–2599, 2000. View at Publisher · View at Google Scholar · View at Scopus
  43. Y. Date, M. Nakazato, H. Yamaguchi et al., “Enterochromaffin-like cells, a cellular source of uroguanylin in rat stomach,” Endocrinology, vol. 140, no. 5, pp. 2398–2404, 1999. View at Scopus
  44. R. K. Blanchard and R. J. Cousins, “Differential display of intestinal mRNAs regulated by dietary zinc,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 14, pp. 6863–6868, 1996. View at Publisher · View at Google Scholar · View at Scopus
  45. R. K. Blanchard and R. J. Cousins, “Upregulation of rat intestinal uroguanylin mRNA by dietary zinc restriction,” American Journal of Physiology, vol. 272, no. 5, pp. G972–G978, 1997. View at Scopus
  46. L. Cui, R. K. Blanchard, L. M. Coy, and R. J. Cousins, “Prouroguanylin overproduction and localization in the intestine of zinc-deficient rats,” Journal of Nutrition, vol. 130, no. 11, pp. 2726–2732, 2000. View at Scopus
  47. R. K. Blanchard and R. J. Cousins, “Regulation of intestinal gene expression by dietary zinc: induction of uroguanylin mRNA by zinc deficiency,” Journal of Nutrition, vol. 130, no. 5, pp. 1393S–1398S, 2000. View at Scopus
  48. C. Ott, B. Jackson, A. Carvalho, R. Greenberg, and S. Carrithers, “Regulation of intestinal uroguanylin (UGN) expression by dietary salt intake,” The FASEB Journal, vol. 16, p. A472, 2000.
  49. A. Perkins, M. F. Goy, and Z. Li, “Uroguanylin is expressed by enterochromaffin cells in the rat gastrointestinal tract,” Gastroenterology, vol. 113, no. 3, pp. 1007–1014, 1997. View at Publisher · View at Google Scholar · View at Scopus
  50. Y. Cetin, M. Kuhn, H. Kulaksiz et al., “Enterochromaffin cells of the digestive system: cellular source of guanylin, a guanylate cyclase-activating peptide,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 8, pp. 2935–2939, 1994. View at Scopus
  51. R. M. London, W. J. Krause, X. Fan, S. L. Eber, and L. R. Forte, “Signal transduction pathways via guanylin and uroguanylin in stomach and intestine,” American Journal of Physiology, vol. 273, no. 1, pp. G93–G105, 1997. View at Scopus
  52. R. C. Wiegand, J. Kato, M. D. Huang, K. F. Fok, J. F. Kachur, and M. G. Currie, “Human guanylin: cDNA isolation, structure, and activity,” FEBS Letters, vol. 311, no. 2, pp. 150–154, 1992. View at Publisher · View at Google Scholar · View at Scopus
  53. R. C. Wiegand, J. Kato, and M. G. Currie, “Rat guanylin cDNA: characterization of the precursor of an endogenous activator of intestinal guanylate cyclase,” Biochemical and Biophysical Research Communications, vol. 185, no. 3, pp. 812–817, 1992. View at Publisher · View at Google Scholar · View at Scopus
  54. X. Fan, F. K. Hamra, R. M. London et al., “Structure and activity of uroguanylin and guanylin from the intestine and urine of rats,” American Journal of Physiology, vol. 273, no. 5, pp. E957–E964, 1997. View at Scopus
  55. J. Rozenfeld, O. Tal, O. Kladnitsky et al., “The pendrin anion exchanger gene is transcriptionally regulated by uroguanylin: a novel enterorenal link,” American Journal of Physiology, vol. 302, no. 5, pp. F614–F624, 2012. View at Publisher · View at Google Scholar
  56. Z. Li, B. Taylor-Blake, A. R. Light, and M. F. Goy, “Guanylin, an endogenous ligand for C-type guanylate cyclase, is produced by goblet cells in the rat intestine,” Gastroenterology, vol. 109, no. 6, pp. 1863–1875, 1995. View at Publisher · View at Google Scholar · View at Scopus
  57. S. Furuya, S. Naruse, and T. Hayakawa, “Intravenous injection of guanylin induces mucus secretion from goblet cells in rat duodenal crypts,” Anatomy and Embryology, vol. 197, no. 5, pp. 359–367, 1998. View at Publisher · View at Google Scholar · View at Scopus
  58. A. B. Vaandrager, A. G. M. Bot, and H. R. de Jonge, “Guanosine 3′,5′-cyclic monophosphate-dependent protein kinase ii mediates heat-stable enterotoxin-provoked chloride secretion in rat intestine,” Gastroenterology, vol. 112, no. 2, pp. 437–443, 1997. View at Publisher · View at Google Scholar · View at Scopus
  59. A. B. Vaandrager, A. G. M. Bot, P. Ruth, A. Pfeifer, F. Hofmann, and H. R. de Jonge, “Differential role of cyclic GMP-dependent protein kinase II in ion transport in murine small intestine and colon,” Gastroenterology, vol. 118, no. 1, pp. 108–114, 2000. View at Scopus
  60. A. C. Chao, F. J. de Sauvage, Y. J. Dong, J. A. Wagner, D. V. Goeddel, and P. Gardner, “Activation of intestinal CFTR Cl channel by heat-stable enterotoxin and guanylin via cAMP-dependent protein kinase,” EMBO Journal, vol. 13, no. 5, pp. 1065–1072, 1994. View at Scopus
  61. T. P. Dousa, “Cyclic-3′,5′-nucleotide phosphodiesterase isozymes in cell biology and pathophysiology of the kidney,” Kidney International, vol. 55, no. 1, pp. 29–62, 1999. View at Publisher · View at Google Scholar · View at Scopus
  62. K. Fawcus, V. J. Gorton, M. L. Lucas, and G. T. A. McEwan, “Stimulation of three distinct guanylate cyclases induces mucosal surface alkalinisation in rat small intestine in vitro,” Comparative Biochemistry and Physiology A, vol. 118, no. 2, pp. 291–295, 1997. View at Publisher · View at Google Scholar · View at Scopus
  63. R. Toriano, M. Ozu, M. T. Politi, R. A. Dorr, M. A. Curto, and C. Capurro, “Uroguanylin regulates net fluid secretion via the NHE2 isoform of the Na+/H+ exchanger in an intestinal cellular model,” Cellular Physiology and Biochemistry, vol. 28, no. 4, pp. 733–742, 2011. View at Publisher · View at Google Scholar
  64. N. S. Joo, R. M. London, H. D. Kim, L. R. Forte, and L. L. Clarke, “Regulation of intestinal Cl and HCO3 secretion by uroguanylin,” American Journal of Physiology, vol. 274, no. 4, pp. G633–G644, 1998. View at Scopus
  65. A. W. Cuthbert, M. E. Hickman, L. J. MacVinish et al., “Chloride secretion in response to guanylin in colonic epithelia from normal and transgenic cystic fibrosis mice,” British Journal of Pharmacology, vol. 112, no. 1, pp. 31–36, 1994. View at Scopus
  66. J. L. Goldstein, J. Sahi, M. Bhuva, T. J. Layden, and M. C. Rao, “Escherichia coli heat-stable enterotoxin-mediated colonic Cl secretion is absent in cystic fibrosis,” Gastroenterology, vol. 107, no. 4, pp. 950–956, 1994. View at Scopus
  67. X. Y. Tien, T. A. Brasitus, M. A. Kaetzel, J. R. Dedman, and D. J. Nelson, “Activation of the cystic fibrosis transmembrane conductance regulator by cGMP in the human colonic cancer cell line, Caco-2,” Journal of Biological Chemistry, vol. 269, no. 1, pp. 51–54, 1994. View at Scopus
  68. L. R. Forte, W. J. Krause, and R. H. Freeman, “Receptors and cGMP signalling mechanism for E. coli enterotoxin in opossum kidney,” American Journal of Physiology, vol. 255, no. 5, pp. F1040–F1046, 1988. View at Scopus
  69. L. R. Forte, W. J. Krause, and R. H. Freeman, “Escherichia coli enterotoxin receptors: localization in opossum kidney, intestine, and testis,” American Journal of Physiology, vol. 257, no. 5, pp. F874–F881, 1989. View at Scopus
  70. W. J. Krause, R. H. Freeman, and L. R. Fort, “Autoradiographic demonstration of specific binding sites for E. coli enterotoxin in various epithelia of the North American opossum,” Cell and Tissue Research, vol. 260, no. 2, pp. 387–394, 1990. View at Scopus
  71. J. R. Hirsch, M. Meyer, H. J. Mägert et al., “cGMP-dependent and -independent inhibition of a K+ conductance by natriuretic peptides: molecular and functional studies in human proximal tubule cells,” Journal of the American Society of Nephrology, vol. 10, no. 3, pp. 472–480, 1999. View at Scopus
  72. J. R. Hirsch, N. Skutta, and E. Schlatter, “Signaling and distribution of NPR-Bi, the human splice form of the natriuretic peptide receptor type B,” American Journal of Physiology, vol. 285, no. 2, pp. F370–F374, 2003. View at Scopus
  73. N. Basu and S. S. Visweswariah, “Defying the stereotype: non-canonical roles of the Peptide hormones guanylin and uroguanylin,” Frontiers in Endocrinology, vol. 2, p. 14, 2011. View at Publisher · View at Google Scholar
  74. J. R. Hirsch, M. Kruhøffer, P. Herter, et al., “Cellular localization, membrane distribution, and possible function of guanylyl cyclases A and 1 in collecting ducts of rat,” Cardiovascular Research, vol. 51, no. 3, pp. 553–561, 2001. View at Publisher · View at Google Scholar · View at Scopus
  75. M. Kuhn, C. K. D. Ng, Y. H. Su et al., “Identification of an orphan guanylate cyclase receptor selectively expressed in mouse testis,” Biochemical Journal, vol. 379, no. 2, pp. 385–393, 2004. View at Publisher · View at Google Scholar · View at Scopus
  76. S. Schulz, B. J. Wedel, A. Matthews, and D. L. Garbers, “The cloning and expression of a new guanylyl cyclase orphan receptor,” Journal of Biological Chemistry, vol. 273, no. 2, pp. 1032–1037, 1998. View at Publisher · View at Google Scholar · View at Scopus
  77. X. Fan, Y. Wang, R. M. London et al., “Signaling pathways for guanylin and uroguanylin in the digestive, renal, central nervous, reproductive, and lymphoid systems,” Endocrinology, vol. 138, no. 11, pp. 4636–4648, 1997. View at Publisher · View at Google Scholar · View at Scopus
  78. S. P. Range, E. D. Holland, G. P. Basten, and A. J. Knox, “Regulation of guanosine 3′:5′-cyclic monophosphate in ovine tracheal epithelial cells,” British Journal of Pharmacology, vol. 120, no. 7, pp. 1249–1254, 1997. View at Publisher · View at Google Scholar · View at Scopus
  79. S. Schulz, T. D. Chrisman, and D. L. Garbers, “Cloning and expression of guanylin. Its existence in various mammalian tissues,” Journal of Biological Chemistry, vol. 267, no. 23, pp. 16019–16021, 1992. View at Scopus
  80. D. W. Laney, E. A. Mann, S. C. Dellon, D. R. Perkins, R. A. Giannella, and M. B. Cohen, “Novel sites for expression of an Escherichia coli heat-stable enterotoxin receptor in the developing rat,” American Journal of Physiology, vol. 263, no. 5, pp. G816–G821, 1992. View at Scopus
  81. T. Gudermann, B. Nurnberg, and G. Schultz, “Receptors and G proteins as primary components of transmembrane signal transduction—part 1: G-protein-coupled receptors: structure and function,” Journal of Molecular Medicine, vol. 73, no. 2, pp. 51–63, 1995. View at Publisher · View at Google Scholar · View at Scopus
  82. T. Okamoto, T. Katada, Y. Murayama, M. Ui, E. Ogata, and I. Nishimoto, “A simple structure encodes G protein-activating function of the IGF-II/mannose 6-phosphate receptor,” Cell, vol. 62, no. 4, pp. 709–717, 1990. View at Publisher · View at Google Scholar · View at Scopus
  83. K. A. Lucas, G. M. Pitari, S. Kazerounian et al., “Guanylyl cyclases and signaling by cyclic GMP,” Pharmacological Reviews, vol. 52, no. 3, pp. 375–413, 2000. View at Scopus
  84. A. B. Vaandrager, E. van der Wiel, and H. R. de Jonge, “Heat-stable enterotoxin activation of immunopurified guanylyl cyclase C. Modulation by adenine nucleotides,” Journal of Biological Chemistry, vol. 268, no. 26, pp. 19598–19603, 1993. View at Scopus
  85. J. K. Crane, M. S. Wehner, E. J. Bolen et al., “Regulation of intestinal guanylate cyclase by the heat-stable enterotoxin of Escherichia coli (STa) and protein kinase C,” Infection and Immunity, vol. 60, no. 12, pp. 5004–5012, 1992. View at Scopus
  86. J. K. Crane and K. L. Shanks, “Phosphorylation and activation of the intestinal guanylyl cyclase receptor for Escherichia coli heat-stable toxin by protein kinase C,” Molecular and Cellular Biochemistry, vol. 165, no. 2, pp. 111–120, 1996. View at Scopus
  87. A. Wada, M. Hasegawa, K. Matsumoto et al., “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 Letters, vol. 384, no. 1, pp. 75–77, 1996. View at Publisher · View at Google Scholar · View at Scopus
  88. N. Roy, M. R. Guruprasad, P. Kondaiah, E. A. Mann, R. A. Giannella, and S. S. Visweswariah, “Protein kinase C regulates transcription of the human guanylate cyclase C gene,” European Journal of Biochemistry, vol. 268, no. 7, pp. 2160–2171, 2001. View at Publisher · View at Google Scholar · View at Scopus
  89. R. Bhandari, K. Suguna, and S. S. Visweswariah, “Guanylyl cyclase C receptor: regulation of catalytic activity by ATP,” Bioscience Reports, vol. 19, no. 3, pp. 179–188, 1999. View at Publisher · View at Google Scholar · View at Scopus
  90. X. Qian, S. Prabhakar, A. Nandi, S. S. Visweswariah, and M. F. Goy, “Expression of GC-C, a receptor-guanylate cyclase, and its endogenous ligands uroguanylin and guanylin along the rostrocaudal axis of the intestine,” Endocrinology, vol. 141, no. 9, pp. 3210–3224, 2000. View at Publisher · View at Google Scholar · View at Scopus
  91. M. R. Crane, M. Hugues, P. D. O'Hanley, and S. A. Waldman, “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,” Molecular Pharmacology, vol. 41, no. 6, pp. 1073–1080, 1992. View at Scopus
  92. F. Albano, T. Brasitus, E. A. Mann, A. Guarino, and R. A. Giannella, “Colonocyte basolateral membranes contain Escherichia coli heat-stable enterotoxin receptors,” Biochemical and Biophysical Research Communications, vol. 284, no. 2, pp. 331–334, 2001. View at Publisher · View at Google Scholar · View at Scopus
  93. E. A. Mann, M. L. Jump, J. Wu, E. Yee, and R. A. Giannella, “Mice lacking the guanylyl cyclase C receptor are resistant to STa-induced intestinal secretion,” Biochemical and Biophysical Research Communications, vol. 239, no. 2, pp. 463–466, 1997. View at Publisher · View at Google Scholar · View at Scopus
  94. S. Schulz, M. J. Lopez, M. Kuhn, and D. L. Garbers, “Disruption of the guanylyl cyclase-C gene leads to a paradoxical phenotype of viable but heat-stable enterotoxin-resistant mice,” Journal of Clinical Investigation, vol. 100, no. 6, pp. 1590–1595, 1997. View at Scopus
  95. A. N. Charney, R. W. Egnor, J. T. Alexander-Chacko, V. Zaharia, E. A. Mann, and R. A. Giannella, “Effect of E. coli heat-stable enterotoxin on colonic transport in guanylyl cyclase C receptor-deficient mice,” American Journal of Physiology, vol. 280, no. 2, pp. G216–G221, 2001. View at Scopus
  96. U. Ganguly, A. G. Chaudhury, A. Basu, and P. C. Sen, “STa-induced translocation of protein kinase C from cytosol to membrane in rat enterocytes,” FEMS Microbiology Letters, vol. 204, no. 1, pp. 65–69, 2001. View at Publisher · View at Google Scholar · View at Scopus
  97. C. S. Weikel, C. L. Spann, C. P. Chambers, J. K. Crane, J. Linden, and E. L. Hewlett, “Phorbol esters enhance the cyclic GMP response of T84 cells to the heat-stable enterotoxin of Escherichia coli (STa),” Infection and Immunity, vol. 58, no. 5, pp. 1402–1407, 1990. View at Scopus
  98. A. Sindić, J. R. Hirsch, A. Velic, H. Piechota, and E. Schlatter, “Guanylin and uroguanylin regulate electrolyte transport in isolated human cortical collecting ducts,” Kidney International, vol. 67, no. 4, pp. 1420–1427, 2005. View at Publisher · View at Google Scholar · View at Scopus
  99. A. Sindić, A. Velic, C. Başoglu et al., “Uroguanylin and guanylin regulate transport of mouse cortical collecting duct independent of guanylate cyclase C,” Kidney International, vol. 68, no. 3, pp. 1008–1017, 2005. View at Publisher · View at Google Scholar · View at Scopus
  100. J. N. Lorenz, M. Nieman, J. Sabo et al., “Uroguanylin knockout mice have increased blood pressure and impaired natriuretic response to enteral NaCl load,” Journal of Clinical Investigation, vol. 112, no. 8, pp. 1244–1254, 2003. View at Publisher · View at Google Scholar · View at Scopus
  101. M. Kuhn, “Function and dysfunction of mammalian membrane guanylyl cyclase receptors: lessons from genetic mouse models and implications for human diseases,” Handbook of Experimental Pharmacology, vol. 191, pp. 47–69, 2009. View at Publisher · View at Google Scholar · View at Scopus
  102. H. Fukae, H. Kinoshita, S. Fujimoto, T. Kita, M. Nakazato, and T. Eto, “Changes in urinary levels and renal expression of uroguanylin on low or high salt diets in rats,” Nephron, vol. 92, no. 2, pp. 373–378, 2002. View at Scopus
  103. K. S. Oh, Y. T. Oh, S. W. Kim, T. Kita, I. Kang, and J. H. Youn, “Gut sensing of dietary K+ intake increases renal K +excretion,” American Journal of Physiology, vol. 301, no. 2, pp. R421–R429, 2011. View at Publisher · View at Google Scholar
  104. N. G. Moss, D. A. Riguera, R. C. Fellner, C. Cazzolla, and M. F. Goy, “Natriuretic and antikaliuretic effects of uroguanylin and prouroguanylin in the rat,” American Journal of Physiology, vol. 299, no. 6, pp. F1433–F1442, 2010. View at Publisher · View at Google Scholar · View at Scopus
  105. X. Qian, N. G. Moss, R. C. Fellner, B. Taylor-Blake, and M. F. Goy, “The rat kidney contains high levels of prouroguanylin (the uroguanylin precursor) but does not express GC-C (the enteric uroguanylin receptor),” American Journal of Physiology, vol. 300, no. 2, pp. F561–F573, 2011. View at Publisher · View at Google Scholar · View at Scopus
  106. S. L. Carrithers, B. Taylor, W. Y. Cai et al., “Guanylyl cyclase-C receptor mRNA distribution along the rat nephron,” Regulatory Peptides, vol. 95, no. 1–3, pp. 65–74, 2000. View at Publisher · View at Google Scholar · View at Scopus
  107. A. A. White, W. J. Krause, J. T. Turner, and L. R. Forte, “Opossum kidney contains a functional receptor for the Escherichia coli heat-stable enterotoxin,” Biochemical and Biophysical Research Communications, vol. 159, no. 1, pp. 363–367, 1989. View at Scopus
  108. S. Fujimoto, H. Kinoshita, S. Hara, M. Nakazato, S. Hisanaga, and T. Eto, “Immunohistochemical localization of uroguanylin in the human kidney,” Nephron, vol. 84, no. 1, pp. 88–89, 2000. View at Scopus
  109. S. Furuya, S. Naruse, E. Ando, K. Nokihara, and T. Hayakawa, “Effect and distribution of intravenously injected 125I-guanylin in rat kidney examined by high-resolution light microscopic radioautography,” Anatomy and Embryology, vol. 196, no. 3, pp. 185–193, 1997. View at Publisher · View at Google Scholar · View at Scopus
  110. R. M. London, S. L. Eber, S. S. Visweswariah, W. J. Krause, and L. R. Forte, “Structure and activity of OK-GC: a kidney receptor guanylate cyclase activated by guanylin peptides,” American Journal of Physiology, vol. 276, no. 6, pp. F882–F891, 1999. View at Scopus
  111. L. M. A. Lessa, L. R. Carraro-Lacroix, R. O. Crajoinas et al., “Mechanisms underlying the inhibitory effects of uroguanylin on NHE3 transport activity in renal proximal tubule,” American Journal of Physiology, vol. 303, no. 10, pp. F1399–F1408, 2012. View at Publisher · View at Google Scholar
  112. L. M. A. Lessa, J. B. O. Amorim, M. C. Fonteles, and G. Malnic, “Effect of renoguanylin on hydrogen/bicarbonate ion transport in rat renal tubules,” Regulatory Peptides, vol. 157, no. 1–3, pp. 37–43, 2009. View at Publisher · View at Google Scholar · View at Scopus
  113. C. M. Macica, Y. Yang, S. C. Hebert, and W. H. Wang, “Arachidonic acid inhibits activity of cloned renal K+ channel, ROMK1,” American Journal of Physiology, vol. 271, no. 3, pp. F588–F594, 1996. View at Scopus
  114. M. Lu, T. Wang, Q. Yan et al., “Absence of small conductance K+ channel (SK) activity in apical membranes of thick ascending limb and cortical collecting duct in ROMK (Bartter's) knockout mice,” Journal of Biological Chemistry, vol. 277, no. 40, pp. 37881–37887, 2002. View at Publisher · View at Google Scholar · View at Scopus
  115. P. Ziltener, C. Mueller, B. Haenig, M. W. Scherz, and O. Nayler, “Urotensin II mediates ERK1/2 phosphorylation and proliferation in GPR14-transfected cell lines,” Journal of Receptors and Signal Transduction, vol. 22, no. 1–4, pp. 155–168, 2002. View at Publisher · View at Google Scholar · View at Scopus
  116. U. Lehner, A. Velić, R. Schroter, E. Schlatter, and A. Sindić, “Ligands and signaling of the G-protein-coupled receptor GPR14, expressed in human kidney cells,” Cellular Physiology and Biochemistry, vol. 20, no. 1–4, pp. 181–192, 2007.
  117. J. Klokkers, P. Langehanenberg, B. Kemper et al., “Atrial natriuretic peptide and nitric oxide signaling antagonizes vasopressin-mediated water permeability in inner medullary collecting duct cells,” American Journal of Physiology, vol. 297, no. 3, pp. F693–F703, 2009. View at Publisher · View at Google Scholar · View at Scopus
  118. M. John, B. Wiedenmann, M. Kruhoffer et al., “Guanylin stimulates regulated secretion from human neuroendocrine pancreatic cells,” Gastroenterology, vol. 114, no. 4, pp. 791–797, 1998. View at Publisher · View at Google Scholar · View at Scopus
  119. H. Kulaksiz, A. Schmid, M. Hönscheid, R. Eissele, J. Klempnauer, and Y. Cetin, “Guanylin in the human pancreas: a novel luminocrine regulatory pathway of electrolyte secretion via cGMP and CFTR in the ductal system,” Histochemistry and Cell Biology, vol. 115, no. 2, pp. 131–145, 2001. View at Publisher · View at Google Scholar · View at Scopus
  120. H. Kulaksiz and Y. Cetin, “Uroguanylin and guanylate cyclase C in the human pancreas: expression and mutuality of ligand/receptor localization as indicators of intracellular paracrine signaling pathways,” Journal of Endocrinology, vol. 170, no. 1, pp. 267–275, 2001. View at Publisher · View at Google Scholar · View at Scopus
  121. K. Schwabe and Y. Cetin, “Guanylin and functional coupling proteins in the hepatobiliary system of rat and guinea pig,” Histochemistry and Cell Biology, vol. 137, no. 5, pp. 589–597, 2012. View at Publisher · View at Google Scholar
  122. L. A. Scheving and W. E. Russell, “Guanylyl cyclase C is up-regulated by nonparenchymal cells and hepatocytes in regenerating rat liver,” Cancer Research, vol. 56, no. 22, pp. 5186–5191, 1996. View at Scopus
  123. E. A. Mann, K. Shanmukhappa, and M. B. Cohen, “Lack of guanylate cyclase C results in increased mortality in mice following liver injury,” BMC Gastroenterology, vol. 10, article 86, 2010. View at Publisher · View at Google Scholar · View at Scopus
  124. Y. Cetin, H. Kulaksiz, P. Redecker et al., “Bronchiolar nonciliated secretory (Clara) cells: source of guanylin in the mammalian lung,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 13, pp. 5925–5929, 1995. View at Publisher · View at Google Scholar · View at Scopus
  125. Z. H. Zhang, F. Jow, R. Numann, and J. Hinson, “The airway-epithelium: a novel site of action by guanylin,” Biochemical and Biophysical Research Communications, vol. 244, no. 1, pp. 50–56, 1998. View at Publisher · View at Google Scholar · View at Scopus
  126. H. Ohbayashi, K. Yamaki, R. Suzuki, and K. Takagi, “Effects of uroguanylin and guanylin against antigen-induced bronchoconstriction and airway microvascular leakage in sensitized guinea- pigs,” Life Sciences, vol. 62, no. 20, pp. 1833–1844, 1998. View at Publisher · View at Google Scholar · View at Scopus
  127. H. Ohbayashi and K. I. Yamaki, “Both inhalant and intravenous uroguanylin inhibit leukotriene C4-induced airway changes,” Peptides, vol. 21, no. 10, pp. 1467–1472, 2000. View at Publisher · View at Google Scholar · View at Scopus
  128. A. Spreca, S. Simonetti, and M. G. Rambotti, “Atrial natriuretic peptide and guanylin-activated guanylate cyclase isoforms in human sweat glands,” Histochemical Journal, vol. 32, no. 12, pp. 725–731, 2000. View at Publisher · View at Google Scholar · View at Scopus
  129. M. Reinecke, I. David, D. Loffing-Cueni et al., “Localization, expression, and characterization of guanylin in the rat adrenal medulla,” Histochemistry and Cell Biology, vol. 106, no. 4, pp. 367–374, 1996. View at Publisher · View at Google Scholar · View at Scopus
  130. M. Jaleel, R. M. London, S. L. Eber, L. R. Forte, and S. S. Visweswariah, “Expression of the receptor guanylyl cyclase C and its ligands in reproductive tissues of the rat: a potential role for a novel signaling pathway in the epididymis,” Biology of Reproduction, vol. 67, no. 6, pp. 1975–1980, 2002. View at Publisher · View at Google Scholar · View at Scopus
  131. C. M. Sousa, A. Havt, C. F. Santos et al., “The relaxation induced by uroguanylin and the expression of natriuretic peptide receptors in human corpora cavernosa,” Journal of Sexual Medicine, vol. 7, no. 11, pp. 3610–3619, 2010. View at Publisher · View at Google Scholar · View at Scopus
  132. M. A. Valentino, J. E. Lin, A. E. Snook et al., “A uroguanylin-GUCY2C endocrine axis regulates feeding in mice,” The Journal of Clinical Investigation, vol. 121, pp. 3578–3588, 2011. View at Publisher · View at Google Scholar
  133. K. A. Steinbrecher, T. M. F. Tuohy, K. H. Goss et al., “Expression of guanylin is downregulated in mouse and human intestinal adenomas,” Biochemical and Biophysical Research Communications, vol. 273, no. 1, pp. 225–230, 2000. View at Publisher · View at Google Scholar · View at Scopus
  134. M. B. Cohen, J. A. Hawkins, and D. P. Witte, “Guanylin mRNA expression in human intestine and colorectal adenocarcinoma,” Laboratory Investigation, vol. 78, no. 1, pp. 101–108, 1998. View at Scopus
  135. K. Shailubhai, H. H. Yu, K. Karunanandaa et al., “Uroguanylin treatment suppresses polyp formation in the Apc(Min/+) mouse and induces apoptosis in human colon adenocarcinoma cells via cyclic GMP,” Cancer Research, vol. 60, no. 18, pp. 5151–5157, 2000. View at Scopus
  136. G. M. Pitari, M. D. Di Guglielmo, J. Park, S. Schulz, and S. A. Waldman, “Guanylyl cyclase C agonists regulate progression through the cell cycle of human colon carcinoma cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 14, pp. 7846–7851, 2001. View at Publisher · View at Google Scholar · View at Scopus
  137. Z. Li, J. W. Knowles, D. Goyeau et al., “Low salt intake down-regulates the guanylin signaling pathway in rat distal colon,” Gastroenterology, vol. 111, no. 6, pp. 1714–1721, 1996. View at Scopus
  138. L. Liu, H. Li, T. Underwood et al., “Cyclic GMP-dependent protein kinase activation and induction by exisulind and CP461 in colon tumor cells,” Journal of Pharmacology and Experimental Therapeutics, vol. 299, no. 2, pp. 583–592, 2001. View at Scopus
  139. M. Suhasini, H. Li, S. M. Lohmann, G. R. Boss, and R. B. Pilz, “Cyclic-GMP-dependent protein kinase inhibits the Ras/mitogen-activated protein kinase pathway,” Molecular and Cellular Biology, vol. 18, no. 12, pp. 6983–6994, 1998. View at Scopus
  140. K. A. Steinbrecher, S. A. Wowk, J. A. Rudolph, D. P. Witte, and M. B. Cohen, “Targeted inactivation of the mouse guanylin gene results in altered dynamics of colonic epithelial proliferation,” American Journal of Pathology, vol. 161, no. 6, pp. 2169–2178, 2002. View at Scopus
  141. M. Camici, “Guanylin peptides and colorectal cancer (CRC),” Biomedicine and Pharmacotherapy, vol. 62, no. 2, pp. 70–76, 2008. View at Publisher · View at Google Scholar · View at Scopus
  142. P. Li, J. E. Lin, S. Schulz, G. M. Pitari, and S. A. Waldman, “Can colorectal cancer be prevented or treated by oral hormone replacement therapy?” Current Molecular Pharmacology, vol. 2, no. 3, pp. 285–292, 2009. View at Scopus
  143. H. R. Wolfe, M. Mendizabal, E. Lleong et al., “In vivo imaging of human colon cancer xenografts in immunodeficient mice using a guanylyl cyclase C-specific ligand,” Journal of Nuclear Medicine, vol. 43, no. 3, pp. 392–399, 2002. View at Scopus
  144. J. Park, S. Schulz, J. Haaf, J. C. Kairys, and S. A. Waldman, “Ectopic expression of guanylyl cyclase C in adenocarcinomas of the esophagus and stomach,” Cancer Epidemiology Biomarkers and Prevention, vol. 11, no. 8, pp. 739–744, 2002. View at Scopus
  145. B. Cagir, A. Gelmann, J. Park et al., “Guanylyl cyclase C messenger RNA is a biomarker for recurrent stage II colorectal cancer,” Annals of Internal Medicine, vol. 131, no. 11, pp. 805–812, 1999. View at Scopus
  146. S. A. Waldman, B. Cagir, J. Rakinic et al., “Use of guanylyl cyclase C for detecting micrometastases in lymph nodes of patients with colon cancer,” Diseases of the Colon and Rectum, vol. 41, no. 3, pp. 310–315, 1998. View at Publisher · View at Google Scholar · View at Scopus
  147. H. Romi, I. Cohen, D. Landau, et al., “Meconium ileus caused by mutations in GUCY2C, encoding the CFTR-activating guanylate cyclase 2C,” The American Journal of Human Genetics, vol. 90, no. 5, pp. 893–899, 2012. View at Publisher · View at Google Scholar
  148. H. Fukae, H. Kinoshita, S. Fujimoto, M. Nakazato, and T. Eto, “Plasma concentration of uroguanylin in patients on maintenance dialysis therapy,” Nephron, vol. 84, no. 3, pp. 206–210, 2000. View at Scopus
  149. M. Kikuchi, S. Fujimoto, H. Fukae et al., “Role of uroguanylin, a peptide with natriuretic activity, in rats with experimental nephrotic syndrome,” Journal of the American Society of Nephrology, vol. 16, no. 2, pp. 392–397, 2005. View at Publisher · View at Google Scholar · View at Scopus
  150. A. Baba, S. Fujimoto, M. Kikuchi, T. Kita, and K. Kitamura, “Effects of uroguanylin on natriuresis in experimental nephrotic rats,” Nephrology, vol. 14, no. 1, pp. 80–85, 2009. View at Publisher · View at Google Scholar · View at Scopus