Guanylin peptides (GPs) family includes guanylin (GN), uroguanylin (UGN), lymphoguanylin, and recently discovered renoguanylin. This growing family is proposed to be intestinal natriuretic peptides. After ingestion of a salty meal, GN and UGN are secreted into the intestinal lumen, where they inhibit sodium absorption and induce anion and water secretion. At the same conditions, those hormones stimulate renal electrolyte excretion by inducing natriuresis, kaliuresis, and diuresis and therefore prevent hypernatremia and hypervolemia after salty meals. In the intestine, a well-known receptor for GPs is guanylate cyclase C (GC-C) whose activation increases intracellular concentration of cGMP. However, in the kidney of GC-C-deficient mice, effects of GPs are unaltered, which could be by new cGMP-independent signaling pathway (G-protein-coupled receptor). This is not unusual as atrial natriuretic peptide also activates two different types of receptors: guanylate cylcase A and clearance receptor which is also G-protein coupled receptor. Physiological role of GPs in other organs (liver, pancreas, lung, sweat glands, and male reproductive system) needs to be discovered. However, it is known that they are involved in pathological conditions like cystic fibrosis, asthma, intestinal tumors, kidney and heart failure, obesity, and metabolic syndrome. 1. Introduction The physiological importance of digestive system is not only to digest and absorb nutrients but also to prepare the body for an increase in blood concentrations of glucose, amino acids, electrolytes, and water. It is well known that several hormones secreted by intestine after a meal, like gastrin, secretin, cholecystokinin, and especially gastric inhibitory peptide increase insulin production even before the concentrations of glucose and amino acids significantly increase in the blood. Lennane et al. in 1975 showed that salt taken per os will increase secretion of electrolyte and water by the kidneys more than the same amount of the salt given intravenously, proposing the existence of intestinal hormones that regulate kidney function [1]. After a salty meal, intestinal natriuretic peptides also known as guanylin peptides (GPs) are secreted by intestine where the inhibit sodium absorption from intestinal lumen by inhibiting sodium/hydrogen exchange (NHE), increase bicarbonate and chloride secretion, inhibit water absorption [2, 3], and increase renal sodium and potassium secretion [4–6]. Effects of GPs on sodium transport in the intestine and the kidneys prevent postprandial hypernatremia, gastric
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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[13]
H. J. M？gert, 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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[21]
A. Sindi？e, C. Basoglu, A. ？er？i 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.
[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.
[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.
[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.
[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.
[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.
[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.
[28]
H. J. M？gert, 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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[71]
J. R. Hirsch, M. Meyer, H. J. M？gert 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.
[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.
[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.
[74]
J. R. Hirsch, M. Kruh？ffer, 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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[98]
A. Sindi？, 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.
[99]
A. Sindi？, A. Velic, C. Ba？oglu 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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[116]
U. Lehner, A. Veli？, R. Schroter, E. Schlatter, and A. Sindi？, “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.
[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.
[119]
H. Kulaksiz, A. Schmid, M. H？nscheid, 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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[141]
M. Camici, “Guanylin peptides and colorectal cancer (CRC),” Biomedicine and Pharmacotherapy, vol. 62, no. 2, pp. 70–76, 2008.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
