Transmembrane guanylate cyclase in intestinal pathophysiology

Current Opinion in Gastroenterology

Volumn 27, Issue 2, 2011, Pages 139-145

  Steinbrecher, Kris A ^a   Cohen, Mitchell B ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

apoptosis; cGMP; chloride channels; colon cancer; gastrointestinal motility; guanylyl cyclase; intestinal epithelial cells; postprandial natriuresis; proliferation

Indexed keywords

GUANYLATE CYCLASE; TRANSMEMBRANE GUANYLATE CYCLASE; UNCLASSIFIED DRUG;

APOPTOSIS; CELL PROLIFERATION; CELL TRANSFORMATION; CHRONIC DISEASE; CONSTIPATION; DIGESTIVE SYSTEM CANCER; EPITHELIUM CELL; GASTROINTESTINAL MOTILITY; GASTROINTESTINAL TRANSIT; HUMAN; INTESTINE EPITHELIUM; INTESTINE MOTILITY; INTESTINE SECRETION; IRRITABLE COLON; NATRIURESIS; NONHUMAN; PATHOPHYSIOLOGY; REVIEW;

ANIMALS; APOPTOSIS; CELL TRANSFORMATION, NEOPLASTIC; CYCLIC GMP; GASTROINTESTINAL NEOPLASMS; GUANYLATE CYCLASE; HUMANS; INTESTINES; MICE; RECEPTORS, GUANYLATE CYCLASE-COUPLED;

EID: 79951681078     PISSN: 02671379     EISSN: None     Source Type: Journal    
DOI: 10.1097/MOG.0b013e328341ead5     Document Type: Review

References (78)

1. Ashman DF, Lipton R, Melicow MM, Price TD. Isolation of adenosine 30 , 50-monophosphate and guanosine 30, 50-monophosphate from rat urine. Biochem Biophys Res Commun 1963; 11:330-334.
2. Kuhn M. Function and dysfunction of mammalian membrane guanylyl cyclase receptors: lessons from genetic mouse models and implications for human diseases. Handb Exp Pharmacol 2009; 191:47-69.
3. Sharma RK. Membrane guanylate cyclase is a beautiful signal transduction machine: overview. Mol Cell Biochem 2010; 334:3-36.
4. Garthwaite J. New insight into the functioning of nitric oxide-receptive guanylyl cyclase: physiological and pharmacological implications. Mol Cell Biochem 2010; 334:221-232.
5. Johnston JM, Kurtz CB, Drossman DA, et al. Pilot study on the effect of linaclotide in patients with chronic constipation. Am J Gastroenterol 2009; 104:125-132.
6. Lembo AJ, Schneier H, Lavins BJ, et al. Efficacy and safety of once daily linaclotide administered orally for 12 weeks in patients with chronic constipation: results from 2 randomized, double-blind, placebo-controlled phase 3 trials. Gastroenterology 2010; 138:S53-S54.
7. Chinkers M, Garbers DL. The protein kinase domain of the ANP receptor is required for signaling. Science 1989; 245:1392-1394. (Pubitemid 19252608)
8. Chinkers M, Garbers DL, Chang MS, et al. A membrane form of guanylate cyclase is an atrial natriuretic peptide receptor. Nature 1989; 338:78-83. (Pubitemid 19076788)
9. Singh S, Lowe DG, Thorpe DS, et al. Membrane guanylate cyclase is a cellsurfacereceptor withhomology toproteinkinases.Nature1988;334:708-712.
10. Potter LR, Garbers DL. Protein kinase C-dependent desensitization of the atrial natriuretic peptide receptor is mediated by dephosphorylation. J Biol Chem 1994; 269:14636-14642.
11. Potter LR, Garbers DL. Dephosphorylation of the guanylyl cyclase-A receptor causes desensitization. J Biol Chem 1992; 267:14531-14534.
12. Ghanekar Y, Chandrashaker A, Visweswariah SS. Cellular refractoriness to the heat-stable enterotoxin peptide is associated with alterations in levels of the differentially glycosylated forms of guanylyl cyclase C. Eur J Biochem 2003; 270:3848-3857. (Pubitemid 37123257)
13. Scott RO, Thelin WR, Milgram SL. A novel PDZ protein regulates the activity of guanylyl cyclase C, the heat-stable enterotoxin receptor. J Biol Chem 2002; 277:22934-22941. (Pubitemid 34967277)
14. 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 1996; 165:111-120. (Pubitemid 26421261)
15. Bakre MM, Ghanekar Y, Visweswariah SS. Homologous desensitization of the human guanylate cyclase C receptor. Cell-specific regulation of catalytic activity. Eur J Biochem 2000; 267:179-187. (Pubitemid 30029752)
16. Castro LR, Verde I, Cooper DM, Fischmeister R. Cyclic guanosine monophosphate compartmentation in rat cardiac myocytes. Circulation 2006; 113:2221-2228.
17. Nausch LW, Ledoux J, Bonev AD, et al. Differential patterning of cGMP in vascular smooth muscle cells revealed by single GFP-linked biosensors. Proc Natl Acad Sci U S A 2008; 105:365-370.
18. Li Z, Goy MF. Peptide-regulated guanylate cyclase pathways in rat colon: in situ localization of GCA, GCC, and guanylin mRNA. Am J Physiol 1993; 265:G394-G402. (Pubitemid 23273646)
19. Sabbatini ME. Natriuretic peptides as regulatory mediators of secretory activity in the digestive system. Regul Pept 2009; 154:5-15.
20. Guo HS, Jin Z, Jin ZY, et al. Comparative study in the effect of C-type natriuretic peptide on gastric motility in various animals. World JGastroenterol 2003; 9:547-552. (Pubitemid 36378095)
21. Chitapanarux T, Chen SL, Lee H, et al. C-type natriuretic peptide induces human colonic myofibroblast relaxation. Am J Physiol Gastrointest Liver Physiol 2004; 286:G31-G36. (Pubitemid 38055833)
22. Rubattu S, Sciarretta S, Morriello A, et al. NPR-C: a component of the natriuretic peptide family with implications in human diseases. J Mol Med 2010; 88:889-897.
23. Guo D, Tan YC, Wang D, et al. A Rac-cGMP signaling pathway. Cell 2007; 128:341-355. (Pubitemid 46123509)
24. Schulz S, Green CK, Yuen PS, Garbers DL. Guanylyl cyclase is a heat-stable enterotoxin receptor. Cell 1990; 63:941-948. (Pubitemid 120034935)
25. Hodson CA, Ambrogi IG, Scott RO, et al. Polarized apical sorting of guanylyl cyclase C is specified by a cytosolic signal. Traffic 2006; 7:456-464. (Pubitemid 43372753)
26. Albano F, de Marco G, Canani RB, et al. Guanylin and E. coli heat-stable enterotoxin induce chloride secretion through direct interaction with basolateral compartment of rat and human colonic cells. Pediatr Res 2005; 58:159-163. (Pubitemid 40967448)
27. Albano F, Brasitus T, Mann EA, et al. Colonocyte basolateral membranes contain Escherichia coli heat-stable enterotoxin receptors. Biochem Biophys Res Commun 2001; 284:331-334. (Pubitemid 32917979)
28. Buccigrossi V, Armellino C, Ruberto E, et al. Polar effects on ion transport and cell proliferation induced by guanylate cyclase-C ligands in intestinal epithelial cells. Pediatr Res 2010. [Epub ahead of print]
29. 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 enterotoxinresistant mice. J Clin Invest 1997; 100:1590-1595. (Pubitemid 27425787)
30. Currie MG, Fok KF, Kato J, et al. Guanylin: an endogenous activator of intestinal guanylate cyclase. Proc Natl Acad Sci U S A 1992; 89:947-951.
31. Hamra FK, Forte LR, Eber SL, et al. Uroguanylin: structure and activity of a second endogenous peptide that stimulates intestinal guanylate cyclase. Proc Natl Acad Sci U S A 1993; 90:10464-10468. (Pubitemid 23347062)
32. Qian X, Moss NG, Fellner RC, Goy MF. Circulating prouroguanylin is processed to its active natriuretic form exclusively within the renal tubules. Endocrinology 2008; 149:4499-4509.
33. Moss NG, Fellner RC, Qian X, et al. Uroguanylin, an intestinal natriuretic peptide, is delivered to the kidney as an unprocessed propeptide. Endocrinology 2008; 149:4486-4498.
34. Carrithers SL, Hill MJ, Johnson BR, et al. Renal effects of uroguanylin and guanylin in vivo. Braz J Med Biol Res 1999; 32:1337-1344. (Pubitemid 129544251)
35. Carrithers SL, Ott CE, Hill MJ, et al. Guanylin and uroguanylin induce natriuresis in mice lacking guanylyl cyclase-C receptor. Kidney Int 2004; 65:40-53. (Pubitemid 38037490)
36. Carrithers SL, Taylor B, Cai WY, et al. Guanylyl cyclase-C receptor mRNA distribution along the rat nephron. Regul Pept 2000; 95:65-74.
37. Laney DW Jr, Mann EA, Dellon SC, et al. Novel sites for expression of an Escherichia coli heat-stable enterotoxin receptor in the developing rat. Am J Physiol 1992; 263:G816-G821.
38. Leinders-Zufall T, Cockerham RE, Michalakis S, et al. Contribution of the receptor guanylyl cyclase GC-D to chemosensory function in the olfactory epithelium. Proc Natl Acad Sci U S A 2007; 104:14507-14512. (Pubitemid 350003291)
39. Cohen MB, Jensen NJ, Hawkins JA, et al. Receptors for Escherichia coli heat stable enterotoxin in human intestine and in a human intestinal cell line (Caco-2). J Cell Physiol 1993; 156:138-144. (Pubitemid 23211272)
40. 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 1992; 41:1073-1080. (Pubitemid 23026107)
41. Mann EA, Cohen MB, Giannella RA. Comparison of receptors for Escherichia coli heat-stable enterotoxin: novel receptor present in IEC-6 cells. Am J Physiol 1993; 264:G172-G178. (Pubitemid 23056004)
42. Sogawa C, Abe A, Tsuji T, et al. Gastrointestinal tract disorder in natriuretic peptide receptor B gene mutant mice. Am J Pathol 2010; 177:822-828.
43. Novaira HJ, Ornellas DS, Ortiga-Carvalho TM, et al. Atrial natriuretic peptide modulates cystic fibrosis transmembrane conductance regulator chloride channel expression in rat proximal colon and human intestinal epithelial cells. J Endocrinol 2006; 189:155-165. (Pubitemid 43670710)
44. Itaba S, Chijiiwa Y, Matsuzaka H, et al. Presence of C-type natriuretic peptide (CNP) in guinea pig caecum: role and mechanisms of CNP in circular smooth muscle relaxation. Neurogastroenterol Motil 2004; 16:375-382. (Pubitemid 38869661)
45. Zhang Y, Piao LH, Huang X, et al. Pacemaker currents modulated by C-type natriuretic peptide in interstitial cells of cajal from murine small intestine. J Physiol Biochem 2006; 62:281-291.
46. Tsuji T, Kunieda T. A loss-of-function mutation in natriuretic peptide receptor 2 (Npr2) gene is responsible for disproportionate dwarfism in cn/cn mouse. J Biol Chem 2005; 280:14288-14292. (Pubitemid 40517331)
47. Tamura N, Doolittle LK, Hammer RE, et al. Critical roles of the guanylyl cyclase B receptor in endochondral ossification and development of female reproductive organs. Proc Natl Acad Sci U S A 2004; 101:17300-17305. (Pubitemid 39627814)
48. Basu N, Arshad N, Visweswariah SS. Receptor guanylyl cyclase C (GC-C): regulation and signal transduction. Mol Cell Biochem 2010; 334:67-80.
49. Mann EA, Jump ML, Wu J, et al. Mice lacking the guanylyl cyclase C receptor are resistant to STa-induced intestinal secretion. Biochem Biophys Res Commun 1997; 239:463-466. (Pubitemid 27488986)
50. Elitsur N, Lorenz JN, Hawkins JA, et al. The proximal convoluted tubule is a target for the uroguanylin-regulated natriuretic response. J Pediatr Gastroenterol Nutr 2006; 43 (Suppl 1):S74-S81. (Pubitemid 44014982)
51. Lorenz JN, Nieman M, Sabo J, et al. Uroguanylin knockout mice have increased blood pressure and impaired natriuretic response to enteral NaCl load. J Clin Invest 2003; 112:1244-1254. (Pubitemid 38056301)
52. Moss NG, Riguera DA, Fellner RC, et al. Natriuretic and antikaliuretic effects of uroguanylin and prouroguanylin in the rat. Am J Physiol Renal Physiol 2010. [Epub ahead of print]
53. Busby RW, Bryant AP, Bartolini WP, et al. Linaclotide, through activation of guanylate cyclase C, acts locally in the gastrointestinal tract to elicit enhanced intestinal secretion and transit. Eur J Pharmacol 2010; 649:328-335.
54. Bryant AP, Busby RW, Bartolini WP, et al. Linaclotide is a potent and selective guanylate cyclase C agonist that elicits pharmacological effects locally in the gastrointestinal tract. Life Sci 2010; 86:760-765.
55. Eutamene H, Bradesi S, Larauche M, et al. Guanylate cyclase C-mediated antinociceptive effects of linaclotide in rodent models of visceral pain. Neurogastroenterol Motil 2010; 22:312-384.
56. Johnston JM, Kurtz CB, Macdougall JE, et al. Linaclotide improves abdominal pain and bowel habits in a phase IIb study of patients with irritable bowel syndrome. Gastroenterology 2010. [Epub ahead of print]
57. You H, Laychock SG. Atrial natriuretic peptide promotes pancreatic islet betacell growth and Akt/Foxo1a/cyclin D2 signaling. Endocrinology 2009; 150: 5455-5465.
58. Chusho H, Tamura N, Ogawa Y, et al. Dwarfism and early death in mice lacking C-type natriuretic peptide. Proc Natl Acad Sci U S A 2001; 98:4016-4021. (Pubitemid 32249890)
59. Komatsu Y, Itoh H, Suga S, et al. Regulation of endothelial production of C-type natriuretic peptide in coculture with vascular smooth muscle cells. Role of the vascular natriuretic peptide system in vascular growth inhibition. Circ Res 1996; 78:606-614. (Pubitemid 26106876)
60. Lenz A, Sun Y, Eichelbaum EJ, et al. Twice-weekly intravenous treatment of pancreatic cancer with atrial natriuretic peptide and vessel dilator. In Vivo 2010; 24:125-129.
61. Gower WR, Vesely BA, Alli AA, Vesely DL. Four peptides decrease human colon adenocarcinoma cell number and DNA synthesis via cyclic GMP. Int J Gastrointest Cancer 2005; 36:77-87.
62. Kong X, Wang X, Xu W, et al. Natriuretic peptide receptor a as a novel anticancer target. Cancer Res 2008; 68:249-256. (Pubitemid 351380126)
63. Pitari GM, Di Guglielmo MD, Park J, et al. Guanylyl cyclase C agonists regulate progression through the cell cycle of human colon carcinoma cells. Proc Natl Acad Sci U S A 2001; 98:7846-7851. (Pubitemid 32642649)
64. Basu N, Bhandari R, Natarajan VT, Visweswariah SS. Cross talk between receptor guanylyl cyclase C and c-src tyrosine kinase regulates colon cancer cell cytostasis. Mol Cell Biol 2009; 29:5277-5289.
65. Li P, Lin JE, Chervoneva I, et al. Homeostatic control of the crypt-villus axis by the bacterial enterotoxin receptor guanylyl cyclase C restricts the proliferating compartment in intestine. Am J Pathol 2007; 171:1847-1858.
66. Lin JE, Li P, Snook AE, et al. The hormone receptor GUCY2C suppresses intestinal tumor formation by inhibiting Akt signaling. Gastroenterology 2010; 138:241-254.
67. Pitari GM, Lin JE, Shah FJ, et al. Enterotoxin preconditioning restores calciumsensing receptor-mediated cytostasis in colon cancer cells. Carcinogenesis 2008; 29:1601-1607.
68. Garin-Laflam MP, Steinbrecher KA, Rudolph JA, et al. Activation of guanylate cyclase C signaling pathway protects intestinal epithelial cells from acute radiation-induced apoptosis. Am J Physiol Gastrointest Liver Physiol 2009; 296:G740-G749.
69. Mann EA, Shanmukhappa K, Cohen MB. Lack of guanylate cyclase C results in increased mortality in mice following liver injury. BMC Gastroenterol 2010; 10:86.
70. Steinbrecher KA, Wowk SA, Rudolph JA, et al. Targeted inactivation of the mouse guanylin gene results in altered dynamics of colonic epithelial proliferation. Am J Pathol 2002; 161:2169-2178. (Pubitemid 35434862)
71. Shailubhai K, Yu HH, Karunanandaa K, et al. Uroguanylin treatment suppresses polyp formation in the Apc(Min/p) mouse and induces apoptosis in human colon adenocarcinoma cells via cyclic GMP. Cancer Res 2000; 60:5151-5157.
72. Carrithers SL, Parkinson SJ,Goldstein S, et al. Escherichia coli heat-stable toxin receptors in human colonic tumors. Gastroenterology 1994; 107:1653-1661.
73. Winn B, Tavares R, Matoso A, et al. Expression of the intestinal biomarkers guanylyl cyclase C and CDX2 in poorly differentiated colorectal carcinomas. Hum Pathol 2010; 41:123-128.
74. Waldman SA, Hyslop T, Schulz S, et al. Association of GUCY2C expression in lymph nodes with time to recurrence and disease-free survival in pN0 colorectal cancer. JAMA 2009; 301:745-752.
75. Cohen MB, Hawkins JA, Witte DP. Guanylin mRNA expression in human intestine and colorectal adenocarcinoma. Lab Invest 1998; 78:101-108. (Pubitemid 28074313)
76. Steinbrecher KA, Tuohy TM, Heppner Goss K, et al. Expression of guanylin is downregulated in mouse and human intestinal adenomas. Biochem Biophys Res Commun 2000; 273:225-230. (Pubitemid 30426891)
77. Giblin MF, Sieckman GL, Watkinson LD, et al. Selective targeting of E. coli heat-stable enterotoxin analogs to human colon cancer cells. Anticancer Res 2006; 26:3243-3251. (Pubitemid 44701492)
78. Giblin MF, Sieckman GL, Shelton TD, et al. In vitro and in vivo evaluation of 177Lu-and 90Y-labeled E. coli heat-stable enterotoxin for specific targeting of uroguanylin receptors on human colon cancers. Nucl Med Biol 2006; 33:481-488. (Pubitemid 43729859)