GCC signaling in colorectal cancer: Is colorectal cancer a paracrine deficiency syndrome?

Drug News and Perspectives

Volumn 22, Issue 6, 2009, Pages 313-318

  Li, P ^a   Lin, J E ^a   Marszlowicz, G P ^b   Valentino, M A ^a   Chang, C ^b   Schulz, S ^a   Pitari, G M ^a   Waldman, Scott A ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b DREXEL UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APC PROTEIN; GENE PRODUCT; GUANYLATE CYCLASE; GUANYLIN; UROGUANYLIN;

CANCER GROWTH; CANCER INVASION; CANCER SUSCEPTIBILITY; CARCINOGENESIS; CELL CYCLE ARREST; CELL DIFFERENTIATION; CELL METABOLISM; CELL PROLIFERATION; COLORECTAL CANCER; GENE MUTATION; GENE SILENCING; GENETIC SUSCEPTIBILITY; GERM LINE; HORMONE DEFICIENCY; HORMONE SUBSTITUTION; HUMAN; INTESTINE CRYPT; INTESTINE MUCOSA; INTESTINE VILLUS; MALIGNANT TRANSFORMATION; NONHUMAN; PARACRINE SIGNALING; PHENOTYPE; REVIEW; TUMOR SUPPRESSOR GENE;

ANIMALS; COLORECTAL NEOPLASMS; DRUG DELIVERY SYSTEMS; GASTROINTESTINAL HORMONES; GUANYLATE CYCLASE; HORMONE REPLACEMENT THERAPY; HUMANS; MICE; NATRIURETIC PEPTIDES; RECEPTORS, PEPTIDE; SIGNAL TRANSDUCTION;

EID: 70350538874     PISSN: 02140934     EISSN: None     Source Type: Journal    
DOI: 10.1358/dnp.2009.22.6.1395254     Document Type: Review

References (78)

1. Cresanta, J.L. Epidemiology of cancer in the United States. Prim Care 1992, 19(3): 419-441
2. Greenwald, P. Colon cancer overview. Cancer 1992, 70(5 Suppl): 1206-1215
3. Jessup, J.M. and Gallick, G.E. The biology of colorectal carcinoma. Curr Probl Cancer 1992, 16(5): 261-328.
4. Meyerhardt, J.A. and Mayer, R.J. Systemic therapy for colorectal cancer. N Engl J Med 2005, 352(5): 476-487
5. Pihl, E., Hughes, E.S., McDermott, F.T., Milne, B.J. and Price, A.B. Disease-free survival and recurrence after resection of colorectal carcinoma. J Surg Oncol 1981, 16(4): 333-341 (Pubitemid 11156437)
6. Sobrero, A., Kerr, D., Glimelius, B. et al. New directions in the treatment of colorectal cancer: a look to the future. Eur J Cancer 2000, 36(5): 559-566 (Pubitemid 30156840)
7. Vogelstein, B., Fearon, E.R., Hamilton, S.R. et al. Genetic alterations during colorectal-tumor development. N Engl J Med 1988, 319(9): 525-532
8. Aaltonen, L.A., Peltomaki, P., Leach, F.S. et al. Clues to the pathogenesis of familial colorectal cancer. Science 1993, 260(5109): 812-816 (Pubitemid 23167611)
9. Lynch, H.T. and de la Chapelle, A. Hereditary colorectal cancer. N Engl J Med 2003, 348(10): 919-932
10. Shailubhai, K., Yu, H.H., Karunanandaa, K. et al. Uroguanylin treatment suppresses polyp formation in the Apc(Min/+) mouse and induces apoptosis in human colon adenocarcinoma cells via cyclic GMP. Cancer Res 2000, 60(18): 5151-5157
11. Pitari, G.M., Zingman, L.V., Hodgson, D.M. et al. Bacterial enterotoxins are associated with resistance to colon cancer. Proc Natl Acad Sci U S A 2003, 100(5): 2695-2699
12. Li, P., Lin, J.E., Chervoneva, I., Schulz, S., Waldman, S.A. and Pitari, G.M. 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(6): 1847-1858
13. Li, P., Lin, J.E., Snook, A.E. et al. Colorectal cancer as a paracrine deficiency syndrome amenable to oral hormone replacement therapy. Clin Transl Sci 2008, 1: 163-167
14. Pitari, G.M., Li, P., Lin, J.E. et al. The paracrine hormone hypothesis of colorectal cancer. Clin Pharmacol Ther 2007, 82(4): 441-447 (Pubitemid 47414353)
15. Pinto, D. and Clevers, H. Wnt, stem cells and cancer in the intestine. Biol Cell 2005, 97(3): 185-196
16. Potten, C.S. and Loeffler, M. Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development 1990, 110(4): 1001-1020
17. Reya, T. and Clevers, H. Wnt signalling in stem cells and cancer. Nature 2005, 434(7035): 843-850 (Pubitemid 40558990)
18. Sancho, E., Batlle, E. and Clevers, H. Signaling pathways in intestinal development and cancer. Annu Rev Cell Dev Biol 2004, 20: 695-723. (Pubitemid 39488655)
19. Yang, Q., Bermingham, N.A., Finegold, M.J. and Zoghbi, H.Y. Requirement of Math1 for secretory cell lineage commitment in the mouse intestine. Science 2001, 294(5549): 2155-2158 (Pubitemid 33150670)
20. Jensen, J., Pedersen, E.E., Galante, P. et al. Control of endodermal endocrine development by Hes-1. Nat Genet 2000, 24(1): 36-44. (Pubitemid 30041417)
21. Crosnier, C., Stamataki, D. and Lewis, J. Organizing cell renewal in the intestine: stem cells, signals and combinatorial control. Nat Rev Genet 2006, 7(5): 349-359
22. Zecchini, V., Domaschenz, R., Winton, D. and Jones, P. Notch signaling regulates the differentiation of post-mitotic intestinal epithelial cells. Genes & Dev 2005, 19: 1686-1691 (Pubitemid 41058364)
23. Kotdovsky, O., Dobiasova, M., Hahn, P., Kolinska, J., Kraml, J. and Pacha, J. Development of gastrointestinal functions. Physiol Res 1995, 44(6): 341-348
24. Bry, L., Falk, P., Huttner, K., Ouellette, A., Midtvedt, T. and Gordon, J.I. Paneth cell differentiation in the developing intestine of normal and transgenic mice. Proc Natl Acad Sci U S A 1994, 91(22): 10335-10339 (Pubitemid 24328991)
25. Gassler, N., Newrzella, D., Bohm, C et al. Molecular characterisation of non-absorptive and absorptive enterocytes in human small intestine. Gut 2006, 55(8): 1084-1089 (Pubitemid 44085672)
26. Aoki, K., Tamai, Y., Horiike, S., Oshima, M. and Taketo, M.M. Colonic polyposis caused by mTOR-mediated chromosomal instability in Apc+/Delta716 Cdx2+/- compound mutant mice. Nat Genet 2003, 35(4): 323-330 (Pubitemid 37486915)
27. Spruck, C.H., Won, K.A. and Reed, S.I. Deregulated cyclin E induces chromosome instability. Nature 1999, 401(6750): 297-300. (Pubitemid 129515546)
28. Morgan, D.O. Cyclin-dependent kinases: engines, clocks, and microprocessors. Annu Rev Cell Dev Biol 1997, 13: 261-291
29. Murray, A.W. Recycling the cell cycle: cyclins revisited. Cell 2004, 116(2): 221-234 (Pubitemid 38167314)
30. Oving, I.M. and Clevers, H.C. Molecular causes of colon cancer. Eur J Clin Invest 2002, 32(6): 448-457
31. Clevers, H. Wnt breakers in colon cancer. Cancer Cell 2004, 5(1): 5-6.
32. Zauber, N.P., Wang, C., Lee, P.S., Redondo, T.C., Bishop, D.T. and Goel, A. Ki-ras gene mutations, LOH of the APC and DCC genes, and microsatellite instability in primary colorectal carcinoma are not associated with micrometastases in pericolonic lymph nodes or with patients' survival. J Clin Pathol 2004, 57(9): 938-942
33. Qiu, Y., Ogawa, H., Miyagi, M. and Misono, K.S. Constitutive activation and uncoupling of the atrial natriuretic peptide receptor by mutations at the dimer interface. Role of the dimer structure in signalling. J Biol Chem 2004, 279(7): 6115-6123 (Pubitemid 38220644)
34. Vijayachandra, K., Guruprasad, M., Bhandari, R. et al. Biochemical characterization of the intracellular domain of the human guanylyl cyclase C receptor provides evidence for a catalytically active homotrimer. Biochemistry 2000, 39(51): 16075-16083
35. Vaandrager, A.B., van der Wiel, E., Horn, M.L., Luthjens, L.H. and de Jonge, H.R. Heat-stable enterotoxin receptor/guanylyl cyclase C is an oligomer consisting of functionally distinct subunits, which are non-covalently linked in the intestine. J Biol Chem 1994, 269(23): 16409-16415
36. Cagir, B., Gelmann, A., Park, J. et al. Guanylyl cyclase C messenger RNA is a biomarker for recurrent stage II colorectal cancer. Ann Intern Med 1999, 131(11): 805-812
37. Carrithers, S.L., Barber, M.T., Biswas, S. et al. Guanylyl cyclase C is a selective marker for metastatic colorectal tumors in human extraintestinal tissues. Proc Natl Acad Sci U S A 1996, 93(25): 14827-14832 (Pubitemid 26419054)
38. Carrithers, S.L., Ott, C.E., Hill, M.J. et al. Guanylin and uroguanylin induce natriuresis in mice lacking guanylyl cyclase-C receptor. Kidney Int 2004, 65(1): 40-53.
39. Carrithers, S.L., Parkinson, S.J., Goldstein, S., Park, P., Robertson, D.C. and Waldman, S.A. Escherichia coll heat-stable toxin receptors in human colonic tumors. Gastroenterology 1994, 107(6): 1653-1661 (Pubitemid 124006525)
40. Frick, G.S., Pitari, G.M., Weinberg, D.S., Hyslop, T., Schulz, S. and Waldman, S.A. Guanylyl cyclase C: a molecular marker for staging and postoperative surveillance of patients with colorectal cancer. Expert Rev Mol Diagn 2005, 5(5): 701-713 (Pubitemid 41337465)
41. Carpick, B.W. and Gariepy, J. The Escherichia coli heat-stable enterotoxin is a long-lived superagonist of guanylin. Infect Immun 1993, 61(11): 4710-4715 (Pubitemid 23320526)
42. Lucas, K.A., Pitari, G.M., Kazerounian, S. et al. Guanylyl cyclases and signaling by cyclic GMP. Pharmacol Rev 2000, 52(3): 375-414.
43. Giannella, R.A. Escherichia coli heat-stable enterotoxins, guanylins, and their receptors: what are they and what do they do? J Lab Clin Med 1995, 125(2): 173-181
44. Sciaky, D., Jenkins, N.A., Gilbert, D.J. et al. Mapping of guanylin to murine chromosome 4 and human chromosome 1p34-p35. Genomics 1995, 26(2): 427-429
45. Sciaky, D., Kosiba, J.L. and Cohen, M.B. Genomic sequence of the murine guanylin gene. Genomics 1994, 24(3): 583-587
46. Birkenkamp-Demtroder, K., Lotte Christensen, L., Harder Olesen, S. et al. Gene expression in colorectal cancer. Cancer Res 2002, 62: 4352-4363
47. Cohen, M.B., Hawkins, J.A. and Witte, D.P. Guanylin mRNA expression in human intestine and colorectal adenocarcinoma. Lab Invest 1998, 78(1): 101-108 (Pubitemid 28074313)
48. Notterman, D.A., Alon, U., Sierk, A.J. and Levine, A.J. Transcriptional gene expression profiles of colorectal adenoma, adenocarcinoma, and normal tissue examined by oligonucleotide arrays. Cancer Res 2001, 61(7): 3124-3130 (Pubitemid 32691964)
49. Steinbrecher, K.A., Tuohy, T.M., Heppner Goss, K. et al. Expression of guanylin is down- regulated in mouse and human intestinal adenomas. Biochem Biophys Res Commun 2000, 273(1): 225-230 (Pubitemid 30426891)
50. Zhang, L., Zhou, W., Velculescu, V.E. et al. Gene expression profiles in normal and cancer cells. Science 1997, 276(5316): 1268-1272 (Pubitemid 27227367)
51. Glebov, O.K., Rodriguez, L.M., Soballe, P. et al. Gene expression patterns distinguish colonoscopically isolated human aberrant crypt foci from normal colonic mucosa. Cancer Epidemiol Biomarkers Prev 2006, 15(11): 2253-2262
52. Miyaki, M., Iijima, T., Kimura, J. et al. Frequent mutation of beta-catenin and APC genes in primary colorectal tumors from patients with hereditary nonpolyposis colorectal cancer. Cancer Res 1999, 59(18): 4506-4509 (Pubitemid 29428947)
53. Sparks, A.B., Morin, P.J., Vogelstein, B. and Kinzler, K.W. Mutational analysis of the APC/beta-catenin/Tcf pathway in colorectal cancer. Cancer Res 1998, 58(6): 1130-1134 (Pubitemid 28183198)
54. Li, P., Lin, J.E., Snook, A.E., Schulz, S., Pitari, G.M. and Waldman, S.A. Colorectal cancer is a paracrine deficiency syndrome which can be prevented and treated by oral hormone replacement therapy. Curr Mol Pharmacol 2008: In press.
55. Pitari, G.M., Di Guglielmo, M.D., Park, J., Schutz, S. and Waldman, S.A. Guanylyl cyclase C agonists regulate progression through the cell cycle of human colon carcinoma cells. Proc Natl Acad Sci U S A 2001, 98(14): 7846-7851
56. Carrithers, S.L., Hill, M.J., Johnson, B.R. et al. Renal effects of uroguanylin and guanylin in vivo. Braz J Med Biol Res 1999, 32(11): 1337-1344
57. Kulaksiz, H., Schmid, A., Honscheid, M., Ramaswamy, A. and Cetin, Y. Clara cell impact in air-side activation of CFTR in small pulmonary airways. Proc Natl Acad Sci U S A 2002, 99(10): 6796-6801
58. Schulz, S., Chrisman, T.D. and Garbers, D.L. Cloning and expression of guanylin. Its existence in various mammalian tissues. J Biol Chem 1992, 267(23): 16019-16021
59. Fonteles, M.C., Carrithers, S.L., Monteiro, H.S. et al. Renal effects of serine-7 analog of lymphoguanylin in ex vivo rat kidney. Am J Physiol Renal Physiol 2001, 280(2): F207-13.
60. London, R.M., Eber, S.L., Visweswariah, S.S., Krause, W.J. and Forte, L.R. Structure and activity of OK-GC: a kidney receptor guanylate cyclase activated by guanylin peptides. Am J Physiol 1999, 276(6 Pt 2): F882-91.
61. Kulaksiz, H., Schlenker, T., Rost, D. et al. Guanylin regulates chloride secretion in the human gallbladder via the bile fluid. Gastroenterology 2004, 126(3): 732-740 (Pubitemid 38298321)
62. Kulaksiz, H. and Cetin, Y. Uroguanylin and guanylate cyclase C in the human pancreas: expression and mutuality of ligand/receptor localization as indicators of intercellular paracrine signaling pathways. J Endocrinol 2001, 170(1): 267-275 (Pubitemid 32677589)
63. Kulaksiz, H., Schmid, A., Honscheid, M., Eissele, R., Klempnauer, J. and Cetin, Y. Guanylin in the human pancreas: a novel luminocrine regulatory pathway of electrolyte secretion via cGMP and CFTR in the ductal system. Histochem Cell Biol 2001, 115(2): 131-145
64. Kulaksiz, H., Rausch, U., Vaccaro, R., Renda, T.G. and Cetin, Y. Guanylin and uroguanylin in the parotid and submandibular glands: potential intrinsic regulators of electrolyte secretion in salivary glands. Histochem Cell Biol 2001, 115(6): 527-533
65. Kulaksiz, H., Rehberg, E., Stremmel, W. and Cetin, Y. Guanylin and functional coupling proteins in the human salivary glands and gland tumors : expression, cellular localization, and target membrane domains. Am J Pathol 2002, 161(2): 655-664 (Pubitemid 36142174)
66. Jaleel, M., London, R.M., Eber, S.L., Forte, L.R. and Visweswariah, S.S. 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. Biol Reprod 2002, 67(6): 1975-1980
67. Birbe, R., Palazzo, J.P., Walters, R., Weinberg, D., Schulz, S. and Waldman, S.A. Guanylyl cyclase C is a marker of intestinal metaplasia, dysplasia, and adenocarcinoma of the gastrointestinal tract. Hum Pathol 2005, 36(2): 170-179 (Pubitemid 40313574)
68. Schulz, S., Hyslop, T., Haaf, J. et al. A validated quantitative assay to detect occult micrometastases by reverse transcriptase- polymerase chain reaction of guanylyl cyclase C in patients with colorectal cancer. Clin Cancer Res 2006, 12(15): 4545-4552 (Pubitemid 44297803)
69. Waldman, S.A., Cagir, B., Rakinic, J. et al. Use of guanylyl cyclase C for detecting micrometastases in lymph nodes of patients with colon cancer. Dis Colon Rectum 1998, 41(3): 310-315 (Pubitemid 28141595)
70. Giannella, R.A. and Mann, E.A. E. coli heat- stable enterotoxin and guanylyl cyclase C: new functions and unsuspected actions. Trans Am Clin Climatol Assoc 2003, 114: 67-85.
71. Sellers, Z.M., Mann, E., Smith, A. et al. Heat- stable enterotoxin of Escherichia coli (STa) can stimulate duodenal HCO3(-) secretion via a novel GC-C- and CFTR-independent pathway. FASEB J 2008, 22(5): 1306-1316 (Pubitemid 351656772)
72. Li, P., Schulz, S., Bombonati, A. et al. Guanylyl cyclase C suppresses intestinal tumorigenesis by restricting proliferation and maintaining genomic integrity. Gastroenterology 2007, 133(2): 599-607. (Pubitemid 47187356)
73. Steinbrecher, K.A., Wowk, S.A., Rudolph, J.A., Witte, D.P. and Cohen, M.B. Targeted inactivation of the mouse guanylin gene results in altered dynamics of colonic epithelial proliferation. Am J Pathol 2002, 161(6): 2169-2178
74. Bui, T. and Thompson, C.B. Cancer's sweet tooth. Cancer Cell 2006, 9(6): 419-420
75. Deberardinis, R.J., Sayed, N., Ditsworth, D. and Thompson, C.B. Brick by brick: metabolism and tumor cell growth. Curr Opin Genet Dev 2008, 18(1): 54-61. (Pubitemid 351694453)
76. Forte, L.R. Guanylin regulatory peptides: structures, biological activities mediated by cyclic GMP and pathobiology. Regul Pept 1999, 81(1-3): 25-39.
77. Lin, J.E., Li, P., Pitari, G.M., Schulz, S. and Waldman, S.A. Guanylyl cyclase C in colorectal cancer: susceptibility gene and potential therapeutic target. Future Oncol 2009, 5(4): 509-522
78. Pitari, G.M., Baksh, R.I., Harris, D.M., Li, P., Kazerounian, S. and Waldman, S.A. Interruption of homologous desensitization in cyclic guanosine 3′,5′-monophosphate signaling restores colon cancer cytostasis by bacterial enterotoxins. Cancer Res 2005, 65(23): 11129-11135 (Pubitemid 41713384)