Interruption of homologous desensitization in cyclic guanosine 3′,5′-monophosphate signaling restores colon cancer cytostasis by bacterial enterotoxins

Cancer Research

Volumn 65, Issue 23, 2005, Pages 11129-11135

  Mario Pitari, Giovanni ^a,b   Baksh, Ronnie I ^a   Harris, David M ^a   Li, Peng ^a   Kazerounian, Shiva ^a   Waldman, Scott A ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL TOXIN; CALCIUM ION; CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; CYCLIC NUCLEOTIDE; ENTEROTOXIN; ION CHANNEL; PHOSPHODIESTERASE V;

ALLOSTERISM; ARTICLE; CALCIUM TRANSPORT; CANCER CELL; CELL MEMBRANE; CELL NUCLEUS; COLON CANCER; COLORECTAL CANCER; CONTROLLED STUDY; CYTOSTASIS; DESENSITIZATION; HUMAN; HUMAN CELL; ION CONDUCTANCE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TACHYPHYLAXIS; THERMOSTABILITY;

3',5'-CYCLIC-GMP PHOSPHODIESTERASE; BACTERIAL TOXINS; CALCIUM; CELL LINE, TUMOR; COLONIC NEOPLASMS; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASES; ENTEROTOXINS; GUANYLATE CYCLASE; HUMANS; PHOSPHORIC DIESTER HYDROLASES; RECEPTORS, PEPTIDE; SIGNAL TRANSDUCTION;

EID: 28244432560     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-05-2381     Document Type: Article

References (50)

1. Jemal A, Tiwari RC, Murray T, et al. Cancer statistics, 2004. CA Cancer J Clin 2004;54:8-29.
2. Descriptive Epidemiology Group (2004) GLOBOCAN 2002 (IARC, Lyon).
3. Adlard JW, Richman SD, Seymour MT, Quirke P. Prediction of the response of colorectal cancer to systemic therapy. Lancet Oncol 2002;3:75-82.
4. Komarova NL, Lengauer C, Vogelstein B, Nowak MA. Dynamics of genetic instability in sporadic and familial colorectal cancer. Cancer Biol Ther 2002;1:685-92.
5. Simon SM, Schindler M. Cell biological mechanisms of multidrug resistance in tumors. Proc Natl Acad Sci U S A 1994;91:3497-504.
6. Wang Z, Shen D, Parsons DW, et al. Mutational analysis of the tyrosine phosphatome in colorectal cancers. Science 2004;304:1164-6.
7. Gottesman MM, Fojo T, Bates SE. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer 2002;2:48-58.
8. Giannella RA. Escherichia coli heat-stable enterotoxins, guanylins, and their receptors: what are they and what do they do? J Lab Clin Med 1995;125:173-81.
9. Schulz S, Green CK, Yuen PS, Garbers DL. Guanylyl cyclase is a heat-stable enterotoxin receptor. Cell 1990; 63:941-8.
10. Lucas KA, Pitari GM, Kazerounian S, et al. Guanylyl cyclases and signaling by cyclic GMP. Pharmacol Rev 2000;52:375-414.
11. 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;90:10464-8.
12. Forte LR. Guanylin regulatory peptides: structures, biological activities mediated by cyclic GMP and pathobiology. Regul Pept 1999;81:25-39.
13. Pitari GM, Zingman LV, Hodgson DM, et al. Bacterial enterotoxins are associated with resistance to colon cancer. Proc Natl Acad Sci U S A 2003;100:2695-9.
14. Shailubhai K, Yu HH, 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;60:5151-7.
15. Pitari GM, Di Guglielmo MD, Park J, Schulz S, Waldman SA. Guanylyl cyclase C agonists regulate progression through the cell cycle of human colon carcinoma cells. Proc Natl Acad Sci U S A 2001;98: 7846-51.
16. 111In-labeled ST-peptide analog for specific-targeting of human colon cancers. Nucl Med Biol 2001;28:903-9.
17. Wolfe HR, Mendizabal M, Lleong E, et al. In vivo imaging of human colon cancer xenografts in immunodeficient mice using a guanylyl cyclase C-specific ligand. J Nucl Med 2002;43:392-9.
18. Birbe R, Palazzo JP, Walters R, et al. Guanylyl cyclase C is a marker of intestinal metaplasia, dysplasia, and adenocarcinoma of the gastrointestinal tract. Hum Pathol 2005;36:170-9.
19. Carrithers SL, Parkinson SJ, Goldstein S, et al. Escherichia coli heat-stable toxin receptors in human colonic tumors. Gastroenterology 1994;107:1653-61.
20. Carrithers SL, Barber MT, 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;93:14327-32.
21. Bakre MM, Visweswariah SS. Dual regulation of heat-stable enterotoxin-mediated cGMP accumulation in T84 cells by receptor desensitization and increased phosphodiesterase activity. FEBS Lett 1997;408:345-9.
22. Singh R. Interaction of guanylyl cyclase C with SH3 domain of Src tyrosine kinase. Yet another mechanism for desensitization. J Biol Chem 2003;278:24342-9.
23. 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;270:3848-57.
24. Beavo JA. Cyclic nucleotide phosphodiesterases: functional implications of multiple isoforms. Physiol Rev 1995;75:725-48.
25. Bakre MM, Sopory S, Visweswariah SS. Expression and regulation of the cGMP-binding, cGMP-specific phosphodiesterase (PDE5) in human colonic epithelial cells: role in the induction of cellular refractoriness to the heat-stable enterotoxin peptide. J Cell Biochem 2000;77:159-67.
26. Corbin JD, Turko IV, Beasley A, Francis SH. Phosphorylation of phosphodiesterase-5 by cyclic nucleotide-dependent protein kinase alters its catalytic and allosteric cGMP-binding activities. Eur J Biochem 2000;267:2760-7.
27. Rybalkin SD, Rybalkina IG, Shimizu-Albergine M, Tang XB, Beavo JA. PDE5 is converted to an activated state upon cGMP binding to the GAF A domain. EMBO J 2003;22:469-78.
28. Smolenski A, Burkhardt AM, Eigenthaler M, et al. Functional analysis of cGMP-dependent protein kinases I and II as mediators of NO/cGMP effects. Naunyn Schmiedebergs Arch Pharmacol 1998;358:134-9.
29. Thomas MK, Francis SH, Corbin JD. Characterization of a purified bovine lung cGMP-binding cGMP phosphodiesterase. J Biol Chem 1990;265:14964-70.
30. Urbanski R, Carrithers SL, Waldman SA. Internalization of E. coli ST mediated by guanylyl cyclase C in T84 human colon carcinoma cells. Biochim Biophys Acta 1995;1245:29-36.
31. Qiu W, Lee B, Lancaster M, et al. Cyclic nucleotide-gated cation channels mediate sodium and calcium influx in rat colon. Am J Physiol 2000;278:C336-43.
32. Meyerhardt JA, Mayer RJ, Systemic therapy for colorectal cancer. N Engl J Med 2005;352:476-87.
33. Salonga D, Danenberg KD, Johnson M, et al. Colorectal tumors responding to 5-fluorouracil have low gene expression levels of dihydropyrimidine dehydrogenase, thymidylate synthase, and thymidine phosphorylase. Clin Cancer Res 2000;6:1322-7.
34. Leichman CG, Lenz HJ, Leichman L, et al. Quantitation of intratumoral thymidylate synthase expression predicts for disseminated colorectal cancer response and resistance to protracted-infusion fluorouracil and weekly leucovorin. J Clin Oncol 1997;15:3223-9.
35. Dean M, Rzhetsky A, Allikmets R. The human ATP-binding cassette (ABC) transporter superfamily. Genome Res 2001;11:1156-66.
36. Cohen MB, Hawkins JA, Witte DP. Guanylin mRNA expression in human intestine and colorectal adenocarcinoma. Lab Invest 1998;78:101-8.
37. Notterman DA, Alon U, Sierk AJ, Levine AJ. Transcriptional gene expression profiles of colorectal adenoma, adenocarcinoma, and normal tissue examined by oligonucleotide arrays. Cancer Res 2001;61:3124-30.
38. Birkenkamp-Demtroder K, Lotte Christensen L, Harder Olesen S, et al. Gene expression in colorectal cancer. Cancer Res 2002;62:4352-63.
39. Rybalkin SD, Rybalkina IG, Feil R, Hofmann F, Beavo JA. Regulation of cGMP-specific phosphodiesterase (PDE5) phosphorylation in smooth muscle cells. J Biol Chem 2002;277:3310-7.
40. Takimoto E, Champion HC, Li M, et al. Chronic inhibition of cyclic GMP phosphodiesterase 5A prevents and reverses cardiac hypertrophy. Nat Med 2005;11: 214-22.
41. Ni XP, Safai M, Rishi R, Baylis C, Humphreys MH. Increased activity of cGMP-specific phosphodiesterase (PDE5) contributes to resistance to atrial natriuretic peptide natriuresis in the pregnant rat. J Am Soc Nephrol 2004;15:1254-60.
42. Mullershausen F, Friebe A, Feil R, et al. Direct activation of PDE5 by cGMP: long-term effects within NO/cGMP signaling. J Cell Biol 2003;160:719-27.
43. Mullershausen F, Russwurm M, Koesling D, Friebe A. In vivo reconstitution of the negative feedback in nitric oxide/cGMP signaling: role of phosphodiesterase type 5 phosphorylation. Mol Biol Cell 2004;15:4023-30.
44. Lincoln TM, Corbin JD. Adenosine 3′:5′-cyclic monophosphate- and guanosine 3′:5′-cyclic monophosphate-dependent protein kinases: possible homologous proteins. Proc Natl Acad Sci U S A 1977;74:3239-43.
45. Kazerounian S, Pitari GM, Shah FJ, et al. Proliferative signaling by store-operated calcium channels opposes colon cancer cell cytostasis induced by bacterial enterotoxins. J Pharmacol Exp Ther 2005;314:1013-22.
46. Steinbrecher KA, Wowk SA, Rudolph JA, Witte DP, Cohen MB. Targeted inactivation of the mouse guanylin gene results in altered dynamics of colonic epithelial proliferation. Am J Pathol 2002;161:2169-78.
47. Goldstein I, Lue TF, Padma-Nathan H, et al. Oral sildenafil in the treatment of erectile dysfunction. Sildenafil Study Group. N Engl J Med 1998;338:1397-404.
48. Sastry BK, Narasimhan C, Reddy NK, Raju BS. Clinical efficacy of sildenafil in primary pulmonary hypertension: a randomized, placebo-controlled, double-blind, crossover study. J Am Coll Cardiol 2004;43: 1149-53.
49. Harrison SA, Reifsnyder DH, Gallis B, Cadd GG, Beavo JA. Isolation and characterization of bovine cardiac muscle cGMP-inhibited phosphodiesterase: a receptor for new cardiotonic drugs. Mol Pharmacol 1986;29:506-14.
50. Butt E, Eigenthaler M, Genieser HG. (Rp)-8-pCPT-cGMPS, a novel cGMP-dependent protein kinase inhibitor. Eur J Pharmacol 1994;269:265-8.