Activation of NF-κB is required for mediating proliferative and antiapoptotic effects of progastrin on proximal colonic crypts of mice, in vivo

Oncogene

Volumn 27, Issue 42, 2008, Pages 5599-5611

  Umar, S ^a   Sarkar, S ^a   Cowey, S ^a   Singh, P ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

Annexin II; ERKs; Fabp PG mice; NEMO; NF B; Progastrin

Indexed keywords

FATTY ACID BINDING PROTEIN; I KAPPA B KINASE ALPHA; I KAPPA B KINASE BETA; I KAPPA B KINASE GAMMA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOCORTIN 2; PROGASTRIN; SYNAPTOTAGMIN I; DNA; GASTRIN; I KAPPA B; MITOGEN ACTIVATED PROTEIN KINASE; NF KAPPAB INHIBITOR ALPHA; NF-KAPPAB INHIBITOR ALPHA; PROTEIN PRECURSOR; TRANSCRIPTION FACTOR RELA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BASOLATERAL MEMBRANE; BINDING AFFINITY; CELL PROLIFERATION; COLON CARCINOGENESIS; CONTROLLED STUDY; CRYPT CELL; DISEASE ASSOCIATION; DOWN REGULATION; ENZYME ACTIVATION; ENZYME DEGRADATION; ENZYME PHOSPHORYLATION; GENE ACTIVATION; HUMAN; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN BLOOD LEVEL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RECEPTOR BINDING; WILD TYPE; ANIMAL; COLON; COLON TUMOR; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY;

MUS;

ANIMALS; ANNEXIN A2; APOPTOSIS; CELL PROLIFERATION; COLON; COLONIC NEOPLASMS; DNA; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FATTY ACID-BINDING PROTEINS; GASTRINS; I-KAPPA B PROTEINS; MICE; NF-KAPPA B; PHOSPHORYLATION; PROTEIN PRECURSORS; TRANSCRIPTION FACTOR RELA;

EID: 52149104026     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2008.169     Document Type: Article

References (44)

1. Ahmed S, Murphy RF, Lovas S. (2005). Importance of N- and C-terminal regions of gastrin-Gly for preferential binding to high and low affinity gastrin-Gly receptors. Peptides 26: 1207-1212.
2. Aly A, Shulkes A, Baldwin GS. (2001). Short term infusion of glycine-extended gastrin(17) stimulates both proliferation and formation of aberrant crypt foci in rat colonic mucosa. Int J Cancer 94: 307-313.
3. Baldwin GS, Hollande F, Yang Z, Karelina Y, Paterson A, Strang R et al. (2001). Biologically active recombinant human progastrin (6-80) contains a tightly bound calcium ion. J Biol Chem 276: 7791-7796.
4. Chicone L, Narayan S, Townsend Jr CM, Singh P. (1989). The presence of a 33-40KDa gastrin binding protein on human and mouse colon cancer. Biochem Biophys Res Commun 164: 512-519.
5. Chung CY, Erickson HP. (1994). Cell surface annexin II is a high affinity receptor for the alternatively spliced segment of tenascin-C. J Cell Biol 126: 539-548.
6. Cobb S, Wood T, Ceci J, Varro A, Velasco M, Singh P. (2004). Intestinal expression of prograstin significantly increases colon carcinogenesis in transgenic mice in response to AOM. Cancer 100: 1311-1323.
7. Dasgupta S, Jana M, Zhou Y, Fung YK, Ghosh S, Pahan K. (2004). Antineuroinflammatory effect of NF-kappaB essential modifier-binding domain peptides in the adoptive transfer model of experimental allergic encephalomyelitis. J Immunol 173: 1344-1354.
8. Dockray GJ, Varro A, Dimaline R. (1996). Gastric endocrine cells: gene expression, processing, and targeting of active products. Physiol Rev 76: 767-798.
9. Ferrand A, Bertrand C, Portolan G, Cui G, Carlson J, Pradayrol L. (2005). Signaling pathways associated with colonic mucosa hyperproliferation in mice overexpressing gastrin precursors. Cancer Res 65: 2770-2777.
10. Fric P, Sovova V, Sloncova E, Lojda Z, Jirasek A, Cermak J. (2000). Different expression of some molecular markers in sporadic cancer of the left and right colon. Eur J Cancer Prev 9: 265-268.
11. Glebov OK, Rodriguez LM, Nakahara K, Jenkins J, Cliatt J, Humbyrd CJ. (2003). Distinguishing right from left colon by the pattern of gene expression. Cancer Epidemiol Biomarkers Prev 12: 755-762.
12. Hajjar KA, Jacovina AT, Chacko J. (1994). An endothelial cell receptor for plasminogen/tissue plasminogen activator. I. Identity with annexin II. J Biol chem 269: 21191-21197.
13. Hayden MS, Ghosh S. (2004). Signaling to NF-kappa B. Genes Dev 18: 2195-2224.
14. Hong MY, Chapkin RS, Wild CP, Morris JS, Wang N, Carroll RJ et al. (1999). Relationship between DNA adduct levels, repair enzyme, and apoptosis as a function of DNA methylation by azoxymethane. Cell Growth Differ 10: 749-758.
15. Iacopetta B. (2002). Are there two sides to colorectal cancer? Int J Cancer 101: 403-408.
16. Johnson LR, McCormack SA. (1994). Physiology of the Gastrointestinal Tract, 3rd edn. Raven Press: New York.
17. Lifshitz S, Lamprecht SA, Benharroch D, Prinsloo I, Polak-Charcon S, Schwartz B. (2001). Apoptosis (programmed cell death) in colonic cells: from normal to transformed stage. Cancer Lett 163: 229-238.
18. Liu LU, Holt PR, Krivosheyev V, Moss SF. (1999). Human right and left colon differ in epithelial cell apoptosis and in expression of Bak, a pro-apoptotic Bcl-2 homologue. Gut 45: 45-50.
19. Marshman E, Ottewell PD, Potten CS, Watson AJ. (2001). Caspase activation during spontaneous and radiation-induced apoptosis in the murine intestine. J Pathol 195: 285-292.
20. May MJ, D'Acquisto F, Madge LA, Glöckner J, Pober JS, Ghosh S. (2000). Selective inhibition of NF-kappaB activation by a peptide that blocks the interaction of NEMO with the IkappaB kinase complex. Science 289: 1550-1554.
21. Mills SJ, Mathers JC, Chapman PD, Burn J, Gunn A. (2001). Colonic crypt cell proliferation state assessed by whole crypt microdissection in sporadic neoplasia and familial adenomatous polyposis. Gut 48: 41-46.
22. Müerköster S, Isberner A, Arlt A, Witt M, Reimann B, Blaszczuk E et al. (2005). Gastrin suppresses growth of CCK2 receptor expressing colon cancer cells by inducing apoptosis in vitro and in vivo. Gastroenterology 129: 952-968.
23. Ortiz-Zapater E, Peiró S, Roda O, Corominas JM, Aguilar S, Ampurdanés C et al. (2007). Tissue plasminogen activator induces pancreatic cancer cell proliferation by a non-catalytic mechanism that requires extracellular signal-regulated kinase 1/2 activation through epidermal growth factor receptor and annexin A2. Am J Pathol 170: 1573-1584.
24. Ottewell PD, Varro A, Dockray GJ, Kirton CM, Watson AJ, Wang TC et al. (2005). COOH-termin al 26-amino acid residues of progastrin are sufficient for stimulation of mitosis in murine colonic epithelium in vivo. Am J Phsyiol Gastrointest Liver Physiol 288: G541-G549.
25. Ottewell PD, Watson AJ, Wang TC, Varro A, Dockray GJ, Pritchard DM. (2003). Progastrin stimulates murine colonic epithelial mitosis after DNA damage. Gastroenterology 124: 1348-1357.
26. Rengifo-Cam W, Singh P. (2004). Role of progastrins and gastrins and their receptors in GI and pancreatic cancers: targets for treatment. Curr Pharm Des 10: 2345-2358.
27. Rengifo-Cam W, Umar S, Sarkar S, Singh P. (2007). Anti-apoptotic effects of progastrin on pancreatic cancer cells are mediated by sustained activation of nuclear factor κB. Cancer Res 67: 7266-7274.
28. Sarkar S, Umar S, Singh G, Singh P. (2007). Progastrin (PG) peptide co-localizes with annexin II (ANX-II), in situ, in human colon cancer cells (HCT-116), expressing autocrine PG, and in intestinal epithelial cells (IEC-18) in response to PG stimulation. Gastroenterology 132: A540-A541.
29. Sato M, Ahnen DJ. (1992). Regional variability of colonocyte growth and differentiation in the rat. Anat Rec 233: 409-414.
30. Seva C, Dickinson CJ, Yamada T. (1994). Growth-promoting effects of glycine-extended progastrin. Science 265: 410-412.
31. Singh P. (2007). Role of annexin-II in GI cancers: interaction with gastrins/progastrins. Cancer Lett 252: 19-35.
32. Singh P, Lu X, Cobb S, Miller BT, Tarasova N, Varro A et al. (2003). Progastrin1-80 stimulates growth of intestinal epithelial cells in vitro via high-affinity binding sites. Am J Physiol Gastrointest Liver Physiol 284: G328-G339.
33. Singh P, Velasco M, Given R, Varro A, Wang TC. (2000A). Progastrin expression predisposes mice to colon carcinomas and adenomas in response to a chemical carcinogen. Gastroenterology 119: 162-171.
34. Singh P, Velasco M, Given R, Wargovich M, Varro A, Wang TC. (2000B). Mice overexpressing progastrin are predisposed for developing aberrant colonic crypt foci in response to AOM. Am J Physiol Gastrointest Liver Physiol 278: G390-G399.
35. Singh P, Wu H, Clark C, Owlia A. (2007). Annexin II binds progastrin and gastrin-like peptides, and mediates growth factor effects of autocrine and exogenous gastrins on colon cancer and intestinal epithelial cells. Oncogene 26: 425-440.
36. Song DH, Rana B, Wolfe JR, Crimmins G, Choi C, Albanese C. (2003). Gastrin-ind uced gastric adenocarcinoma growth is mediated through cyclin D1. Am J Physiol Gastrointest Liver Physiol 285: G217-G222.
37. Umar S, Morris AP, Kourouma F, Sellin JH. (2003). Dietary pectin and calcium inhibit colonic proliferation in vivo by differing mechanisms. Cell Prolif 36: 361-375.
38. Umar S, Sellin JH, Morris AP. (2000). Increased nuclear translocation of catalytically active PKC-zeta during mouse colonocyte hyperproliferation. Am J Physiol Gastrointest Liver Physiol 279: G223-G237.
39. Umar S, Wang Y, Morris AP, Sellin JH. (2007). Dual alterations in casein kinase I-epsilon and GSK-3beta modulate beta-catenin stability in hyperproliferating colonic epithelia. Am J Physiol Gastrointest Liver Physiol 292: G599-G5607.
40. Wang TC, Koh TJ, Varro A, Cahill RJ, Dangler CA, Fox JG et al. (1996). Processing and proliferative effects of human progastrin in transgenic mice. J Clin Invest 98: 1918-1929.
41. Wang Y, Xiang GS, Kourouma F, Umar S. (2006). Citrobacter rodentium-induced NF-kappa B activation in hyperproliferating colonic epithelia: role of p65 (Ser(536)) phosphorylation. Br J Pharmacol 148: 814-824.
42. Watanabe T, Kobunai T, Toda E, Yamamoto Y, Kanazawa T, Kazama Y. (2006). Distal colorectal cancers with microsatellite instability (MSI) display distinct gene expression profiles that are different from proximal MSI cancers. Cancer Res 66: 9804-9808.
43. Wu H, Owlia A, Singh P. (2003). Precursor peptide progastrin(1-80) reduces apoptosis of intestinal epithelial cells and upregulates cytochrome c oxidase Vb levels and synthesis of ATP. Am J Physiol Gastrointest Liver Physiol 285: G1097-G1110.
44. Zizzo MG, Mule F, Serio R. (2006). Inhibitory responses to exogenous adenosine in murine proximal and distal colon. Br J Pharmacol 148: 956-963.