P53 gene mutation increases progastrin dependent colonic proliferation and colon cancer formation in mice

Cancer Investigation

Volumn 30, Issue 4, 2012, Pages 275-286

  Ramanathan, Vigneshwaran ^a   Jin, Guangchun ^a   Westphalen, Christoph Benedikt ^a   Whelan, Ashley ^a   Dubeykovskiy, Alexander ^a   Takaishi, Shigeo ^a   Wang, Timothy C ^a  

^a NewYork Presbyterian Hospital   (United States)

Author keywords

Azoxymethane; Colon cancer; Lgr5; P53; Progastrin

Indexed keywords

AZOXYMETHANE; BROXURIDINE; PROGASTRIN; PROTEIN P53;

ABERRANT CRYPT FOCUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL COUNT; CELL PROLIFERATION; COLON CARCINOGENESIS; CONTROLLED STUDY; GENE MUTATION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; STEM CELL; TRANSGENIC MOUSE;

ABERRANT CRYPT FOCI; ANIMALS; AZOXYMETHANE; CARCINOGENS; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; COLONIC NEOPLASMS; DISEASE MODELS, ANIMAL; FEMALE; GASTRINS; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUTATION; PROTEIN PRECURSORS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84860165742     PISSN: 07357907     EISSN: 15324192     Source Type: Journal    
DOI: 10.3109/07357907.2012.657814     Document Type: Article

References (50)

1. American Cancer Society. Cancer Facts & Figures 2010. Atlanta, GA: ACS, 2010.
2. Jemal A, Murray T, Samuels A, Ghafoor A, Ward E, Tun MJ. Cancer statistics, 2003. CA Cancer J Clin 2003;53:5-26.
3. Fearon ER, Hamilton SR, Vogelstein B. Clonal analysis of human colorectal tumors. Science 1987;238:193-197. (Pubitemid 17139720)
4. Groden J, Tliveris A, Samowitz W, Carlson M, Gelbert L, Albertsen H, Joslyn G, Stevens J, Spirio L, Robertson M, et al. Identifca-tion and characterization of the familial adenomatous polyposis coli gene. Cell 1991;66:589-600.
5. Fearon ER, Cho KR, Nigro JM, Kern SE, Simons JW, Ruppert JM, Hamilton SR, Preisinger AC, Tomas G, Kinzler KW, et al. Iden-tification of a chromosome 18q gene that is altered in colorectal cancers. Science 1990;247:49-56.
6. Vousden KH, Lane DP. p53 in health and disease. Nat Rev Mol Cell Biol 2007;8:275-283. (Pubitemid 46474662)
7. Bose I, Ghosh B. The p53-MDM2 network: from oscillations to apoptosis. J Biosci 2007;32:991-997. (Pubitemid 47435530)
8. Olive KP, Tuveson DA, Ruhe ZC, Yin B, Willis NA, Bronson RT, Crowley D, Jacks T. Mutant p53 gain of function in two mouse models of Li-Fraumeni syndrome. Cell 2004;119:847-860. (Pubitemid 40017690)
9. Jackson EL, Olive KP, Tuveson DA, Bronson R, Crowley D, Brown M, Jacks T. The diferential effects of mutant p53 al-leles on advanced murine lung cancer. Cancer Res 2005;65: 10280-10288. (Pubitemid 41743720)
10. Hu Y, Le Leu RK, Young GP. Absence of acute apoptotic response to genotoxic carcinogens in p53-defcient mice is associated with increased susceptibility to azoxymethane-induced colon tumours. Int J Cancer 2005;115:561-567. (Pubitemid 40656713)
11. Singh P, Velasco M, Given R, Varro A, Wang TC. Progastrin expression predisposes mice to colon carcinomas and adenomas in response to a chemical carcinogen. Gastroenterology 2000;119:162-171. (Pubitemid 30452589)
12. Lipkin M, Newmark H. Application of intermediate biomarkers and the prevention of cancer of the large intestine. Prog Clin Biol Res 1988;279:135-150.
13. Dockray GJ. Gastrin-releasing peptide: an identity crisis at 30? Lancet 2001;358:778-779. (Pubitemid 32868723)
14. Wang TC, Koh TJ, Varro A, Cahill RJ, Dangler CA, Fox JG, Dock-ray GJ. Processing and proliferative effects of human progastrin in transgenic mice. J Clin Invest 1996;98:1918-1929. (Pubitemid 26359210)
15. Singh P, Velasco M, Given R, Wargovich M, Varro A, Wang TC. Mice overexpressing progastrin are predisposed for developing aberrant colonic crypt foci in response to AOM. Am J Physiol Gas-trointest Liver Physiol 2000;278:G390-G399. (Pubitemid 30152484)
16. ChenD,Zhao CM,Dockray GJ, Varro A, Van HoekA,Sinclair NF, Wang TC, Koh TJ. Glycine-extended gastrin synergizes with gas-trin 17 to stimulate acid secretion in gastrin-defcient mice. Gas-troenterology 2000;119:756-765.
17. Koh TJ, Field JK, Varro A, Liloglou T, Fielding P, Cui G, Houghton J, Dockray GJ, Wang TC. Glycine-extended gastrin promotes the growth of lung cancer. Cancer Res 2004;64:196-201. (Pubitemid 38114098)
18. Kochman ML, DelValle J, Dickinson CJ, Boland CR. Post-translational processing of gastrin in neoplastic human colonic tissues. Biochem Biophys Res Commun 1992;189:1165-1169. (Pubitemid 23032497)
19. Koh TJ, Dockray GJ, Varro A, Cahill RJ, Dangler CA, Fox JG, Wang TC. Overexpression of glycine-extended gastrin in trans-genic mice results in increased colonic proliferation. J Clin Invest 1999;103:1119-1126. (Pubitemid 29207245)
20. Baldwin GS, Hollande F, Yang Z, Karelina Y, Paterson A, Strang R, Fourmy D, Neumann G, Shulkes A. Biologically active recom-binant human progastrin(6-80) contains a tightly bound calcium ion. J Biol Chem 2001;276:7791-7796.
21. Brown D, Yallampalli U, Owlia A, Singh P. pp60c-Src Kinase mediates growth effects of the full-length precursor progastrin1-80 peptide on rat intestinal epithelial cells, in vitro. Endocrinology 2003;144:201-211. (Pubitemid 36076109)
22. Hollande F, Lee DJ, Choquet A, Roche S, Baldwin GS. Adherens junctions and tight junctions are regulated via diferent pathways by progastrin in epithelial cells. J Cell Sci 2003;116:1187-1197. (Pubitemid 36410658)
23. Singh P, Lu X, Cobb S, Miller BT, Tarasova N, Varro A, Owlia A. Progastrin1-80 stimulates growth of intestinal epithelial cells in vitro via high-afnity binding sites. Am J Physiol Gastrointest Liver Physiol 2003;284:G328-G339. (Pubitemid 36120139)
24. Pannequin J, Delaunay N, Buchert M, Surrel F, Bourgaux JF, Ryan J, Boireau S, Coelho J, Pelegrin A, Singh P, Shulkes A, Yim M, Baldwin GS, Pignodel C, Lambeau G, Jay P, Joubert D, Hollande F. Beta-catenin/Tcf-4 inhibition afer progastrin targeting reduces growth and drives diferentiation of intestinal tumors. Gastroen-terology 2007;133:1554-1568. (Pubitemid 350047462)
25. Ottewell PD, Varro A, Dockray GJ, Kirton CM, Watson AJ, Wang TC, Dimaline R, Pritchard DM. COOH-terminal 26-amino acid residues of progastrin are sufcient for stimulation of mitosis in murine colonic epithelium in vivo. Am J Physiol Gastrointest Liver Physiol 2005;288:G541-G549. (Pubitemid 40261754)
26. Seva C, Dickinson CJ, Yamada T. Growth-promoting effects of glycine-extended progastrin. Science 1994;265:410-412. (Pubitemid 24259977)
27. Siddheshwar RK, Gray JC, Kelly SB. Plasma levels of progastrin but not amidated gastrin or glycine extended gastrin are elevated in patients with colorectal carcinoma. Gut 2001;48:47-52. (Pubitemid 32042641)
28. Konturek PC, Bielanski W, Konturek SJ, Hartwich A, Pierzchalski P, Gonciarz M, Marlicz K, Starzynska T, Zuchowicz M, Darasz Z, Gotze JP, Rehfeld J, F.Hahn EG. Progastrin and cyclooxygenase-2 in colorectal cancer. Dig Dis Sci 2002;47:1984-1991. (Pubitemid 35024809)
29. Chang WW, Leblond CP. Renewal of the epithelium in the descending colon of the mouse. I. Presence of three cell populations: vacuolated-columnar, mucous and argentafn. Am J Anat 1971;131:73-99.
30. Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozi-jnsen M, Haegebarth A, Korving J, Begthel H, Peters PJ, Clevers H. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007;449:1003-1007. (Pubitemid 350014593)
31. McLellan EA, Bird RP. Specifcity study to evaluate induction of aberrant crypts in murine colons. Cancer Res 1988;48:6183-6186. (Pubitemid 18266820)
32. BoseDasgupta S, Ganguly A, Roy A, Mukherjee T, Majumder HK. A novel ATP-binding cassette transporter, ABCG6 is involved in chemoresistance of Leishmania. Mol Biochem Parasitol 2008;158:176-188. (Pubitemid 351248781)
33. Piard F, Martin L, Chapusot C, Ponnelle T, Faivre J. Genetic pathways in colorectal cancer: interest for the pathologist. Ann Pathol 2002;22:277-288. (Pubitemid 35238465)
34. Giannakis M, Stappenbeck TS, Mills JC, Leip DG, Lovett M, Clifon SW, Ippolito JE, Glasscock JI, Arumugam M, Brent MR, Gordon JI. Molecular properties of adult mouse gastric and intestinal epithelial progenitors in their niches. J Biol Chem 2006;281:11292-11300. (Pubitemid 43855554)
35. Gerbe F, van Es JH, Makrini L, Brulin B, Mellitzer G, Robine S, Romagnolo B, Shroyer NF, Bourgaux JF, Pignodel C, Clevers H, Jay P. Distinct ATOH1 and Neurog3 requirements defne tuf cells as a new secretory cell type in the intestinal epithelium. J Cell Biol 2011;192:767-780.
36. Gerbe F, Brulin B, Makrini L, Legraverend C, Jay P. DCAMKL-1 expression identifes Tuf cells rather than stem cells in the adult mouse intestinal epithelium. Gastroenterology 2009;137:2179-2180; author reply 2180-2181.
37. May R, Riehl TE, Hunt C, Sureban SM, Anant S, Houchen CW. Identification of a novel putative gastrointestinal stem cell and adenoma stem cell marker, doublecortin and CaM kinase-like-1, following radiation injury and in adenomatous polyposis coli/multiple intestinal neoplasia mice. Stem Cells 2008;26:630-637.
38. Saqui-Salces M, Keeley TM, Grosse AS, Qiao XT, El-Zaatari M, Gumucio DL, Samuelson LC, Merchant JL. Gastric tuf cells express DCLK1 and are expanded in hyperplasia. Histochem Cell Biol 2011;136:191-204.
39. Goldstein I, Marcel V, Olivier M, Oren M, Rotter V, Hainaut P. Understanding wild-type and mutant p53 activities in human cancer: new landmarks on the way to targeted therapies. Cancer Gene Ter 2011;18:2-11.
40. Symonds H, Krall L, Remington L, Saenz-Robles M, Lowe S, Jacks T, Van Dyke T. p53-dependent apoptosis suppresses tumor growth and progression in vivo. Cell 1994;78:703-711.
41. Wargovich MJ, Chen CD, Harris C, Yang E, Velasco M. Inhibition of aberrant crypt growth by non-steroidal anti-infammatory agents and diferentiation agents in the rat colon. Int J Cancer 1995;60:515-519.
42. McLellan EA, Bird RP. Aberrant crypts: potential preneoplastic lesions in the murine colon. Cancer Res 1988;48:6187-6192. (Pubitemid 18266821)
43. Corpet DE, Tache S. Most effective colon cancer chemopreventive agents in rats: a systematic review of aberrant crypt foci and tumor data, ranked by potency. Nutr Cancer 2002;43:1-21. (Pubitemid 35387251)
44. Karlin DA, McBath M, Jones RD, Elwyn KE, Romsdahl MM. Hy-pergastrinemia and colorectal carcinogenesis in the rat. Cancer Lett 1985;29:73-78.
45. Takayama T, Katsuki S, Takahashi Y, Ohi M, Nojiri S, Sakamaki S, Kato J, Kogawa K, Miyake H, Niitsu Y. Aberrant crypt foci of the colon as precursors of adenoma and cancer. N Engl J Med 1998;339:1277-1284. (Pubitemid 28496193)
46. Hu Y, Martin J, Le Leu R, Young GP. The colonic response to geno-toxic carcinogens in the rat: regulation by dietary fbre. Carcino-genesis 2002;23:1131-1137. (Pubitemid 34814770)
47. Gryfe R, Swallow C, Bapat B, Redston M, Gallinger S, Couture J. Molecular biology of colorectal cancer. Curr Probl Cancer 1997;21:233-300.
48. Levine AJ, Hu W, Feng Z. The P53 pathway: what questions remain to be explored? Cell Death Difer 2006;13:1027-1036.
49. Pan H, Griep AE. Temporally distinct patterns of p53-dependent and p53-independent apoptosis during mouse lens development. Genes Dev 1995;9:2157-2169.
50. Nemeth J, Taylor B, Pauwels S, Varro A, Dockray GJ. Identification of progastrin derived peptides in colorectal carcinoma extracts. Gut 1993;34:90-95. (Pubitemid 23015957)