A common role for various human truncated adenomatous polyposis coli isoforms in the control of beta-catenin activity and cell proliferation

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Chandra, Shree Harsha Vijaya ^a   Wacker, Ingrid ^a   Appelt, Uwe Kurt ^a   Behrens, Jürgen ^a   Schneikert, Jean ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

APC PROTEIN; BETA CATENIN; ISOPROTEIN; PROTEASOME; SHORT HAIRPIN RNA;

ARTICLE; CANCER CELL; CANCER INHIBITION; CELL EXPANSION; CELL POPULATION; CELL PROLIFERATION; COLON CARCINOGENESIS; COLORECTAL CANCER; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR BIOLOGY; MUTATION CLUSTER REGION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; RNA INTERFERENCE; SIGNAL TRANSDUCTION; UPREGULATION; WILD TYPE; COLORECTAL TUMOR; GENE DELETION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

ADENOMATOUS POLYPOSIS COLI PROTEIN; BETA CATENIN; CELL LINE, TUMOR; CELL PROLIFERATION; COLORECTAL NEOPLASMS; DOWN-REGULATION; HUMANS; PROTEIN ISOFORMS; RNA INTERFERENCE; SEQUENCE DELETION; TRANSCRIPTION, GENETIC;

EID: 84859239880     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034479     Document Type: Article

References (49)

1. Behrens J, von Kries JP, Kuhl M, Bruhn L, Wedlich D, et al. (1996) Functional interaction of beta-catenin with the transcription factor LEF-1. Nature 382: 638-642.
2. MacDonald BT, Tamai K, He X, (2009) Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell 17: 9-26.
3. Molenaar M, van de Wetering M, Oosterwegel M, Peterson-Maduro J, Godsave S, et al. (1996) XTcf-3 transcription factor mediates beta-catenin-induced axis formation in Xenopus embryos. Cell 86: 391-399.
4. Groden J, Thliveris A, Samowitz W, Carlson M, Gelbert L, et al. (1991) Identification and characterization of the familial adenomatous polyposis coli gene. Cell 66: 589-600.
5. Fearnhead NS, Britton MP, Bodmer WF, (2001) The ABC of APC. Hum Mol Genet 10: 721-733.
6. Kinzler KW, Vogelstein B, (1996) Lessons from hereditary colorectal cancer. Cell 87: 159-170.
7. Fodde R, Edelmann W, Yang K, van Leeuwen C, Carlson C, et al. (1994) A targeted chain-termination mutation in the mouse Apc gene results in multiple intestinal tumors. Proc Natl Acad Sci U S A 91: 8969-8973.
8. Oshima M, Oshima H, Kitagawa K, Kobayashi M, Itakura C, et al. (1995) Loss of Apc heterozygosity and abnormal tissue building in nascent intestinal polyps in mice carrying a truncated Apc gene. Proc Natl Acad Sci U S A 92: 4482-4486.
9. Pollard P, Deheragoda M, Segditsas S, Lewis A, Rowan A, et al. (2009) The Apc 1322T mouse develops severe polyposis associated with submaximal nuclear beta-catenin expression. Gastroenterology 136: 2204-2213 e2201-2213.
10. Sansom OJ, Reed KR, Hayes AJ, Ireland H, Brinkmann H, et al. (2004) Loss of Apc in vivo immediately perturbs Wnt signaling, differentiation, and migration. Genes Dev 18: 1385-1390.
11. Shibata H, Toyama K, Shioya H, Ito M, Hirota M, et al. (1997) Rapid colorectal adenoma formation initiated by conditional targeting of the Apc gene. Science 278: 120-123.
12. Schneikert J, Behrens J, (2007) The canonical Wnt signalling pathway and its APC partner in colon cancer development. Gut 56: 417-425.
13. Albuquerque C, Breukel C, van der Luijt R, Fidalgo P, Lage P, et al. (2002) The 'just-right' signaling model: APC somatic mutations are selected based on a specific level of activation of the beta-catenin signaling cascade. Hum Mol Genet 11: 1549-1560.
14. Lewis A, Segditsas S, Deheragoda M, Pollard P, Jeffery R, et al. (2010) Severe polyposis in Apc(1322T) mice is associated with submaximal Wnt signalling and increased expression of the stem cell marker Lgr5. Gut 59: 1680-1686.
15. Schneikert J, Behrens J, (2006) Truncated APC is required for cell proliferation and DNA replication. Int J Cancer 119: 74-79.
16. Kohler EM, Chandra SH, Behrens J, Schneikert J, (2009) Beta-catenin degradation mediated by the CID domain of APC provides a model for the selection of APC mutations in colorectal, desmoid and duodenal tumours. Hum Mol Genet 18: 213-226.
17. Roberts DM, Pronobis MI, Poulton JS, Waldmann JD, Stephenson EM, et al. (2011) Deconstructing the sscatenin destruction complex: mechanistic roles for the tumor suppressor APC in regulating Wnt signaling. Mol Biol Cell.
18. Kawamata T, Tomari Y, (2010) Making RISC. Trends Biochem Sci 35: 368-376.
19. Root DE, Hacohen N, Hahn WC, Lander ES, Sabatini DM, (2006) Genome-scale loss-of-function screening with a lentiviral RNAi library. Nat Methods 3: 715-719.
20. Jho EH, Zhang T, Domon C, Joo CK, Freund JN, et al. (2002) Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol Cell Biol 22: 1172-1183.
21. Lustig B, Jerchow B, Sachs M, Weiler S, Pietsch T, et al. (2002) Negative feedback loop of Wnt signaling through upregulation of conductin/axin2 in colorectal and liver tumors. Mol Cell Biol 22: 1184-1193.
22. Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, et al. (2007) Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449: 1003-1007.
23. Oliver FJ, de la Rubia G, Rolli V, Ruiz-Ruiz MC, de Murcia G, et al. (1998) Importance of poly(ADP-ribose) polymerase and its cleavage in apoptosis. Lesson from an uncleavable mutant. J Biol Chem 273: 33533-33539.
24. Dikovskaya D, Schiffmann D, Newton IP, Oakley A, Kroboth K, et al. (2007) Loss of APC induces polyploidy as a result of a combination of defects in mitosis and apoptosis. J Cell Biol 176: 183-195.
25. Schneikert J, Grohmann A, Behrens J, (2007) Truncated APC regulates the transcriptional activity of beta-catenin in a cell cycle dependent manner. Hum Mol Genet 16: 199-209.
26. Kohler EM, Derungs A, Daum G, Behrens J, Schneikert J, (2008) Functional definition of the mutation cluster region of adenomatous polyposis coli in colorectal tumours. Hum Mol Genet 17: 1978-1987.
27. Krieghoff E, Behrens J, Mayr B, (2006) Nucleo-cytoplasmic distribution of {beta}-catenin is regulated by retention. J Cell Sci 119: 1453-1463.
28. Wang H, Promkan M, Liu G, Chakrabarty S, (2008) Switch of transforming growth factor beta function from tumor suppression to stimulation in adenomatous polyposis coli (APC) knocked-down human colon carcinoma cells. Cancer Lett 272: 253-259.
29. Taurin S, Sandbo N, Qin Y, Browning D, Dulin NO, (2006) Phosphorylation of beta-catenin by cyclic AMP-dependent protein kinase. J Biol Chem 281: 9971-9976.
30. Zhu G, Wang Y, Huang B, Liang J, Ding Y, et al. (2011) A Rac1/PAK1 cascade controls beta-catenin activation in colon cancer cells. Oncogene.
31. Yang J, Zhang W, Evans PM, Chen X, He X, et al. (2006) Adenomatous polyposis coli (APC) differentially regulates beta-catenin phosphorylation and ubiquitination in colon cancer cells. J Biol Chem 281: 17751-17757.
32. Nielsen M, Bik E, Hes FJ, Breuning MH, Vasen HF, et al. (2007) Genotype-phenotype correlations in 19 Dutch cases with APC gene deletions and a literature review. Eur J Hum Genet 15: 1034-1042.
33. Sieber OM, Heinimann K, Gorman P, Lamlum H, Crabtree M, et al. (2002) Analysis of chromosomal instability in human colorectal adenomas with two mutational hits at APC. Proc Natl Acad Sci U S A 99: 16910-16915.
34. Nieuwenhuis MH, Vasen HF, (2007) Correlations between mutation site in APC and phenotype of familial adenomatous polyposis (FAP): a review of the literature. Crit Rev Oncol Hematol 61: 153-161.
35. Hong Y, Cervantes RB, Tichy E, Tischfield JA, Stambrook PJ, (2007) Protecting genomic integrity in somatic cells and embryonic stem cells. Mutat Res 614: 48-55.
36. Cheung AF, Carter AM, Kostova KK, Woodruff JF, Crowley D, et al. (2010) Complete deletion of Apc results in severe polyposis in mice. Oncogene 29: 1857-1864.
37. McCart AE, Vickaryous NK, Silver A, (2008) Apc mice: models, modifiers and mutants. Pathol Res Pract 204: 479-490.
38. Gupta PK, Sahota A, Boyadjiev SA, Bye S, Shao C, et al. (1997) High frequency in vivo loss of heterozygosity is primarily a consequence of mitotic recombination. Cancer Res 57: 1188-1193.
39. Haigis KM, Dove WF, (2003) A Robertsonian translocation suppresses a somatic recombination pathway to loss of heterozygosity. Nat Genet 33: 33-39.
40. Gaspar C, Cardoso J, Franken P, Molenaar L, Morreau H, et al. (2008) Cross-species comparison of human and mouse intestinal polyps reveals conserved mechanisms in adenomatous polyposis coli (APC)-driven tumorigenesis. Am J Pathol 172: 1363-1380.
41. Behlke MA, (2006) Progress towards in vivo use of siRNAs. Mol Ther 13: 644-670.
42. Manjunath N, Dykxhoorn DM, (2010) Advances in synthetic siRNA delivery. Discov Med 9: 418-430.
43. Schwarz DS, Ding H, Kennington L, Moore JT, Schelter J, et al. (2006) Designing siRNA that distinguish between genes that differ by a single nucleotide. PLoS Genet 2: e140.
44. Rowan AJ, Lamlum H, Ilyas M, Wheeler J, Straub J, et al. (2000) APC mutations in sporadic colorectal tumors: A mutational "hotspot" and interdependence of the "two hits". Proc Natl Acad Sci U S A 97: 3352-3357.
45. Brummelkamp TR, Bernards R, Agami R, (2002) A system for stable expression of short interfering RNAs in mammalian cells. Science 296: 550-553.
46. Sirven A, Ravet E, Charneau P, Zennou V, Coulombel L, et al. (2001) Enhanced transgene expression in cord blood CD34(+)-derived hematopoietic cells, including developing T cells and NOD/SCID mouse repopulating cells, following transduction with modified trip lentiviral vectors. Mol Ther 3: 438-448.
47. Sangrar W, Gao Y, Scott M, Truesdell P, Greer PA, (2007) Fer-mediated cortactin phosphorylation is associated with efficient fibroblast migration and is dependent on reactive oxygen species generation during integrin-mediated cell adhesion. Mol Cell Biol 27: 6140-6152.
48. van de Wetering M, Cavallo R, Dooijes D, van Beest M, van Es J, et al. (1997) Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell 88: 789-799.
49. Staal FJ, Noort Mv M, Strous GJ, Clevers HC, (2002) Wnt signals are transmitted through N-terminally dephosphorylated beta-catenin. EMBO Rep 3: 63-68.