CIN by Wnt: Growth pathways, mitotic control and chromosomal instability in cancer

Cell Cycle

Volumn 5, Issue 18, 2006, Pages 2077-2081

  Hadjihannas, Michel V ^a   Behrens, Jürgen ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Adenomatous polyposis coli; Chromosomal instability; Colorectal cancer; Conductin axin2; Mitosis; Spindle checkpoint; Wnt signaling; catenin

Indexed keywords

AXIN; BETA CATENIN; PROTEIN AXIN2; UNCLASSIFIED DRUG;

CELL CYCLE PROGRESSION; CHROMOSOMAL INSTABILITY; COLORECTAL CANCER; GENE MUTATION; GENOMIC INSTABILITY; HUMAN; MITOSIS; PHENOTYPE; REVIEW;

EID: 33749677868     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.5.18.3282     Document Type: Review

References (66)

1. Tanaka K, Mukae N, Dewar H, van Breugel M, James EK, Prescott AR, Antony C, Tanaka TU. Molecular mechanisms of kinetochore capture by spindle microtubules. Nature 2005; 434:987-94.
2. Tanaka TU, Rachidi N, Janke C, Pereira G, Galova M, Schiebel E, Stark MJ, Nasmyth K. Evidence that the Ipl1-Sli15 (Aurora kinase-INCENP) complex promotes chromosome bi-orientation by altering kinetochorespindle pole connections. Cell 2002; 108:317-29.
3. Sumara I, Gimenez-Abian JF, Gerlich D, Hirota T, Kraft C, de la Torre C, Ellenberg J, Peters JM. Roles of polo-like kinase 1 in the assembly of functional mitotic spindles. Curr Biol 2004; 14:1712-22.
4. Ahonen LJ, Kallio MJ, Daum JR, Bolton M, Manke IA, Yaffe MB, Stukenberg PT, Gorbsky GJ. Polo-like kinase 1 creates the tension-sensing 3F3/2 phosphoepitope and modulates the association of spindle-checkpoint proteins at kinetochores. Curr Biol 2005; 15:1078-89.
5. Peters JM. The anaphase-promoting complex: Proteolysis in mitosis and beyond. Mol Cell 2002; 9:931-43.
6. Pinsky BA, Biggins S. The spindle checkpoint: Tension versus attachment. Trends Cell Biol 2005; 15:486-93.
7. Meraldi P, Draviam VM, Sorger PK. Timing and checkpoints in the regulation of mitotic progression. Dev Cell 2004; 7:45-60.
8. Jallepalli PV, Waizenegger IC, Bunz F, Langer S, Speicher MR, Peters JM, Kinzler KW, Vogelstein B, Lengauer C. Securin is required for chromosomal stability in human cells. Cell 2001; 105:445-57.
9. Cahill DP, Lengauer C, Yu J, Riggins GJ, Willson JK, Markowitz SD, Kinzler KW, Vogelstein B. Mutations of mitotic checkpoint genes in human cancers. Nature 1998; 392:300-3.
10. Jallepalli PV, Lengauer C. Chromosome segregation and cancer: Cutting through the mystery. Nat Rev Cancer 2001; 1:109-17.
11. Rajagopalan H, Nowak MA, Vogelstein B, Lengauer C. The significance of unstable chromosomes in colorectal cancer. Nat Rev Cancer 2003; 3:695-701.
12. Rajagopalan H, Jallepalli PV, Rago C, Velculescu VE, Kinzler KW, Vogelstein B, Lengauer C. Inactivation of hCDC4 can cause chromosomal instability. Nature 2004; 428:77-81.
13. Cahill DP, da Costa LT, Carson-Walter EB, Kinzler KW, Vogelstein B, Lengauer C. Characterization of MAD2B and other mitotic spindle checkpoint genes. Genomics 1999; 58:181-7.
14. Kemp Z, Rowan A, Chambers W, Wortham N, Halford S, Sieber O, Mortensen N, von Herbay A, Gunther T, Ilyas M, Tomlinson I. CDC4 mutations occur in a subset of colorectal cancers but are not predicted to cause loss of function and are not associated with chromosomal instability. Cancer Res 2005; 65:11361-6.
15. Imai Y, Shiratori Y, Kato N, Inoue T, Omata M. Mutational inactivation of mitotic checkpoint genes, hsMAD2 and hBUB1, is rare in sporadic digestive tract cancers. Jpn J Cancer Res 1999; 90:837-40.
16. Sieber OM, Heinimann K, Tomlinson IP. Genomic instability-the engine of tumorigenesis? Nat Rev Cancer 2003; 3:701-8.
17. Nowak MA, Komarova NL, Sengupta A, Jallepalli PV, Shih Ie M, Vogelstein B, Lengauer C. The role of chromosomal instability in tumor initiation. Proc Natl Acad Sci USA 2002; 99:16226-31.
18. Lengauer C, Kinzler KW, Vogelstein B. Genetic instability in colorectal cancers. Nature 1997; 386:623-7.
19. Seidensticker MJ, Behrens J. Biochemical interactions in the wnt pathway. Biochim Biophys Acta 2000; 1495:168-82.
20. Lustig B, Behrens J. The Wnt signaling pathway and its role in tumor development. J Cancer Res Clin Oncol 2003; 129:199-221.
21. Behrens J, Jerchow BA, Wurtele M, Grimm J, Asbrand C, Wirtz R, Kuhl M, Wedlich D, Birchmeier W. Functional interaction of an axin homolog, conductin, with beta-catenin, APC, and GSK3beta. Science 1998; 280:596-9.
22. Bhanot P, Brink M, Samos CH, Hsieh JC, Wang Y, Macke JP, Andrew D, Nathans J, Nusse R. A new member of the frizzled family from Drosophila functions as a Wingless receptor. Nature 1996; 382:225-30.
23. He X, Saint-Jeannet JP, Wang Y, Nathans J, Dawid I, Varmus H. A member of the Frizzled protein family mediating axis induction by Wnt-5A. Science 1997; 275:1652-4.
24. Behrens J. The role of the Wnt signalling pathway in colorectal tumorigenesis. Biochem Soc Trans 2005; 33:672-5.
25. Behrens J, von Kries JP, Kuhl M, Bruhn L, Wedlich D, Grosschedl R, Birchmeier W. Functional interaction of beta-catenin with the transcription factor LEF-1. Nature 1996; 382:638-42.
26. Tetsu O, McCormick F. Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 1999; 398:422-6.
27. He TC, Sparks AB, Rago C, Hermeking H, Zawel L, da Costa LT, Morin PJ, Vogelstein B, Kinzler KW. Identification of c-MYC as a target of the APC pathway. Science 1998; 281:1509-12.
28. Bach SP, Renehan AG, Potten CS. Stem cells: The intestinal stem cell as a paradigm. Carcinogenesis 2000; 21:469-76.
29. Morin PJ, Sparks AB, Korinek V, Barker N, Clevers H, Vogelstein B, Kinzler KW. Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 1997; 275:1787-90.
30. Roberts LR, Gores GJ. Hepatocellular carcinoma: Molecular pathways and new therapeutic targets. Semin Liver Dis 2005; 25:212-25.
31. Fox S, Dharmarajan A. WNT signaling in malignant mesothelioma. Front Biosci 2006; 11:2106-12.
32. Oliva E, Sarrio D, Brachtel EF, Sanchez-Estevez C, Soslow RA, Moreno-Bueno G, Palacios J. High frequency of beta-catenin mutations in borderline endometrioid tumours of the ovary. J Pathol 2006; 208:708-13.
33. Sparks AB, Morin PJ, Vogelstein B, Kinzler KW. Mutational analysis of the APC/beta-catenin/Tcf pathway in colorectal cancer. Cancer Res 1998; 58:1130-4.
34. Peltomaki P. Deficient DNA mismatch repair: A common etiologic factor for colon cancer. Hum Mol Genet 2001; 10:735-40.
35. Marra G, Boland CR. Hereditary nonpolyposis colorectal cancer: The syndrome, the genes, and historical perspectives. J Natl Cancer Inst 1995; 87:1114-25.
36. Zumbrunn J, Kinoshita K, Hyman AA, Nathke IS. Binding of the adenomatous polyposis coli protein to microtubules increases microtubule stability and is regulated by GSK3 beta phosphorylation. Curr Biol 2001; 11:44-9.
37. Green RA, Kaplan KB. Chromosome instability in colorectal tumor cells is associated with defects in microtubule plus-end attachments caused by a dominant mutation in APC. J Cell Biol 2003; 163:949-61.
38. Kaplan KB, Burds AA, Swedlow JR, Bekir SS, Sorger PK, Nathke IS. A role for the Adenomatous Polyposis Coli protein in chromosome segregation. Nat Cell Biol 2001; 3:429-32.
39. Fodde R, Kuipers J, Rosenberg C, Smits R, Kielman M, Gaspar C, van Es JH, Breukel C, Wiegant J, Giles RH, Clevers H. Mutations in the APC tumour suppressor gene cause chromosomal instability. Nat Cell Biol 2001; 3:433-8.
40. Fodde R, Smits R, Clevers H. APC, signal transduction and genetic instability in colorectal cancer. Nat Rev Cancer 2001; 1:55-67.
41. Lustig B, Jerchow B, Sachs M, Weiler S, Pietsch T, Karsten U, van de Wetering M, Clevers H, Schlag PM, Birchmeier W, Behrens J. Negative feedback loop of Wnt signaling through upregulation of conductin/axin2 in colorectal and liver tumors. Mol Cell Biol 2002; 22:1184-93.
42. Leung JY, Kolligs FT, Wu R, Zhai Y, Kuick R, Hanash S, Cho KR, Fearon ER. Activation of AXIN2 expression by beta-catenin-T cell factor. A feedback repressor pathway regulating Wnt signaling. J Biol Chem 2002; 277:21657-65.
43. Hadjihannas MV, Bruckner M, Jerchow B, Birchmeier W, Dietmaier W, Behrens J. Aberrant Wnt/{beta}-catenin signaling can induce chromosomal instability in colon cancer. Proc Natl Acad Sci USA 2006; 103:10747-52.
44. Hanisch A, Wehner A, Nigg EA, Sillje HH. Different Plk1 functions show distinct dependencies on Polo-Box domain-mediated targeting. Mol Biol Cell 2006; 17:448-59.
45. Jang YJ, Lin CY, Ma S, Erikson RL. Functional studies on the role of the C-terminal domain of mammalian polo-like kinase. Proc Natl Acad Sci USA 2002; 99:1984-9.
46. Bobinnec Y, Morin X, Debec A. Shaggy/GSK-3beta kinase localizes to the centrosome and to specialized cytoskeletal structures in Drosophila. Cell Motil Cytoskeleton 2006; 63:313-20.
47. 2/M and apoptosis. Mol Biol Cell 2003; 14:2844-60.
48. Wakefield JG, Stephens DJ, Tavare JM. A role for glycogen synthase kinase-3 in mitotic spindle dynamics and chromosome alignment. J Cell Sci 2003; 116:637-46.
49. Kaplan DD, Meigs TE, Kelly P, Casey PJ. Identification of a role for beta-catenin in the establishment of a bipolar mitotic spindle. J Biol Chem 2004; 279:10829-32.
50. Brumer Y, Michor F, Shakhnovich EI. Genetic instability and the quasispecies model. J Theor Biol 2006; 241:216-22.
51. Liu W, Dong X, Mai M, Seelan RS, Taniguchi K, Krishnadath KK, Halling KC, Cunningham JM, Boardman LA, Qian C, Christensen E, Schmidt SS, Roche PC, Smith DI, Thibodeau SN. Mutations in AXIN2 cause colorectal cancer with defective mismatch repair by activating beta-catenin/TCF signalling. Nat Genet 2000; 26:146-7.
52. Koinuma K, Yamashita Y, Liu W, Hatanaka H, Kurashina K, Wada T, Takada S, Kaneda R, Choi YL, Fujiwara SI, Miyakura Y, Nagai H, Mano H. Epigenetic silencing of AXIN2 in colorectal carcinoma with microsatellite instability. Oncogene 2006; 25:139-46.
53. Hernando E, Nahle Z, Juan G, Diaz-Rodriguez E, Alaminos M, Hemann M, Michel L, Mittal V, Gerald W, Benezra R, Lowe SW, Cordon-Cardo C. Rb inactivation promotes genomic instability by uncoupling cell cycle progression from mitotic control. Nature 2004; 430:797-802.
54. Weinberg RA. The retinoblastoma protein and cell cycle control. Cell 1995; 81:323-30.
55. Planas-Silva MD, Weinberg RA. The restriction point and control of cell proliferation. Curr Opin Cell Biol 1997; 9:768-72.
56. Hughes TA, Brady HJ. E2F1 up-regulates the expression of the tumour suppressor axin2 both by activation of transcription and by mRNA stabilisation. Biochem Biophys Res Commun 2005; 329:1267-74.
57. Hughes TA, Brady HJ. Cross-talk between pRb/E2F and Wnt/beta-catenin pathways: E2F1 induces axin2 leading to repression of Wnt signalling and to increased cell death. Exp Cell Res 2005; 303:32-46.
58. Hughes TA, Brady HJ. Regulation of axin2 expression at the levels of transcription, translation and protein stability in lung and colon cancer. Cancer Lett 2006; 233:338-47.
59. Hara A, Sakata K, Yamada Y, Kuno T, Kitaori N, Oyama T, Hirose Y, Murakami A, Tanaka T, Mori H. Suppression of beta-catenin mutation by dietary exposure of auraptene, a citrus antioxidant, in N,N-diethylnitrosamine-induced hepatocellular carcinomas in rats. Oncol Rep 2005; 14:345-51.
60. Hu R, Khor TO, Shen G, Jeong WS, Hebbar V, Chen C, Xu C, Reddy B, Chada K, Kong AN. Cancer chemoprevention of intestinal polyposis in ApcMin/+ mice by sulforaphane, a natural product derived from cruciferous vegetable. Carcinogenesis 2006.
61. Delage B, Bairras C, Buaud B, Pallet V, Cassand P. A high-fat diet generates alterations in nuclear receptor expression: Prevention by vitamin A and links with cyclooxygenase-2 and beta-catenin. Int J Cancer 2005; 116:839-46.
62. Groubet R, Pallet V, Delage B, Redonnet A, Higueret P, Cassand P. Hyperlipidic diets induce early alterations of the vitamin A signalling pathway in rat colonic mucosa. Endocr Regul 2003; 37:137-44.
63. Misikangas M, Pajari AM, Paivarinta E, Mutanen M. Promotion of adenoma growth by dietary inulin is associated with increase in cyclin D1 and decrease in adhesion proteins in Min/+ mice mucosa. J Nutr Biochem 2005; 16:402-9.
64. Ubagai T, Ochiai M, Kawamori T, Imai H, Sugimura T, Nagao M, Nakagama H. Efficient induction of rat large intestinal tumors with a new spectrum of mutations by intermittent administration of 2-amino-1-methyl-6-phenylimidazo[4, 5-b]pyridine in combination with a high fat diet. Carcinogenesis 2002; 23:197-200.
65. Woo RA, Poon RY. Activated oncogenes promote and cooperate with chromosomal instability for neoplastic transformation. Genes Dev 2004; 18:1317-30.
66. Woo RA, Poon RY. Gene mutations and aneuploidy: The instability that causes cancer. Cell Cycle 2004; 3:1101-3.