Cables1 is a tumor suppressor gene that regulates intestinal tumor progression in ApcMin mice

Cancer Biology and Therapy

Volumn 14, Issue 7, 2013, Pages 672-678

  Arnason, Thomas ^a   Pino, Maria S ^b,c   Yilmaz, Omer ^a   Kirley, Sandra D ^a   Rueda, Bo R ^b   Chung, Daniel C ^b   Zukerberg, Lawrence R ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD UNIVERSITY   (United States)

^c Medical Oncology Unit   (Italy)

Author keywords

catenin; Adenocarcinoma; ApcMin mice; Cables1; Chromosome 18q; Colorectal cancer; Tumor suppressor gene

Indexed keywords

BETA CATENIN; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CABLES1 GENE; CANCER CELL; CELL FUNCTION; CHROMOSOME 18Q; COLON CANCER; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENE FUNCTION; GENE INACTIVATION; GENOTYPE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; INTESTINE CARCINOMA; INTESTINE EPITHELIUM CELL; MALE; MOUSE; NONHUMAN; STEM CELL; TUMOR GROWTH; TUMOR SUPPRESSOR GENE; TUMOR VOLUME; WNT SIGNALING PATHWAY;

ADENOCARCINOMA; APCMINMICE; CABLES1; CHROMOSOME 18Q; COLORECTAL CANCER; Î2-CATENIN; TUMOR SUPPRESSOR GENE;

ANIMALS; BETA CATENIN; CARRIER PROTEINS; CELL TRANSFORMATION, NEOPLASTIC; CYCLINS; DISEASE PROGRESSION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, TUMOR SUPPRESSOR; HUMANS; INTESTINAL NEOPLASMS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHOSPHOPROTEINS; SIGNAL TRANSDUCTION;

EID: 84881148535     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.25089     Document Type: Article

References (29)

1. Grady WM, Carethers JM. Genomic and epigenetic instability in colorectal cancer pathogenesis. Gastroenterology 2008; 135: 1079-99; PMID:18773902; http://dx.doi.org/10.1053/j.gastro. 2008.07.076
2. Vogelstein B, Fearon ER, Hamilton SR, Kern SE, Preisinger AC, Leppert M, et al. Genetic alterations during colorectal-tumor development. N Engl J Med 1988; 319: 525-32; PMID:2841597; http://dx.doi.org/10.1056/NEJM198809013190901
3. Tarafa G, Villanueva A, Farré L, Rodríguez J, Musulén E, Reyes G, et al. DCC and SMAD4 alterations in human colorectal and pancreatic tumor dissemination. Oncogene 2000; 19: 546-55; PMID:10698524; http://dx.doi.org/10.1038/sj.onc.1203353
4. Keino-Masu K, Masu M, Hinck L, Leonardo ED, Chan SS, Culotti JG, et al. Deleted in Colorectal Cancer (DCC) encodes a netrin receptor. Cell 1996; 87: 175-85; PMID:8861902; http://dx.doi.org/10.1016/S0092-8674(00)81336-7
5. Fazeli A, Dickinson SL, Hermiston ML, Tighe RV, Steen RG, Small CG, et al. Phenotype of mice lacking functional Deleted in colorectal cancer (Dcc) gene. Nature 1997; 386: 796-804; PMID:9126737; http://dx.doi.org/10.1038/ 386796a0
6. Takagi Y, Kohmura H, Futamura M, Kida H, Tanemura H, Shimokawa K, et al. Somatic alterations of the DPC4 gene in human colorectal cancers in vivo. Gastroenterology 1996; 111: 1369-72; PMID:8898652; http://dx.doi.org/10.1053/ gast.1996. v111.pm8898652
7. Takagi Y, Koumura H, Futamura M, Aoki S, Ymaguchi K, Kida H, et al. Somatic alterations of the SMAD- 2 gene in human colorectal cancers. Br J Cancer 1998; 78: 1152-5; PMID:9820171; http://dx.doi.org/10.1038/bjc.1998.645
8. Wu CL, Kirley SD, Xiao H, Chuang Y, Chung DC, Zukerberg LR. Cables enhances cdk2 tyrosine 15 phosphorylation by Wee1, inhibits cell growth, and is lost in many human colon and squamous cancers. Cancer Res 2001; 61: 7325-32; PMID:11585773
9. Zukerberg LR, Patrick GN, Nikolic M, Humbert S, Wu CL, Lanier LM, et al. Cables links Cdk5 and c-Abl and facilitates Cdk5 tyrosine phosphorylation, kinase upregulation, and neurite outgrowth. Neuron 2000; 26: 633-46; PMID:10896159; http://dx.doi.org/10.1016/S0896-6273(00)81200-3
10. Rhee J, Buchan T, Zukerberg L, Lilien J, Balsamo J. Cables links Robo-bound Abl kinase to N-cadherinbound beta-catenin to mediate Slit-induced modulation of adhesion and transcription. Nat Cell Biol 2007; 9: 883-92; PMID:17618275; http://dx.doi.org/10.1038/ncb1614
11. Tan D, Kirley S, Li Q, Ramnath N, Slocum HK, Brooks JS, et al. Loss of cables protein expression in human non-small cell lung cancer: a tissue microarray study. Hum Pathol 2003; 34: 143-9; PMID:12612882; http://dx.doi.org/10.1053/hupa.2003.26
12. DeBernardo RL, Littell RD, Luo H, Duska LR, Oliva E, Kirley SD, et al. Defining the extent of cables loss in endometrial cancer subtypes and its effectiveness as an inhibitor of cell proliferation in malignant endometrial cells in vitro and in vivo. Cancer Biol Ther 2005; 4: 103-7; PMID:15662117; http://dx.doi.org/10.4161/cbt.4.1.1433
13. Park Y, Sakamoto H, Kirley SD, Ogino S, Kawasaki T, Kwon E, et al. The Cables gene on chromosome 18q is silenced by promoter hypermethylation and allelic loss in human colorectal cancer. Am J Pathol 2007; 171: 1509-19; PMID:17982127; http://dx.doi.org/10.2353/ajpath.2007.070331
14. Zukerberg LR, DeBernardo RL, Kirley SD, D'Apuzzo M, Lynch MP, Littell RD, et al. Loss of cables, a cyclin-dependent kinase regulatory protein, is associated with the development of endometrial hyperplasia and endometrial cancer. Cancer Res 2004; 64: 202-8; PMID:14729625; http://dx.doi.org/10.1158/ 0008-5472.CAN-03-2833
15. Kirley SD, D'Apuzzo M, Lauwers GY, Graeme-Cook F, Chung DC, Zukerberg LR. The Cables gene on chromosome 18Q regulates colon cancer progression in vivo. Cancer Biol Ther 2005; 4: 861-3; PMID:16210915; http://dx.doi.org/10.4161/cbt.4. 8.1894
16. Kirley SD, Rueda BR, Chung DC, Zukerberg LR. Increased growth rate, delayed senescense and decreased serum dependence characterize cables-deficient cells. Cancer Biol Ther 2005; 4: 654-8; PMID:15908791; http://dx.doi.org/10. 4161/cbt.4.6.1732
17. Yilmaz OH, Katajisto P, Lamming DW, Gültekin Y, Bauer-Rowe KE, Sengupta S, et al. mTORC1 in the Paneth cell niche couples intestinal stem-cell function to calorie intake. Nature 2012; 486: 490-5; PMID:22722868
18. Sato T, van Es JH, Snippert HJ, Stange DE, Vries RG, van den Born M, et al. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 2011; 469: 415-8; PMID:21113151; http://dx.doi.org/10.1038/nature09637
19. Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N, Stange DE, et al. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 2009; 459: 262-5; PMID:19329995; http://dx.doi.org/10. 1038/nature07935
20. Boland CR, Sato J, Appelman HD, Bresalier RS, Feinberg AP. Microallelotyping defines the sequence and tempo of allelic losses at tumour suppressor gene loci during colorectal cancer progression. Nat Med 1995; 1: 902-9; PMID:7585215; http://dx.doi.org/10.1038/nm0995-902
21. Takaku K, Wrana JL, Robertson EJ, Taketo MM. No effects of Smad2 (madh2) null mutation on malignant progression of intestinal polyps in Apc(delta716) knockout mice. Cancer Res 2002; 62: 4558-61; PMID:12183405
22. Hamamoto T, Beppu H, Okada H, Kawabata M, Kitamura T, Miyazono K, et al. Compound disruption of smad2 accelerates malignant progression of intestinal tumors in apc knockout mice. Cancer Res 2002; 62: 5955-61; PMID:12384562
23. Takaku K, Oshima M, Miyoshi H, Matsui M, Seldin MF, Taketo MM. Intestinal tumorigenesis in compound mutant mice of both Dpc4 (Smad4) and Apc genes. Cell 1998; 92: 645-56; PMID:9506519; http://dx.doi.org/10.1016/S0092-8674(00)81132-0
24. Alberici P, Jagmohan-Changur S, De Pater E, Van Der Valk M, Smits R, Hohenstein P, et al. Smad4 haploinsufficiency in mouse models for intestinal cancer. Oncogene 2006; 25: 1841-51; PMID:16288217; http://dx.doi.org/10.1038/sj. onc.1209226
25. Thompson MB. The Min mouse: a genetic model for intestinal carcinogenesis. Toxicol Pathol 1997; 25: 329-32; PMID:9210266; http://dx.doi.org/10.1177/019262339702500312
26. McCart AE, Vickaryous NK, Silver A. Apc mice: models, modifiers and mutants. Pathol Res Pract 2008; 204: 479-90; PMID:18538487; http://dx.doi.org/ 10.1016/j.prp.2008.03.004
27. Silverman KA, Koratkar R, Siracusa LD, Buchberg AM. Identification of the modifier of Min 2 (Mom2) locus, a new mutation that influences Apc-induced intestinal neoplasia. Genome Res 2002; 12: 88-97; PMID:11779834; http://dx.doi.org/10.1101/gr.206002
28. White BD, Chien AJ, Dawson DW. Dysregulation of Wnt/β-catenin signaling in gastrointestinal cancers. Gastroenterology 2012; 142: 219-32; PMID:22155636; http://dx.doi.org/10.1053/j.gastro.2011.12.001
29. Wong SC, Chan AT, Chan JK, Lo YM. Nuclear betacatenin and Ki-67 expression in choriocarcinoma and its pre-malignant form. J Clin Pathol 2006; 59: 387-92; PMID:16467170; http://dx.doi.org/10.1136/jcp.2005.026666