Notch1 counteracts WNT/β-catenin signaling through chromatin modification in colorectal cancer

Journal of Clinical Investigation

Volumn 122, Issue 9, 2012, Pages 3248-3259

  Kim, Hyun A ^a   Koo, Bon Kyoung ^a   Cho, Ji Hoon ^b   Kim, Yoon Young ^a,b   Seong, Jinwoo ^a   Chang, Hee Jin ^c   Oh, Young Min ^b   Stange, Daniel E ^d   Park, Jae Gahb ^c   Hwang, Daehee ^b   Kong, Young Yun ^a  

^a Seoul National University   (South Korea)

^b Pohang University of Science and Technology (POSTECH)   (South Korea)

^c National Cancer Center   (South Korea)

^d UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; HISTONE METHYLTRANSFERASE; NOTCH1 RECEPTOR; WNT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CHROMATIN IMMUNOPRECIPITATION; COLON POLYPOSIS; COLORECTAL CANCER; CONTROLLED STUDY; EPIGENETICS; GENE EXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; MICROARRAY ANALYSIS; NONHUMAN; PRIORITY JOURNAL;

ADENOCARCINOMA; ADENOMA; ADENOMATOUS POLYPOSIS COLI PROTEIN; ANALYSIS OF VARIANCE; ANIMALS; BETA CATENIN; CELL LINE, TUMOR; CHROMATIN; COLORECTAL NEOPLASMS; GENE EXPRESSION REGULATION, NEOPLASTIC; HOMEODOMAIN PROTEINS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KAPLAN-MEIER ESTIMATE; MICE; MICE, TRANSGENIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROMOTER REGIONS, GENETIC; PROTEIN METHYLTRANSFERASES; PROTEIN-SERINE-THREONINE KINASES; RECEPTOR, NOTCH1; TRANSCRIPTOME; TUMOR SUPPRESSOR PROTEINS; VIMENTIN; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 84865988309     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI61216     Document Type: Article

References (55)

1. Fodde R, Smits R, Clevers H. APC, signal transduction and genetic instability in colorectal cancer. Nat Rev Cancer. 2001;1(1):55-67. (Pubitemid 33741881)
2. Kinzler KW, Vogelstein B. Lessons from hereditary colorectal cancer. Cell. 1996;87(2):159-170. (Pubitemid 26358996)
3. Grady WM, Carethers JM. Genomic and epigenetic instability in colorectal cancer pathogenesis. Gastroenterology. 2008;135(4):1079-1099.
4. Sancho E, Batlle E, Clevers H. Signaling pathways in intestinal development and cancer. Annu Rev Cell Dev Biol. 2004;20:695-723. (Pubitemid 39488655)
5. Katoh M. Networking of WNT, FGF, Notch, BMP, and Hedgehog signaling pathways during carcinogenesis. Stem Cell Rev. 2007;3(1):30-38. (Pubitemid 47472809)
6. van de Wetering M, et al. The beta-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell. 2002;111(2):241-250.
7. Nakamura T, Tsuchiya K, Watanabe M. Crosstalk between Wnt and Notch signaling in intestinal epithelial cell fate decision. J Gastroenterol. 2007;42(9):705-710. (Pubitemid 47456757)
8. Vooijs M, Liu Z, Kopan R. Notch: architect, landscaper, and guardian of the intestine. Gastroenterology. 2011;141(2):448-459.
9. Fre S, Huyghe M, Mourikis P, Robine S, Louvard D, Artavanis-Tsakonas S. Notch signals control the fate of immature progenitor cells in the intestine. Nature. 2005;435(7044):964-968. (Pubitemid 40896323)
10. van Es JH, et al. Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature. 2005;435(7044):959-963.
11. Fre S, et al. Notch and Wnt signals cooperatively control cell proliferation and tumorigenesis in the intestine. Proc Natl Acad Sci U S A. 2009;106(15):6309-6314.
12. Rodilla V, et al. Jagged1 is the pathological link between Wnt and Notch pathways in colorectal cancer. Proc Natl Acad Sci U S A. 2009;106(15):6315-6320.
13. Akiyoshi T, et al. Gamma-secretase inhibitors enhance taxane-induced mitotic arrest and apoptosis in colon cancer cells. Gastroenterology. 2008;134(1):131-144. (Pubitemid 350309314)
14. Peignon G, et al. Complex interplay between betacatenin signalling and Notch effectors in intestinal tumorigenesis. Gut. 2011;60(2):166-176.
15. Murtaugh LC, Stanger BZ, Kwan KM, Melton DA. Notch signaling controls multiple steps of pancreatic differentiation. Proc Natl Acad Sci U S A. 2003;100(25):14920-14925. (Pubitemid 37517992)
16. Madison BB, Dunbar L, Qiao XT, Braunstein K, Braunstein E, Gumucio DL. Cis elements of the villin gene control expression in restricted domains of the vertical (crypt) and horizontal (duodenum, cecum) axes of the intestine. J Biol Chem. 2002;277(36):33275-33283. (Pubitemid 34984848)
17. Jho EH, Zhang T, Domon C, Joo CK, Freund JN, Costantini F. Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol Cell Biol. 2002;22(4):1172-1183. (Pubitemid 34094853)
18. Takahashi M, et al. Isolation of a novel human gene, APCDD1, as a direct target of the beta-Catenin/T-cell factor 4 complex with probable involvement in colorectal carcinogenesis. Cancer Res. 2002;62(20):5651-5656. (Pubitemid 35204716)
19. Yan D, et al. Elevated expression of axin2 and hnkd mRNA provides evidence that Wnt/beta -catenin signaling is activated in human colon tumors. Proc Natl Acad Sci U S A. 2001;98(26):14973-14978. (Pubitemid 34013954)
20. Zirn B, et al. Target genes of the WNT/beta-catenin pathway in Wilms tumors. Genes Chromosomes Cancer. 2006;45(6):565-574. (Pubitemid 43727163)
21. Petrova TV, et al. Transcription factor PROX1 induces colon cancer progression by promoting the transition from benign to highly dysplastic phenotype. Cancer Cell. 2008;13(5):407-419. (Pubitemid 351609440)
22. Pirot P, van Grunsven LA, Marine JC, Huylebroeck D, Bellefroid EJ. Direct regulation of the Nrarp gene promoter by the Notch signaling pathway. Biochem Biophys Res Commun. 2004;322(2):526-534. (Pubitemid 39490336)
23. Lamar E, et al. Nrarp is a novel intracellular component of the Notch signaling pathway. Genes Dev. 2001;15(15):1885-1899. (Pubitemid 32738619)
24. Krebs LT, Deftos ML, Bevan MJ, Gridley T. The Nrarp gene encodes an ankyrin-repeat protein that is transcriptionally regulated by the notch signaling pathway. Dev Biol. 2001;238(1):110-119. (Pubitemid 32939290)
25. Duncan AW, et al. Integration of Notch and Wnt signaling in hematopoietic stem cell maintenance. Nat Immunol. 2005;6(3):314-322. (Pubitemid 41724769)
26. Soubeyran P, et al. Cdx1 promotes differentiation in a rat intestinal epithelial cell line. Gastroenterology. 1999;117(6):1326-1338.
27. Chen X, Halberg RB, Burch RP, Dove WF. Intestinal adenomagenesis involves core molecular signatures of the epithelial-mesenchymal transition. J Mol Histol. 2008;39(3):283-294.
28. Smith JJ, et al. Experimentally derived metastasis gene expression profile predicts recurrence and death in patients with colon cancer. Gastroenterology. 2010;138(3):958-968.
29. Lachner M, O'Carroll D, Rea S, Mechtler K, Jenuwein T. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature. 2001;410(6824):116-120. (Pubitemid 32225847)
30. Nakayama J, Rice JC, Strahl BD, Allis CD, Grewal SI. Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science. 2001;292(5514):110-113. (Pubitemid 32289138)
31. Schotta G, et al. Central role of Drosophila SU(VAR)3-9 in histone H3-K9 methylation and heterochromatic gene silencing. EMBO J. 2002;21(5):1121-1131. (Pubitemid 34206185)
32. Rottinger E, Croce J, Lhomond G, Besnardeau L, Gache C, Lepage T. Nemo-like kinase (NLK) acts downstream of Notch/Delta signalling to downregulate TCF during mesoderm induction in the sea urchin embryo. Development. 2006;133(21):4341-4353. (Pubitemid 44830676)
33. Takada I, et al. A histone lysine methyltransferase activated by non-canonical Wnt signalling suppresses PPAR-gamma transactivation. Nat Cell Biol. 2007;9(11):1273-1285. (Pubitemid 350042359)
34. Ranganathan P, Weaver KL, Capobianco AJ. Notch signalling in solid tumours: a little bit of everything but not all the time. Nat Rev Cancer. 2011;11(5):338-351.
35. Radtke F, Raj K. The role of Notch in tumorigenesis: oncogene or tumour suppressor? Nat Rev Cancer. 2003;3(10):756-767. (Pubitemid 37328814)
36. Riccio O, et al. Loss of intestinal crypt progenitor cells owing to inactivation of both Notch1 and Notch2 is accompanied by derepression of CDK inhibitors p27Kip1 and p57Kip2. EMBO Rep. 2008;9(4):377-383.
37. + in intestinal adenomas from Min mice. Cancer Res. 1994;54(22):5947-5952.
38. Shoemaker AR, Luongo C, Moser AR, Marton LJ, Dove WF. Somatic mutational mechanisms involved in intestinal tumor formation in Min mice. Cancer Res. 1997;57(10):1999-2006. (Pubitemid 27209733)
39. Sonoshita M, et al. Suppression of colon cancer metastasis by Aes through inhibition of Notch signaling. Cancer Cell. 2011;19(1):125-137.
40. Chen G, Courey AJ. Groucho/TLE family proteins and transcriptional repression. Gene. 2000;249(1-2):1-16. (Pubitemid 30265483)
41. Wang WF, Wang YG, Reginato AM, Plotkina S, Gridley T, Olsen BR. Growth defect in Grg5 null mice is associated with reduced Ihh signaling in growth plates. Dev Dyn. 2002;224(1):79-89. (Pubitemid 34464935)
42. Roose J, et al. The Xenopus Wnt effector XTcf-3 interacts with Groucho-related transcriptional repressors. Nature. 1998;395(6702):608-612. (Pubitemid 28475715)
43. Babaei-Jadidi R, et al. FBXW7 influences murine intestinal homeostasis and cancer, targeting Notch, Jun, and DEK for degradation. J Exp Med. 2011;208(2):295-312.
44. Koo BK, et al. Notch signaling promotes the generation of EphrinB1-positive intestinal epithelial cells. Gastroenterology. 2009;137(1):145-155.
45. Hayward P, Kalmar T, Arias AM. Wnt/Notch signalling and information processing during development. Development. 2008;135(3):411-424.
46. Axelrod JD, Matsuno K, Artavanis-Tsakonas S, Perrimon N. Interaction between Wingless and Notch signaling pathways mediated by dishevelled. Science. 1996;271(5257):1826-1832.
47. Devgan V, Mammucari C, Millar SE, Brisken C, Dotto GP. p21WAF1/Cip1 is a negative transcriptional regulator of Wnt4 expression downstream of Notch1 activation. Genes Dev. 2005;19(12):1485-1495. (Pubitemid 41003015)
48. Foltz DR, Santiago MC, Berechid BE, Nye JS. Glycogen synthase kinase-3beta modulates notch signaling and stability. Curr Biol. 2002;12(12):1006-1011. (Pubitemid 34703331)
49. Brack AS, Conboy IM, Conboy MJ, Shen J, Rando TA. A temporal switch from notch to Wnt signaling in muscle stem cells is necessary for normal adult myogenesis. Cell Stem Cell. 2008;2(1):50-59.
50. Alves-Guerra MC, Ronchini C, Capobianco AJ. Mastermind-like 1 Is a specific coactivator of beta-catenin transcription activation and is essential for colon carcinoma cell survival. Cancer Res. 2007;67(18):8690-8698. (Pubitemid 47437444)
51. Iso T, Kedes L, Hamamori Y. HES and HERP families: multiple effectors of the Notch signaling pathway. J Cell Physiol. 2003;194(3):237-255. (Pubitemid 36176887)
52. Ku JL, Park JG. Biology of SNU cell lines. Cancer Res Treat. 2005;37(1):1-19.
53. Bolstad BM, Irizarry RA, Astrand M, Speed TP. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics. 2003;19(2):185-193. (Pubitemid 36181903)
54. Hwang D, et al. A data integration methodology for systems biology. Proc Natl Acad Sci U S A. 2005;102(48):17296-17301. (Pubitemid 41740860)
55. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4(1):44-57.