Genetic amplification of the NOTCH modulator LNX2 upregulates the WNT/β-catenin pathway in colorectal cancer

Cancer Research

Volumn 73, Issue 6, 2013, Pages 2003-2013

  Camps, Jordi ^a   Pitt, Jason J ^a   Emons, Georg ^a,b   Hummon, Amanda B ^a,c   Case, Chanelle M ^a   Grade, Marian ^a,b   Jones, Tamara L ^a   Nguyen, Quang T ^a   Ghadimi, B Michael ^b   Beissbarth, Tim ^b   Difilippantonio, Michael J ^a   Caplen, Natasha J ^a   Ried, Thomas ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^c UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; JAGGED1; NOTCH RECEPTOR; ONCOPROTEIN; PROTEIN LNX2; UNCLASSIFIED DRUG;

AMPLICON; ARTICLE; BETA CATENIN SIGNALING PATHWAY; CANCER SURVIVAL; CELL VIABILITY; COLORECTAL CANCER; COMPARATIVE GENOMIC HYBRIDIZATION; CONTROLLED STUDY; COPY NUMBER VARIATION; DIS3 GENE; DOWN REGULATION; GENE AMPLIFICATION; GENE EXPRESSION PROFILING; GENE MAPPING; GENE OVEREXPRESSION; GPR180 GENE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; KLF5 GENE; LNX2 GENE; MAJOR CLINICAL STUDY; NUCLEOTIDE SEQUENCE; NUPL1 GENE; ONCOGENE; OPEN READING FRAME; POLR1D GENE; POMP GENE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN FUNCTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SLC7A1 GENE; UPREGULATION; WNT SIGNALING PATHWAY;

BETA CATENIN; CARRIER PROTEINS; COLORECTAL NEOPLASMS; COMPARATIVE GENOMIC HYBRIDIZATION; FLOW CYTOMETRY; HUMANS; RECEPTORS, NOTCH; RNA INTERFERENCE; TRANSCRIPTION, GENETIC; UP-REGULATION; WNT PROTEINS;

EID: 84875477576     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-3159     Document Type: Article

References (49)

1. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA Cancer J Clin 2010;60:277-300.
2. Fearon ER, Vogelstein B. Agenetic model for colorectal tumorigenesis. Cell 1990;61:759-67.
3. Ried T, Knutzen R, Steinbeck R, Blegen H, Schrock E, Heselmeyer K, et al. Comparative genomic hybridization reveals a specific pattern of chromosomal gains and losses during the genesis of colorectal tumors. Genes Chromosomes Cancer 1996;15:234-45.
4. Albertson DG, Collins C, McCormick F, Gray JW. Chromosome aberrations in solid tumors. Nat Genet 2003;34:369-76.
5. Ried T. Homage to Theodor Boveri (1862-1915): Boveri's theory of cancer as a disease of the chromosomes, and the landscape of genomic imbalances in human carcinomas. Environ Mol Mutagen 2009;50:593-601.
6. Beroukhim R, Mermel CH, Porter D, Wei G, Raychaudhuri S, Donovan J, et al. The landscape of somatic copy-number alteration across human cancers. Nature 2010;463:899-905.
7. Ried T, Heselmeyer-Haddad K, Blegen H, Schrock E, Auer G. Genomic changes defining the genesis, progression, and malignancy potential in solid human tumors: a phenotype/genotype correlation. Genes Chromosomes Cancer 1999;25:195-204.
8. Heim S, Mitelman F. Cancer cytogenetics. 3rd ed. Hoboken, NJ: John Wiley & Sons; 2009.
9. Camps J, Grade M, Nguyen QT, Hormann P, Becker S, Hummon AB, et al. Chromosomal breakpoints in primary colon cancer cluster at sites of structural variants in the genome. Cancer Res 2008; 68:1284-95.
10. Chin K, DeVries S, Fridlyand J, Spellman PT, Roydasgupta R, Kuo WL, et al. Genomic and transcriptional aberrations linked to breast cancer pathophysiologies. Cancer Cell 2006;10:529-41.
11. Grade M, Hormann P, Becker S, Hummon AB, Wangsa D, Varma S, et al. Gene expression profiling reveals a massive, aneuploidy-dependent transcriptional deregulation and distinct differences between lymph node-negative and lymph node-positive colon carcinomas. Cancer Res 2007;67:41-56.
12. Pollack JR, Sorlie T, Perou CM, Rees CA, Jeffrey SS, Lonning PE, et al. Microarray analysis reveals a major direct role of DNA copy number alteration in the transcriptional program of human breast tumors. Proc Natl Acad Sci U S A 2002;99:12963-8.
13. Ried T, Hu Y, Difilippantonio MJ, Ghadimi BM, Grade M, Camps J. The consequences of chromosomal aneuploidy on the transcriptome of cancer cells. Biochim Biophys Acta 2012;1819:784-93.
14. Tsafrir D, Bacolod M, Selvanayagam Z, Tsafrir I, Shia J, Zeng Z, et al. Relationship of gene expression and chromosomal abnormalities in colorectal cancer. Cancer Res 2006;66:2129-37.
15. Grade M, Hummon AB, Camps J, Emons G, Spitzner M, Gaedcke J, et al. A genomic strategy for the functional validation of colorectal cancer genes identifies potential therapeutic targets. Int J Cancer 2011;128:1069-79.
16. Chin L, Hahn WC, Getz G, Meyerson M. Making sense of cancer genomic data. Genes Dev 2011;25:534-55.
17. Ried T. Laboratory of Thomas Ried. 2013 [cited; Available from: http://www.riedlab.nci.nih.gov/index.php/protocols.
18. 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;19:185-93.
19. Gautier L,Cope L, Bolstad BM, Irizarry RA. affy - Analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 2004;20:307-15.
20. Camps J, Nguyen QT, Padilla-Nash HM, Knutsen T, McNeil NE, Wangsa D, et al. Integrative genomics reveals mechanisms of copy number alterations responsible for transcriptional deregulation in colorectal cancer. Genes Chromosomes Cancer 2009;48: 1002-17.
21. Nandan MO, McConnell BB, Ghaleb AM, Bialkowska AB, Sheng H, Shao J, et al. Kruppel-like factor 5 mediates cellular transformation during oncogenic KRAS-induced intestinal tumorigenesis. Gastroenterology 2008;134:120-30.
22. Shimokawa T, Furukawa Y, Sakai M, Li M, Miwa N, Lin YM, et al. Involvement of theFGF18 gene in colorectal carcinogenesis, as a novel downstream target of the beta-catenin/T-cell factor complex. Cancer Res 2003;63:6116-20.
23. Sonvilla G, Allerstorfer S, Heinzle C, Stattner S, Karner J, Klimpfinger M, et al. Fibroblast growth factor receptor 3-IIIc mediates colorectal cancer growth and migration. Br J Cancer 2010;102:1145-56.
24. Sonvilla G, Allerstorfer S, Stattner S, Karner J, Klimpfinger M, Fischer H, et al. FGF18 in colorectal tumour cells: autocrine and paracrine effects. Carcinogenesis 2008;29:15-24.
25. Nandan MO, Yang VW. The role of Kruppel-like factors in the reprogramming of somatic cells to induced pluripotent stem cells. Histol Histopathol 2009;24:1343-55.
26. Parisi S, Passaro F, Aloia L, Manabe I, Nagai R, Pastore L, et al. Klf5 is involved in self-renewal of mouse embryonic stem cells. J Cell Sci 2008;121:2629-34.
27. Sabates-Bellver J, Van der Flier LG, de Palo M, Cattaneo E, Maake C, Rehrauer H, et al. Transcriptome profile of human colorectal adenomas. Mol Cancer Res 2007;5:1263-75.
28. Segal E, Yelensky R, Koller D. Genome-wide discovery of transcriptional modules from DNA sequence and gene expression. Bioinformatics 2003;19(Suppl 1):i273-82.
29. Myllykangas S, Bohling T, Knuutila S. Specificity, selection and significance of gene amplifications in cancer. Semin Cancer Biol 2007;17:42-55.
30. Network TCGA. Comprehensive molecular characterization of human colon and rectal cancer. Nature 2012;487:330-7.
31. Upender MB, Habermann JK, McShane LM, Korn EL, Barrett JC, Difilippantonio MJ, et al. Chromosome transfer induced aneuploidy results in complex dysregulation of the cellular transcriptome in immortalized and cancer cells. Cancer Res 2004;64:6941-9.
32. Firestein R, Bass AJ, Kim SY, Dunn IF, Silver SJ, Guney I, et al. CDK8 is a colorectal cancer oncogene that regulates beta-catenin activity. Nature 2008;455:547-51.
33. Salari K, Spulak ME, Cuff J, Forster AD, Giacomini CP, Huang S, et al. CDX2 is an amplified lineage-survival oncogene in colorectal cancer. Proc Natl Acad Sci U S A 2012;109:E3196-205.
34. Dulak AM, Schumacher S, van Lieshout J, Imamura Y, Fox C, Shim B, et al. Gastrointestinal adenocarcinomas of the esophagus, stomach and colon exhibit distinct patterns of genome instability and oncogenesis. Cancer Res 2012;72:4383-93.
35. Sheffer M, Bacolod MD, Zuk O, Giardina SF, Pincas H, Barany F, et al. Association of survival and disease progression with chromosomal instability: a genomic exploration of colorectal cancer. Proc Natl Acad Sci U S A 2009;106:7131-6.
36. Brosens RP, Haan JC, Carvalho B, Rustenburg F, Grabsch H, Quirke P, et al. Candidate driver genes in focal chromosomal aberrations of stage II colon cancer. J Pathol 2010;221:411-24.
37. Bass AJ, Watanabe H, Mermel CH, Yu S, Perner S, Verhaak RG, et al. SOX2 is an amplified lineage-survival oncogene in lung and esophageal squamous cell carcinomas. Nat Genet 2009;41:1238-42.
38. Gen Y, Yasui K, Zen Y, Zen K, Dohi O, Endo M, et al. SOX2 identified as a target gene for the amplification at 3q26 that is frequently detected in esophageal squamous cell carcinoma. Cancer Genet Cytogenet 2010; 202:82-93.
39. Takanen JO. The Human Protein Atlas. 2013 [cited; Available from: http://www.proteinatlas.org/ENSG00000139517/cancer.
40. Rice DS, Northcutt GM, Kurschner C. The Lnx family proteins function as molecular scaffolds for Numb family proteins. Mol Cell Neurosci 2001;18:525-40.
41. Nie J, McGill MA, Dermer M, Dho SE, Wolting CD, McGlade CJ. LNX functions as a RING type E3 ubiquitin ligase that targets the cell fate determinant Numb for ubiquitin-dependent degradation. EMBO J 2002;21:93-102.
42. 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;435:964-8.
43. Nakamura T, Torimura T, Sakamoto M, Hashimoto O, Taniguchi E, Inoue K, et al. Significance and therapeutic potential of endothelial progenitor cell transplantation in a cirrhotic liver rat model. Gastroenterology 2007;133:91-107.
44. Pinto D, Gregorieff A, Begthel H, Clevers H. Canonical Wnt signals are essential for homeostasis of the intestinal epithelium. Genes Dev 2003;17:1709-13.
45. Vooijs M, Liu Z, Kopan R. Notch: architect, landscaper, and guardian of the intestine. Gastroenterology 2011;141:448-59.
46. Fre S, Pallavi SK, Huyghe M, Lae M, Janssen KP, Robine S, et al. Notch and Wnt signals cooperatively control cell proliferation and tumorigenesis in the intestine. Proc Natl Acad Sci U S A 2009; 106:6309-14.
47. Guilmeau S, Flandez M, Mariadason JM, Augenlicht LH. Heterogeneity of Jagged1 expression in human and mouse intestinal tumors: implications for targeting Notch signaling. Oncogene 2010;29:992-1002.
48. Rodilla V, Villanueva A, Obrador-Hevia A, Robert-Moreno A, Fernandez-Majada V, Grilli A, et al. Jagged1 is the pathological link between Wnt and Notch pathways in colorectal cancer. Proc Natl Acad SciUSA 2009;106:6315-20.
49. Klaus A, Birchmeier W. Wnt signalling and its impact on development and cancer. Nat Rev Cancer 2008;8:387-98.