Chromosomal Instability in BRAF Mutant, Microsatellite Stable Colorectal Cancers

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Bond, Catherine E ^a,b   Umapathy, Aarti ^a   Buttenshaw, Ron L ^a,c   Wockner, Leesa ^a   Leggett, Barbara A ^a,b,d   Whitehall, Vicki L J ^a,c  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c Pathology Queensland   (Australia)

^d ROYAL BRISBANE AND WOMEN'S HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE; K RAS PROTEIN; PROTEIN P53;

AGED; ARTICLE; CANCER STAGING; CANCER SURVIVAL; CHROMOSOMAL INSTABILITY; CHROMOSOME 17P; CHROMOSOME 18Q; CHROMOSOME 5Q; CHROMOSOME 8P; COLORECTAL CANCER; CONTROLLED STUDY; CPG ISLAND; FEMALE; GENE LOCUS; GENE MUTATION; HETEROZYGOSITY LOSS; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MICROSATELLITE INSTABILITY; ONCOGENE; ONCOGENE BRAF; ONCOGENE K RAS; PHENOTYPE; TUMOR SUPPRESSOR GENE; WILD TYPE;

AGED; CHROMOSOMAL INSTABILITY; COLORECTAL NEOPLASMS; CPG ISLANDS; FEMALE; HUMANS; LOSS OF HETEROZYGOSITY; MALE; MICROSATELLITE INSTABILITY; PROTO-ONCOGENE PROTEINS B-RAF;

EID: 84867705940     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047483     Document Type: Article

References (65)

1. Fearon ER, Vogelstein B, (1990) A genetic model for colorectal tumorigenesis. Cell 61: 759-767.
2. Jass JR, Do KA, Simms LA, Iino H, Wynter C, et al. (1998) Morphology of sporadic colorectal cancer with DNA replication errors. Gut 42: 673-679.
3. Iino H, Jass JR, Simms LA, Young J, Leggett B, et al. (1999) DNA microsatellite instability in hyperplastic polyps, serrated adenomas, and mixed polyps: a mild mutator pathway for colorectal cancer? J Clin Pathol 52: 5-9.
4. Jass JR, Biden KG, Cummings MC, Simms LA, Walsh M, et al. (1999) Characterisation of a subtype of colorectal cancer combining features of the suppressor and mild mutator pathways. J Clin Pathol 52: 455-460.
5. Leggett B, Whitehall V, (2010) Role of the serrated pathway in colorectal cancer pathogenesis. Gastroenterology 138: 2088-2100.
6. Rosenberg DW, Yang S, Pleau DC, Greenspan EJ, Stevens RG, et al. (2007) Mutations in BRAF and KRAS differentially distinguish serrated versus non-serrated hyperplastic aberrant crypt foci in humans. Cancer Res 67: 3551-3554.
7. Spring KJ, Zhao ZZ, Karamatic R, Walsh MD, Whitehall VL, et al. (2006) High prevalence of sessile serrated adenomas with BRAF mutations: a prospective study of patients undergoing colonoscopy. Gastroenterology 131: 1400-1407.
8. Toyota M, Ho C, Ahuja N, Jair KW, Li Q, et al. (1999) Identification of differentially methylated sequences in colorectal cancer by methylated CpG island amplification. Cancer Res 59: 2307-2312.
9. Kambara T, Simms LA, Whitehall VL, Spring KJ, Wynter CV, et al. (2004) BRAF mutation is associated with DNA methylation in serrated polyps and cancers of the colorectum. Gut 53: 1137-1144.
10. Peyssonnaux C, Eychene A, (2001) The Raf/MEK/ERK pathway: new concepts of activation. Biol Cell 93: 53-62.
11. Rajagopalan H, Bardelli A, Lengauer C, Kinzler KW, Vogelstein B, et al. (2002) Tumorigenesis: RAF/RAS oncogenes and mismatch-repair status. Nature 418: 934.
12. Koinuma K, Shitoh K, Miyakura Y, Furukawa T, Yamashita Y, et al. (2004) Mutations of BRAF are associated with extensive hMLH1 promoter methylation in sporadic colorectal carcinomas. Int J Cancer 108: 237-242.
13. Kane MF, Loda M, Gaida GM, Lipman J, Mishra R, et al. (1997) Methylation of the hMLH1 promoter correlates with lack of expression of hMLH1 in sporadic colon tumors and mismatch repair-defective human tumor cell lines. Cancer Res 57: 808-811.
14. Ionov Y, Peinado MA, Malkhosyan S, Shibata D, Perucho M, (1993) Ubiquitous somatic mutations in simple repeated sequences reveal a new mechanism for colonic carcinogenesis. Nature 363: 558-561.
15. Lothe RA, Peltomaki P, Meling GI, Aaltonen LA, Nystrom-Lahti M, et al. (1993) Genomic instability in colorectal cancer: relationship to clinicopathological variables and family history. Cancer Res 53: 5849-5852.
16. Sinicrope FA, Rego RL, Halling KC, Foster N, Sargent DJ, et al. (2006) Prognostic impact of microsatellite instability and DNA ploidy in human colon carcinoma patients. Gastroenterology 131: 729-737.
17. Popat S, Hubner R, Houlston RS, (2005) Systematic review of microsatellite instability and colorectal cancer prognosis. J Clin Oncol 23: 609-618.
18. Jass JR, (2007) Classification of colorectal cancer based on correlation of clinical, morphological and molecular features. Histopathology 50: 113-130.
19. Ogino S, Nosho K, Kirkner GJ, Kawasaki T, Meyerhardt JA, et al. (2009) CpG island methylator phenotype, microsatellite instability, BRAF mutation and clinical outcome in colon cancer. Gut 58: 90-96.
20. Samowitz WS, Sweeney C, Herrick J, Albertsen H, Levin TR, et al. (2005) Poor survival associated with the BRAF V600E mutation in microsatellite-stable colon cancers. Cancer Res 65: 6063-6069.
21. Kakar S, Deng G, Sahai V, Matsuzaki K, Tanaka H, et al. (2008) Clinicopathologic characteristics, CpG island methylator phenotype, and BRAF mutations in microsatellite-stable colorectal cancers without chromosomal instability. Arch Pathol Lab Med 132: 958-964.
22. Ogino S, Shima K, Meyerhardt J, McCleary N, Ng K, et al. (2012) Predictive and Prognostic Roles of BRAF Mutation in Stage III Colon Cancer: Results from Intergroup Trial CALGB 89803. Clin Cancer Res 18(3): 890-900.
23. Vogelstein B, Fearon ER, Hamilton SR, Kern SE, Preisinger AC, et al. (1988) Genetic alterations during colorectal-tumor development. N Engl J Med 319: 525-532.
24. Goel A, Arnold CN, Niedzwiecki D, Chang DK, Ricciardiello L, et al. (2003) Characterization of sporadic colon cancer by patterns of genomic instability. Cancer Res 63: 1608-1614.
25. O'Brien MJ, Yang S, Mack C, Xu H, Huang CS, et al. (2006) Comparison of microsatellite instability, CpG island methylation phenotype, BRAF and KRAS status in serrated polyps and traditional adenomas indicates separate pathways to distinct colorectal carcinoma end points. Am J Surg Pathol 30: 1491-1501.
26. Watanabe T, Kobunai T, Yamamoto Y, Matsuda K, Ishihara S, et al. (2012) Chromosomal Instability (CIN) Phenotype, CIN High or CIN Low, Predicts Survival for Colorectal Cancer. J Clin Oncol 30(18): 2256-2264.
27. Chang SC, Lin JK, Yang SH, Wang HS, Li AF, et al. (2006) Relationship between genetic alterations and prognosis in sporadic colorectal cancer. Int J Cancer 118: 1721-1727.
28. Walther A, Houlston R, Tomlinson I, (2008) Association between chromosomal instability and prognosis in colorectal cancer: a meta-analysis. Gut 57: 941-950.
29. Goel A, Nagasaka T, Arnold CN, Inoue T, Hamilton C, et al. (2007) The CpG island methylator phenotype and chromosomal instability are inversely correlated in sporadic colorectal cancer. Gastroenterology 132: 127-138.
30. Ogino S, Kawasaki T, Kirkner GJ, Ohnishi M, Fuchs CS, (2007) 18q loss of heterozygosity in microsatellite stable colorectal cancer is correlated with CpG island methylator phenotype-negative (CIMP-0) and inversely with CIMP-low and CIMP-high. BMC Cancer 7: 72.
31. Halling KC, French AJ, McDonnell SK, Burgart LJ, Schaid DJ, et al. (1999) Microsatellite instability and 8p allelic imbalance in stage B2 and C colorectal cancers. J Natl Cancer Inst 91: 1295-1303.
32. Ogino S, Nosho K, Irahara N, Shima K, Baba Y, et al. (2009) Prognostic significance and molecular associations of 18q loss of heterozygosity: a cohort study of microsatellite stable colorectal cancers. J Clin Oncol 27: 4591-4598.
33. American Joint Committee on Cancer (2010) AJCC Cancer Staging Handbook. Edge S, Byrd D, Compton C, Fritz A, Greene F, et al., editors. New York: Springer-Verlag.
34. Boland CR, Thibodeau SN, Hamilton SR, Sidransky D, Eshleman JR, et al. (1998) A National Cancer Institute Workshop on Microsatellite Instability for cancer detection and familial predisposition: development of international criteria for the determination of microsatellite instability in colorectal cancer. Cancer Res 58: 5248-5257.
35. Nagasaka T, Koi M, Kloor M, Gebert J, Vilkin A, et al. (2008) Mutations in both KRAS and BRAF may contribute to the methylator phenotype in colon cancer. Gastroenterology 134: 1950-1960, 1960 e1951.
36. Weisenberger DJ, Siegmund KD, Campan M, Young J, Long TI, et al. (2006) CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer. Nat Genet 38: 787-793.
37. Bond CE, Umapathy A, Ramsnes I, Greco SA, Zhao ZZ, et al. (2012) P53 mutation is common in microsatellite stable, BRAF mutant colorectal cancers. Int J Cancer 130(7): 1567-1576.
38. Vogelstein B, Fearon ER, Kern SE, Hamilton SR, Preisinger AC, et al. (1989) Allelotype of colorectal carcinomas. Science 244: 207-211.
39. Derynck R, Akhurst RJ, Balmain A, (2001) TGF-beta signaling in tumor suppression and cancer progression. Nat Genet 29: 117-129.
40. Siegel PM, Massague J, (2003) Cytostatic and apoptotic actions of TGF-beta in homeostasis and cancer. Nat Rev Cancer 3: 807-821.
41. Javelaud D, Mauviel A, (2005) Crosstalk mechanisms between the mitogen-activated protein kinase pathways and Smad signaling downstream of TGF-beta: implications for carcinogenesis. Oncogene 24: 5742-5750.
42. Kretzschmar M, Doody J, Timokhina I, Massague J, (1999) A mechanism of repression of TGFbeta/Smad signaling by oncogenic Ras. Genes Dev 13: 804-816.
43. Derks S, Bosch LJ, Niessen HE, Moerkerk PT, van den Bosch SM, et al. (2009) Promoter CpG island hypermethylation- and H3K9me3 and H3K27me3-mediated epigenetic silencing targets the deleted in colon cancer (DCC) gene in colorectal carcinogenesis without affecting neighboring genes on chromosomal region 18q21. Carcinogenesis 30: 1041-1048.
44. Cheng YW, Pincas H, Bacolod MD, Schemmann G, Giardina SF, et al. (2008) CpG island methylator phenotype associates with low-degree chromosomal abnormalities in colorectal cancer. Clin Cancer Res 14: 6005-6013.
45. Dar AA, Goff LW, Majid S, Berlin J, El-Rifai W, (2010) Aurora kinase inhibitors-rising stars in cancer therapeutics? Mol Cancer Ther 9: 268-278.
46. Baba Y, Nosho K, Shima K, Irahara N, Kure S, et al. (2009) Aurora-A expression is independently associated with chromosomal instability in colorectal cancer. Neoplasia 11: 418-425.
47. Katayama H, Ota T, Jisaki F, Ueda Y, Tanaka T, et al. (1999) Mitotic kinase expression and colorectal cancer progression. J Natl Cancer Inst 91: 1160-1162.
48. Lin ZZ, Jeng YM, Hu FC, Pan HW, Tsao HW, et al. (2010) Significance of Aurora B overexpression in hepatocellular carcinoma. Aurora B Overexpression in HCC. BMC Cancer 10: 461.
49. Kurai M, Shiozawa T, Shih HC, Miyamoto T, Feng YZ, et al. (2005) Expression of Aurora kinases A and B in normal, hyperplastic, and malignant human endometrium: Aurora B as a predictor for poor prognosis in endometrial carcinoma. Hum Pathol 36: 1281-1288.
50. Bonet C, Giuliano S, Ohanna M, Bille K, Allegra M, et al. (2012) Aurora B is regulated by the Mitogen-activated Protein Kinase/Extracellular Signal-regulated Kinase MAPK/ERK signaling pathway and is a valuable potential target in melanoma cells. J Biol Chem 287(35): 29887-29898.
51. Diep CB, Thorstensen L, Meling GI, Skovlund E, Rognum TO, et al. (2003) Genetic tumor markers with prognostic impact in Dukes' stages B and C colorectal cancer patients. J Clin Oncol 21: 820-829.
52. Lanza G, Matteuzzi M, Gafa R, Orvieto E, Maestri I, et al. (1998) Chromosome 18q allelic loss and prognosis in stage II and III colon cancer. Int J Cancer 79: 390-395.
53. Watanabe T, Wu TT, Catalano PJ, Ueki T, Satriano R, et al. (2001) Molecular predictors of survival after adjuvant chemotherapy for colon cancer. N Engl J Med 344: 1196-1206.
54. Tanaka T, Watanabe T, Kitayama J, Kanazawa T, Kazama Y, et al. (2009) Chromosome 18q deletion as a novel molecular predictor for colorectal cancer with simultaneous hepatic metastasis. Diagn Mol Pathol 18: 219-225.
55. Bertagnolli MM, Redston M, Compton CC, Niedzwiecki D, Mayer RJ, et al. (2011) Microsatellite Instability and Loss of Heterozygosity at Chromosomal Location 18q: Prospective Evaluation of Biomarkers for Stages II and III Colon Cancer-A Study of CALGB 9581 and 89803. J Clin Oncol 29: 3153-3162.
56. Vlajnic T, Andreozzi MC, Schneider S, Tornillo L, Karamitopoulou E, et al. (2011) VEGFA gene locus (6p12) amplification identifies a small but highly aggressive subgroup of colorectal cancer [corrected] patients. Mod Pathol 24: 1404-1412.
57. Lehmann K, Janda E, Pierreux CE, Rytomaa M, Schulze A, et al. (2000) Raf induces TGFbeta production while blocking its apoptotic but not invasive responses: a mechanism leading to increased malignancy in epithelial cells. Genes Dev 14: 2610-2622.
58. Hollingsworth SJ, Drye ER, Tou SI, Boulos PB, (2005) Expression of angiogenic VEGF-A (soluble isoforms 121, 165) and lymphangiogenic VEGF-C in colorectal cancers with micro-satellite instability. J Surg Oncol 92: 317-325.
59. Markowitz S, Wang J, Myeroff L, Parsons R, Sun L, et al. (1995) Inactivation of the type II TGF-beta receptor in colon cancer cells with microsatellite instability. Science 268: 1336-1338.
60. Pino MS, Kikuchi H, Zeng M, Herraiz MT, Sperduti I, et al. (2010) Epithelial to mesenchymal transition is impaired in colon cancer cells with microsatellite instability. Gastroenterology 138: 1406-1417.
61. Andersen CL, Lamy P, Thorsen K, Kjeldsen E, Wikman F, et al. (2011) Frequent genomic loss at chr16p13.2 is associated with poor prognosis in colorectal cancer. Int J Cancer 129(*): 1848-1858.
62. Lassmann S, Weis R, Makowiec F, Roth J, Danciu M, et al. (2007) Array CGH identifies distinct DNA copy number profiles of oncogenes and tumor suppressor genes in chromosomal- and microsatellite-unstable sporadic colorectal carcinomas. J Mol Med 85: 293-304.
63. Trautmann K, Terdiman JP, French AJ, Roydasgupta R, Sein N, et al. (2006) Chromosomal instability in microsatellite-unstable and stable colon cancer. Clin Cancer Res 12: 6379-6385.
64. Andersen CL, Wiuf C, Kruhoffer M, Korsgaard M, Laurberg S, et al. (2007) Frequent occurrence of uniparental disomy in colorectal cancer. Carcinogenesis 28: 38-48.
65. Melcher R, Hartmann E, Zopf W, Herterich S, Wilke P, et al. (2011) LOH and copy neutral LOH (cnLOH) act as alternative mechanism in sporadic colorectal cancers with chromosomal and microsatellite instability. Carcinogenesis 32: 636-642.