Endometrial tumour BRAF mutations and MLH1 promoter methylation as predictors of germline mismatch repair gene mutation status: A literature review

Familial Cancer

Volumn 13, Issue 1, 2014, Pages 1-12

  Metcalf, Alexander M ^a   Spurdle, Amanda B ^a  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

BRAF V600E; Endometrial cancer; Lynch syndrome; MLH1 methylation

Indexed keywords

B RAF KINASE; PROTEIN MLH1; BRAF PROTEIN, HUMAN; MLH1 PROTEIN, HUMAN; NUCLEAR PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ENDOMETRIUM CARCINOMA; ENDOMETRIUM TUMOR; EXON; FEMALE; GENE MUTATION; GENETIC VARIABILITY; HETEROZYGOTE; HUMAN; MISMATCH REPAIR; PREDICTIVE VALUE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN METHYLATION; REVIEW; DNA METHYLATION; GENETICS; GERMLINE MUTATION; MUTATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; DNA METHYLATION; DNA MISMATCH REPAIR; ENDOMETRIAL NEOPLASMS; FEMALE; GERM-LINE MUTATION; HUMANS; MUTATION; NUCLEAR PROTEINS; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS B-RAF;

EID: 84896825792     PISSN: 13899600     EISSN: 15737292     Source Type: Journal    
DOI: 10.1007/s10689-013-9671-6     Document Type: Review

References (65)

1. Lynch HT, Lynch PM, Lanspa SJ, Snyder CL, Lynch JF, Boland CR (2009) Review of the Lynch syndrome: history, molecular genetics, screening, differential diagnosis, and medicolegal ramifications. Clin Genet 76(1):1-18
2. Leenen CH, van Lier MG, van Doorn HC, van Leerdam ME, Kooi SG, de Waard J, Hoedemaeker RF, van den Ouweland AM, Hulspas SM, Dubbink HJ, Kuipers EJ, Wagner A, Dinjens WN, Steyerberg EW (2012) Prospective evaluation of molecular screening for Lynch syndrome in patients with endometrial cancer ≤70 years. Gynecol Oncol 125(2):414-420
3. Gruber SB, Thompson WD (1996) A population-based study of endometrial cancer and familial risk in younger women. Cancer and Steroid Hormone Study Group. Cancer Epidemiol Biomarkers Prev 5(6):411-417 (Pubitemid 26182653)
4. Hampel H, Frankel W, Panescu J, Lockman J, Sotamaa K, Fix D, Comeras I, La Jeunesse J, Nakagawa H, Westman JA, Prior TW, Clendenning M, Penzone P, Lombardi J, Dunn P, Cohn DE, Copeland L, Eaton L, Fowler J, Lewandowski G, Vaccarello L, Bell J, Reid G, de la Chapelle A (2006) Screening for Lynch syndrome (hereditary nonpolyposis colorectal cancer) among endometrial cancer patients. Cancer Res 66(15):7810-7817 (Pubitemid 44289242)
5. Dinh TA, Rosner BI, Atwood JC, Boland CR, Syngal S, Vasen HF, Gruber SB, Burt RW (2011) Health benefits and cost-effectiveness of primary genetic screening for Lynch syndrome in the general population. Cancer Prev Res (Phila) 4(1):9-22
6. Ladabaum U, Wang G, Terdiman J, Blanco A, Kuppermann M, Boland CR, Ford J, Elkin E, Phillips KA (2011) Strategies to identify the Lynch syndrome among patients with colorectal cancer: a cost-effectiveness analysis. Ann Intern Med 155(2):69-79
7. Win AK, Lindor NM, Winship I, Tucker KM, Buchanan DD, Young JP, Rosty C, Leggett B, Giles GG, Goldblatt J, Macrae FA, Parry S, Kalady MF, Baron JA, Ahnen DJ, Marchand LL, Gallinger S, Haile RW, Newcomb PA, Hopper JL, Jenkins MA (2013) Risks of colorectal and other cancers after endometrial cancer for women with Lynch syndrome. J Natl Cancer Inst 105(4):274-279
8. Jarvinen HJ, Aarnio M (2000) Surveillance on mutation carriers of DNA mismatch repair genes. Ann Chir Gynaecol 89(3):207-210
9. Stupart DA, Goldberg PA, Algar U, Ramesar R (2009) Surveillance colonoscopy improves survival in a cohort of subjects with a single mismatch repair gene mutation. Colorectal Dis 11(2):126-130
10. de Jong AE, Hendriks YM, Kleibeuker JH, de Boer SY, Cats A, Griffioen G, Nagengast FM, Nelis FG, Rookus MA, Vasen HF (2006) Decrease in mortality in Lynch syndrome families because of surveillance. Gastroenterology 130(3):665-671 (Pubitemid 43374516)
11. Villella JA, Parmar M, Donohue K, Fahey C, Piver MS, Rodabaugh K (2006) Role of prophylactic hysterectomy in patients at high risk for hereditary cancers. Gynecol Oncol 102(3):475-479 (Pubitemid 44353643)
12. Natarajan N, Watson P, Silva-Lopez E, Lynch HT (2010) Comparison of extended colectomy and limited resection in patients with Lynch syndrome. Dis Colon Rectum 53(1):77-82
13. Hampel H, Frankel WL, Martin E, Arnold M, Khanduja K, Kuebler P, Nakagawa H, Sotamaa K, Prior TW, Westman J, Panescu J, Fix D, Lockman J, Comeras I, de la Chapelle A (2005) Screening for the Lynch syndrome (hereditary nonpolyposis colorectal cancer). N Engl J Med 352(18):1851-1860
14. Gylling A, Ridanpaa M, Vierimaa O, Aittomaki K, Avela K, Kaariainen H, Laivuori H, Poyhonen M, Sallinen SL, Wallgren-Pettersson C, Jarvinen HJ, Mecklin JP, Peltomaki P (2009) Large genomic rearrangements and germline epimutations in Lynch syndrome. Int J Cancer 124(10):2333-2340
15. Chan TL, Yuen ST, Kong CK, Chan YW, Chan AS, Ng WF, Tsui WY, Lo MW, Tam WY, Li VS, Leung SY (2006) Heritable germline epimutation of MSH2 in a family with hereditary nonpolyposis colorectal cancer. Nat Genet 38(10):1178-1183 (Pubitemid 44470364)
16. Lagerstedt Robinson K, Liu T, Vandrovcova J, Halvarsson B, Clendenning M, Frebourg T, Papadopoulos N, Kinzler KW, Vogelstein B, Peltomaki P, Kolodner RD, Nilbert M, Lindblom A (2007) Lynch syndrome (hereditary nonpolyposis colorectal cancer) diagnostics. J Natl Cancer Inst 99(4):291-299 (Pubitemid 47073492)
17. Heald B, Plesec T, Liu X, Pai R, Patil D, Moline J, Sharp RR, Burke CA, Kalady MF, Church J, Eng C (2013) Implementation of universal microsatellite instability and immunohistochemistry screening for diagnosing Lynch syndrome in a large academic medical center. J Clin Oncol 31(10):1336-1340
18. Cunningham JM, Christensen ER, Tester DJ, Kim CY, Roche PC, Burgart LJ, Thibodeau SN (1998) Hypermethylation of the hMLH1 promoter in colon cancer with microsatellite instability. Cancer Res 58(15):3455-3460 (Pubitemid 28371090)
19. Gurin CC, Federici MG, Kang L, Boyd J (1999) Causes and consequences of microsatellite instability in endometrial carcinoma. Cancer Res 59(2):462-466 (Pubitemid 29048884)
20. Domingo E, Laiho P, Ollikainen M, Pinto M, Wang L, French AJ, Westra J, Frebourg T, Espin E, Armengol M, Hamelin R, Yamamoto H, Hofstra RM, Seruca R, Lindblom A, Peltomaki P, Thibodeau SN, Aaltonen LA, Schwartz S Jr (2004) BRAF screening as a low-cost effective strategy for simplifying HNPCC genetic testing. J Med Genet 41(9):664-668 (Pubitemid 39208606)
21. Cossio SL, Koehler-Santos P, Pessini SA, Monego H, Edelweiss MI, Meurer L, Errami A, Coffa J, Bock H, Saraiva-Pereira ML, Ashton-Prolla P, Prolla JC (2010) Clinical and histomolecular endometrial tumor characterization of patients at-risk for Lynch syndrome in South of Brazil. Fam Cancer 9(2):131-139
22. Pijnenborg JM, Dam-de Veen GC, de Haan J, van Engeland M, Groothuis PG (2004) Defective mismatch repair and the development of recurrent endometrial carcinoma. Gynecol Oncol 94(2):550-559 (Pubitemid 39024566)
23. Furlan D, Carnevali I, Marcomini B, Cerutti R, Dainese E, Capella C, Riva C (2006) The high frequency of de novo promoter methylation in synchronous primary endometrial and ovarian carcinomas. Clin Cancer Res 12(11 Pt 1):3329-3336
24. Broaddus RR, Lynch HT, Chen LM, Daniels MS, Conrad P, Munsell MF, White KG, Luthra R, Lu KH (2006) Pathologic features of endometrial carcinoma associated with HNPCC: a comparison with sporadic endometrial carcinoma. Cancer 106(1):87-94 (Pubitemid 43032552)
25. Deng G, Chen A, Hong J, Chae HS, Kim YS (1999) Methylation of CpG in a small region of the hMLH1 promoter invariably correlates with the absence of gene expression. Cancer Res 59(9):2029-2033 (Pubitemid 29217657)
26. Feng YZ, Shiozawa T, Miyamoto T, Kashima H, Kurai M, Suzuki A, Konishi I (2005) BRAF mutation in endometrial carcinoma and hyperplasia: correlation with KRAS and p53 mutations and mismatch repair protein expression. Clin Cancer Res 11(17):6133-6138 (Pubitemid 41262939)
27. McConechy MK, Ding J, Cheang MC, Wiegand KC, Senz J, Tone AA, Yang W, Prentice LM, Tse K, Zeng T, McDonald H, Schmidt AP, Mutch DG, McAlpine JN, Hirst M, Shah SP, Lee CH, Goodfellow PJ, Gilks CB, Huntsman DG (2012) Use of mutation profiles to refine the classification of endometrial carcinomas. J Pathol 228(1):20-30
28. Mutch DG, Powell MA, Mallon MA, Goodfellow PJ (2004) RAS/RAF mutation and defective DNA mismatch repair in endometrial cancers. Am J Obstet Gynecol 190(4):935-942 (Pubitemid 38561508)
29. Joensuu EI, Abdel-Rahman WM, Ollikainen M, Ruosaari S, Knuutila S, Peltomaki P (2008) Epigenetic signatures of familial cancer are characteristic of tumor type and family category. Cancer Res 68(12):4597-4605
30. Yoon SN, Ku JL, Shin YK, Kim KH, Choi JS, Jang EJ, Park HC, Kim DW, Kim MA, Kim WH, Lee TS, Kim JW, Park NH, Song YS, Kang SB, Lee HP, Jeong SY, Park JG (2008) Hereditary nonpolyposis colorectal cancer in endometrial cancer patients. Int J Cancer 122(5):1077-1081 (Pubitemid 351214005)
31. Salvesen HB, MacDonald N, Ryan A, Iversen OE, Jacobs IJ, Akslen LA, Das S (2000) Methylation of hMLH1 in a population-based series of endometrial carcinomas. Clin Cancer Res 6(9):3607-3613
32. Kanaya T, Kyo S, Sakaguchi J, Maida Y, Nakamura M, Takakura M, Hashimoto M, Mizumoto Y, Inoue M (2005) Association of mismatch repair deficiency with PTEN frameshift mutations in endometrial cancers and the precursors in a Japanese population. Am J Clin Pathol 124(1):89-96 (Pubitemid 40944379)
33. Peterson LM, Kipp BR, Halling KC, Kerr SE, Smith DI, Distad TJ, Clayton AC, Medeiros F (2012) Molecular characterization of endometrial cancer: a correlative study assessing microsatellite instability, MLH1 hypermethylation, DNA mismatch repair protein expression, and PTEN, PIK3CA, KRAS, and BRAF mutation analysis. Int J Gynecol Pathol 31(3):195-205
34. Klarskov L, Ladelund S, Holck S, Roenlund K, Lindebjerg J, Elebro J, Halvarsson B, von Salome J, Bernstein I, Nilbert M (2010) Interobserver variability in the evaluation of mismatch repair protein immunostaining. Hum Pathol 41(10):1387-1396
35. Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, Teague J, Woffendin H, Garnett MJ, Bottomley W, Davis N, Dicks E, Ewing R, Floyd Y, Gray K, Hall S, Hawes R, Hughes J, Kosmidou V, Menzies A, Mould C, Parker A, Stevens C, Watt S, Hooper S, Wilson R, Jayatilake H, Gusterson BA, Cooper C, Shipley J, Hargrave D, Pritchard-Jones K, Maitland N, Chenevix-Trench G, Riggins GJ, Bigner DD, Palmieri G, Cossu A, Flanagan A, Nicholson A, Ho JW, Leung SY, Yuen ST, Weber BL, Seigler HF, Darrow TL, Paterson H, Marais R, Marshall CJ, Wooster R, Stratton MR, Futreal PA (2002) Mutations of the BRAF gene in human cancer. Nature 417(6892):949-954 (Pubitemid 34716871)
36. Chakraborty A, Narkar A, Mukhopadhyaya R, Kane S, D'Cruz A, Rajan MG (2012) BRAF V600E mutation in papillary thyroid carcinoma: significant association with node metastases and extra thyroidal invasion. Endocr Pathol 23(2):83-93
37. Forbes SA, Bindal N, Bamford S, Cole C, Kok CY, Beare D, Jia M, Shepherd R, Leung K, Menzies A, Teague JW, Campbell PJ, Stratton MR, Futreal PA (2011) COSMIC: mining complete cancer genomes in the catalogue of somatic mutations in cancer. Nucleic Acids Res 39(Database issue):D945-D950
38. Parsons MT, Buchanan DD, Thompson B, Young JP, Spurdle AB (2012) Correlation of tumour BRAF mutations and MLH1 methylation with germline mismatch repair (MMR) gene mutation status: a literature review assessing utility of tumour features for MMR variant classification. J Med Genet 49(3):151-157
39. Moreno-Bueno G, Sanchez-Estevez C, Palacios J, Hardisson D, Shiozawa T (2006) Low frequency of BRAF mutations in endometrial and in cervical carcinomas. Clin Cancer Res 12(12):3865, author reply 3865-3866
40. Peiro G, Peiro FM, Ortiz-Martinez F, Planelles M, Sanchez-Tejada L, Alenda C, Ceballos S, Sanchez-Paya J, Laforga JB (2013) Association of mammalian target of rapamycin with aggressive type II endometrial carcinomas and poor outcome: a potential target treatment. Hum Pathol 44(2):218-225
41. Beadling C, Heinrich MC, Warrick A, Forbes EM, Nelson D, Justusson E, Levine J, Neff TL, Patterson J, Presnell A, McKinley A, Winter LJ, Dewey C, Harlow A, Barney O, Druker BJ, Schuff KG, Corless CL (2011) Multiplex mutation screening by mass spectrometry evaluation of 820 cases from a personalized cancer medicine registry. J Mol Diagn 13(5):504-513
42. Kawaguchi M, Yanokura M, Banno K, Kobayashi Y, Kuwabara Y, Kobayashi M, Nomura H, Hirasawa A, Susumu N, Aoki D (2009) Analysis of a correlation between the BRAF V600E mutation and abnormal DNA mismatch repair in patients with sporadic endometrial cancer. Int J Oncol 34(6):1541-1547
43. Mizumoto Y, Kyo S, Mori N, Sakaguchi J, Ohno S, Maida Y, Hashimoto M, Takakura M, Inoue M (2007) Activation of ERK1/2 occurs independently of KRAS or BRAF status in endometrial cancer and is associated with favorable prognosis. Cancer Sci 98(5):652-658 (Pubitemid 46563440)
44. He M, Breese V, Hang S, Zhang C, Xiong J, Jackson C (2013) BRAF V600E Mutations in Endometrial Adenocarcinoma. Diagn Mol Pathol 22(1):35-40
45. Jalloul RJ, Elshaikh MA, Ali-Fehmi R, Haley MM, Yoon J, Mahan M, Munkarah AR (2012) Mucinous adenocarcinoma of the endometrium: case series and review of the literature. Int J Gynecol Cancer 22(5):812-818
46. Tavassoli FA, Devilee P (2003) Pathology and genetics of tumours of the breast and female genital organs. WHO classification of tumours. IARC Press, Lyon
47. Helmle KE, Otto CJ, Constantinescu G, Honore LH, Andrew SE (2005) Variable MLH1 promoter methylation patterns in endometrial carcinomas of endometrioid subtype lacking DNA mismatch repair. Int J Gynecol Cancer 15(6):1089-1096 (Pubitemid 43110157)
48. Varley KE, Mutch DG, Edmonston TB, Goodfellow PJ, Mitra RD (2009) Intra-tumor heterogeneity of MLH1 promoter methylation revealed by deep single molecule bisulfite sequencing. Nucleic Acids Res 37(14):4603-4612
49. Bouzourene H, Taminelli L, Chaubert P, Monnerat C, Seelentag W, Sandmeier D, Andrejevic S, Matter M, Bosman F, Benhattar J (2006) A cost-effective algorithm for hereditary nonpolyposis colorectal cancer detection. Am J Clin Pathol 125(6):823-831 (Pubitemid 43801531)
50. Yan HL, Hao LQ, Jin HY, Xing QH, Xue G, Mei Q, He J, He L, Sun SH (2008) Clinical features and mismatch repair genes analyses of Chinese suspected hereditary non-polyposis colorectal cancer: a cost-effective screening strategy proposal. Cancer Sci 99(4):770-780 (Pubitemid 351448082)
51. Perez-Carbonell L, Alenda C, Paya A, Castillejo A, Barbera VM, Guillen C, Rojas E, Acame N, Gutierrez-Avino FJ, Castells A, Llor X, Andreu M, Soto JL, Jover R (2010) Methylation analysis of MLH1 improves the selection of patients for genetic testing in Lynch syndrome. J Mol Diagn 12(4):498-504
52. Gausachs M, Mur P, Corral J, Pineda M, Gonzalez S, Benito L, Menendez M, Espinas JA, Brunet J, Iniesta MD, Gruber SB, Lazaro C, Blanco I, Capella G (2012) MLH1 promoter hypermethylation in the analytical algorithm of Lynch syndrome: a cost-effectiveness study. Eur J Hum Genet 20(7):762-768
53. Bosse T, Ter Haar NT, Seeber LM, Diest PJ, Hes FJ, Vasen HF, Nout RA, Creutzberg CL, Morreau H, Smit VT (2013) Loss of ARID1A expression and its relationship with PI3K-Akt pathway alterations, TP53 and microsatellite instability in endometrial cancer. Mod Pathol. doi:10.1038/modpathol.2013.96
54. Kandoth C, Schultz N, Cherniack AD, Akbani R, Liu Y, Shen H, Robertson AG, Pashtan I, Shen R, Benz CC, Yau C, Laird PW, Ding L, Zhang W, Mills GB, Kucherlapati R, Mardis ER, Levine DA (2013) Integrated genomic characterization of endometrial carcinoma. Nature 497(7447):67-73
55. Salvesen HB, Kumar R, Stefansson I, Angelini S, MacDonald N, Smeds J, Jacobs IJ, Hemminki K, Das S, Akslen LA (2005) Low frequency of BRAF and CDKN2A mutations in endometrial cancer. Int J Cancer 115(6):930-934 (Pubitemid 40791834)
56. Pappa KI, Choleza M, Markaki S, Giannikaki E, Kyroudi A, Vlachos G, Voulgaris Z, Anagnou NP (2006) Consistent absence of BRAF mutations in cervical and endometrial cancer despite KRAS mutation status. Gynecol Oncol 100(3):596-600 (Pubitemid 43246877)
57. Kang S, Lee JM, Jeon ES, Lee S, Kim H, Kim HS, Seo SS, Park SY, Sidransky D, Dong SM (2006) RASSF1A hypermethylation and its inverse correlation with BRAF and/or KRAS mutations in MSI-associated endometrial carcinoma. Int J Cancer 119(6):1316-1321 (Pubitemid 44258806)
58. Pijnenborg JM, Dam-de Veen GC, Kisters N, Delvoux B, van Engeland M, Herman JG, Groothuis PG (2007) RASSF1A methylation and K-ras and B-raf mutations and recurrent endometrial cancer. Ann Oncol 18(3):491-497 (Pubitemid 46359628)
59. Stewart CJ, Amanuel B, Grieu F, Carrello A, Iacopetta B (2010) KRAS mutation and microsatellite instability in endometrial adenocarcinomas showing MELF-type myometrial invasion. J Clin Pathol 63(7):604-608
60. Janku F, Tsimberidou AM, Garrido-Laguna I, Wang X, Luthra R, Hong DS, Naing A, Falchook GS, Moroney JW, Piha-Paul SA, Wheler JJ, Moulder SL, Fu S, Kurzrock R (2011) PIK3CA mutations in patients with advanced cancers treated with PI3 K/AKT/mTOR axis inhibitors. Mol Cancer Ther 10(3):558-565
61. Gonzalez-Bosquet J, Calcei J, Wei JS, Garcia-Closas M, Sherman ME, Hewitt S, Vockley J, Lissowska J, Yang HP, Khan J, Chanock S (2011) Detection of somatic mutations by high-resolution DNA melting (HRM) analysis in multiple cancers. PLoS ONE 6(1):e14522
62. Deqin M, Chen Z, Nero C, Patel KP, Daoud EM, Cheng H, Djordjevic B, Broaddus RR, Medeiros LJ, Rashid A, Luthra R (2012) Somatic deletions of the polyA tract in the 3′ untranslated region of epidermal growth factor receptor are common in microsatellite instability-high endometrial and colorectal carcinomas. Arch Pathol Lab Med 136(5):510-516
63. Garcia-Dios DA, Lambrechts D, Coenegrachts L, Vandenput I, Capoen A, Webb PM, Ferguson K, ANECS, Akslen LA, Claes B, Vergote I, Moerman P, Van Robays J, Marcickiewicz J, Salvesen HB, Spurdle AB, Amant F (2013) High-throughput interrogation of PIK3CA, PTEN, KRAS, FBXW7 and TP53 mutations in primary endometrial carcinoma. Gynecol Oncol 128(2):327-334
64. Strazzullo M, Cossu A, Baldinu P, Colombino M, Satta MP, Tanda F, De Bonis ML, Cerase A, D'Urso M, D'Esposito M, Palmieri G (2003) High-resolution methylation analysis of the hMLH1 promoter in sporadic endometrial and colorectal carcinomas. Cancer 98(7):1540-1546 (Pubitemid 37151511)
65. Walsh MD, Cummings MC, Buchanan DD, Dambacher WM, Arnold S, McKeone D, Byrnes R, Barker MA, Leggett BA, Gattas M, Jass JR, Spurdle AB, Young J, Obermair A (2008) Molecular, pathologic, and clinical features of early-onset endometrial cancer: identifying presumptive Lynch syndrome patients. Clin Cancer Res 14(6):1692-1700 (Pubitemid 351469453)