Prognostic relevance of aberrant DNA methylation in G1 and G2 pancreatic neuroendocrine tumors

Neuroendocrinology

Volumn 100, Issue 1, 2014, Pages 26-34

  Stefanoli, Michele ^a   La Rosa, Stefano ^a   Sahnane, Nora ^a   Romualdi, Chiara ^b   Pastorino, Roberta ^c   Marando, Alessandro ^a   Capella, Carlo ^a   Sessa, Fausto ^a   Furlan, Daniela ^a  

^a UNIVERSITY OF INSUBRIA   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

^c UNIVERSITY OF PAVIA   (Italy)

Author keywords

Copy number alterations; DNA hypermethylation; LINE 1 hypomethylation; Pancreatic neuroendocrine tumors

Indexed keywords

ADULT; AGED; ARTICLE; CANCER DIAGNOSIS; CANCER GRADING; CANCER MORTALITY; CANCER PROGNOSIS; CANCER RECURRENCE; CANCER STAGING; DIAGNOSTIC TEST ACCURACY STUDY; DNA METHYLATION; FEMALE; GENE DOSAGE; HUMAN; LONG INTERSPERSED REPEAT; MAJOR CLINICAL STUDY; MALE; MULTIPLEX LIGATION DEPENDENT PROBE AMPLIFICATION; PANCREATIC NEUROENDOCRINE TUMOR; PYROSEQUENCING; TUMOR CLASSIFICATION; TUMOR SUPPRESSOR GENE; TUMOR VOLUME; ADOLESCENT; CLUSTER ANALYSIS; COPY NUMBER VARIATION; GENETICS; KAPLAN MEIER METHOD; MIDDLE AGED; NEUROENDOCRINE TUMORS; PANCREATIC NEOPLASMS; PATHOLOGY; PROGNOSIS; RECEIVER OPERATING CHARACTERISTIC; SENSITIVITY AND SPECIFICITY; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; CLUSTER ANALYSIS; DNA COPY NUMBER VARIATIONS; DNA METHYLATION; FEMALE; HUMANS; KAPLAN-MEIER ESTIMATE; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; MALE; MIDDLE AGED; NEOPLASM STAGING; NEUROENDOCRINE TUMORS; PANCREATIC NEOPLASMS; PROGNOSIS; ROC CURVE; SENSITIVITY AND SPECIFICITY; YOUNG ADULT;

EID: 84912572968     PISSN: 00283835     EISSN: 14230194     Source Type: Journal    
DOI: 10.1159/000365449     Document Type: Article

References (46)

1. Jiao Y, Shi C, Edil BH, de Wilde RF, Klimstra DS, Maitra A, Schulick RD, Tang LH, Wolfgang CL, Choti MA, Velculescu VE, Diaz LA Jr, Vogelstein B, Kinzler KW, Hruban RH, Papadopoulos N: DAXX/ATRX, MEN1, and mTOR pathway genes are frequently altered in pancreatic neuroendocrine tumors. Science 2011; 331: 1199-1203.
2. Arnold CN, Nagasaka T, Goel A, Scharf I, Grabowski P, Sosnowski A, Schmitt-Graff A, Boland CR, Arnold R, Blum HE: Molecular characteristics and predictors of survival in patients with malignant neuroendocrine tumors. Int J Cancer 2008; 123: 1556-1564.
3. Arnold CN, Sosnowski A, Schmitt-Graff A, Arnold R, Blum HE: Analysis of molecular pathways in sporadic neuroendocrine tumors of the gastro-entero-pancreatic system. Int J Cancer 2007; 120: 2157-2164.
4. Malpeli G, Amato E, Dandrea M, Fumagalli C, Debattisti V, Boninsegna L, Pelosi G, Falconi M, Scarpa A: Methylation-associated down-regulation of RASSF1A and upregulation of RASSF1C in pancreatic endocrine tumors. BMC Cancer 2011; 11: 351.
5. Pizzi S, Azzoni C, Bottarelli L, Campanini N, D'Adda T, Pasquali C, Rossi G, Rindi G, Bordi C: RASSF1A promoter methylation and 3p21.3 loss of heterozygosity are features of foregut, but not midgut and hindgut, malignant endocrine tumours. J Pathol 2005; 206: 409-416.
6. House MG, Herman JG, Guo MZ, Hooker CM, Schulick RD, Lillemoe KD, Cameron JL, Hruban RH, Maitra A, Yeo CJ: Aberrant hypermethylation of tumor suppressor genes in pancreatic endocrine neoplasms. Ann Surg 2003; 238: 423-431.
7. Baylin SB, Herman JG: DNA hypermethylation in tumorigenesis: Epigenetics joins genetics. Trends Genet 2000; 16: 168-174.
8. Chan AO, Kim SG, Bedeir A, Issa JP, Hamilton SR, Rashid A: CpG island methylation in carcinoid and pancreatic endocrine tumors. Oncogene 2003; 22: 924-934.
9. Schmitt AM, Schmid S, Rudolph T, Anlauf M, Prinz C, Kloppel G, Moch H, Heitz PU, Komminoth P, Perren A: VHL inactivation is an important pathway for the development of malignant sporadic pancreatic endocrine tumors. Endocr Relat Cancer 2009; 16: 1219-1227.
10. Choi IS, Estecio MR, Nagano Y, Kim do H, White JA, Yao JC, Issa JP, Rashid A: Hypomethylation of LINE-1 and Alu in well-differentiated neuroendocrine tumors (pancreatic endocrine tumors and carcinoid tumors) . Mod Pathol 2007; 20: 802-810.
11. Stricker I, Tzivras D, Nambiar S, Wulf J, Liffers ST, Vogt M, Verdoodt B, Tannapfel A, Mirmohammadsadegh A: Site-and grade-specific diversity of LINE1 methylation pattern in gastroenteropancreatic neuroendocrine tumours. Anticancer Res 2012; 32: 3699-3706.
12. Deng G, Nguyen A, Tanaka H, Matsuzaki K, Bell I, Mehta KR, Terdiman JP, Waldman FM, Kakar S, Gum J, Crawley S, Sleisenger MH, Kim YS: Regional hypermethylation and global hypomethylation are associated with altered chromatin conformation and histone acetylation in colorectal cancer. Int J Cancer 2006; 118: 2999-3005.
13. Matsuzaki K, Deng G, Tanaka H, Kakar S, Miura S, Kim YS: The relationship between global methylation level, loss of heterozygosity, and microsatellite instability in sporadic colorectal cancer. Clin Cancer Res 2005; 11: 8564-8569.
14. Estecio MR, Gharibyan V, Shen L, Ibrahim AE, Doshi K, He R, Jelinek J, Yang AS, Yan PS, Huang TH, Tajara EH, Issa JP: LINE-1 hypomethylation in cancer is highly variable and inversely correlated with microsatellite instability. PLoS One 2007; 2: E399.
15. Frigola J, Sole X, Paz MF, Moreno V, Esteller M, Capella G, Peinado MA: Differential DNA hypermethylation and hypomethylation signatures in colorectal cancer. Hum Mol Genet 2005; 14: 319-326.
16. Ehrlich M: Cancer-linked DNA hypomethylation and its relationship to hypermethylation. Curr Top Microbiol Immunol 2006; 310: 251-274.
17. La Rosa S, Klersy C, Uccella S, Dainese L, Albarello L, Sonzogni A, Doglioni C, Capella C, Solcia E: Improved histologic and clinicopathologic criteria for prognostic evaluation of pancreatic endocrine tumors. Hum Pathol 2009; 40: 30-40.
18. Rindi G, Falconi M, Klersy C, Albarello L, Boninsegna L, Buchler MW, Capella C, Caplin M, Couvelard A, Doglioni C, Delle Fave G, Fischer L, Fusai G, de Herder WW, Jann H, Komminoth P, de Krijger RR, La Rosa S, Luong TV, Pape U, Perren A, Ruszniewski P, Scarpa A, Schmitt A, Solcia E, Wiedenmann B: TNM staging of neoplasms of the endocrine pancreas: Results from a large international cohort study. J Natl Cancer Inst 2012; 104: 764-777.
19. Rindi G, Kloppel G, Alhman H, Caplin M, Couvelard A, de Herder WW, Erikssson B, Falchetti A, Falconi M, Komminoth P, Korner M, Lopes JM, McNicol AM, Nilsson O, Perren A, Scarpa A, Scoazec JY, Wiedenmann B: TNM staging of foregut (neuro) endocrine tumors: A consensus proposal including a grading system. Virchows Arch 2006; 449: 395-401.
20. Van Dongen JJ, Langerak AW, Bruggemann M, Evans PA, Hummel M, Lavender FL, Delabesse E, Davi F, Schuuring E, Garcia-Sanz R, Van Krieken JH, Droese J, Gonzalez D, Bastard C, White HE, Spaargaren M, Gonzalez M, Parreira A, Smith JL, Morgan GJ, Kneba M, Macintyre EA: Design and standardization of PCR primers and protocols for detection of clonal immunoglobulin and T-cell receptor gene recombinations in suspect lymphoproliferations: Report of the BIOMED-2 concerted action BMH4-CT98-3936. Leukemia 2003; 17: 2257-2317.
21. Joensuu EI, Abdel-Rahman WM, Ollikainen M, Ruosaari S, Knuutila S, Peltomaki P: Epigenetic signatures of familial cancer are characteristic of tumor type and family category. Cancer Res 2008; 68: 4597-4605.
22. Verma M, Srivastava S: Epigenetics in cancer: Implications for early detection and prevention. Lancet Oncol 2002; 3: 755-763.
23. Laird PW: The power and the promise of DNA methylation markers. Nat Rev Cancer 2003; 3: 253-266.
24. La Rosa S, Marando A, Furlan D, Sahnane N, Capella C: Colorectal poorly differentiated neuroendocrine carcinomas and mixed adenoneuroendocrine carcinomas: Insights into the diagnostic immunophenotype, assessment of methylation profile, and search for prognostic markers. Am J Surg Pathol 2012; 36: 601-611.
25. Furlan D, Sahnane N, Mazzoni M, Pastorino R, Carnevali I, Stefanoli M, Ferretti A, Chiaravalli AM, La Rosa S, Capella C: Diagnostic utility of MS-MLPA in DNA methylation profiling of adenocarcinomas and neuroendocrine carcinomas of the colon-rectum. Virchows Arch 2013; 462: 47-56.
26. Homig-Holzel C, Savola S: Multiplex ligation-dependent probe amplification (MLPA) in tumor diagnostics and prognostics. Diagn Mol Pathol 2012; 21: 189-206.
27. Yang AS, Estecio MR, Doshi K, Kondo Y, Tajara EH, Issa JP: A simple method for estimating global DNA methylation using bisulfite PCR of repetitive DNA elements. Nucleic Acids Res 2004; 32: E38.
28. Raftery CF: Model-based clustering, discriminant analysis, and density estimation. J Am Stat Assoc 2002; 97: 611-631.
29. Schwarz G: Estimating the dimension of a model. Ann Stat 1978; 6: 461-464.
30. Baba Y, Huttenhower C, Nosho K, Tanaka N, Shima K, Hazra A, Schernhammer ES, Hunter DJ, Giovannucci EL, Fuchs CS, Ogino S: Epigenomic diversity of colorectal cancer indicated by LINE-1 methylation in a database of 869 tumors. Mol Cancer 2010; 9: 125.
31. Yachida S, Vakiani E, White CM, Zhong Y, Saunders T, Morgan R, de Wilde RF, Maitra A, Hicks J, Demarzo AM, Shi C, Sharma R, Laheru D, Edil BH, Wolfgang CL, Schulick RD, Hruban RH, Tang LH, Klimstra DS, Iacobuzio-Donahue CA: Small cell and large cell neuroendocrine carcinomas of the pancreas are genetically similar and distinct from welldifferentiated pancreatic neuroendocrine tumors. Am J Surg Pathol 2012; 36: 173-184.
32. Toyota M, Ahuja N, Ohe-Toyota M, Herman JG, Baylin SB, Issa JP: CpG island methylator phenotype in colorectal cancer. Proc Natl Acad Sci USA 1999; 96: 8681-8686.
33. Dejeux E, Olaso R, Dousset B, Audebourg A, Gut IG, Terris B, Tost J: Hypermethylation of the IgF2 differentially methylated region 2 is a specific event in insulinomas leading to lossof-imprinting and overexpression. Endocr Relat Cancer 2009; 16: 939-952.
34. Ehrlich M: DNA methylation in cancer: Too much, but also too little. Oncogene 2002; 21: 5400-5413.
35. Nosho K, Irahara N, Shima K, Kure S, Kirkner GJ, Schernhammer ES, Hazra A, Hunter DJ, Quackenbush J, Spiegelman D, Giovannucci EL, Fuchs CS, Ogino S: Comprehensive biostatistical analysis of CpG island methylator phenotype in colorectal cancer using a large population-based sample. PLoS One 2008; 3: E3698.
36. Eden A, Gaudet F, Waghmare A, Jaenisch R: Chromosomal instability and tumors promoted by DNA hypomethylation. Science 2003; 300: 455.
37. Roman-Gomez J, Jimenez-Velasco A, Agirre X, Castillejo JA, Navarro G, San Jose-Eneriz E, Garate L, Cordeu L, Cervantes F, Prosper F, Heiniger A, Torres A: Repetitive DNA hypomethylation in the advanced phase of chronic myeloid leukemia. Leuk Res 2008; 32: 487-490.
38. Gaudet F, Hodgson JG, Eden A, Jackson-Grusby L, Dausman J, Gray JW, Leonhardt H, Jaenisch R: Induction of tumors in mice by genomic hypomethylation. Science 2003; 300: 489-492.
39. Saito K, Kawakami K, Matsumoto I, Oda M, Watanabe G, Minamoto T: Long interspersed nuclear element-1 hypomethylation is a marker of poor prognosis in stage IA nonsmall cell lung cancer. Clin Cancer Res 2010; 16: 2418-2426.
40. Pattamadilok J, Huapai N, Rattanatanyong P, Vasurattana A, Triratanachat S, Tresukosol D, Mutirangura A: LINE-1 hypomethylation level as a potential prognostic factor for epithelial ovarian cancer. Int J Gynecol Cancer 2008; 18: 711-717.
41. Watanabe Y, Maekawa M: Methylation of DNA in cancer. Adv Clin Chem 2010; 52: 145-167.
42. Silver A, Sengupta N, Propper D, Wilson P, Hagemann T, Patel A, Parker A, Ghosh A, Feakins R, Dorudi S, Suraweera N: A distinct DNA methylation profile associated with microsatellite and chromosomal stable sporadic colorectal cancers. Int J Cancer 2012; 130: 1082-1092.
43. Toyota M, Suzuki H: Epigenetic drivers of genetic alterations. Adv Genet 2010; 70: 309-323.
44. Martinez JG, Perez-Escuredo J, Castro-Santos P, Marcos CA, Pendas JL, Fraga MF, Hermsen MA: Hypomethylation of LINE-1, and not centromeric SAT-a, is associated with centromeric instability in head and neck squamous cell carcinoma. Cell Oncol (Dordr) 2012; 35: 259-267.
45. Furlan D, Sahnane N, Bernasconi B, Frattini M, Tibiletti MG, Molinari F, Marando A, Zhang L, Vanoli A, Casnedi S, Adsay V, Notohara K, Albarello L, Asioli S, Sessa F, Capella C, La Rosa S: APC alterations are frequently involved in the pathogenesis of acinar cell carcinoma of the pancreas, mainly through gene loss and promoter hypermethylation. Virchows Arch 2014; 464: 553-564.
46. Stuppia L, Antonucci I, Palka G, Gatta V: Use of the MLPA assay in the molecular diagnosis of gene copy number alterations in human genetic diseases. Int J Mol Sci 2012; 13: 3245-3276.