Colorectal cancer DNA methylation marker panel validated with high performance in Non-Hodgkin lymphoma

Epigenetics

Volumn 9, Issue 3, 2013, Pages 428-436

  Bethge, Nicole ^a,b   Lothe, Ragnhild A ^a,b   Honne, Hilde ^a,b   Andresen, Kim ^a,b   Trøen, Gunhild ^a   Eknæs, Mette ^a,b   Liestøl, Knut ^b   Holte, Harald ^b,c   Delabie, Jan ^a   Smeland, Erlend B ^a,b   Lind, Guro E ^a,b  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

^c OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

Biomarker; CNRIP1; Diagnosis; Epigenetic; Lymphoma; MAL; Methylation; Prognosis; SNCA; SPG20

Indexed keywords

BIOCHEMICAL MARKER; DNA; RITUXIMAB;

ADULT; AGED; ALPHA INTERNEXIN GENE; ALPHA SYNUCLEIN GENE; ARTICLE; CANNABINOID RECEPTOR INTERACTING PROTEIN 1 GENE; COLORECTAL CANCER; CONTROLLED STUDY; DNA METHYLATION; FEMALE; FIBRILLIN 1 GENE; GENE; GENE EXPRESSION; GENE LOCUS; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MONOTHERAPY; MYELIN AND LYMPHOCYTE PROTEIN GENE; NONHODGKIN LYMPHOMA; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; RECEIVER OPERATING CHARACTERISTIC; SENSITIVITY AND SPECIFICITY; SHORT TANDEM REPEAT; SPARTIN GENE; SURVIVAL; VALIDATION STUDY;

BIOMARKER; CNRIP1; DIAGNOSIS; EPIGENETIC; LYMPHOMA; MAL; METHYLATION; PROGNOSIS; SNCA; SPG20;

ADULT; AGED; AGED, 80 AND OVER; ALPHA-SYNUCLEIN; CASE-CONTROL STUDIES; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; DNA METHYLATION; FEMALE; HUMANS; LYMPHOMA, NON-HODGKIN; MALE; MIDDLE AGED; PROGNOSIS; PROMOTER REGIONS, GENETIC; PROTEINS; TUMOR MARKERS, BIOLOGICAL;

EID: 84899136511     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.27554     Document Type: Article

References (58)

1. American Cancer Society. Cancer Facts & Figures 2013. American Cancer Society. 2013
2. Seto M. Genetic and epigenetic factors involved in B-cell lymphomagenesis. Cancer Sci 2004; 95:704-10; PMID:15471554; http://dx.doi. org/10.1111/j.1349-7006.2004.tb03249.x
3. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144:646-74; PMID:21376230; http://dx.doi.org/10.1016/j. cell.2011.02.013
4. Shi H, Guo J, Duff DJ, Rahmatpanah F, Chitima-Matsiga R, Al-Kuhlani M, Taylor KH, Sjahputera O, Andreski M, Wooldridge JE, et al. Discovery of novel epigenetic markers in non-Hodgkin's lymphoma. Carcinogenesis 2007; 28:60-70; PMID:16774933; http://dx.doi.org/10.1093/carcin/bgl092
5. Esteller M. Profiling aberrant DNA methylation in hematologic neoplasms: a view from the tip of the iceberg. Clin Immunol 2003; 109:80-8; PMID:14585279; http://dx.doi.org/10.1016/ S1521-6616(03)00208-0
6. Harden SV, Sanderson H, Goodman SN, Partin AAW, Walsh PC, Epstein JI, Sidransky D. Quantitative GSTP1 methylation and the detection of prostate adenocarcinoma in sextant biopsies. J Natl Cancer Inst 2003; 95:1634-7; PMID:14600096; http://dx.doi.org/10.1093/jnci/djg082
7. Agathanggelou A, Cooper WN, Latif F. Role of the Ras-association domain family 1 tumor suppressor gene in human cancers. Cancer Res 2005; 65:3497-508; PMID:15867337; http://dx.doi. org/10.1158/0008-5472.CAN-04-4088
8. Hesson LB, Cooper WN, Latif F. The role of RASSF1A methylation in cancer. Dis Markers 2007; 23:73-87; PMID:17325427; http://dx.doi. org/10.1155/2007/291538
9. Lind GE, Danielsen SA, Ahlquist T, Merok MA, Andresen K, Skotheim RI, Hektoen M, Rognum TO, Meling GI, Hoff G, et al. Identification of an epigenetic biomarker panel with high sensitivity and specificity for colorectal cancer and adenomas. Mol Cancer 2011; 10:85; PMID:21777459; http://dx.doi. org/10.1186/1476-4598-10-85
10. Lind GE, Ahlquist T, Kolberg M, Berg M, Eknaes M, Alonso MA, Kallioniemi A, Meling GI, Skotheim RI, Rognum TO, et al. Hypermethylated MAL gene-a silent marker of early colon tumorigenesis. J Transl Med 2008; 6:13; PMID:18346269; http://dx.doi. org/10.1186/1479-5876-6-13
11. Lind GE, Raiborg C, Danielsen SA, Rognum TO, Thiis-Evensen E, Hoff G, Nesbakken A, Stenmark H, Lothe RA. SPG20, a novel biomarker for early detection of colorectal cancer, encodes a regulator of cytokinesis. Oncogene 2011; 30:3967-78; PMID:21499309; http://dx.doi.org/10.1038/ onc.2011.109
12. Copie-Bergman C, Gaulard P, Maouche-Chrétien L, Brière J, Haioun C, Alonso MA, Roméo PH, Leroy K. The MAL gene is expressed in primary mediastinal large B-cell lymphoma. Blood 1999; 94:3567-75; PMID:10552968
13. Pike BL, Greiner TC, Wang X, Weisenburger DD, Hsu YH, Renaud G, Wolfsberg TG, Kim M, Weisenberger DJ, Siegmund KD, et al. DNA methylation profiles in diffuse large B-cell lymphoma and their relationship to gene expression status. Leukemia 2008; 22:1035-43; PMID:18288132; http://dx.doi.org/10.1038/leu.2008.18
14. O'Riain C, O'Shea DM, Yang Y, Le Dieu R, Gribben JG, Summers K, Yeboah-Afari J, Bhaw-Rosun L, Fleischmann C, Mein CA, et al. Array-based DNA methylation profiling in follicular lymphoma. Leukemia 2009; 23:1858-66; PMID:19587707; http://dx.doi.org/10.1038/leu.2009.114
15. Wang XM, Greiner TC, Bibikova M, Pike BL, Siegmund KD, Sinha UK, Müschen M, Jaeger EB, Weisenburger DD, Chan WC, et al. Identification and functional relevance of de novo DNA methylation in cancerous B-cell populations. J Cell Biochem 2010; 109:818-27; PMID:20069569
16. Taylor KH, Kramer RS, Davis JW, Guo J, Duff DJ, Xu D, Caldwell CW, Shi H. Ultradeep bisulfite sequencing analysis of DNA methylation patterns in multiple gene promoters by 454 sequencing. Cancer Res 2007; 67:8511-8; PMID:17875690; http:// dx.doi.org/10.1158/0008-5472.CAN-07-1016
17. Daibata M, Nemoto Y, Bandobashi K, Kotani N, Kuroda M, Tsuchiya M, Okuda H, Takakuwa T, Imai S, Shuin T, et al. Promoter hypermethylation of the bone morphogenetic protein-6 gene in malignant lymphoma. Clin Cancer Res 2007; 13:3528-35; PMID:17575215; http://dx.doi.org/10.1158/1078-0432.CCR-06-2766
18. Eberth S, Schneider B, Rosenwald A, Hartmann EM, Romani J, Zaborski M, Siebert R, Drexler HG, Quentmeier H. Epigenetic regulation of CD44 in Hodgkin and non-Hodgkin lymphoma. BMC Cancer 2010; 10:517; PMID:20920234; http:// dx.doi.org/10.1186/1471-2407-10-517
19. Grønbaek K, Ralfkiaer U, Dahl C, Hother C, Burns JS, Kassem M, Worm J, Ralfkiaer EM, Knudsen LM, Hokland P, et al. Frequent hypermethylation of DBC1 in malignant lymphoproliferative neoplasms. Mod Pathol 2008; 21:632-8; PMID:18264085; http://dx.doi.org/10.1038/modpathol.2008.27
20. Hagiwara K, Nagai H, Li Y, Ohashi H, Hotta T, Saito H. Frequent DNA methylation but not mutation of the ID4 gene in malignant lymphoma. J Clin Exp Hematop 2007; 47:15-8; PMID:17510533; http:// dx.doi.org/10.3960/jslrt.47.15
21. Amara K, Trimeche M, Ziadi S, Laatiri A, Hachana M, Korbi S. Prognostic significance of aberrant promoter hypermethylation of CpG islands in patients with diffuse large B-cell lymphomas. Ann Oncol 2008; 19:1774-86; PMID:18539616; http:// dx.doi.org/10.1093/annonc/mdn374
22. Bennett LB, Schnabel JL, Kelchen JM, Taylor KH, Guo J, Arthur GL, Papageorgio CN, Shi H, Caldwell CW. DNA hypermethylation accompanied by transcriptional repression in follicular lymphoma. Genes Chromosomes Cancer 2009; 48:828-41; PMID:19530241; http://dx.doi.org/10.1002/ gcc.20687
23. Choi JH, Li Y, Guo J, Pei L, Rauch TA, Kramer RS, Macmil SL, Wiley GB, Bennett LB, Schnabel JL, et al. Genome-wide DNA methylation maps in follicular lymphoma cells determined by methylation-enriched bisulfite sequencing. PLoS One 2010; 5:e13020; PMID:20927367; http://dx.doi. org/10.1371/journal.pone.0013020
24. Shaknovich R, Geng H, Johnson NA, Tsikitas L, Cerchietti L, Greally JM, Gascoyne RD, Elemento O, Melnick A. DNA methylation signatures define molecular subtypes of diffuse large B-cell lymphoma. Blood 2010; 116:e81-9; PMID:20610814; http:// dx.doi.org/10.1182/blood-2010-05-285320
25. Lee SM, Lee EJ, Ko Y-H, Lee SH, Maeng L, Kim K-M. Prognostic significance of O6-methylguanine DNA methyltransferase and p57 methylation in patients with diffuse large B-cell lymphomas. APMIS 2009; 117:87-94; PMID:19239430; http://dx.doi. org/10.1111/j.1600-0463.2008.00017.x
26. Ying J, Li H, Murray P, Gao Z, Chen YW, Wang Y, Lee KY, Chan AT, Ambinder RF, Srivastava G, et al. Tumor-specific methylation of the 8p22 tumor suppressor gene DLC1 is an epigenetic biomarker for Hodgkin, nasal NK/T-cell and other types of lymphomas. Epigenetics 2007; 2:15-21; PMID:17965626; http://dx.doi.org/10.4161/ epi.2.1.3883
27. Seng TJ, Low JSW, Li H, Cui Y, Goh HK, Wong MLY, Srivastava G, Sidransky D, Califano J, Steenbergen RD, et al. The major 8p22 tumor suppressor DLC1 is frequently silenced by methylation in both endemic and sporadic nasopharyngeal, esophageal, and cervical carcinomas, and inhibits tumor cell colony formation. Oncogene 2007; 26:934-44; PMID:16862168; http://dx.doi.org/10.1038/ sj.onc.1209839
28. Low JSW, Tao Q, Ng KM, Goh HK, Shu XS, Woo WL, Ambinder RF, Srivastava G, Shamay M, Chan AT, et al. A novel isoform of the 8p22 tumor suppressor gene DLC1 suppresses tumor growth and is frequently silenced in multiple common tumors. Oncogene 2011; 30:1923-35; PMID:21217778; http://dx.doi.org/10.1038/onc.2010.576
29. Li Y, Nagai H, Ohno T, Yuge M, Hatano S, Ito E, Mori N, Saito H, Kinoshita T. Aberrant DNA methylation of p57(KIP2) gene in the promoter region in lymphoid malignancies of B-cell phenotype. Blood 2002; 100:2572-7; PMID:12239171; http:// dx.doi.org/10.1182/blood-2001-11-0026
30. Rosenwald A, Wright G, Leroy K, Yu X, Gaulard P, Gascoyne RD, Chan WC, Zhao T, Haioun C, Greiner TC, et al. Molecular diagnosis of primary mediastinal B cell lymphoma identifies a clinically favorable subgroup of diffuse large B cell lymphoma related to Hodgkin lymphoma. J Exp Med 2003; 198:851-62; PMID:12975453; http://dx.doi. org/10.1084/jem.20031074
31. Horne HN, Lee PS, Murphy SK, Alonso MA, Olson JA Jr., Marks JR. Inactivation of the MAL gene in breast cancer is a common event that predicts benefit from adjuvant chemotherapy. Mol Cancer Res 2009; 7:199-209; PMID:19208741; http://dx.doi. org/10.1158/1541-7786.MCR-08-0314
32. Hayslip J, Montero A. Tumor suppressor gene methylation in follicular lymphoma: a comprehensive review. Mol Cancer 2006; 5:44; PMID:17026765; http://dx.doi.org/10.1186/1476-4598-5-44
33. Tsai HC, Baylin SB. Cancer epigenetics: linking basic biology to clinical medicine. Cell Res 2011; 21:502-17; PMID:21321605; http://dx.doi.org/10.1038/ cr.2011.24
34. Guan H, Xie L, Leithäuser F, Flossbach L, Möller P, Wirth T, Ushmorov A. KLF4 is a tumor suppressor in B-cell non-Hodgkin lymphoma and in classic Hodgkin lymphoma. Blood 2010; 116:1469-78; PMID:20519630; http://dx.doi.org/10.1182/ blood-2009-12-256446
35. Yusuf I, Kharas MG, Chen J, Peralta RQ, Maruniak A, Sareen P, Yang VW, Kaestner KH, Fruman DA. KLF4 is a FOXO target gene that suppresses B cell proliferation. Int Immunol 2008; 20:671-81; PMID:18375530; http://dx.doi.org/10.1093/ intimm/dxn024
36. Kawano S, Miller CW, Gombart AF, Bartram CR, Matsuo Y, Asou H, Sakashita A, Said J, Tatsumi E, Koeffler HP. Loss of p73 gene expression in leukemias/lymphomas due to hypermethylation. Blood 1999; 94:1113-20; PMID:10419905
37. Nistala H, Lee-Arteaga S, Smaldone S, Siciliano G, Carta L, Ono RN, Sengle G, Arteaga-Solis E, Levasseur R, Ducy P, et al. Fibrillin-1 and-2 differentially modulate endogenous TGF-β and BMP bioavailability during bone formation. J Cell Biol 2010; 190:1107-21; PMID:20855508; http://dx.doi. org/10.1083/jcb.201003089
38. Wang Y, Yu Q, Cho AH, Rondeau G, Welsh J, Adamson E, Mercola D, McClelland M. Survey of differentially methylated promoters in prostate cancer cell lines. Neoplasia 2005; 7:748-60; PMID:16207477; http://dx.doi.org/10.1593/ neo.05289
39. Slater AA, Alokail M, Gentle D, Yao M, Kovacs G, Maher ER, Latif F. DNA methylation profiling distinguishes histological subtypes of renal cell carcinoma. Epigenetics 2013; 8:252-67; PMID:23428843; http://dx.doi.org/10.4161/ epi.23817
40. Yan PS, Venkataramu C, Ibrahim A, Liu JC, Shen RZ, Diaz NM, Centeno B, Weber F, Leu YW, Shapiro CL, et al. Mapping geographic zones of cancer risk with epigenetic biomarkers in normal breast tissue. Clin Cancer Res 2006; 12:6626-36; PMID:17121881; http://dx.doi.org/10.1158/1078-0432.CCR-06-0467
41. Matsumoto L, Takuma H, Tamaoka A, Kurisaki H, Date H, Tsuji S, Iwata A. CpG demethylation enhances alpha-synuclein expression and affects the pathogenesis of Parkinson's disease. PLoS One 2010; 5:e15522; PMID:21124796; http://dx.doi. org/10.1371/journal.pone.0015522
42. Jowaed A, Schmitt I, Kaut O, Wüllner U. Methylation regulates alpha-synuclein expression and is decreased in Parkinson's disease patients' brains. J Neurosci 2010; 30:6355-9; PMID:20445061; http://dx.doi. org/10.1523/JNEUROSCI.6119-09.2010
43. Sx A. Xu Q, Hu Yc, Song Cy, Guo Jf, Shen L et al. Hypomethylation of SNCA in blood of patients with sporadic Parkinson's disease. Journal of the Neurological Sciences 2013, ISSN 0022-510X.
44. Schimmack S, Lawrence B, Svejda B, Alaimo D, Schmitz-Winnenthal H, Fischer L, Büchler MW, Kidd M, Modlin I. The clinical implications and biologic relevance of neurofilament expression in gastroenteropancreatic neuroendocrine neoplasms. Cancer 2012; 118:2763-75; PMID:21990041; http:// dx.doi.org/10.1002/cncr.26592
45. Duffy MJ, Napieralski R, Martens JWM, Span PN, Spyratos F, Sweep FCGJ, Brunner N, Foekens JA, Schmitt M; EORTC PathoBiology Group. Methylated genes as new cancer biomarkers. Eur J Cancer 2009; 45:335-46; PMID:19138839; http:// dx.doi.org/10.1016/j.ejca.2008.12.008
46. Chim CS, Liang R, Tam CYY, Kwong YL. Methylation of p15 and p16 genes in acute promyelocytic leukemia: potential diagnostic and prognostic significance. J Clin Oncol 2001; 19:2033-40; PMID:11283136
47. Shiozawa E, Takimoto M, Makino R, Adachi D, Saito B, Yamochi-Onizuka T, Yamochi T, Shimozuma J, Maeda T, Kohno Y, et al. Hypermethylation of CpG islands in p16 as a prognostic factor for diffuse large B-cell lymphoma in a high-risk group. Leuk Res 2006; 30:859-67; PMID:16406514; http://dx.doi. org/10.1016/j.leukres.2005.11.004
48. Villuendas R, Sánchez-Beato M, Martínez JC, Saez AI, Martinez-Delgado B, García JF, Mateo MS, Sanchez-Verde L, Benítez J, Martínez P, et al. Loss of p16/INK4A protein expression in non-Hodgkin's lymphomas is a frequent finding associated with tumor progression. Am J Pathol 1998; 153:887-97; PMID:9736037; http://dx.doi.org/10.1016/ S0002-9440(10)65630-1
49. De S, Shaknovich R, Riester M, Elemento O, Geng H, Kormaksson M, Jiang Y, Woolcock B, Johnson N, Polo JM, et al. Aberration in DNA methylation in B-cell lymphomas has a complex origin and increases with disease severity. PLoS Genet 2013; 9:e1003137; PMID:23326238; http://dx.doi.org/10.1371/ journal.pgen.1003137
50. Lee GW, Kang JH, Kim IS, Kim HG, Ko GH, Lee JH, Kim DC, Song DH, Yang JW, Lee JS. Is inactivation of O6-methylguanine DNA methyltransferase still a favorable prognostic factor of patients with diffuse large B-cell lymphoma in the era of R-CHOP chemotherapy? Leuk Lymphoma 2009; 50:1992-8; PMID:19860620; http://dx.doi. org/10.3109/10428190903312462
51. Esteller M, Gaidano G, Goodman SN, Zagonel V, Capello D, Botto B, Rossi D, Gloghini A, Vitolo U, Carbone A, et al. Hypermethylation of the DNA repair gene O(6)-methylguanine DNA methyltransferase and survival of patients with diffuse large B-cell lymphoma. J Natl Cancer Inst 2002; 94:26-32; PMID:11773279; http://dx.doi. org/10.1093/jnci/94.1.26
52. Uccella S, Cerutti R, Placidi C, Marchet S, Carnevali I, Bernasconi B, Proserpio I, Pinotti G, Tibiletti MG, Furlan D, et al. MGMT methylation in diffuse large B-cell lymphoma: validation of quantitative methylation-specific PCR and comparison with MGMT protein expression. J Clin Pathol 2009; 62:715-23; PMID:19638543; http://dx.doi. org/10.1136/jcp.2009.064741
53. Sehn LH. Optimal use of prognostic factors in non-Hodgkin lymphoma. Hematology Am Soc Hematol Educ Program 2006; 295-302; PMID:17124075; http://dx.doi.org/10.1182/asheducation-2006.1.295
54. Kwong YL. Predicting the outcome in non-Hodgkin lymphoma with molecular markers. Br J Haematol 2007; 137:273-87; PMID:17408399; http://dx.doi. org/10.1111/j.1365-2141.2007.06571.x
55. Lübbert M, Rüter BH, Claus R, Schmoor C, Schmid M, Germing U, Kuendgen A, Rethwisch V, Ganser A, Platzbecker U, et al. A multicenter phase II trial of decitabine as first-line treatment for older patients with acute myeloid leukemia judged unfit for induction chemotherapy. Haematologica 2012; 97:393-401; PMID:22058219; http://dx.doi. org/10.3324/haematol.2011.048231
56. Fenaux P, Mufti GJ, Hellstrom-Lindberg E, Santini V, Finelli C, Giagounidis A, Schoch R, Gattermann N, Sanz G, List A, et al.; International Vidaza High-Risk MDS Survival Study Group. Efficacy of azacitidine compared with that of conventional care regimens in the treatment of higher-risk myelodysplastic syndromes: a randomised, open-label, phase III study. Lancet Oncol 2009; 10:223-32; PMID:19230772; http://dx.doi.org/10.1016/S1470-2045(09)70003-8
57. Schoofs T, Müller-Tidow C. DNA methylation as a pathogenic event and as a therapeutic target in AML. Cancer Treat Rev 2011; 37(Suppl 1):S13-8; PMID:21612874; http://dx.doi.org/10.1016/j. ctrv.2011.04.013
58. Weisenberger DJ, Campan M, Long TI, Kim M, Woods C, Fiala E, Ehrlich M, Laird PW. Analysis of repetitive element DNA methylation by MethyLight. Nucleic Acids Res 2005; 33:6823-36; PMID:16326863; http://dx.doi.org/10.1093/nar/ gki987