LINE-1 hypomethylation status of circulating cell-free DNA in plasma as a biomarker for colorectal cancer

Oncotarget

Volumn 8, Issue 7, 2017, Pages 11906-11916

  Nagai, Yuzo ^a,b   Sunami, Eiji ^a   Yamamoto, Yoko ^a   Hata, Keisuke ^a   Okada, Satoshi ^a   Murono, Koji ^a   Yasuda, Koji ^a   Otani, Kensuke ^a   Nishikawa, Takeshi ^a   Tanaka, Toshiaki ^a   Kiyomatsu, Tomomichi ^a   Kawai, Kazushige ^a   Nozawa, Hiroaki ^a   Ishihara, Soichiro ^a   Hoon, Dave S B ^b   Watanabe, Toshiaki ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b JOHN WAYNE CANCER INSTITUTE   (United States)

Author keywords

Cell free DNA; Colorectal cancer; Hypomethylation; LINE 1; Plasma

Indexed keywords

CIRCULATING CELL-FREE DNA; DNA; UNCLASSIFIED DRUG; TUMOR MARKER;

ADULT; ADVANCED CANCER; ALLELE; ARTICLE; BLOOD LEVEL; CANCER GROWTH; CANCER PATIENT; CANCER SIZE; CANCER STAGING; CANCER TISSUE; CIRCULATING CELL-FREE DNA BLOOD LEVEL; COLORECTAL CANCER; CONTROLLED STUDY; DIAGNOSTIC TEST ACCURACY STUDY; DISTANT METASTASIS; DNA DETERMINATION; DNA METHYLATION; EARLY CANCER DIAGNOSIS; FEMALE; GENE DOSAGE; GENE EXPRESSION; GOLD STANDARD; HUMAN; HUMAN TISSUE; LONG INTERSPERSED NUCLEAR ELEMENT 1 HYPOMETHYLATION; MAJOR CLINICAL STUDY; MALE; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RECEIVER OPERATING CHARACTERISTIC; REFERENCE VALUE; RETROSPECTIVE STUDY; SENSITIVITY AND SPECIFICITY; BLOOD; COLORECTAL TUMOR; DISEASE EXACERBATION; GENETICS; LONG INTERSPERSED NUCLEAR ELEMENT; PATHOLOGY; PROGNOSIS;

ADULT; BIOMARKERS, TUMOR; COLORECTAL NEOPLASMS; DISEASE PROGRESSION; DNA METHYLATION; DNA, NEOPLASM; FEMALE; HUMANS; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; MALE; PROGNOSIS;

EID: 85012921650     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.14439     Document Type: Article

References (42)

1. Brenner H, Kloor M, Pox CP. Colorectal cancer. Lancet. 2014; 383: 1490-1502.
2. Crowley E, Di Nicolantonio F, Loupakis F, Bardelli A. Liquid biopsy: monitoring cancer-genetics in the blood. Nat Rev Clin Oncol. 2013; 10: 472-484.
3. Heitzer E, Ulz P, Geigl JB. Circulating tumor DNA as a liquid biopsy for cancer. Clin Chem. 2015; 61: 112-123.
4. Schwarzenbach H, Hoon DS, Pantel K. Cell-free nucleic acids as biomarkers in cancer patients. Nat Rev Cancer. 2011; 11: 426-437.
5. Heyn H, Esteller M. DNA methylation profiling in the clinic: applications and challenges. Nature Reviews Genetics. 2012; 13: 679-692.
6. Elbarbary RA, Lucas BA, Maquat LE. Retrotransposons as regulators of gene expression. Science. 2016; 351: aac7247.
7. Cordaux R, Batzer MA. The impact of retrotransposons on human genome evolution. Nat Rev Genet. 2009; 10: 691-703.
8. Antelo M, Balaguer F, Shia J, Shen Y, Hur K, Moreira L, Cuatrecasas M, Bujanda L, Giraldez MD, Takahashi M, Cabanne A, Barugel ME, et al. A high degree of LINE-1 hypomethylation is a unique feature of early-onset colorectal cancer. PLoS One. 2012; 7: e45357.
9. Ogino S, Nosho K, Kirkner GJ, Kawasaki T, Chan AT, Schernhammer ES, Giovannucci EL, Fuchs CS. A cohort study of tumoral LINE-1 hypomethylation and prognosis in colon cancer. J Natl Cancer Inst. 2008; 100: 1734-1738.
10. 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.
11. Rhee YY, Kim MJ, Bae JM, Koh JM, Cho NY, Juhnn YS, Kim D, Kang GH. Clinical outcomes of patients with microsatellite-unstable colorectal carcinomas depend on L1 methylation level. Ann Surg Oncol. 2012; 19: 3441-3448.
12. Sunami E, de Maat M, Vu A, Turner RR, Hoon DS. LINE-1 hypomethylation during primary colon cancer progression. PLoS One. 2011; 6: e18884.
13. van Hoesel AQ, van de Velde CJ, Kuppen PJ, Liefers GJ, Putter H, Sato Y, Elashoff DA, Turner RR, Shamonki JM, de Kruijf EM, van Nes JG, Giuliano AE, et al. Hypomethylation of LINE-1 in primary tumor has poor prognosis in young breast cancer patients: a retrospective cohort study. Breast Cancer Res Treat. 2012; 134: 1103-1114.
14. Bae JM, Shin SH, Kwon HJ, Park SY, Kook MC, Kim YW, Cho NY, Kim N, Kim TY, Kim D, Kang GH. ALU and LINE-1 hypomethylations in multistep gastric carcinogenesis and their prognostic implications. Int J Cancer. 2012; 131: 1323-1331.
15. Shigaki H, Baba Y, Watanabe M, Murata A, Iwagami S, Miyake K, Ishimoto T, Iwatsuki M, Baba H. LINE-1 hypomethylation in gastric cancer, detected by bisulfite pyrosequencing, is associated with poor prognosis. Gastric Cancer. 2013; 16: 480-487.
16. Hoshimoto S, Kuo CT, Chong KK, Takeshima TL, Takei Y, Li MW, Huang SK, Sim MS, Morton DL, Hoon DS. AIM1 and LINE-1 epigenetic aberrations in tumor and serum relate to melanoma progression and disease outcome. J Invest Dermatol. 2012; 132: 1689-1697.
17. Harada K, Baba Y, Ishimoto T, Chikamoto A, Kosumi K, Hayashi H, Nitta H, Hashimoto D, Beppu T, Baba H. LINE-1 methylation level and patient prognosis in a database of 208 hepatocellular carcinomas. Ann Surg Oncol. 2015; 22: 1280-1287.
18. Benard A, van de Velde CJ, Lessard L, Putter H, Takeshima L, Kuppen PJ, Hoon DS. Epigenetic status of LINE-1 predicts clinical outcome in early-stage rectal cancer. Br J Cancer. 2013; 109: 3073-3083.
19. Mima K, Nowak JA, Qian ZR, Cao Y, Song M, Masugi Y, Shi Y, da Silva A, Gu M, Li W, Hamada T, Zhang X, et al. Tumor LINE-1 methylation level and colorectal cancer location in relation to patient survival. Oncotarget. 2016. [Epub ahead of print]. doi: 10.18632/oncotarget.10398.
20. de Maat MF, Umetani N, Sunami E, Turner RR, Hoon DS. Assessment of methylation events during colorectal tumor progression by absolute quantitative analysis of methylated alleles. Mol Cancer Res. 2007; 5: 461-471.
21. Schisterman EF, Perkins NJ, Liu A, Bondell H. Optimal cutpoint and its corresponding Youden Index to discriminate individuals using pooled blood samples. Epidemiology. 2005; 16: 73-81.
22. Pox CP, Altenhofen L, Brenner H, Theilmeier A, Von Stillfried D, Schmiegel W. Efficacy of a nationwide screening colonoscopy program for colorectal cancer. Gastroenterology. 2012; 142: 1460-1467.
23. Kuipers EJ, Rosch T, Bretthauer M. Colorectal cancer screening-optimizing current strategies and new directions. Nat Rev Clin Oncol. 2013; 10: 130-142.
24. Hirai HW, Tsoi KK, Chan JY, Wong SH, Ching JY, Wong MC, Wu JC, Chan FK, Sung JJ, Ng SC. Systematic review with meta-analysis: faecal occult blood tests show lower colorectal cancer detection rates in the proximal colon in colonoscopy-verified diagnostic studies. Aliment Pharmacol Ther. 2016; 43: 755-764
25. Imperiale TF, Ransohoff DF, Itzkowitz SH, Levin TR, Lavin P, Lidgard GP, Ahlquist DA, Berger BM. Multitarget stool DNA testing for colorectal-cancer screening. N Engl J Med. 2014; 370: 1287-1297.
26. Chiu HM, Lee YC, Tu CH, Chen CC, Tseng PH, Liang JT, Shun CT, Lin JT, Wu MS. Association between early stage colon neoplasms and false-negative results from the fecal immunochemical test. Clin Gastroenterol Hepatol. 2013; 11: 832-838.
27. Smith RA, Andrews K, Brooks D, DeSantis CE, Fedewa SA, Lortet-Tieulent J, Manassaram-Baptiste D, Brawley OW, Wender RC. Cancer screening in the United States, 2016: A review of current American Cancer Society guidelines and current issues in cancer screening. CA Cancer J Clin. 2016; 66: 96-114.
28. von Wagner C, Baio G, Raine R, Snowball J, Morris S, Atkin W, Obichere A, Handley G, Logan RF, Rainbow S, Smith S, Halloran S, et al. Inequalities in participation in an organized national colorectal cancer screening programme: results from the first 2.6 million invitations in England. Int J Epidemiol. 2011; 40: 712-718.
29. Taber JM, Aspinwall LG, Heichman KA, Kinney AY. Preferences for blood-based colon cancer screening differ by race/ethnicity. Am J Health Behav. 2014; 38: 351-361.
30. Tanaka K, Okamoto A. Degradation of DNA by bisulfite treatment. Bioorg Med Chem Lett. 2007; 17: 1912-1915.
31. Church TR, Wandell M, Lofton-Day C, Mongin SJ, Burger M, Payne SR, Castanos-Velez E, Blumenstein BA, Rosch T, Osborn N, Snover D, Day RW, et al. Prospective evaluation of methylated SEPT9 in plasma for detection of asymptomatic colorectal cancer. Gut. 2014; 63: 317-325.
32. Nicholson BD, Shinkins B, Pathiraja I, Roberts NW, James TJ, Mallett S, Perera R, Primrose JN, Mant D. Blood CEA levels for detecting recurrent colorectal cancer. Cochrane Database Syst Rev. 2015: Cd011134.
33. Frattini M, Gallino G, Signoroni S, Balestra D, Lusa L, Battaglia L, Sozzi G, Bertario L, Leo E, Pilotti S, Pierotti MA. Quantitative and qualitative characterization of plasma DNA identifies primary and recurrent colorectal cancer. Cancer Lett. 2008; 263: 170-181.
34. Flamini E, Mercatali L, Nanni O, Calistri D, Nunziatini R, Zoli W, Rosetti P, Gardini N, Lattuneddu A, Verdecchia GM, Amadori D. Free DNA and carcinoembryonic antigen serum levels: an important combination for diagnosis of colorectal cancer. Clin Cancer Res. 2006; 12: 6985-6988.
35. Schwarzenbach H, Stoehlmacher J, Pantel K, Goekkurt E. Detection and monitoring of cell-free DNA in blood of patients with colorectal cancer. Ann N Y Acad Sci. 2008; 1137: 190-196.
36. Danese E, Montagnana M, Minicozzi AM, De Matteis G, Scudo G, Salvagno GL, Cordiano C, Lippi G, Guidi GC. Real-time polymerase chain reaction quantification of free DNA in serum of patients with polyps and colorectal cancers. Clin Chem Lab Med. 2010; 48: 1665-1668.
37. Ogino S, Kawasaki T, Nosho K, Ohnishi M, Suemoto Y, Kirkner GJ, Fuchs CS. LINE-1 hypomethylation is inversely associated with microsatellite instability and CpG island methylator phenotype in colorectal cancer. Int J Cancer. 2008; 122: 2767-2773.
38. Matsunoki A, Kawakami K, Kotake M, Kaneko M, Kitamura H, Ooi A, Watanabe G, Minamoto T. LINE-1 methylation shows little intra-patient heterogeneity in primary and synchronous metastatic colorectal cancer. BMC Cancer. 2012; 12: 574.
39. Baba Y, Murata A, Watanabe M, Baba H. Clinical implications of the LINE-1 methylation levels in patients with gastrointestinal cancer. Surg Today. 2014; 44: 1807-1816.
40. Terry MB, Delgado-Cruzata L, Vin-Raviv N, Wu HC, Santella RM. DNA methylation in white blood cells Association with risk factors in epidemiologic studies. Epigenetics. 2011; 6: 828-837.
41. Hoon DS, Spugnardi M, Kuo C, Huang SK, Morton DL, Taback B. Profiling epigenetic inactivation of tumor suppressor genes in tumors and plasma from cutaneous melanoma patients. Oncogene. 2004; 23: 4014-4022.
42. Yamashita S, Takahashi S, McDonell N, Watanabe N, Niwa T, Hosoya K, Tsujino Y, Shirai T, Ushijima T. Methylation silencing of transforming growth factor-beta receptor type II in rat prostate cancers. Cancer Res. 2008; 68: 2112-2121.