Cancer Epidemiology
Volume 34, Issue 2 , Pages 194-199 , April 2010

Immunoprecipitation of nucleosomal DNA is a novel procedure to improve the sensitivity of serum screening for the p16 hypermethylation associated with colon cancer

  • Jun Sakamoto

      Affiliations

    • Division of Gastroenterology and Hematology/Oncology, Department of Medicine, Asahikawa Medical College, 2-1-1-1, Midorigaoka-Higashi, Asahikawa, Hokkaido 078-8510, Japan
  • ,
  • Mikihiro Fujiya

      Affiliations

    • Division of Gastroenterology and Hematology/Oncology, Department of Medicine, Asahikawa Medical College, 2-1-1-1, Midorigaoka-Higashi, Asahikawa, Hokkaido 078-8510, Japan
    • Corresponding Author InformationCorresponding author. Tel.: +81 166 68 2462; fax: +81 166 68 2469.
  • ,
  • Kotaro Okamoto

      Affiliations

    • Division of Gastroenterology and Hematology/Oncology, Department of Medicine, Asahikawa Medical College, 2-1-1-1, Midorigaoka-Higashi, Asahikawa, Hokkaido 078-8510, Japan
  • ,
  • Toshie Nata

      Affiliations

    • Division of Gastroenterology and Hematology/Oncology, Department of Medicine, Asahikawa Medical College, 2-1-1-1, Midorigaoka-Higashi, Asahikawa, Hokkaido 078-8510, Japan
  • ,
  • Yuhei Inaba

      Affiliations

    • Division of Gastroenterology and Hematology/Oncology, Department of Medicine, Asahikawa Medical College, 2-1-1-1, Midorigaoka-Higashi, Asahikawa, Hokkaido 078-8510, Japan
  • ,
  • Kentaro Moriichi

      Affiliations

    • Division of Gastroenterology and Hematology/Oncology, Department of Medicine, Asahikawa Medical College, 2-1-1-1, Midorigaoka-Higashi, Asahikawa, Hokkaido 078-8510, Japan
  • ,
  • Hiroki Tanabe

      Affiliations

    • Division of Gastroenterology and Hematology/Oncology, Department of Medicine, Asahikawa Medical College, 2-1-1-1, Midorigaoka-Higashi, Asahikawa, Hokkaido 078-8510, Japan
  • ,
  • Yusuke Mizukami

      Affiliations

    • Division of Gastroenterology and Hematology/Oncology, Department of Medicine, Asahikawa Medical College, 2-1-1-1, Midorigaoka-Higashi, Asahikawa, Hokkaido 078-8510, Japan
  • ,
  • Jiro Watari

      Affiliations

    • Division of Upper Gastroenterology, Department of Internal Medicine, Hyogo College of Medicine, Nishinomiya, Hyogo, Japan
  • ,
  • Toshifumi Ashida

      Affiliations

    • Division of Gastroenterology and Hematology/Oncology, Department of Medicine, Asahikawa Medical College, 2-1-1-1, Midorigaoka-Higashi, Asahikawa, Hokkaido 078-8510, Japan
  • ,
  • Yutaka Kohgo

      Affiliations

    • Division of Gastroenterology and Hematology/Oncology, Department of Medicine, Asahikawa Medical College, 2-1-1-1, Midorigaoka-Higashi, Asahikawa, Hokkaido 078-8510, Japan

,Accepted 5 January 2010.

References 

  1. Fearon ER, Vogelstein B. A genetic model for colorectal tumorigenesis. Cell. 1990;61(5):759–767
  2. Hollstein M, Sidransky D, Vogelstein B. Harris CC. p53 mutations in human cancers. Science. 1991;253(5015):49–53
  3. Nishisho I, Nakamura Y, Miyoshi Y, Miki Y, Ando H, Horii A, et al. Mutations of chromosome 5q21 genes in FAP and colorectal cancer patients. Science. 1991;253(5020):665–669
  4. Tada M, Omata M, Kawai S, Saisho H, Ohgto M, Saiki RS, et al. Detection of ras gene mutations in pancreatic juice and peripheral blood of patients with pancreatic adenocarcinoma. Cancer Res. 1993;53(11):2472–2474
  5. Hibi K, Robinson R, Wu L, Hamilton SR, Sidransky D, Jen J. Molecular detection of genetic alterations in the serum of colorectal cancer patients. Cancer Res. 1997;58(7):1405–1407
  6. Anker P, lefort F, Vasioukhin C, Lyautey J, Lederrey C, Chen XQ, et al. K-ras mutations are found in DNA extracted from the plasma of patients with colorectal cancer. Gastroenterology. 1997;112(4):1114–1120
  7. Hsieh JS, Lin SR, Chang MY, Chen FM, Lu CY, Huang TJ, et al. APC, K-ras, and p53 gene mutations in colorectal cancer patients: correlation to clinicopathologic features and postoperative surveillance. Am Surg. 2005;71(4):336–343
  8. Silva JM, Dominguez G, Garcia JM, Gonzalez R, Villanueva MJ, Navarro F, et al. Presence of tumor DNA in plasma of breast cancer patients: clinicopathological correlations. Cancer Res. 1999;59(13):3251–3256
  9. Esteller M, Sanchez-Cespedes M, Rosell R, Sidransky D, Baylin SB, Herman JG. Detection of aberrant promoter hypermethylation of tumor suppressor genes in serum DNA from non-small cell lung cancer patients. Cancer Res. 1999;59(1):67–70
  10. Wong IH, Lo YM, Zhang J, Liew CT, Ng MHL, Wong N, et al. Detection of aberrant p16 methylation in the plasma and serum of liver cancer patients. Cancer Res. 1999;59(1):71–73
  11. Hibi K, Taguchi M, Nakayama H, Takase T, Kasai Y, Ito K, et al. Molecular detection of p16 promoter methylation in the serum of patients with esophageal squamous cell carcinoma. Clin Cancer Res. 2001;7(10):3135–3138
  12. Zou HZ, Yu BM, Wang JYS, Cang H, Gao F, Li DH, et al. Detection of aberrant p16 methylation in the serum of colorectal cancer patients. Clin Cancer Res. 2002;8(1):188–191
  13. Lee TL, Leung WK, Chan MWY, Ng EKW, Tong JHM, Lo KW, et al. Detection of gene promoter hypermethylation in the tumor and serum of patients with gastric carcinoma. Clin Cancer Res. 2002;8(6):1761–1766
  14. Nakayama G, Hibi K, Nakayama H, Kodera Y, Ito K, Akiyama S, et al. A highly sensitive method for the detection of p16 methylation in the serum of colorectal cancer patients. Anticancer Res. 2007;27(3B):1459–1463
  15. Tan SH, Ida H, Lau QC, Goh BC, Chieng WS, Loh M, et al. Detection of promoter hypermethylation in serum samples of cancer patients by methylation-specific polymerase chain reaction for tumour suppressor genes including RUNX3. Oncol Rep. 2007;18(5):1225–1230
  16. Ulivi P, Zoli W, Calistri D, Fabbri F, Tesei A, Rosetti M, et al. p16INK4A and CDH13 hypermethylation in tumor and serum of non-small cell lung cancer patients. J Cell Physiol. 2006;206(3):611–615
  17. Hoffmann AC, Vallböhmer D, Prenzel K, Metzger R, Heitmann M, Neiss S, et al. Methylated DAPK and APC promoter DNA detection in peripheral blood is significantly associated with apparent residual tumor and outcome. J Cancer Res Clin Oncol. 2009;135(9):1231–1237
  18. Herman JG, Graff JR, Myohanen S, Nelkin BD, Baylin SB, Methylation-specific PCR. A novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci. 1996;93(18):9821–9826
  19. Grunau C, Clark SJ, Rosenthal A. Bisulfite genomic sequencing: systematic investigation of critical experimental parameters. Nucleic Acids Res. 2001;129(13):E65–E75
  20. Ballestar E, Paz MF, Valle L, Wei S, Fraga MF, Espada J, et al. Methyl-CpG binding proteins identify novel sites of epigenetic inactivation in human cancer. EMBO J. 2003;22(23):6335–6345
  21. Weber M, Davies JJ, Wittig D, Oakeley EJ, Haase M, Lam WL, et al. Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells. Nat Genet. 2005;37(8):853–862
  22. Thu KL, Vucic EA, Kennett JY, Heryet C, Brown CJ, Lam WL, et al. Methylated DNA immunoprecipitation. J Vis Exp. 2009;(23):pii: 935. doi:10.3791/935
  23. Vucic EA, Wilson IM, Campbell JM, Lam WL. Methylation analysis by DNA immunoprecipitation (MeDIP). Methods Mol Biol. 2009;556:141–153
  24. Mohn F, Weber M, Schübeler D, Roloff TC. Methylated DNA immunoprecipitation (MeDIP). Methods Mol Biol. 2009;507:55–64
  25. Pelizzola M, Koga Y, Urban AE, Krauthammer M, Weissman S, Halaban R, et al. MEDME: an experimental and analytical methodology for the estimation of DNA methylation levels based on microarray derived MeDIP-enrichment. Genome Res. 2008;18(10):1652–1659
  26. Meehan RR, Lewis JD, McKay S, Kleiner EL, Bird AP. Identification of a mammalian protein that binds specifically to DNA containing methylated CpGs. Cell. 1989;58(3):499–507
  27. Boyes J, Bird A. DNA methylation inhibits transcription indirectly via a methyl-CpG binding protein. Cell. 1991;64(6):1123–1134
  28. Cross SH, Meehan RR, Nan X, Bird A. A component of the transcriptional repressor MeCP1 shares a motif with DNA methyltransferase and HRX proteins. Nat Genet. 1997;16(3):256–259
  29. Jost JP, Hofsteenge J. The repressor MDBP-2 is a member of the histone H1 family that binds preferentially in vitro and in vivo to methylated nonspecific DNA sequences. Proc Natl Acad Sci USA. 1992;89(20):9499–9503
  30. Jiang CL, Jin SG, Pfeifer GP. MBD3L1 is a transcriptional repressor that interacts with methyl-CpG-binding protein 2 (MBD2) and components of the NuRD complex. J Biol Chem. 2004;279(50):52456–52464
  31. Rumore PM, Steinman CR. Endogenous circulating DNA in systemic lupus erythematosus. Occurrence as multimeric complexes bound to histone. J Clin Invest. 1990;86(1):69–74
  32. Konishi N, Nakamura M, Kishi M, Nishimine M, Ishida E, Shimada K. DNA hypermethylation status of multiple genes in prostate adenocarcinomas. Jpn J Cancer Res. 2002;93(7):767–773
  33. Hsieh CJ, Klump B, Holzmann K, Borchard F, Gregor M, Porschen R. Hypermethylation of the p16INK4a promoter in colectomy specimens of patients with long-standing and extensive ulcerative colitis. Cancer Res. 1998;58(17):3942–3945
  34. Jahr S, Hentze H, Enblisch S, Hardt D, Fackelmayer FO, Hesch RD, et al. DNA fragment in the blood plasma of cancer patients: quantitations and evidence for their origin from apoptotic and necrotic cells. Cancer Res. 2001;61(4):1659–1665
  35. Esteller M, Corn PG, Baylin SB, Herman JG. A gene hypermethylation profile of human cancer. Cancer Res. 2001;61(8):3225–3229
  36. Yoshiura K, Kanai Y, Ochiai A, Shimoyama Y, Sugimura T, Hirohashi S. Silencing of the E-cadherin invasion-suppressor gene by CpG methylation in human carcinomas. Proc Natl Acad Sci. 1995;92(16):7416–7419
  37. Herman JG, Umar A, Polyak K, Graff JR, Ahuja N, Issa JJ, et al. Incidence and function consequences of hMLH1 promoter hypermethylation in colorectal carcinoma. Proc. Natl Acad Sci USA. 1998;95(12):6870–6875
  38. Virmani AK, Rathi A, Sathyanarayana UG, Padar A, Huang CX, Cunnigham HT, et al. Aberrant methylation of the adenomatous polyposis coli (APC) gene promoter 1A in breast and lung carcinomas. Clin Cancer Res. 2001;7(7):1998–2004
  39. Kim TY, Lee HJ, Hwang KS, Lee M, Kim JW, Bang YJ, et al. Methylation of RUNX3 in various types of human cancers and premalignant stages of gastric carcinoma. Lab Invest. 2004;84(4):479–484

PII: S1877-7821(10)00007-X

doi: 10.1016/j.canep.2010.01.004

Cancer Epidemiology
Volume 34, Issue 2 , Pages 194-199 , April 2010