Detection of methylated Septin 9 in tissue and plasma of colorectal patients with neoplasia and the relationship to the amount of circulating cell-free DNA

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Tóth, Kinga ^a   Wasserkort, Reinhold ^b,d   Sipos, Ferenc ^a   Kalmár, Alexandra ^a,c   Wichmann, Barnabás ^c   Leiszter, Katalin ^a   Valcz, Gábor ^c   Juhász, Márk ^a   Miheller, Pál ^a   Patai, Árpád V ^a   Tulassay, Zsolt ^a,c   Molnár, Béla ^a,c  

^a SEMMELWEIS UNIVERSITY   (Hungary)

^b EPIGENOMICS AG   (Germany)

^c INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^d FRAUNHOFER INSTITUTE FOR CELL THERAPY AND IMMUNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BISULFITE; DNA; METHYLATED SEPTIN 9; SEPTIN; SEPTIN 9; TUMOR MARKER; UNCLASSIFIED DRUG; SEPT9 PROTEIN, HUMAN;

ARTICLE; COLORECTAL ADENOMA; COLORECTAL CANCER; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CORRELATION ANALYSIS; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; REFERENCE VALUE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TISSUE LEVEL; ADENOMA; ADULT; AGED; BLOOD; CASE CONTROL STUDY; COLORECTAL TUMOR; FEMALE; GENETICS; MALE; METABOLISM; METHYLATION; MIDDLE AGED; PATHOLOGY;

ADENOMA; ADULT; AGED; BIOMARKERS, TUMOR; CASE-CONTROL STUDIES; COLORECTAL NEOPLASMS; DNA; FEMALE; HUMANS; MALE; METHYLATION; MIDDLE AGED; SEPTINS;

EID: 84919491632     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0115415     Document Type: Article

References (51)

1. Ferlay J, Autier P, Boniol M, Heanue M, Colombet M, et al. (2007) Estimates of the cancer incidence and mortality in Europe in 2006. Ann Oncol 18: 581-592.
2. Pignone M, Saha S, Hoerger T, Mandelblatt J (2002) Cost-effectiveness analyses of colorectal cancer screening: a systematic review for the U.S. Preventive Services Task Force. Ann Intern Med 137: 96-104.
3. Siegel R, Desantis C, Virgo K, Stein K, Mariotto A, et al. (2012) Cancer treatment and survivorship statistics, 2012. CA Cancer J Clin 62: 220-241.
4. Vogelstein B, Fearon ER, Hamilton SR, Kern SE, Preisinger AC, et al. (1988) Genetic alterations during colorectal-tumor development. N Engl J Med 319: 525-532.
5. Smith RA, Cokkinides V, Brooks D, Saslow D, Brawley OW (2010) Cancer screening in the United States, 2010: a review of current American Cancer Society guidelines and issues in cancer screening. CA Cancer J Clin 60: 99-119.
6. Lieberman DA (2009) Clinical practice. Screening for Colorectal Cancer. N Engl J Med 361: 1179-1187.
7. Levin B, Lieberman DA, McFarland B, Andrews KS, Brooks D, et al. (2008) Screening and surveillance for the early detection of colorectal cancer and adenomatous polyps, 2008: a joint guideline from the American Cancer Society, the US Multi-Society Task Force on Colorectal Cancer, and the American College of Radiology. Gastroenterology 134: 1570-1595.
8. Federici A, Giorgi Rossi P, Borgia P, Bartolozzi F, Farchi S, et al. (2005) The immunochemical faecal occult blood test leads to higher compliance than the guaiac for colorectal cancer screening programmes: a cluster randomized controlled trial. J Med Screen 12: 83-88.
9. Denters MJ, Deutekom M, Bossuyt PM, Stroobants AK, Fockens P, et al. (2012) Lower risk of advanced neoplasia among patients with a previous negative result from a fecal test for colorectal cancer. Gastroenterology 142: 497-504.
10. Ahlquist DA, Zou H, Domanico M, Mahoney DW, Yab TC, et al. (2012) Next-generation stool DNA test accurately detects colorectal cancer and large adenomas. Gastroenterology 142: 248-256.
11. Wang JY, Hsieh JS, Chang MY, Huang TJ, Chen FM, et al. (2004) Molecular detection of APC, K-ras, and p53 mutations in the serum of colorectal cancer patients as circulating biomarkers. World J Surg 28: 721-726.
12. Lofton-Day C, Model F, Devos T, Tetzner R, Distler J, et al. (2008) DNA methylation biomarkers for blood-based colorectal cancer screening. Clin Chem 54: 414-423.
13. Grützmann R, Molnar B, Pilarsky C, Habermann JK, Schlag PM, et al. (2008) Sensitive detection of colorectal cancer in peripheral blood by septin 9 DNA methylation assay. PLoS One 3: e3759.
14. deVos T, Tetzner R, Model F, Weiss G, Schuster M, et al. (2009) Circulating methylated SEPT9 DNA in plasma is a biomarker for colorectal cancer. Clin Chem 55: 1337-1346.
15. Hall PA, Russell SE (2004) The pathobiology of the septin gene family. J Pathol 204: 489-505.
16. Estey MP, Kim MS, Trimble WS (2011) Septins. Curr Biol 21: R384-387.
17. McDade SS, Hall PA, Russell SE (2007) Translational control of SEPT9 isoforms is perturbed in disease. Hum Mol Genet 16: 742-752.
18. Russell SE, McIlhatton MA, Burrows JF, Donaghy PG, Chanduloy S, et al. (2000) Isolation and mapping of a human septin gene to a region on chromosome 17q, commonly deleted in sporadic epithelial ovarian tumors. Cancer Res 60: 4729-4734.
19. Connolly D, Yang Z, Castaldi M, Simmons N, Oktay MH, et al. (2011) Septin 9 isoform expression, localization and epigenetic changes during human and mouse breast cancer progression. Breast Cancer Res 13: R76.
20. Burrows JF, Chanduloy S, McIlhatton MA, Nagar H, Yeates K, et al. (2003) Altered expression of the septin gene, SEPT9, in ovarian neoplasia. J Pathol 201: 581-588.
21. Montagna C, Lyu MS, Hunter K, Lukes L, Lowther W, et al. (2003) The Septin 9 (MSF) gene is amplified and overexpressed in mouse mammary gland adenocarcinomas and human breast cancer cell lines. Cancer Res 63: 2179-2187.
22. Tatsumi K, Taki T, Taniwaki M, Nakamura H, Taguchi J, et al. (2001) The CDCREL1 gene fused to MLL in de novo acute myeloid leukemia with t(11;22)(q23;q11.2) and its frequent expression in myeloid leukemia cell lines. Genes Chromosomes Cancer 30: 230-235.
23. Kim HJ, Ki CS, Park Q, Koo HH, Yoo KH, et al. (2003) MLL/SEPTIN6 chimeric transcript from inv ins(X;11)(q24;q23q13) in acute monocytic leukemia: report of a case and review of the literature. Genes Chromosomes Cancer 38: 8-12.
24. Kojima K, Sakai I, Hasegawa A, Niiya H, Azuma T, et al. (2004) FLJ10849, a septin family gene, fuses MLL in a novel leukemia cell line CNLBC1 derived from chronic neutrophilic leukemia in transformation with t(4;11)(q21;q23). Leukemia 18: 998-1005.
25. Tanaka M, Tanaka T, Matsuzaki S, Seto Y, Matsuda T, et al. (2003) Rapid and quantitative detection of human septin family Bradeion as a practical diagnostic method of colorectal and urologic cancers. Med Sci Monit 9: MT61-68.
26. Amir S, Golan M, Mabjeesh NJ (2010) Targeted knockdown of SEPT9-v1 inhibits tumor growth and angiogenesis of human prostate cancer cells concomitant with disruption of hypoxia-inducible factor-1 pathway. Mol Cancer Res 8: 643-652.
27. Kim DS, Hubbard SL, Peraud A, Salhia B, Sakai K, et al. (2004) Analysis of mammalian septin expression in human malignant brain tumors. Neoplasia 6: 168-178.
28. Tóth K, Galamb O, Spisák S, Wichmann B, Sipos F, et al. (2011) The influence of methylated septin 9 gene on RNA and protein level in colorectal cancer. Pathol Oncol Res 17: 503-509.
29. Tóth K, Sipos F, Kalmár A, Patai AV, Wichmann B, et al. (2012) Detection of methylated SEPT9 in plasma is a reliable screening method for both left- and right-sided colon cancers. PLoS One 7: e46000.
30. Tänzer M, Balluff B, Distler J, Hale K, Leodolter A, et al. (2010) Performance of epigenetic markers SEPT9 and ALX4 in plasma for detection of colorectal precancerous lesions. PLoS One 5: e9061.
31. Warren JD, Xiong W, Bunker AM, Vaughn CP, Furtado LV, et al. (2011) Septin 9 methylated DNA is a sensitive and specific blood test for colorectal cancer. BMC Med 9: 133.
32. Church TR, Wandell M, Lofton-Day C, Mongin SJ, Burger M, et al. (2014) Prospective evaluation of methylated SEPT9 in plasma for detection of asymptomatic colorectal cancer. Gut 63: 317-325.
33. He Q, Chen HY, Bai EQ, Luo YX, Fu RJ, et al. (2010) Development of a multiplex MethyLight assay for the detection of multigene methylation in human colorectal cancer. Cancer Genet Cytogenet 202: 1-10.
34. Johnson DA, Barclay RL, Mergener K, Weiss G, König T, et al. (2014) Plasma Septin9 versus fecal immunochemical testing for colorectal cancer screening: a) prospective multicenter study. PLoS One 9: e98238.
35. Wasserkort R, Kalmar A, Valcz G, Spisak S, Krispin M, et al. (2013) Aberrant septin 9 DNA methylation in colorectal cancer is restricted to a single CpG island. BMC Cancer 13: 398.
36. Ahlquist DA, Taylor WR, Mahoney DW, Zou H, Domanico M, et al. (2012) The stool DNA test is more accurate than the plasma septin 9 test in detecting colorectal neoplasia. Clin Gastroenterol Hepatol 10: 272-277.
37. Gormally E, Caboux E, Vineis P, Hainaut P (2007) Circulating free DNA in plasma or serum as biomarker of carcinogenesis: practical aspects and biological significance. Mutat Res 635: 105-117.
38. van der Vaart M, Pretorius PJ (2007) The origin of circulating free DNA. Clin Chem 53: 2215.
39. Boni L, Cassinotti E, Canziani M, Dionigi G, Rovera F, et al. (2007) Free circulating DNA as possible tumour marker in colorectal cancer. Surg Oncol (Suppl 1): 29-31.
40. Danese E, Montagnana M, Minicozzi AM, De Matteis G, Scudo G, et al.2010) Real-time polymerase chain reaction quantification of free DNA in serum of patients with polyps and colorectal cancers. Clin Chem Lab Med 48: 1665-1668.
41. Bischoff FZ, Lewis DE, Simpson JL (2005) Cell-free fetal DNA in maternal blood: kinetics, source and structure. Hum Reprod Update 11: 59-67.
42. Atamaniuk J, Stuhlmeier KM, Vidotto C, Tschan H, Dossenbach-Glaninger A, et al. (2008) Effects of ultra-marathon on circulating DNA and mRNA expression of pro- and anti-apoptotic genes in mononuclear cells. Eur J Appl Physiol 104: 711-717.
43. Breitbach S, Tug S, Simon P (2012) Circulating cell-free DNA: an up-coming molecular marker in exercisephysiology. Sports Med 42: 565-586.
44. Taback B, O'Day SJ, Hoon DS (2004) Quantification of circulating DNA in the plasma and serum of cancer patients. Ann N Y Acad Sci 1022: 17-24.
45. Elshimali YI, Khaddour H, Sarkissyan M, Wu Y, Vadgama JV (2013) The Clinical Utilization of Circulating Cell Free DNA (CCFDNA) in Blood of Cancer Patients. Int J Mol Sci 14: 18925-18958.
46. Danese E, Minicozzi AM, Benati M, Montagnana M, Paviati E (2013) Epigenetic alteration: new insights moving from tissue to plasma - the example of PCDH10 promoter methylation in colorectal cancer. Br J Cancer 109: 807-813.
47. Jahr S, Hentze H, Englisch S, Hardt D, Fackelmayer FO (2001) DNA fragments in the blood plasma of cancer patients: quantitations and evidence for their origin from apoptotic and necrotic cells. Cancer Res 61: 1659-1665.
48. van der Vaart M, Pretorius PJ (2007) The origin of circulating free DNA. Clin Chem 53: 2215.
49. Manderson AP, Carlucci F, Lachmann PJ, Lazarus RA, Festenstein RJ, et al. (2006) The in vivo expression of actin/salt-resistant hyperactive DNase I inhibits the development of anti-ssDNA and antihistone autoantibodies in a murine model of systemic lupus erythematosus. Arthritis Res Ther 8: R68.
50. Tamkovich SN, Cherepanova AV, Kolesnikova EV, Rykova EY, Pyshnyi DV, et al. (2006) Circulating DNA and DNase activity in human blood. Ann N Y Acad Sci 1075: 191-196.
51. Tamkovich SN, Cherepanova AV, Bryzgunova OE, Kolesnikova EV, Permyakova VI, et al. (2008) Deoxyribonuclease activity in biological fluids of healthy donors and cancer patinets. Bull Exp Biol Med 146: 89-91.