Colorectal Cancer Blood-Based Biomarkers

Nina Hauptman, Damjan Glavač, Nina Hauptman, Damjan Glavač

Abstract

Mortality and morbidity associated with colorectal cancer (CRC) are increasing globally, partly due to lack of early detection of the disease. The screening is usually performed with colonoscopy, which is invasive and unpleasant, discouraging participation in the screening. As a source of noninvasive and easily accessible biomarkers, liquid biopsies are emerging. Blood-based biomarkers have the potential as diagnostic and prognostic tool in CRC. Early stage detection of CRC with high sensitivity and specificity would likely lead to higher participation in the screening test. It would also improve the prognosis of the disease and improve the recurrence risk. In this review, we summarize the potential biomarkers for early detection and monitoring of CRC.

References

    1. Siegel R., Desantis C., Jemal A. Colorectal cancer statistics, 2014. CA: A Cancer Journal for Clinicians. 2014;64(2):104–117. doi: 10.3322/caac.21220.
    1. Smith R. A., Manassaram-Baptiste D., Brooks D., et al. Cancer screening in the United States, 2015: a review of current American cancer society guidelines and current issues in cancer screening. CA: A Cancer Journal for Clinicians. 2015;65(1):30–54. doi: 10.3322/caac.21261.
    1. Pino M. S., Chung D. C. The chromosomal instability pathway in colon cancer. Gastroenterology. 2010;138(6):2059–2072. doi: 10.1053/j.gastro.2009.12.065.
    1. Rawson J. B., Bapat B. Epigenetic biomarkers in colorectal cancer diagnostics. Expert Review of Molecular Diagnostics. 2012;12(5):499–509. doi: 10.1586/erm.12.39.
    1. Newton K. F., Newman W., Hill J. Review of biomarkers in colorectal cancer. Colorectal Disease. 2012;14(1):3–17. doi: 10.1111/j.1463-1318.2010.02439.x.
    1. Yoruker E. E., Holdenrieder S., Gezer U. Blood-based biomarkers for diagnosis, prognosis and treatment of colorectal cancer. Clinica Chimica Acta. 2016;455:26–32. doi: 10.1016/j.cca.2016.01.016.
    1. Locker G. Y., Hamilton S., Harris J., et al. ASCO 2006 update of recommendations for the use of tumor markers in gastrointestinal cancer. Journal of Clinical Oncology. 2006;24(33):5313–5327. doi: 10.1200/JCO.2006.08.2644.
    1. Hundt S., Haug U., Brenner H. Blood markers for early detection of colorectal cancer: a systematic review. Cancer Epidemiology, Biomarkers & Prevention. 2007;16(10):1935–1953. doi: 10.1158/1055-9965.EPI-06-0994.
    1. Nicolini A., Ferrari P., Duffy M. J., et al. Intensive risk-adjusted follow-up with the CEA, TPA, CA19.9, and CA72.4 tumor marker panel and abdominal ultrasonography to diagnose operable colorectal cancer recurrences: effect on survival. Archives of Surgery. 2010;145(12):1177–1183. doi: 10.1001/archsurg.2010.251.
    1. Levy M., Visokai V., Lipska L., Topolcan O. Tumor markers in staging and prognosis of colorectal carcinoma. Neoplasma. 2008;55(2):138–142.
    1. Bystrom P., Berglund Å., Nygren P., et al. Evaluation of predictive markers for patients with advanced colorectal cancer. Acta Oncologica. 2012;51(7):849–859. doi: 10.3109/0284186X.2012.705020.
    1. Holdenrieder S., Stieber P., Liska V., et al. Cytokeratin serum biomarkers in patients with colorectal cancer. Anticancer Research. 2012;32(5):1971–1976.
    1. Allard W. J., Matera J., Miller M. C., et al. Tumor cells circulate in the peripheral blood of all major carcinomas but not in healthy subjects or patients with nonmalignant diseases. Clinical Cancer Research. 2004;10(20):6897–6904. doi: 10.1158/1078-0432.CCR-04-0378.
    1. Glaves D. Correlation between circulating cancer cells and incidence of metastases. British Journal of Cancer. 1983;48(5):665–673. doi: 10.1038/bjc.1983.248.
    1. Chang Y. S., di Tomaso E., McDonald D. M., Jones R., Jain R. K., Munn L. L. Mosaic blood vessels in tumors: frequency of cancer cells in contact with flowing blood. Proceedings of the National Academy of Sciences of the United States of America. 2000;97(26):14608–14613. doi: 10.1073/pnas.97.26.14608.
    1. Weiss L., Mayhew E., Rapp D. G., Holmes J. C. Metastatic inefficiency in mice bearing B16 melanomas. British Journal of Cancer. 1982;45(1):44–53. doi: 10.1038/bjc.1982.6.
    1. Luzzi K. J., MacDonald I. C., Schmidt E. E., et al. Multistep nature of metastatic inefficiency: dormancy of solitary cells after successful extravasation and limited survival of early micrometastases. The American Journal of Pathology. 1998;153(3):865–873. doi: 10.1016/S0002-9440(10)65628-3.
    1. Wong C. W., Lee A., Shientag L., et al. Apoptosis: an early event in metastatic inefficiency. Cancer Research. 2001;61(1):333–338.
    1. Weiss L., Nannmark U., Johansson B. R., Bagge U. Lethal deformation of cancer cells in the microcirculation: a potential rate regulator of hematogenous metastasis. International Journal of Cancer. 1992;50(1):103–107. doi: 10.1002/ijc.2910500121.
    1. Barbera-Guillem E., Weiss L. Cancer-cell traffic in the liver. III. Lethal deformation of B16 melanoma cells in liver sinusoids. International Journal of Cancer. 1993;54(5):880–884. doi: 10.1002/ijc.2910540526.
    1. Berezovskaya O., Schimmer A. D., Glinskii A. B., et al. Increased expression of apoptosis inhibitor protein XIAP contributes to anoikis resistance of circulating human prostate cancer metastasis precursor cells. Cancer Research. 2005;65(6):2378–2386. doi: 10.1158/0008-5472.CAN-04-2649.
    1. Al-Mehdi A. B., Tozawa K., Fisher A. B., Shientag L., Lee A., Muschel R. J. Intravascular origin of metastasis from the proliferation of endothelium-attached tumor cells: a new model for metastasis. Nature Medicine. 2000;6(1):100–102. doi: 10.1038/71429.
    1. Glinsky V. V., Glinsky G. V., Glinskii O. V., et al. Intravascular metastatic cancer cell homotypic aggregation at the sites of primary attachment to the endothelium. Cancer Research. 2003;63(13):3805–3811. doi: 10.1016/j.urolonc.2003.12.009.
    1. Kallergi G., Papadaki M. A., Politaki E., Mavroudis D., Georgoulias V., Agelaki S. Epithelial to mesenchymal transition markers expressed in circulating tumour cells of early and metastatic breast cancer patients. Breast Cancer Research. 2011;13(3, article R59) doi: 10.1186/bcr2896.
    1. Kasimir-Bauer S., Hoffmann O., Wallwiener D., Kimmig R., Fehm T. Expression of stem cell and epithelial-mesenchymal transition markers in primary breast cancer patients with circulating tumor cells. Breast Cancer Research. 2012;14(1):p. R15. doi: 10.1186/bcr3099.
    1. Aktas B., Tewes M., Fehm T., Hauch S., Kimmig R., Kasimir-Bauer S. Stem cell and epithelial-mesenchymal transition markers are frequently overexpressed in circulating tumor cells of metastatic breast cancer patients. Breast Cancer Research. 2009;11(4, article R46) doi: 10.1186/bcr2333.
    1. Lecharpentier A., Vielh P., Perez-Moreno P., Planchard D., Soria J. C., Farace F. Detection of circulating tumour cells with a hybrid (epithelial/mesenchymal) phenotype in patients with metastatic non-small cell lung cancer. British Journal of Cancer. 2011;105(9):1338–1341. doi: 10.1038/bjc.2011.405.
    1. Raimondi C., Gradilone A., Naso G., et al. Epithelial-mesenchymal transition and stemness features in circulating tumor cells from breast cancer patients. Breast Cancer Research and Treatment. 2011;130(2):449–455. doi: 10.1007/s10549-011-1373-x.
    1. Armstrong A. J., Marengo M. S., Oltean S., et al. Circulating tumor cells from patients with advanced prostate and breast cancer display both epithelial and mesenchymal markers. Molecular Cancer Research. 2011;9(8):997–1007. doi: 10.1158/1541-7786.MCR-10-0490.
    1. Yu M., Bardia A., Wittner B. S., et al. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science. 2013;339(6119):580–584. doi: 10.1126/science.1228522.
    1. Chen C. L., Mahalingam D., Osmulski P., et al. Single-cell analysis of circulating tumor cells identifies cumulative expression patterns of EMT-related genes in metastatic prostate cancer. Prostate. 2013;73(8):813–826. doi: 10.1002/pros.22625.
    1. Labelle M., Begum S., Hynes R. O. Direct signaling between platelets and cancer cells induces an epithelial-mesenchymal-like transition and promotes metastasis. Cancer Cell. 2011;20(5):576–590. doi: 10.1016/j.ccr.2011.09.009.
    1. Tsuji T., Ibaragi S., Hu G. F. Epithelial-mesenchymal transition and cell cooperativity in metastasis. Cancer Research. 2009;69(18):7135–7139. doi: 10.1158/0008-5472.CAN-09-1618.
    1. Wicki A., Lehembre F., Wick N., Hantusch B., Kerjaschki D., Christofori G. Tumor invasion in the absence of epithelial-mesenchymal transition: podoplanin-mediated remodeling of the actin cytoskeleton. Cancer Cell. 2006;9(4):261–272. doi: 10.1016/j.ccr.2006.03.010.
    1. Baccelli I., Schneeweiss A., Riethdorf S., et al. Identification of a population of blood circulating tumor cells from breast cancer patients that initiates metastasis in a xenograft assay. Nature Biotechnology. 2013;31(6):539–544. doi: 10.1038/nbt.2576.
    1. Navin N., Kendall J., Troge J., et al. Tumour evolution inferred by single-cell sequencing. Nature. 2011;472(7341):90–94. doi: 10.1038/nature09807.
    1. Gerlinger M., Rowan A. J., Horswell S., et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. The New England Journal of Medicine. 2012;366(10):883–892. doi: 10.1056/NEJMoa1113205.
    1. Gasch C., Bauernhofer T., Pichler M., et al. Heterogeneity of epidermal growth factor receptor status and mutations of KRAS/PIK3CA in circulating tumor cells of patients with colorectal cancer. Clinical Chemistry. 2013;59(1):252–260. doi: 10.1373/clinchem.2012.188557.
    1. Nadal R., Fernandez A., Sanchez-Rovira P., et al. Biomarkers characterization of circulating tumour cells in breast cancer patients. Breast Cancer Research. 2012;14(3, article R71) doi: 10.1186/bcr3180.
    1. Carvalho F. L., Simons B. W., Antonarakis E. S., et al. Tumorigenic potential of circulating prostate tumor cells. Oncotarget. 2013;4(3):413–421. doi: 10.18632/oncotarget.895.
    1. Mandel P., Metais P. Les acides nucleiques du plasma sanguin chez l’homme. Comptes Rendus des Seances de la Societe de Biologie et de Ses Filiales. 1948;142(3-4):241–243.
    1. Zhong X. Y., von Mühlenen I., Li Y., et al. Increased concentrations of antibody-bound circulatory cell-free DNA in rheumatoid arthritis. Clinical Chemistry. 2007;53(9):1609–1614. doi: 10.1373/clinchem.2006.084509.
    1. Jahr S., Hentze H., Englisch S., et al. DNA fragments in the blood plasma of cancer patients: quantitations and evidence for their origin from apoptotic and necrotic cells. Cancer Research. 2001;61(4):1659–1665.
    1. Frattini M., Gallino G., Signoroni S., et al. Quantitative analysis of plasma DNA in colorectal cancer patients: a novel prognostic tool. Annals of the New York Academy of Sciences. 2006;1075:185–190. doi: 10.1196/annals.1368.025.
    1. Boni L., Cassinotti E., Canziani M., Dionigi G., Rovera F., Dionigi R. Free circulating DNA as possible tumour marker in colorectal cancer. Surgical Oncology. 2007;16(Supplement 1):S29–S31. doi: 10.1016/j.suronc.2007.10.004.
    1. Schwarzenbach H., Stoehlmacher J., Pantel K., Goekkurt E. Detection and monitoring of cell-free DNA in blood of patients with colorectal cancer. Annals of the New York Academy of Sciences. 2008;1137:190–196. doi: 10.1196/annals.1448.025.
    1. Lee T. H., Montalvo L., Chrebtow V., Busch M. P. Quantitation of genomic DNA in plasma and serum samples: higher concentrations of genomic DNA found in serum than in plasma. Transfusion. 2001;41(2):276–282. doi: 10.1046/j.1537-2995.2001.41020276.x.
    1. Chan K. C., Yeung S. W., Lui W. B., Rainer T. H., Lo Y. M. Effects of preanalytical factors on the molecular size of cell-free DNA in blood. Clinical Chemistry. 2005;51(4):781–4. doi: 10.1373/clinchem.2004.046219.
    1. Fleischhacker M., Schmidt B. Circulating nucleic acids (CNAs) and cancer—a survey. Biochimica et Biophysica Acta (BBA) - Reviews on Cancer. 2007;1775(1):181–232. doi: 10.1016/j.bbcan.2006.10.001.
    1. Yu J., Gu G., Ju S. Recent advances in clinical applications of circulating cell-free DNA integrity. Laboratoriums Medizin. 2014;45(1):6–11. doi: 10.1309/lmkkox6ujzqgw0ea.
    1. Umetani N., Kim J., Hiramatsu S., et al. Increased integrity of free circulating DNA in sera of patients with colorectal or periampullary cancer: direct quantitative PCR for ALU repeats. Clinical Chemistry. 2006;52(6):1062–1069. doi: 10.1373/clinchem.2006.068577.
    1. Leszinski G., Lehner J., Gezer U., Holdenrieder S. Increased DNA integrity in colorectal cancer. In Vivo. 2014;28(3):299–303.
    1. Mouliere F., Robert B., Arnau Peyrotte E., et al. High fragmentation characterizes tumour-derived circulating DNA. PLoS One. 2011;6(9, article e23418) doi: 10.1371/journal.pone.0023418.
    1. Mead R., Duku M., Bhandari P., Cree I. A. Circulating tumour markers can define patients with normal colons, benign polyps, and cancers. British Journal of Cancer. 2011;105(2):239–245. doi: 10.1038/bjc.2011.230.
    1. Hao T. B., Shi W., Shen X. J., et al. Circulating cell-free DNA in serum as a biomarker for diagnosis and prognostic prediction of colorectal cancer. British Journal of Cancer. 2014;111(8):1482–1489. doi: 10.1038/bjc.2014.470.
    1. Boland C. R., Thibodeau S. N., Hamilton S. R., et al. A National Cancer Institute Workshop on Microsatellite Instability for cancer detection and familial predisposition: development of international criteria for the determination of microsatellite instability in colorectal cancer. Cancer Research. 1998;58(22):5248–5257.
    1. Kim G. P., Colangelo L. H., Wieand H. S., et al. Prognostic and predictive roles of high-degree microsatellite instability in colon cancer: a National Cancer Institute-National Surgical Adjuvant Breast and Bowel Project Collaborative Study. Journal of Clinical Oncology. 2007;25(7):767–772. doi: 10.1200/JCO.2006.05.8172.
    1. Taback B., Saha S., Hoon D. S. Comparative analysis of mesenteric and peripheral blood circulating tumor DNA in colorectal cancer patients. Annals of the New York Academy of Sciences. 2006;1075:197–203. doi: 10.1196/annals.1368.027.
    1. Lazarev I., Leibovitch L., Czeiger D., et al. Cell-free DNA blood levels in colorectal cancer patients do not correlate with mismatch repair-proficiency. In Vivo. 2014;28(3):349–354.
    1. Ling E., Fich A., Man S., Wolfson M., Mikhailowsky R., Lamprecht S. A. Detection of tumor mutant APC DNA in plasma of patients with sporadic colorectal cancer. In Vivo. 2000;14(4):543–546.
    1. Diehl F., Li M., Dressman D., et al. Detection and quantification of mutations in the plasma of patients with colorectal tumors. Proceedings of the National Academy of Sciences of the United States of America. 2005;102(45):16368–16373. doi: 10.1073/pnas.0507904102.
    1. Wang J. Y., Hsieh J. S., Chang M. Y., et al. Molecular detection of APC, K-ras, and p53 mutations in the serum of colorectal cancer patients as circulating biomarkers. World Journal of Surgery. 2004;28(7):721–726. doi: 10.1007/s00268-004-7366-8.
    1. Ito S., Hibi K., Nakayama H., et al. Detection of tumor DNA in serum of colorectal cancer patients. Japanese Journal of Cancer Research. 2002;93(11):1266–1269. doi: 10.1111/j.1349-7006.2002.tb01233.x.
    1. Selaru F. M., David S., Meltzer S. J., Hamilton J. P. Epigenetic events in gastrointestinal cancer. The American Journal of Gastroenterology. 2009;104(8):1910–1912. doi: 10.1038/ajg.2008.145.
    1. Ehrlich M. DNA hypomethylation in cancer cells. Epigenomics. 2009;1(2):239–259. doi: 10.2217/epi.09.33.
    1. Mu W. P., Wang J., Niu Q., Shi N., Lian H. F. Clinical significance and association of RUNX3 hypermethylation frequency with colorectal cancer: a meta-analysis. OncoTargets and Therapy. 2014;7:1237–1245. doi: 10.2147/OTT.S62103.
    1. Wang Y., Long Y., Xu Y., et al. Prognostic and predictive value of CpG island methylator phenotype in patients with locally advanced nonmetastatic sporadic colorectal cancer. Gastroenterology Research and Practice. 2014;2014:7. doi: 10.1155/2014/436985.436985
    1. Benard A., Zeestraten E. C., Goossens-Beumer I. J., et al. DNA methylation of apoptosis genes in rectal cancer predicts patient survival and tumor recurrence. Apoptosis. 2014;19(11):1581–1593. doi: 10.1007/s10495-014-1022-z.
    1. Deng D., Liu Z., Du Y. Epigenetic alterations as cancer diagnostic, prognostic, and predictive biomarkers. Advances in Genetics. 2010;71:125–176. doi: 10.1016/B978-0-12-380864-6.00005-5.
    1. Warren J. D., Xiong W., Bunker A. M., et al. Septin 9 methylated DNA is a sensitive and specific blood test for colorectal cancer. BMC Medicine. 2011;9:p. 133. doi: 10.1186/1741-7015-9-133.
    1. Church T. R., Wandell M., Lofton-Day C., et al. Prospective evaluation of methylated SEPT9 in plasma for detection of asymptomatic colorectal cancer. Gut. 2014;63(2):317–325. doi: 10.1136/gutjnl-2012-304149.
    1. Herbst A., Rahmig K., Stieber P., et al. Methylation of NEUROG1 in serum is a sensitive marker for the detection of early colorectal cancer. The American Journal of Gastroenterology. 2011;106(6):1110–1118. doi: 10.1038/ajg.2011.6.
    1. Suzuki H., Yamamoto E., Maruyama R., Niinuma T., Kai M. Biological significance of the CpG island methylator phenotype. Biochemical and Biophysical Research Communications. 2014;455(1-2):35–42. doi: 10.1016/j.bbrc.2014.07.007.
    1. Tan S. H., Ida H., Lau Q. C., et al. Detection of promoter hypermethylation in serum samples of cancer patients by methylation-specific polymerase chain reaction for tumour suppressor genes including RUNX3. Oncology Reports. 2007;18(5):1225–1230. doi: 10.3892/or.18.5.1225.
    1. Herbst A., Wallner M., Rahmig K., et al. Methylation of helicase-like transcription factor in serum of patients with colorectal cancer is an independent predictor of disease recurrence. European Journal of Gastroenterology & Hepatology. 2009;21(5):565–569. doi: 10.1097/MEG.0b013e328318ecf2.
    1. Wallner M., Herbst A., Behrens A., et al. Methylation of serum DNA is an independent prognostic marker in colorectal cancer. Clinical Cancer Research. 2006;12(24):7347–7352. doi: 10.1158/1078-0432.CCR-06-1264.
    1. Kim M. S., Chang X., Yamashita K., et al. Aberrant promoter methylation and tumor suppressive activity of the DFNA5 gene in colorectal carcinoma. Oncogene. 2008;27(25):3624–3634. doi: 10.1038/sj.onc.1211021.
    1. Ahlquist D. A., Taylor W. R., Mahoney D. W., et al. The stool DNA test is more accurate than the plasma septin 9 test in detecting colorectal neoplasia. Clinical Gastroenterology and Hepatology. 2012;10(3):272–277.e1. doi: 10.1016/j.cgh.2011.10.008.
    1. Weber J. A., Baxter D. H., Zhang S., et al. The microRNA spectrum in 12 body fluids. Clinical Chemistry. 2010;56(11):1733–1741. doi: 10.1373/clinchem.2010.147405.
    1. Chang D. H., Rutledge J. R., Patel A. A., Heerdt B. G., Augenlicht L. H., Korst R. J. The effect of lung cancer on cytokine expression in peripheral blood mononuclear cells. PLoS One. 2013;8(6, article e64456) doi: 10.1371/journal.pone.0064456.
    1. Kopreski M. S., Benko F. A., Kwak L. W., Gocke C. D. Detection of tumor messenger RNA in the serum of patients with malignant melanoma. Clinical Cancer Research. 1999;5(8):1961–1965.
    1. Tsouma A., Aggeli C., Lembessis P., et al. Multiplex RT-PCR-based detections of CEA, CK20 and EGFR in colorectal cancer patients. World Journal of Gastroenterology. 2010;16(47):5965–5974.
    1. Xu D., Li X. F., Zheng S., Jiang W. Z. Quantitative real-time RT-PCR detection for CEA, CK20 and CK19 mRNA in peripheral blood of colorectal cancer patients. Journal of Zhejiang University Science. B. 2006;7(6):445–451. doi: 10.1631/jzus.2006.B0445.
    1. Shen C., Hu L., Xia L., Li Y. Quantitative real-time RT-PCR detection for survivin, CK20 and CEA in peripheral blood of colorectal cancer patients. Japanese Journal of Clinical Oncology. 2008;38(11):770–776. doi: 10.1093/jjco/hyn105.
    1. Ganepola G. A., Nizin J., Rutledge J. R., Chang D. H. Use of blood-based biomarkers for early diagnosis and surveillance of colorectal cancer. World Journal of Gastrointestinal Oncology. 2014;6(4):83–97. doi: 10.4251/wjgo.v6.i4.83.
    1. Marshall K. W., Mohr S., Khettabi F. E., et al. A blood-based biomarker panel for stratifying current risk for colorectal cancer. International Journal of Cancer. 2010;126(5):1177–1186. doi: 10.1002/ijc.24910.
    1. Yip K. T., Das P. K., Suria D., Lim C. R., Ng G. H., Liew C. C. A case-controlled validation study of a blood-based seven-gene biomarker panel for colorectal cancer in Malaysia. Journal of Experimental & Clinical Cancer Research. 2010;29:p. 128. doi: 10.1186/1756-9966-29-128.
    1. Cortez M. A., Bueso-Ramos C., Ferdin J., Lopez-Berestein G., Sood A. K., Calin G. A. MicroRNAs in body fluids—the mix of hormones and biomarkers. Nature Reviews Clinical Oncology. 2011;8(8):467–477. doi: 10.1038/nrclinonc.2011.76.
    1. Croce C. M. Causes and consequences of microRNA dysregulation in cancer. Nature Reviews Genetics. 2009;10(10):704–714. doi: 10.1038/nrg2634.
    1. Kasinski A. L., Slack F. J. MicroRNAs en route to the clinic: progress in validating and targeting microRNAs for cancer therapy. Nature Reviews Cancer. 2011;11(12):849–864. doi: 10.1038/nrc3166.
    1. Slack F. J. MicroRNAs regulate expression of oncogenes. Clinical Chemistry. 2013;59(1):325–326. doi: 10.1373/clinchem.2011.181016.
    1. Mitchell P. S., Parkin R. K., Kroh E. M., et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proceedings of the National Academy of Sciences of the United States of America. 2008;105(30):10513–10518. doi: 10.1073/pnas.0804549105.
    1. Vickers K. C., Palmisano B. T., Shoucri B. M., Shamburek R. D., Remaley A. T. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nature Cell Biology. 2011;13(4):423–433. doi: 10.1038/ncb2210.
    1. Berger F., Reiser M. F. Micro-RNAs as potential new molecular biomarkers in oncology: have they reached relevance for the clinical imaging sciences? Theranostics. 2013;3(12):943–952. doi: 10.7150/thno.7445.
    1. Wang Q., Huang Z., Ni S., et al. Plasma miR-601 and miR-760 are novel biomarkers for the early detection of colorectal cancer. PLoS One. 2012;7(9, article e44398) doi: 10.1371/journal.pone.0044398.
    1. Giraldez M. D., Lozano J. J., Ramírez G., et al. Circulating microRNAs as biomarkers of colorectal cancer: results from a genome-wide profiling and validation study. Clinical Gastroenterology and Hepatology. 2013;11(6):681–688.e3. doi: 10.1016/j.cgh.2012.12.009.
    1. Kanaan Z., Roberts H., Eichenberger M. R., et al. A plasma microRNA panel for detection of colorectal adenomas. Annals of Surgery. 2013;258(3):400–408. doi: 10.1097/SLA.0b013e3182a15bcc.
    1. Ahmed F. E., Amed N. C., Vos P. W., et al. Diagnostic microRNA markers to screen for sporadic human colon cancer in blood. Cancer Genomics Proteomics. 2012;9(4):179–192.
    1. Huang Z., Huang D., Ni S., Peng Z., Sheng W., Du X. Plasma microRNAs are promising novel biomarkers for early detection of colorectal cancer. International Journal of Cancer. 2010;127(1):118–126. doi: 10.1002/ijc.25007.
    1. Liu G. H., Zhou Z. G., Chen R., et al. Serum miR-21 and miR-92a as biomarkers in the diagnosis and prognosis of colorectal cancer. Tumour Biology. 2013;34(4):2175–2181. doi: 10.1007/s13277-013-0753-8.
    1. Pu X. X., Huang G. L., Guo H. Q., et al. Circulating miR-221 directly amplified from plasma is a potential diagnostic and prognostic marker of colorectal cancer and is correlated with p53 expression. Journal of Gastroenterology and Hepatology. 2010;25(10):1674–1680. doi: 10.1111/j.1440-1746.2010.06417.x.
    1. Panzitt K., Tschernatsch M. M., Guelly C., et al. Characterization of HULC, a novel gene with striking up-regulation in hepatocellular carcinoma, as noncoding RNA. Gastroenterology. 2007;132(1):330–342. doi: 10.1053/j.gastro.2006.08.026.
    1. Arita T., Ichikawa D., Konishi H., et al. Circulating long non-coding RNAs in plasma of patients with gastric cancer. Anticancer Research. 2013;33(8):3185–3193.
    1. Dong L., Qi P., Xu M. D., et al. Circulating CUDR, LSINCT-5 and PTENP1 long noncoding RNAs in sera distinguish patients with gastric cancer from healthy controls. International Journal of Cancer. 2015;137(5):1128–1135. doi: 10.1002/ijc.29484.
    1. Tong Y. S., Wang X. W., Zhou X. L., et al. Identification of the long non-coding RNA POU3F3 in plasma as a novel biomarker for diagnosis of esophageal squamous cell carcinoma. Molecular Cancer. 2015;14:p. 3. doi: 10.1186/1476-4598-14-3.
    1. Graham L. D., Pedersen S. K., Brown G. S., et al. Colorectal neoplasia differentially expressed (CRNDE), a novel gene with elevated expression in colorectal adenomas and adenocarcinomas. Genes & Cancer. 2011;2(8):829–840. doi: 10.1177/1947601911431081.
    1. Zhao W., Song M., Zhang J., Kuerban M., Wang H. Combined identification of long non-coding RNA CCAT1 and HOTAIR in serum as an effective screening for colorectal carcinoma. International Journal of Clinical and Experimental Pathology. 2015;8(11):14131–14140.
    1. Rutter M., Saunders B., Wilkinson K., et al. Severity of inflammation is a risk factor for colorectal neoplasia in ulcerative colitis. Gastroenterology. 2004;126(2):451–459. doi: 10.1053/j.gastro.2003.11.010.
    1. Eaden J. A., Abrams K. R., Mayberry J. F. The risk of colorectal cancer in ulcerative colitis: a meta-analysis. Gut. 2001;48(4):526–535. doi: 10.1136/gut.48.4.526.
    1. Prior P., Gyde S. N., Macartney J. C., Thompson H., Waterhouse J. A., Allan R. N. Cancer morbidity in ulcerative colitis. Gut. 1982;23(6):490–497. doi: 10.1136/gut.23.6.490.
    1. Riddell R. H., Goldman H., Ransohoff D. F., et al. Dysplasia in inflammatory bowel disease: standardized classification with provisional clinical applications. Human Pathology. 1983;14(11):931–968. doi: 10.1016/s0046-8177(83)80175-0.
    1. Ellis E. M. Reactive carbonyls and oxidative stress: potential for therapeutic intervention. Pharmacology & Therapeutics. 2007;115(1):13–24. doi: 10.1016/j.pharmthera.2007.03.015.
    1. Keshavarzian A., Sedghi S., Kanofsky J., et al. Excessive production of reactive oxygen metabolites by inflamed colon: analysis by chemiluminescence probe. Gastroenterology. 1992;103(1):177–185. doi: 10.1016/0016-5085(92)91111-g.
    1. Keshavarzian A., Banan A., Farhadi A., et al. Increases in free radicals and cytoskeletal protein oxidation and nitration in the colon of patients with inflammatory bowel disease. Gut. 2003;52(5):720–728. doi: 10.1136/gut.52.5.720.
    1. Roessner A., Kuester D., Malfertheiner P., Schneider-Stock R. Oxidative stress in ulcerative colitis-associated carcinogenesis. Pathology, Research and Practice. 2008;204(7):511–524. doi: 10.1016/j.prp.2008.04.011.
    1. Bressenot A., Cahn V., Danese S., Peyrin-Biroulet L. Microscopic features of colorectal neoplasia in inflammatory bowel diseases. World Journal of Gastroenterology. 2014;20(12):3164–3172. doi: 10.3748/wjg.v20.i12.3164.
    1. Brentnall T. A., Crispin D. A., Rabinovitch P. S., et al. Mutations in the p53 gene: an early marker of neoplastic progression in ulcerative colitis. Gastroenterology. 1994;107(2):369–378. doi: 10.1016/0016-5085(94)90161-9.
    1. Brentnall T. A., Crispin D. A., Bronner M. P., et al. Microsatellite instability in non-neoplastic mucosa from patients with chronic ulcerative colitis. Cancer Research. 1996;56(6):1237–1240.
    1. Chen R., Rabinovitch P. S., Crispin D. A., et al. DNA fingerprinting abnormalities can distinguish ulcerative colitis patients with dysplasia and cancer from those who are dysplasia/cancer-free. The American Journal of Pathology. 2003;162(2):665–672. doi: 10.1016/S0002-9440(10)63860-6.
    1. Chen R., Rabinovitch P. S., Crispin D. A., Emond M. J., Bronner M. P., Brentnall T. A. The initiation of colon cancer in a chronic inflammatory setting. Carcinogenesis. 2005;26(9):1513–9. doi: 10.1093/carcin/bgi106.
    1. Chen R., Bronner M. P., Crispin D. A., Rabinovitch P. S., Brentnall T. A. Characterization of genomic instability in ulcerative colitis neoplasia leads to discovery of putative tumor suppressor regions. Cancer Genetics and Cytogenetics. 2005;162(2):99–106. doi: 10.1016/j.cancergencyto.2005.04.006.
    1. Lai L. A., Risques R. A., Bronner M. P., et al. Pan-colonic field defects are detected by CGH in the colons of UC patients with dysplasia/cancer. Cancer Letters. 2012;320(2):180–188. doi: 10.1016/j.canlet.2012.02.031.
    1. O'Sullivan J. N., Bronner M. P., Brentnall T. A., et al. Chromosomal instability in ulcerative colitis is related to telomere shortening. Nature Genetics. 2002;32(2):280–284. doi: 10.1038/ng989.
    1. Rabinovitch P. S., Dziadon S., Brentnall T. A., et al. Pancolonic chromosomal instability precedes dysplasia and cancer in ulcerative colitis. Cancer Research. 1999;59(20):5148–5153.
    1. Risques R. A., Lai L. A., Himmetoglu C., et al. Ulcerative colitis-associated colorectal cancer arises in a field of short telomeres, senescence, and inflammation. Cancer Research. 2011;71(5):1669–1679. doi: 10.1158/0008-5472.CAN-10-1966.
    1. Itzkowitz S. H. Molecular biology of dysplasia and cancer in inflammatory bowel disease. Gastroenterology Clinics of North America. 2006;35(3):553–571. doi: 10.1016/j.gtc.2006.07.002.
    1. O'Connor P. M., Lapointe T. K., Beck P. L., Buret A. G. Mechanisms by which inflammation may increase intestinal cancer risk in inflammatory bowel disease. Inflammatory Bowel Diseases. 2010;16(8):1411–1420. doi: 10.1002/ibd.21217.
    1. Itzkowitz S. H., Yio X. Inflammation and cancer IV. Colorectal cancer in inflammatory bowel disease: the role of inflammation. American Journal of Physiology Gastrointestinal and Liver Physiology. 2004;287(1):G7–17. doi: 10.1152/ajpgi.00079.2004.
    1. Terzic J., Grivennikov S., Karin E., Karin M. Inflammation and colon cancer. Gastroenterology. 2010;138(6):2101–2114.e5. doi: 10.1053/j.gastro.2010.01.058.
    1. Kisiel J. B., Garrity-Park M. M., Taylor W. R., Smyrk T. C., Ahlquist D. A. Methylated eyes absent 4 (EYA4) gene promotor in non-neoplastic mucosa of ulcerative colitis patients with colorectal cancer: evidence for a field effect. Inflammatory Bowel Diseases. 2013;19(10):2079–2083. doi: 10.1097/MIB.0b013e31829b3f4d.
    1. Brentnall T. A., Pan S., Bronner M. P., et al. Proteins that underlie neoplastic progression of ulcerative colitis. Proteomics Clinical Applications. 2009;3(11):p. 1326. doi: 10.1002/prca.200900061.
    1. May D., Pan S., Crispin D. A., et al. Investigating neoplastic progression of ulcerative colitis with label-free comparative proteomics. Journal of Proteome Research. 2011;10(1):200–209. doi: 10.1021/pr100574p.
    1. Salk J. J., Salipante S. J., Risques R. A., et al. Clonal expansions in ulcerative colitis identify patients with neoplasia. Proceedings of the National Academy of Sciences of the United States of America. 2009;106(49):20871–20876. doi: 10.1073/pnas.0909428106.
    1. Yoshizawa S., Matsuoka K., Inoue N., et al. Clinical significance of serum p53 antibodies in patients with ulcerative colitis and its carcinogenesis. Inflammatory Bowel Diseases. 2007;13(7):865–873. doi: 10.1002/ibd.20112.
    1. Paraskevi A., Theodoropoulos G., Papaconstantinou I., Mantzaris G., Nikiteas N., Gazouli M. Circulating microRNA in inflammatory bowel disease. Journal of Crohn's & Colitis. 2012;6(9):900–904. doi: 10.1016/j.crohns.2012.02.006.
    1. Wu F., Guo N. J., Tian H., et al. Peripheral blood microRNAs distinguish active ulcerative colitis and Crohn’s disease. Inflammatory Bowel Diseases. 2011;17(1):241–250. doi: 10.1002/ibd.21450.
    1. Duttagupta R., DiRienzo S., Jiang R., et al. Genome-wide maps of circulating miRNA biomarkers for ulcerative colitis. PLoS One. 2012;7(2, article e31241) doi: 10.1371/journal.pone.0031241.

Source: PubMed

Подписаться