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Published in: BMC Cancer 1/2013

Open Access 01-12-2013 | Research article

Potentiality of a triple microRNA classifier: miR-193a-3p, miR-23a and miR-338-5p for early detection of colorectal cancer

Authors: Fung Lin Yong, Chee Wei Law, Chee Woon Wang

Published in: BMC Cancer | Issue 1/2013

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Abstract

Background

MicroRNAs (miRNAs) are short, non-coding RNA molecules that act as regulators of gene expression. Circulating blood miRNAs offer great potential as cancer biomarkers. The objective of this study was to correlate the differential expression of miRNAs in tissue and blood in the identification of biomarkers for early detection of colorectal cancer (CRC).

Methods

The study was divided into two phases: (I) Marker discovery by miRNA microarray using paired cancer tissues (n = 30) and blood samples (CRC, n = 42; control, n = 18). (II) Marker validation by stem-loop reverse transcription real time PCR using an independent set of paired cancer tissues (n = 30) and blood samples (CRC, n = 70; control, n = 32). Correlation analysis was determined by Pearson’s test. Logistic regression and receiver operating characteristics curve analyses were applied to obtain diagnostic utility of the miRNAs.

Results

Seven miRNAs (miR-150, miR-193a-3p, miR-23a, miR-23b, miR-338-5p, miR-342-3p and miR-483-3p) have been found to be differentially expressed in both tissue and blood samples. Significant positive correlations were observed in the tissue and blood levels of miR-193a-3p, miR-23a and miR-338-5p. Moreover, increased expressions of these miRNAs were detected in the more advanced stages. MiR-193a-3p, miR-23a and miR-338-5p were demonstrated as a classifier for CRC detection, yielding a receiver operating characteristic curve area of 0.887 (80.0% sensitivity, 84.4% specificity and 83.3% accuracy).

Conclusion

Dysregulations in circulating blood miRNAs are reflective of those in colorectal tissues. The triple miRNA classifier of miR-193a-3p, miR-23a and miR-338-5p appears to be a potential blood biomarker for early detection of CRC.
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Literature
2.
go back to reference Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D: Global cancer statistics. CA Cancer J Clin. 2011, 61: 69-90. 10.3322/caac.20107.CrossRefPubMed Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D: Global cancer statistics. CA Cancer J Clin. 2011, 61: 69-90. 10.3322/caac.20107.CrossRefPubMed
3.
go back to reference Bray F, Jemal A, Grey N, Ferlay J, Forman D: Global cancer transitions according to the Human Development Index (2008–2030): a population-based study. Lancet Oncol. 2012, 13 (8): 790-801. 10.1016/S1470-2045(12)70211-5.CrossRefPubMed Bray F, Jemal A, Grey N, Ferlay J, Forman D: Global cancer transitions according to the Human Development Index (2008–2030): a population-based study. Lancet Oncol. 2012, 13 (8): 790-801. 10.1016/S1470-2045(12)70211-5.CrossRefPubMed
4.
go back to reference American Cancer Society: Cancer Facts & Figures 2012. 2012, Atlanta: American Cancer Society American Cancer Society: Cancer Facts & Figures 2012. 2012, Atlanta: American Cancer Society
5.
go back to reference Zainal Ariffin O, Nor Saleha IT: National Cancer Registry Report 2007. 2011, Malaysia: Ministry of Healthy Zainal Ariffin O, Nor Saleha IT: National Cancer Registry Report 2007. 2011, Malaysia: Ministry of Healthy
6.
go back to reference McFarland EG, Levin B, Lieberman DA, Pickhardt PJ, Johnson CD, Glick SN, Brooks D, Smith RA: Revised colorectal screening guidelines: joint effort of the American Cancer Society, U.S. Multisociety Task Force on Colorectal Cancer, and American College of Radiology. Radiology. 2008, 248: 717-720. 10.1148/radiol.2483080842.CrossRefPubMed McFarland EG, Levin B, Lieberman DA, Pickhardt PJ, Johnson CD, Glick SN, Brooks D, Smith RA: Revised colorectal screening guidelines: joint effort of the American Cancer Society, U.S. Multisociety Task Force on Colorectal Cancer, and American College of Radiology. Radiology. 2008, 248: 717-720. 10.1148/radiol.2483080842.CrossRefPubMed
8.
go back to reference Neri E, Faggioni L, Cerri F, Turini F, Angeli S, Cini L, Perrone F, Paolicchi F, Bartolozzi C: CT colonography versus double-contrast barium enema for screening of colorectal cancer: comparison of radiation burden. Abdom Imaging. 2010, 35: 596-601. 10.1007/s00261-009-9568-x.CrossRefPubMed Neri E, Faggioni L, Cerri F, Turini F, Angeli S, Cini L, Perrone F, Paolicchi F, Bartolozzi C: CT colonography versus double-contrast barium enema for screening of colorectal cancer: comparison of radiation burden. Abdom Imaging. 2010, 35: 596-601. 10.1007/s00261-009-9568-x.CrossRefPubMed
9.
go back to reference Choong MK, Tsafnat G: Genetic and epigenetic biomarkers of colorectal cancer. Clin Gastroenterol Hepatol. 2012, 10: 9-15. 10.1016/j.cgh.2011.04.020.CrossRefPubMed Choong MK, Tsafnat G: Genetic and epigenetic biomarkers of colorectal cancer. Clin Gastroenterol Hepatol. 2012, 10: 9-15. 10.1016/j.cgh.2011.04.020.CrossRefPubMed
10.
go back to reference Khalid-de Bakker CA, Jonkers DM, Sanduleanu S, de Bruïne AP, Meijer GA, Janssen JB, van Engeland M, Stockbrügger RW, Masclee AA: Test performance of immunologic fecal occult blood testing and sigmoidoscopy compared with primary colonoscopy screening for colorectal advanced adenomas. Cancer Prev Res. 2011, 4 (10): 1563-1571. 10.1158/1940-6207.CAPR-11-0076.CrossRef Khalid-de Bakker CA, Jonkers DM, Sanduleanu S, de Bruïne AP, Meijer GA, Janssen JB, van Engeland M, Stockbrügger RW, Masclee AA: Test performance of immunologic fecal occult blood testing and sigmoidoscopy compared with primary colonoscopy screening for colorectal advanced adenomas. Cancer Prev Res. 2011, 4 (10): 1563-1571. 10.1158/1940-6207.CAPR-11-0076.CrossRef
11.
go back to reference Imperiale TF, Ransohoff DF, Itzkowitz SH, Turnbull BA, Ross ME: Fecal DNA versus fecal occult blood for colorectal-cancer screening in an average risk population. N Engl J Med. 2004, 351: 2704-2714. 10.1056/NEJMoa033403.CrossRefPubMed Imperiale TF, Ransohoff DF, Itzkowitz SH, Turnbull BA, Ross ME: Fecal DNA versus fecal occult blood for colorectal-cancer screening in an average risk population. N Engl J Med. 2004, 351: 2704-2714. 10.1056/NEJMoa033403.CrossRefPubMed
12.
go back to reference Zou H, Taylor WR, Harrington JJ, Hussain FTN, Cao X, Loprinzi CL, Levine TR, Rex DK, Ahnen D, Knigge KL, et al: High detection rates of colorectal neoplasia by stool DNA testing with a novel digital melt curve assay. Gastroenterology. 2009, 136: 459-470. 10.1053/j.gastro.2008.10.023.CrossRefPubMed Zou H, Taylor WR, Harrington JJ, Hussain FTN, Cao X, Loprinzi CL, Levine TR, Rex DK, Ahnen D, Knigge KL, et al: High detection rates of colorectal neoplasia by stool DNA testing with a novel digital melt curve assay. Gastroenterology. 2009, 136: 459-470. 10.1053/j.gastro.2008.10.023.CrossRefPubMed
13.
go back to reference U.S. Preventive Services Task Force: Screening for colorectal cancer: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med. 2008, 149 (9): 627-637.CrossRef U.S. Preventive Services Task Force: Screening for colorectal cancer: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med. 2008, 149 (9): 627-637.CrossRef
14.
go back to reference Ahlquist DA, Sargent DJ, Loprinzi CL, Levin TR, Rex DK, Ahnen DJ, Knigge K, Lance MP, Burgart LJ, Hamilton SR, et al: Stool DNA and occult blood testing for screen detection of colorectal neoplasia. Ann Intern Med. 2008, 149 (7): 441-450. 10.7326/0003-4819-149-7-200810070-00004.CrossRefPubMedPubMedCentral Ahlquist DA, Sargent DJ, Loprinzi CL, Levin TR, Rex DK, Ahnen DJ, Knigge K, Lance MP, Burgart LJ, Hamilton SR, et al: Stool DNA and occult blood testing for screen detection of colorectal neoplasia. Ann Intern Med. 2008, 149 (7): 441-450. 10.7326/0003-4819-149-7-200810070-00004.CrossRefPubMedPubMedCentral
15.
go back to reference Bartel DP: MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004, 116: 281-297. 10.1016/S0092-8674(04)00045-5.CrossRefPubMed Bartel DP: MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004, 116: 281-297. 10.1016/S0092-8674(04)00045-5.CrossRefPubMed
17.
go back to reference Li L-C, Okino ST, Zhao H, Pookot D, Place RF, Urakami S, Enokida H, Dahiya R: Small dsRNAs induce transcriptional activation in human cells. Proc Natl Acad Sci USA. 2006, 103 (46): 17337-17342. 10.1073/pnas.0607015103.CrossRefPubMedPubMedCentral Li L-C, Okino ST, Zhao H, Pookot D, Place RF, Urakami S, Enokida H, Dahiya R: Small dsRNAs induce transcriptional activation in human cells. Proc Natl Acad Sci USA. 2006, 103 (46): 17337-17342. 10.1073/pnas.0607015103.CrossRefPubMedPubMedCentral
18.
go back to reference Lee RC, Feinbaum RL, Ambros V: The C.elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell. 1993, 75: 843-854. 10.1016/0092-8674(93)90529-Y.CrossRefPubMed Lee RC, Feinbaum RL, Ambros V: The C.elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell. 1993, 75: 843-854. 10.1016/0092-8674(93)90529-Y.CrossRefPubMed
19.
go back to reference Kozamara A, Griffiths-Jones S: miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res. 2011, 39: D152-D157. 10.1093/nar/gkq1027.CrossRef Kozamara A, Griffiths-Jones S: miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res. 2011, 39: D152-D157. 10.1093/nar/gkq1027.CrossRef
20.
go back to reference Esquela-Kerscher A, Slack FJ: Oncomirs - microRNAs with a role in cancer. Nat Rev Cancer. 2006, 6: 259-269.CrossRefPubMed Esquela-Kerscher A, Slack FJ: Oncomirs - microRNAs with a role in cancer. Nat Rev Cancer. 2006, 6: 259-269.CrossRefPubMed
21.
go back to reference Bueno MJ, Malumbres M: MicroRNA and the cell cycle. Biochim Biophys Acta. 2011, 1812 (5): 592-601. 10.1016/j.bbadis.2011.02.002.CrossRefPubMed Bueno MJ, Malumbres M: MicroRNA and the cell cycle. Biochim Biophys Acta. 2011, 1812 (5): 592-601. 10.1016/j.bbadis.2011.02.002.CrossRefPubMed
22.
go back to reference Henegan HM, Miller N, Kerin MJ: MiRNAs as biomarkers and therapeutic targets in cancer. Curr Opin Pharmacol. 2010, 10: 543-550. 10.1016/j.coph.2010.05.010.CrossRef Henegan HM, Miller N, Kerin MJ: MiRNAs as biomarkers and therapeutic targets in cancer. Curr Opin Pharmacol. 2010, 10: 543-550. 10.1016/j.coph.2010.05.010.CrossRef
23.
go back to reference Lima RT, Busacca S, Almeida GM, Gaudino G, Fennell DA, Vasconcelos MH: MicroRNA regulation of core apoptosis pathways in cancer. Eur J Cancer. 2011, 47: 163-174. 10.1016/j.ejca.2010.11.005.CrossRefPubMed Lima RT, Busacca S, Almeida GM, Gaudino G, Fennell DA, Vasconcelos MH: MicroRNA regulation of core apoptosis pathways in cancer. Eur J Cancer. 2011, 47: 163-174. 10.1016/j.ejca.2010.11.005.CrossRefPubMed
24.
go back to reference Calin GA, Sevignani C, Dumitru CD, Hyslop T, Noch E, Yendamuri S, Shimizu M, Rattan S, Bullrich F, Negrini M, et al: Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc Natl Acad Sci USA. 2004, 101 (9): 2999-3004. 10.1073/pnas.0307323101.CrossRefPubMedPubMedCentral Calin GA, Sevignani C, Dumitru CD, Hyslop T, Noch E, Yendamuri S, Shimizu M, Rattan S, Bullrich F, Negrini M, et al: Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc Natl Acad Sci USA. 2004, 101 (9): 2999-3004. 10.1073/pnas.0307323101.CrossRefPubMedPubMedCentral
25.
go back to reference Koturbash I, Zemp FJ, Pogribny I, Kovalchuk O: Small molecules with big effects: the role of the microRNAome in cancer and carcinogenesis. Mutat Res. 2011, 722: 94-105. 10.1016/j.mrgentox.2010.05.006.CrossRefPubMed Koturbash I, Zemp FJ, Pogribny I, Kovalchuk O: Small molecules with big effects: the role of the microRNAome in cancer and carcinogenesis. Mutat Res. 2011, 722: 94-105. 10.1016/j.mrgentox.2010.05.006.CrossRefPubMed
26.
go back to reference Babashah S, Soleimani M: The oncogenic and tumour suppresive roles of microRNAs in cancer and apoptosis. Eur J Cancer. 2011, 47: 1127-1137. 10.1016/j.ejca.2011.02.008.CrossRefPubMed Babashah S, Soleimani M: The oncogenic and tumour suppresive roles of microRNAs in cancer and apoptosis. Eur J Cancer. 2011, 47: 1127-1137. 10.1016/j.ejca.2011.02.008.CrossRefPubMed
27.
go back to reference Groce CM: Causes and consequences of microRNA dysregulation in cancer. Nat Rev Genet. 2009, 10: 704-714. 10.1038/nrg2634.CrossRef Groce CM: Causes and consequences of microRNA dysregulation in cancer. Nat Rev Genet. 2009, 10: 704-714. 10.1038/nrg2634.CrossRef
28.
go back to reference Liu M, Chen H: The role of microRNAs in colorectal cancer. J Genet Genomics. 2010, 37: 347-358. 10.1016/S1673-8527(09)60053-9.CrossRefPubMed Liu M, Chen H: The role of microRNAs in colorectal cancer. J Genet Genomics. 2010, 37: 347-358. 10.1016/S1673-8527(09)60053-9.CrossRefPubMed
29.
go back to reference Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, Visone R, Lorio M, Roldo C, Ferracin M, et al: A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA. 2006, 103 (7): 2257-2261. 10.1073/pnas.0510565103.CrossRefPubMedPubMedCentral Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, Visone R, Lorio M, Roldo C, Ferracin M, et al: A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA. 2006, 103 (7): 2257-2261. 10.1073/pnas.0510565103.CrossRefPubMedPubMedCentral
30.
31.
go back to reference Weber JA, Baxter DH, Zhang S, Huang DY, Huang KH, Lee MJ, Galas DJ, Wang K: The microRNA spectrum in 12 body fluids. Clin Chem. 2010, 56 (11): 1733-1741. 10.1373/clinchem.2010.147405.CrossRefPubMedPubMedCentral Weber JA, Baxter DH, Zhang S, Huang DY, Huang KH, Lee MJ, Galas DJ, Wang K: The microRNA spectrum in 12 body fluids. Clin Chem. 2010, 56 (11): 1733-1741. 10.1373/clinchem.2010.147405.CrossRefPubMedPubMedCentral
32.
go back to reference Link A, Balaguer F, Shen Y, Nagasaka T, Lozano JJ, Boland CR, Goel A: Fecal microRNAs as novel biomarkers for colon cancer screening. Cancer Epidemiol Biomarkers Prev. 2010, 19 (7): 1766-1774. 10.1158/1055-9965.EPI-10-0027.CrossRefPubMedPubMedCentral Link A, Balaguer F, Shen Y, Nagasaka T, Lozano JJ, Boland CR, Goel A: Fecal microRNAs as novel biomarkers for colon cancer screening. Cancer Epidemiol Biomarkers Prev. 2010, 19 (7): 1766-1774. 10.1158/1055-9965.EPI-10-0027.CrossRefPubMedPubMedCentral
33.
go back to reference Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO: Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007, 9: 654-659. 10.1038/ncb1596.CrossRefPubMed Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO: Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007, 9: 654-659. 10.1038/ncb1596.CrossRefPubMed
34.
go back to reference Hunter MP, Ismail N, Zhang X, Aguda BD, Lee EJ, Yu L, Xiao T, Schafer J, Ting Lee M-L, Schmittgen TD, et al: Detection of microRNA expression in human peripheral blood microvesicles. PLoS One. 2008, 3 (11): e3694-10.1371/journal.pone.0003694.CrossRefPubMedPubMedCentral Hunter MP, Ismail N, Zhang X, Aguda BD, Lee EJ, Yu L, Xiao T, Schafer J, Ting Lee M-L, Schmittgen TD, et al: Detection of microRNA expression in human peripheral blood microvesicles. PLoS One. 2008, 3 (11): e3694-10.1371/journal.pone.0003694.CrossRefPubMedPubMedCentral
35.
go back to reference Di Stefano V, Zaccagnini G, Capogrossi MC, Martelli F: microRNAs as peripheral blood biomarkers of cardiovascular disease. Vascul Pharmacol. 2011, 55: 111-118. 10.1016/j.vph.2011.08.001.CrossRefPubMed Di Stefano V, Zaccagnini G, Capogrossi MC, Martelli F: microRNAs as peripheral blood biomarkers of cardiovascular disease. Vascul Pharmacol. 2011, 55: 111-118. 10.1016/j.vph.2011.08.001.CrossRefPubMed
36.
go back to reference Zhang J, Zhao H, Gao Y, Zhang W: Secretory miRNAs as novel cancer biomarkers. Biochim Biophys Acta. 2012, 1826 (1): 32-43.PubMed Zhang J, Zhao H, Gao Y, Zhang W: Secretory miRNAs as novel cancer biomarkers. Biochim Biophys Acta. 2012, 1826 (1): 32-43.PubMed
37.
go back to reference Zampetaki A, Kiechl S, Drozdov I, Willeit P, Mayr U, Prokopi M, Mayr A, Weger S, Oberhollenzer F, Bonora E, et al: Plasma microRNA profiling reveals loss of endothelial miR-126 and other microRNAs in type 2 diabetes. Circ Res. 2010, 107: 810-817. 10.1161/CIRCRESAHA.110.226357.CrossRefPubMed Zampetaki A, Kiechl S, Drozdov I, Willeit P, Mayr U, Prokopi M, Mayr A, Weger S, Oberhollenzer F, Bonora E, et al: Plasma microRNA profiling reveals loss of endothelial miR-126 and other microRNAs in type 2 diabetes. Circ Res. 2010, 107: 810-817. 10.1161/CIRCRESAHA.110.226357.CrossRefPubMed
38.
go back to reference Schrauder MG, Strick R, Schulz-Wendtland R, Strissel PL, Kahmann L, Loehberg CR, Lux MP, Jud SM, Hartmann A, Hein A, et al: Circulating micro-RNAs as potential blood-based markers for early stage breast cancer detection. PLoS One. 2012, 7 (1): e29770-10.1371/journal.pone.0029770.CrossRefPubMedPubMedCentral Schrauder MG, Strick R, Schulz-Wendtland R, Strissel PL, Kahmann L, Loehberg CR, Lux MP, Jud SM, Hartmann A, Hein A, et al: Circulating micro-RNAs as potential blood-based markers for early stage breast cancer detection. PLoS One. 2012, 7 (1): e29770-10.1371/journal.pone.0029770.CrossRefPubMedPubMedCentral
39.
go back to reference Heneghan HM, Miller N, Lowery AJ, Sweeney KJ, Newell J: Circulating microRNAs as novel minimally invasive biomarkers for breast cancer. Ann Surg. 2010, 251: 499-505. 10.1097/SLA.0b013e3181cc939f.CrossRefPubMed Heneghan HM, Miller N, Lowery AJ, Sweeney KJ, Newell J: Circulating microRNAs as novel minimally invasive biomarkers for breast cancer. Ann Surg. 2010, 251: 499-505. 10.1097/SLA.0b013e3181cc939f.CrossRefPubMed
40.
go back to reference Kosaka N, Iguchi H, Ochiya T: Circulating microRNA in body fluid: a new potential biomarker for cancer diagnosis and prognosis. Cancer Sci. 2010, 101 (10): 2087-2092. 10.1111/j.1349-7006.2010.01650.x.CrossRefPubMed Kosaka N, Iguchi H, Ochiya T: Circulating microRNA in body fluid: a new potential biomarker for cancer diagnosis and prognosis. Cancer Sci. 2010, 101 (10): 2087-2092. 10.1111/j.1349-7006.2010.01650.x.CrossRefPubMed
41.
go back to reference Turchinovich A, Weiz L, Langheinz A, Burwinkel B: Characterization of extracellular miRNA. Nucleic Acids Res. 2011, 39 (16): 7223-7233. 10.1093/nar/gkr254.CrossRefPubMedPubMedCentral Turchinovich A, Weiz L, Langheinz A, Burwinkel B: Characterization of extracellular miRNA. Nucleic Acids Res. 2011, 39 (16): 7223-7233. 10.1093/nar/gkr254.CrossRefPubMedPubMedCentral
42.
go back to reference Luo X, Burwinkel B, Tao S, Brenner H: MicroRNA signatures: novel biomarker for colorectal cancer?. Cancer Epidemiol Biomarkers Prev. 2011, 20 (7): 1272-1286. 10.1158/1055-9965.EPI-11-0035.CrossRefPubMed Luo X, Burwinkel B, Tao S, Brenner H: MicroRNA signatures: novel biomarker for colorectal cancer?. Cancer Epidemiol Biomarkers Prev. 2011, 20 (7): 1272-1286. 10.1158/1055-9965.EPI-11-0035.CrossRefPubMed
43.
go back to reference Schroeder A, Mueller O, Stocker S, Salowsky R, Leiber M, Gassmann M, Lightfoot S, Menzel W, Granzow M, Ragg T: The RIN: an RNA integrity number for assigning integrity values to RNA measurements. BMC Mol Biol. 2006, 7: 3-10.1186/1471-2199-7-3.CrossRefPubMedPubMedCentral Schroeder A, Mueller O, Stocker S, Salowsky R, Leiber M, Gassmann M, Lightfoot S, Menzel W, Granzow M, Ragg T: The RIN: an RNA integrity number for assigning integrity values to RNA measurements. BMC Mol Biol. 2006, 7: 3-10.1186/1471-2199-7-3.CrossRefPubMedPubMedCentral
44.
go back to reference Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP: Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003, 4: 249-264. 10.1093/biostatistics/4.2.249.CrossRefPubMed Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP: Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003, 4: 249-264. 10.1093/biostatistics/4.2.249.CrossRefPubMed
45.
go back to reference Jordan JA, Durso MB: Real-time polymerase chain reaction for detecting bacterial DNA directly from blood of neonates being evaluated for Sepsis. J Mol Diagn. 2005, 7 (5): 575-581. 10.1016/S1525-1578(10)60590-9.CrossRefPubMedPubMedCentral Jordan JA, Durso MB: Real-time polymerase chain reaction for detecting bacterial DNA directly from blood of neonates being evaluated for Sepsis. J Mol Diagn. 2005, 7 (5): 575-581. 10.1016/S1525-1578(10)60590-9.CrossRefPubMedPubMedCentral
46.
go back to reference Caraguel CGB, Stryhn H, Gagne N, Dohoo IR, Hammell KL: Selection of a cutoff value for real-time polymerase chain reaction results to fit a diagnostic purpose: analytical and epidemiologic approaches. J Vet Diagn Invest. 2011, 23: 2-15. 10.1177/104063871102300102.CrossRefPubMed Caraguel CGB, Stryhn H, Gagne N, Dohoo IR, Hammell KL: Selection of a cutoff value for real-time polymerase chain reaction results to fit a diagnostic purpose: analytical and epidemiologic approaches. J Vet Diagn Invest. 2011, 23: 2-15. 10.1177/104063871102300102.CrossRefPubMed
48.
49.
go back to reference Piepoli A, Tavano F, Copetti M, Mazza T, Palumbo O, Panza A, di Mola FF, Pazienza V, Mazzoccoli G, Biscaglia G, et al: Mirna expression profiles identify drivers in colorectal and pancreatic cancers. PLoS One. 2012, 7 (3): e33663-10.1371/journal.pone.0033663.CrossRefPubMedPubMedCentral Piepoli A, Tavano F, Copetti M, Mazza T, Palumbo O, Panza A, di Mola FF, Pazienza V, Mazzoccoli G, Biscaglia G, et al: Mirna expression profiles identify drivers in colorectal and pancreatic cancers. PLoS One. 2012, 7 (3): e33663-10.1371/journal.pone.0033663.CrossRefPubMedPubMedCentral
50.
go back to reference Hamfjord J, Stangeland AM, Hughes T, Skrede ML, Tveit KM, Ikdahl T, Kure EH: Differential expression of miRNAs in colorectal cancer: comparison of paired tumor tissue and adjacent normal mucosa using high-throughput sequencing. PLoS One. 2012, 7 (4): e34150-10.1371/journal.pone.0034150.CrossRefPubMedPubMedCentral Hamfjord J, Stangeland AM, Hughes T, Skrede ML, Tveit KM, Ikdahl T, Kure EH: Differential expression of miRNAs in colorectal cancer: comparison of paired tumor tissue and adjacent normal mucosa using high-throughput sequencing. PLoS One. 2012, 7 (4): e34150-10.1371/journal.pone.0034150.CrossRefPubMedPubMedCentral
51.
go back to reference Ahmed FE, Amed NC, Vos PW, Bonnerup C, Atkins JN, Casey M, Nuovo GJ, Naziri W, WIley JE, Allison RR: Diagnostic microRNA markers to screen for sporadic human colon cancer in blood. Cancer Genomics Proteomics. 2012, 9 (4): 179-192.PubMed Ahmed FE, Amed NC, Vos PW, Bonnerup C, Atkins JN, Casey M, Nuovo GJ, Naziri W, WIley JE, Allison RR: Diagnostic microRNA markers to screen for sporadic human colon cancer in blood. Cancer Genomics Proteomics. 2012, 9 (4): 179-192.PubMed
52.
go back to reference Ng EK, Chong WW, Jin H, Lam EK, Shin VY, Yu J: Differential expression of microRNAs in plasma of patients with colorectal cancer: a potential marker for colorectal cancer screening. Gut. 2009, 58: 1375-1381. 10.1136/gut.2008.167817.CrossRefPubMed Ng EK, Chong WW, Jin H, Lam EK, Shin VY, Yu J: Differential expression of microRNAs in plasma of patients with colorectal cancer: a potential marker for colorectal cancer screening. Gut. 2009, 58: 1375-1381. 10.1136/gut.2008.167817.CrossRefPubMed
53.
go back to reference Benjamin H, Lebanony D, Rosenwald S, Cohen L, Gibori H, Barabash N, Ashkenazi K, Goren E, Meiri E, Morgenstern S, et al: A diagnostic assay based on microRNA expression accurately identifies malignant pleural mesothelioma. J Mol Diagn. 2010, 12 (6): 771-779. 10.2353/jmoldx.2010.090169.CrossRefPubMedPubMedCentral Benjamin H, Lebanony D, Rosenwald S, Cohen L, Gibori H, Barabash N, Ashkenazi K, Goren E, Meiri E, Morgenstern S, et al: A diagnostic assay based on microRNA expression accurately identifies malignant pleural mesothelioma. J Mol Diagn. 2010, 12 (6): 771-779. 10.2353/jmoldx.2010.090169.CrossRefPubMedPubMedCentral
54.
go back to reference Baumhoer D, Zillmer S, Unger K, Rosemann M, Atkinson MJ, Irmler M, Beckers J, Siggelkow H, Von Luettichau I, Jundt G, et al: MicroRNA profiling with correlation to gene expression revealed the oncogenic miR-17-92 cluster to be up-regulated in osteosarcoma. Cancer Genet. 2012, 205: 212-219. 10.1016/j.cancergen.2012.03.001.CrossRefPubMed Baumhoer D, Zillmer S, Unger K, Rosemann M, Atkinson MJ, Irmler M, Beckers J, Siggelkow H, Von Luettichau I, Jundt G, et al: MicroRNA profiling with correlation to gene expression revealed the oncogenic miR-17-92 cluster to be up-regulated in osteosarcoma. Cancer Genet. 2012, 205: 212-219. 10.1016/j.cancergen.2012.03.001.CrossRefPubMed
55.
go back to reference Kozaki K, Imoto I, Mogi S, Omura K, Inazawa J: Exploration of tumor-suppressive microRNAs silenced by DNA hypermethylation in oral cancer. Cancer Res. 2008, 68 (7): 2094-2105. 10.1158/0008-5472.CAN-07-5194.CrossRefPubMed Kozaki K, Imoto I, Mogi S, Omura K, Inazawa J: Exploration of tumor-suppressive microRNAs silenced by DNA hypermethylation in oral cancer. Cancer Res. 2008, 68 (7): 2094-2105. 10.1158/0008-5472.CAN-07-5194.CrossRefPubMed
56.
go back to reference Jahid S, Sun J, Edwards RA, Dizon D, Panarelli NC, Milsom JW, Sikandar SS, Gumus ZH, Lipkin SM: miR-23a promotes the transition from indolent to invasive colorectal cancer. Cancer Discov. 2012, 2 (6): 540-553. 10.1158/2159-8290.CD-11-0267.CrossRefPubMedPubMedCentral Jahid S, Sun J, Edwards RA, Dizon D, Panarelli NC, Milsom JW, Sikandar SS, Gumus ZH, Lipkin SM: miR-23a promotes the transition from indolent to invasive colorectal cancer. Cancer Discov. 2012, 2 (6): 540-553. 10.1158/2159-8290.CD-11-0267.CrossRefPubMedPubMedCentral
57.
go back to reference Chen X, Ba Y, Ma L, Cai X, Yin Y, Wang K, Guo J, Zhang Y, Chen J, Guo X, et al: Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res. 2008, 18: 997-1006. 10.1038/cr.2008.282.CrossRefPubMed Chen X, Ba Y, Ma L, Cai X, Yin Y, Wang K, Guo J, Zhang Y, Chen J, Guo X, et al: Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res. 2008, 18: 997-1006. 10.1038/cr.2008.282.CrossRefPubMed
58.
go back to reference Zhu LH, Liu T, Tang H, Tian RQ, Su C, Liu M, Li X: MicroRNA-23a promotes the growth of gastric adenocarcinoma cell line MGC803 and downregulates interleukin-6 receptor. FEBS J. 2010, 277: 3726-3734. 10.1111/j.1742-4658.2010.07773.x.CrossRefPubMed Zhu LH, Liu T, Tang H, Tian RQ, Su C, Liu M, Li X: MicroRNA-23a promotes the growth of gastric adenocarcinoma cell line MGC803 and downregulates interleukin-6 receptor. FEBS J. 2010, 277: 3726-3734. 10.1111/j.1742-4658.2010.07773.x.CrossRefPubMed
59.
go back to reference Chhabra R, Dubey R, Saini N: Cooperative and individualistic functions of the microRNAs in the miR23a ~ 27a ~ 24-2 cluster and its implication in human diseases. Mol Cancer. 2010, 9: 232-10.1186/1476-4598-9-232.CrossRefPubMedPubMedCentral Chhabra R, Dubey R, Saini N: Cooperative and individualistic functions of the microRNAs in the miR23a ~ 27a ~ 24-2 cluster and its implication in human diseases. Mol Cancer. 2010, 9: 232-10.1186/1476-4598-9-232.CrossRefPubMedPubMedCentral
60.
go back to reference Willert K, Jones KA: Wnt signaling: is the party in the nucleus?. Genes Dev. 2006, 20: 1394-1404. 10.1101/gad.1424006.CrossRefPubMed Willert K, Jones KA: Wnt signaling: is the party in the nucleus?. Genes Dev. 2006, 20: 1394-1404. 10.1101/gad.1424006.CrossRefPubMed
61.
go back to reference Rogler CE, LeVoci L, Ader T, Massimi A, Tchaikovskaya T, Norel R, Rogler LE: MicroRNA-23b cluster microRNAs regulate transforming growth factor-beta/bone morphogenetic protein signaling and liver stem cell differentiation by targeting smads. Hepatology. 2009, 50: 575-584. 10.1002/hep.22982.CrossRefPubMed Rogler CE, LeVoci L, Ader T, Massimi A, Tchaikovskaya T, Norel R, Rogler LE: MicroRNA-23b cluster microRNAs regulate transforming growth factor-beta/bone morphogenetic protein signaling and liver stem cell differentiation by targeting smads. Hepatology. 2009, 50: 575-584. 10.1002/hep.22982.CrossRefPubMed
62.
go back to reference Gao P, Tchernyshyov I, Chang TC, Lee YS, Kita K, Ochi T, Zeller K, De Marzo AM, Van Eyk JE, Mendell JT, et al: c-Myc suppression of miR-23a/b enhances mitochondrial glutaminase and glutamine metabolism. Nature. 2009, 458 (7239): 762-765. 10.1038/nature07823.CrossRefPubMedPubMedCentral Gao P, Tchernyshyov I, Chang TC, Lee YS, Kita K, Ochi T, Zeller K, De Marzo AM, Van Eyk JE, Mendell JT, et al: c-Myc suppression of miR-23a/b enhances mitochondrial glutaminase and glutamine metabolism. Nature. 2009, 458 (7239): 762-765. 10.1038/nature07823.CrossRefPubMedPubMedCentral
63.
go back to reference Saumet A, Vetter G, Bouttier M, Portales-Casamar E, Wasserman WW, Maurin T, Mari B, Barbry P, Vallar L, Friederich E, et al: Transcriptional repression of microRNA genes by PML-RARA increases expression of key cancer proteins in acute promyelocytic leukemia. Blood. 2009, 113 (2): 412-421.CrossRefPubMed Saumet A, Vetter G, Bouttier M, Portales-Casamar E, Wasserman WW, Maurin T, Mari B, Barbry P, Vallar L, Friederich E, et al: Transcriptional repression of microRNA genes by PML-RARA increases expression of key cancer proteins in acute promyelocytic leukemia. Blood. 2009, 113 (2): 412-421.CrossRefPubMed
64.
go back to reference Schetter AJ, Leung SY, Sohn JJ, Zanetti KA, Bowman ED, Yanaihara N, Yuen ST, Chan TL, Kwong DLW, Au GKH, et al: MicroRNA expression profiles associated with prognosis and therapeutic outcome in colon adenocarcinoma. JAMA. 2008, 299 (4): 425-436. 10.1001/jama.299.4.425.CrossRefPubMedPubMedCentral Schetter AJ, Leung SY, Sohn JJ, Zanetti KA, Bowman ED, Yanaihara N, Yuen ST, Chan TL, Kwong DLW, Au GKH, et al: MicroRNA expression profiles associated with prognosis and therapeutic outcome in colon adenocarcinoma. JAMA. 2008, 299 (4): 425-436. 10.1001/jama.299.4.425.CrossRefPubMedPubMedCentral
65.
go back to reference Budhu A, Jia HL, Forgues M, Liu CG, Goldstein D, Lam A, Zanetti KA, Ye QH, Qin LX, Croce CM, et al: Identification of metastasis-related microRNAs in hepatocellular carcinoma. Hepatology. 2008, 47 (3): 897-907. 10.1002/hep.22160.CrossRefPubMed Budhu A, Jia HL, Forgues M, Liu CG, Goldstein D, Lam A, Zanetti KA, Ye QH, Qin LX, Croce CM, et al: Identification of metastasis-related microRNAs in hepatocellular carcinoma. Hepatology. 2008, 47 (3): 897-907. 10.1002/hep.22160.CrossRefPubMed
66.
go back to reference Wong TS, Liu XB, Wong BYH, Ng WM, Yuen APW, Wei WI: Mature miR-184 as potential oncogenic microRNA of squamous cell carcinoma of tongue. Clin Cancer Res. 2008, 14 (9): 2588-2592. 10.1158/1078-0432.CCR-07-0666.CrossRefPubMed Wong TS, Liu XB, Wong BYH, Ng WM, Yuen APW, Wei WI: Mature miR-184 as potential oncogenic microRNA of squamous cell carcinoma of tongue. Clin Cancer Res. 2008, 14 (9): 2588-2592. 10.1158/1078-0432.CCR-07-0666.CrossRefPubMed
67.
go back to reference Ju JA, Huang YC, Lan SH, Wang TH, Lin PC, Lee JC, Niu KC, Tian YF, Liu HS: Identification of colorectal cancer recurrence-related microRNAs. GMBHS. 2012, 4: 19-20. Ju JA, Huang YC, Lan SH, Wang TH, Lin PC, Lee JC, Niu KC, Tian YF, Liu HS: Identification of colorectal cancer recurrence-related microRNAs. GMBHS. 2012, 4: 19-20.
Metadata
Title
Potentiality of a triple microRNA classifier: miR-193a-3p, miR-23a and miR-338-5p for early detection of colorectal cancer
Authors
Fung Lin Yong
Chee Wei Law
Chee Woon Wang
Publication date
01-12-2013
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2013
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/1471-2407-13-280

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