Advertisement

Molecular Diagnosis & Therapy

, Volume 18, Issue 3, pp 303–308 | Cite as

Circulating microRNA Testing for the Early Diagnosis and Follow-up of Colorectal Cancer Patients

  • Andrew Fesler
  • Jingting Jiang
  • Haiyan Zhai
  • Jingfang Ju
Review Article

Abstract

Early detection of colorectal cancer (CRC) is key for prevention and the ability to impact long-term survival of CRC patients. However, the compliance rate of recommended colonoscopy for the population aged from 50 to 75 years is only 50–75 % in the US. A highly sensitive and specific non-invasive test is needed to enhance CRC management. As for late-stage patients, a non-invasive prognostic biomarker is also critical for improving patient treatment protocols. The discovery that non-coding microRNAs (miRNAs) are stable in body fluids such as plasma, serum and exosomes presents the opportunity to develop novel strategies, taking advantage of circulating miRNAs as early diagnostic biomarkers of CRC. The goal of using circulating miRNA-based prognostic biomarkers for CRC patients has been pursued extensively. In this review, we will try to cover the major recent advancements at the frontier of this research area.

Keywords

Chronic Lymphocytic Leukemia Reverse Transcription Polymerase Chain Reaction Advanced Adenoma Adenoma Patient miRNA Quantification 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments and Disclosures

This study was supported by R01CA155019 (Jingfang Ju) and R33CA147966 (Jingfang Ju). The authors have no conflicts of interest that are directly relevant to the content of this article.

References

  1. 1.
    American Cancer Society. Cancer facts and figures. Atlanta: American Cancer Society; 2013. p. 1–64.Google Scholar
  2. 2.
    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(5):843–54.PubMedCrossRefGoogle Scholar
  3. 3.
    Wightman B, Ha I, Ruvkun G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell. 1993;75(5):855–62 pii: 0092-8674(93)90530-4.PubMedCrossRefGoogle Scholar
  4. 4.
    Pillai RS, Bhattacharyya SN, Artus CG, Zoller T, Cougot N, Basyuk E, et al. Inhibition of translational initiation by Let-7 MicroRNA in human cells. Science. 2005;309(5740):1573–6.PubMedCrossRefGoogle Scholar
  5. 5.
    Ruvkun G. Clarifications on miRNA and cancer. Science. 2006;311(5757):36–7.PubMedCrossRefGoogle Scholar
  6. 6.
    Calin GA, Dumitru CD, Shimizu M, Bichi R, Zupo S, Noch E, et al. Frequent deletions and down-regulation of micro-RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci U S A. 2002;99(24):15524–9. doi: 10.1073/pnas.242606799.PubMedCrossRefPubMedCentralGoogle Scholar
  7. 7.
    Xi Y, Nakajima G, Gavin E, Morris CG, Kudo K, Hayashi K, et al. Systematic analysis of microRNA expression of RNA extracted from fresh frozen and formalin-fixed paraffin-embedded samples. RNA. 2007;13(10):1668–74. doi: 10.1261/rna.642907.PubMedCrossRefPubMedCentralGoogle Scholar
  8. 8.
    Li J, Smyth P, Flavin R, Cahill S, Denning K, Aherne S, et al. Comparison of miRNA expression patterns using total RNA extracted from matched samples of formalin-fixed paraffin-embedded (FFPE) cells and snap frozen cells. BMC Biotechnol. 2007;7:36. doi: 10.1186/1472-6750-7-36.PubMedCrossRefPubMedCentralGoogle Scholar
  9. 9.
    Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL, et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci U S A. 2008;105(30):10513–8. doi: 10.1073/pnas.0804549105.PubMedCrossRefPubMedCentralGoogle Scholar
  10. 10.
    Kosaka N, Iguchi H, Yoshioka Y, Takeshita F, Matsuki Y, Ochiya T. Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem. 2010;285(23):17442–52. doi: 10.1074/jbc.M110.107821.PubMedCrossRefPubMedCentralGoogle Scholar
  11. 11.
    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(6):654–9. doi: 10.1038/ncb1596.PubMedCrossRefGoogle Scholar
  12. 12.
    Pritchard CC, Kroh E, Wood B, Arroyo JD, Dougherty KJ, Miyaji MM, et al. Blood cell origin of circulating microRNAs: a cautionary note for cancer biomarker studies. Cancer Prev Res (Phila). 2012;5(3):492–7. doi: 10.1158/1940-6207.CAPR-11-0370.CrossRefGoogle Scholar
  13. 13.
    Wang K, Zhang S, Weber J, Baxter D, Galas DJ. Export of microRNAs and microRNA-protective protein by mammalian cells. Nucleic Acids Res. 2010;38(20):7248–59. doi: 10.1093/nar/gkq601.PubMedCrossRefPubMedCentralGoogle Scholar
  14. 14.
    Kim DJ, Linnstaedt S, Palma J, Park JC, Ntrivalas E, Kwak-Kim JY, et al. Plasma components affect accuracy of circulating cancer-related microRNA quantitation. J Mol Diagn. 2012;14(1):71–80. doi: 10.1016/j.jmoldx.2011.09.002.PubMedCrossRefPubMedCentralGoogle Scholar
  15. 15.
    Koberle V, Pleli T, Schmithals C, Augusto Alonso E, Haupenthal J, Bonig H, et al. Differential stability of cell-free circulating microRNAs: implications for their utilization as biomarkers. PloS ONE. 2013;8(9):e75184. doi: 10.1371/journal.pone.0075184.
  16. 16.
    Wang Q, Huang Z, Ni S, Xiao X, Xu Q, Wang L, et al. Plasma miR-601 and miR-760 are novel biomarkers for the early detection of colorectal cancer. PloS ONE. 2012;7(9):e44398. doi: 10.1371/journal.pone.0044398.PubMedCrossRefPubMedCentralGoogle Scholar
  17. 17.
    Yang IP, Tsai HL, Huang CW, Huang MY, Hou MF, Juo SH, et al. The functional significance of microRNA-29c in patients with colorectal cancer: a potential circulating biomarker for predicting early relapse. PloS One. 2013;8(6):e66842. doi: 10.1371/journal.pone.0066842.PubMedCrossRefPubMedCentralGoogle Scholar
  18. 18.
    Toiyama Y, Hur K, Tanaka K, Inoue Y, Kusunoki M, Boland CR, et al. Serum miR-200c is a novel prognostic and metastasis-predictive biomarker in patients with colorectal cancer. Ann Surg. 2013. doi: 10.1097/SLA.0b013e3182a6909d.Google Scholar
  19. 19.
    Wang B, Zhang Q. The expression and clinical significance of circulating microRNA-21 in serum of five solid tumors. J Cancer Res Clin Oncol. 2012;138(10):1659–66. doi: 10.1007/s00432-012-1244-9.PubMedCrossRefGoogle Scholar
  20. 20.
    Huang Z, Huang D, Ni S, Peng Z, Sheng W, Du X. Plasma microRNAs are promising novel biomarkers for early detection of colorectal cancer. Int J Cancer. 2010;127(1):118–26. doi: 10.1002/ijc.25007.PubMedCrossRefGoogle Scholar
  21. 21.
    Vega AB, Pericay C, Moya I, Ferrer A, Dotor E, Pisa A, et al. microRNA expression profile in stage III colorectal cancer: circulating miR-18a and miR-29a as promising biomarkers. Oncol Rep. 2013;30(1):320–6. doi: 10.3892/or.2013.2475.Google Scholar
  22. 22.
    Nugent M, Miller N, Kerin MJ. Circulating miR-34a levels are reduced in colorectal cancer. J Surg Oncol. 2012;106(8):947–52. doi: 10.1002/jso.23174.PubMedCrossRefGoogle Scholar
  23. 23.
    Kjersem JB, Ikdahl T, Lingjaerde OC, Guren T, Tveit KM, Kure EH. Plasma microRNAs predicting clinical outcome in metastatic colorectal cancer patients receiving first-line oxaliplatin-based treatment. Mol Oncol. 2013;. doi: 10.1016/j.molonc.2013.09.001.PubMedGoogle Scholar
  24. 24.
    Jung EJ, Santarpia L, Kim J, Esteva FJ, Moretti E, Buzdar AU, et al. Plasma microRNA 210 levels correlate with sensitivity to trastuzumab and tumor presence in breast cancer patients. Cancer. 2012;118(10):2603–14. doi: 10.1002/cncr.26565.PubMedCrossRefGoogle Scholar
  25. 25.
    Cortez MA, Calin GA. MicroRNA identification in plasma and serum: a new tool to diagnose and monitor diseases. Expert Opin Biol Ther. 2009;9(6):703–11. doi: 10.1517/14712590902932889.PubMedCrossRefGoogle Scholar
  26. 26.
    Leidner RS, Li L, Thompson CL. Dampening enthusiasm for circulating microRNA in breast cancer. PloS ONE. 2013;8(3):e57841. doi: 10.1371/journal.pone.0057841.PubMedCrossRefPubMedCentralGoogle Scholar
  27. 27.
    Kanaan Z, Roberts H, Eichenberger MR, Billeter A, Ocheretner G, Pan J, et al. A plasma microRNA panel for detection of colorectal adenomas: a step toward more precise screening for colorectal cancer. Ann Surg. 2013;258(3):400–8. doi: 10.1097/SLA.0b013e3182a15bcc.PubMedCrossRefGoogle Scholar
  28. 28.
    Toiyama Y, Takahashi M, Hur K, Nagasaka T, Tanaka K, Inoue Y, et al. Serum miR-21 as a diagnostic and prognostic biomarker in colorectal cancer. J Natl Cancer Inst. 2013;105(12):849–59. doi: 10.1093/jnci/djt101.PubMedCrossRefGoogle Scholar
  29. 29.
    Wang LG, Gu J. Serum microRNA-29a is a promising novel marker for early detection of colorectal liver metastasis. Cancer Epidemiol. 2012;36(1):e61–7. doi: 10.1016/j.canep.2011.05.002.PubMedCrossRefGoogle Scholar
  30. 30.
    Ng EK, Chong WW, Jin H, Lam EK, Shin VY, Yu J, et al. Differential expression of microRNAs in plasma of patients with colorectal cancer: a potential marker for colorectal cancer screening. Gut. 2009;58(10):1375–81. doi: 10.1136/gut.2008.167817.PubMedCrossRefGoogle Scholar
  31. 31.
    Pu XX, Huang GL, Guo HQ, Guo CC, Li H, Ye S, 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. J Gastroenterol Hepatol. 2010;25(10):1674–80. doi: 10.1111/j.1440-1746.2010.06417.x.PubMedCrossRefGoogle Scholar
  32. 32.
    Liu GH, Zhou ZG, Chen R, Wang MJ, Zhou B, Li Y, et al. Serum miR-21 and miR-92a as biomarkers in the diagnosis and prognosis of colorectal cancer. Tumour Biol. 2013;34(4):2175–81. doi: 10.1007/s13277-013-0753-8.PubMedCrossRefGoogle Scholar
  33. 33.
    Yong FL, Law CW, Wang CW. Potentiality of a triple microRNA classifier: miR-193a-3p, miR-23a and miR-338-5p for early detection of colorectal cancer. BMC Cancer. 2013;13:280. doi: 10.1186/1471-2407-13-280.PubMedCrossRefPubMedCentralGoogle Scholar
  34. 34.
    Yamada N, Nakagawa Y, Tsujimura N, Kumazaki M, Noguchi S, Mori T, et al. Role of intracellular and extracellular microRNA-92a in colorectal cancer. Transl Oncol. 2013;6(4):482–92.PubMedCrossRefPubMedCentralGoogle Scholar
  35. 35.
    Cheng H, Zhang L, Cogdell DE, Zheng H, Schetter AJ, Nykter M, et al. Circulating plasma MiR-141 is a novel biomarker for metastatic colon cancer and predicts poor prognosis. PloS ONE. 2011;6(3):e17745. doi: 10.1371/journal.pone.0017745.PubMedCrossRefPubMedCentralGoogle Scholar
  36. 36.
    Wang P, Zou F, Zhang X, Li H, Dulak A, Tomko RJ Jr, et al. microRNA-21 negatively regulates Cdc25A and cell cycle progression in colon cancer cells. Cancer Res. 2009;69(20):8157–65. doi: 10.1158/0008-5472.CAN-09-1996.PubMedCrossRefPubMedCentralGoogle Scholar
  37. 37.
    Moriyama T, Ohuchida K, Mizumoto K, Yu J, Sato N, Nabae T, et al. MicroRNA-21 modulates biological functions of pancreatic cancer cells including their proliferation, invasion, and chemoresistance. Mol Cancer Ther. 2009;8(5):1067–74. doi: 10.1158/1535-7163.MCT-08-0592.PubMedCrossRefGoogle Scholar
  38. 38.
    Slaby O, Svoboda M, Fabian P, Smerdova T, Knoflickova D, Bednarikova M, et al. Altered expression of miR-21, miR-31, miR-143 and miR-145 is related to clinicopathologic features of colorectal cancer. Oncology. 2007;72(5–6):397–402. doi: 10.1159/000113489.PubMedCrossRefGoogle Scholar
  39. 39.
    Luo X, Stock C, Burwinkel B, Brenner H. Identification and evaluation of plasma MicroRNAs for early detection of colorectal cancer. PloS ONE. 2013;8(5):e62880. doi: 10.1371/journal.pone.0062880.PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Andrew Fesler
    • 1
  • Jingting Jiang
    • 2
  • Haiyan Zhai
    • 1
  • Jingfang Ju
    • 1
  1. 1.Translational Research Laboratory, Department of Pathology, BST, L-9, Room 185, Stony Brook MedicineStony Brook UniversityStony BrookUSA
  2. 2.Department of Tumor BiotherapyThe Third Affiliated Hospital of Soochow UniversityChangzhouPeople’s Republic of China

Personalised recommendations