The diagnostic and prognostic role of microRNA in colorectal cancer-a comprehensive review

Journal of Cancer

Volumn 4, Issue 3, 2013, Pages 281-295

  Mazeh, Haggi ^a   Mizrahi, Ido ^a   Ilyayev, Nadia ^a   Halle, David ^a   Brücher, Björn LDM ^a,b,c,d   Bilchik, Anton ^b,c,d,e   Protic, Mladjan ^b,c,d,f   Daumer, Martin ^b,c,g   Stojadinovic, Alexander ^b,c,d,h   Avital, Itzhak ^g,h   Nissan, Aviram ^b,c,d,i  

^a HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^b Theodor Billroth Academy   (Germany)

^c International Consortium of Research Excellence   (Germany)

^d US Military Cancer Institute   (United States)

^e JOHN WAYNE CANCER INSTITUTE   (United States)

^f Clinical Center of Vojvodina   (Serbia)

^g Sylvia Lawry Centre   (Germany)

^h WALTER REED ARMY MEDICAL CENTER   (United States)

ⁱ Bon Secours Cancer Institute   (United States)

Author keywords

Colorectal cancer; microRNA

Indexed keywords

CARBOHYDRATE ANTIGEN; CARCINOEMBRYONIC ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 12P35; INTERLEUKIN 6; INTERLEUKIN 8; MICRORNA; MICRORNA 1; MICRORNA 10B; MICRORNA 124; MICRORNA 125B; MICRORNA 126; MICRORNA 141; MICRORNA 143; MICRORNA 145; MICRORNA 146A; MICRORNA 155; MICRORNA 192; MICRORNA 200C; MICRORNA 21; MICRORNA 210; MICRORNA 22; MICRORNA 221; MICRORNA 222; MICRORNA 24; MICRORNA 29A; MICRORNA 31; MOLECULAR MARKER; PROTEIN P53; UNINDEXED DRUG;

3' UNTRANSLATED REGION; ACUTE GRANULOCYTIC LEUKEMIA; ADENOMA; ADENOMATOUS POLYP; ADJUVANT CHEMOTHERAPY; BARIUM ENEMA; BLADDER CANCER; BLEEDING; BREAST CANCER; CAENORHABDITIS ELEGANS; CANCER DIAGNOSIS; CANCER GROWTH; CANCER PATIENT; CANCER SCREENING; CANCER SPECIFIC SURVIVAL; CANCER STAGING; CELL MATURATION; CHROMOSOMAL INSTABILITY; CHRONIC LYMPHATIC LEUKEMIA; CLINICAL PRACTICE; CLINICAL RESEARCH; COLON MUCOSA; COLON POLYPOSIS; COLONOSCOPY; COLORECTAL CANCER; COMPUTED TOMOGRAPHIC COLONOGRAPHY; COMPUTER ASSISTED TOMOGRAPHY; CPG ISLAND; DISEASE FREE SURVIVAL; DNA MARKER; DNA SCREENING; DNA SEQUENCE; DYSPLASIA; EARLY CANCER; EPITHELIUM CELL; FOLLOW UP; GASTROINTESTINAL HEMORRHAGE; GENE TARGETING; GLIOBLASTOMA; HUMAN; HUMAN GENOME; INTESTINE PREPARATION; INVASIVE CARCINOMA; KIDNEY CANCER; LIVER CELL CARCINOMA; LIVER METASTASIS; LUNG CANCER; LYMPH NODE METASTASIS; MALIGNANT TRANSFORMATION; MASS SPECTROMETRY; MELANOMA; MICROSATELLITE INSTABILITY; MOLECULAR GENETICS; OCCULT BLOOD; ONCOGENE K RAS; OVARY CANCER; OVERALL SURVIVAL; PANCREAS CANCER; PERFORATION; PRECANCER; PROGRESSION FREE SURVIVAL; PROMOTER REGION; PROTEIN EXPRESSION; RECURRENCE FREE SURVIVAL; RECURRENCE RISK; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; RNA EXTRACTION; SAMPLE SIZE; SENSITIVITY AND SPECIFICITY; SIGMOID; SIGMOIDOSCOPE; SIGMOIDOSCOPY; SINGLE NUCLEOTIDE POLYMORPHISM; STOMACH CANCER; SURVIVAL RATE; THYROID CANCER; TUMOR INVASION; TUMOR SUPPRESSOR GENE; TUMOR VOLUME; UPREGULATION;

EID: 84883032059     PISSN: None     EISSN: 18379664     Source Type: Journal    
DOI: 10.7150/jca.5836     Document Type: Review

References (144)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA Cancer J Clin 2012;62:10-29.
2. Rex DK, Johnson DA, Anderson JC, Schoenfeld PS, Burke CA, Inadomi JM. American College of Gastroenterology guidelines for colorectal cancer screening 2009 [corrected]. Am J Gastroenterol 2009;104:739-50.
3. Levin B, Lieberman DA, McFarland B, et al. 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 2008;134:1570-95.
4. Cash BD, Banerjee S, Anderson MA, et al. Ethnic issues in endoscopy. Gastrointest Endosc 2010;71:1108-12.
5. O'Connell JB, Maggard MA, Ko CY. Colon cancer survival rates with the new American Joint Committee on Cancer sixth edition staging. J Natl Cancer Inst 2004;96:1420-5.
6. Vogelstein B, Fearon ER, Hamilton SR, et al. Genetic alterations during colorectal-tumor development. N Engl J Med 1988;319:525-32.
7. Winawer SJ, Zauber AG, Ho MN, et al. Prevention of colorectal cancer by colonoscopic polypectomy. The National Polyp Study Workgroup. N Engl J Med 1993;329:1977-81.
8. Mandel JS, Bond JH, Church TR, et al. Reducing mortality from colorectal cancer by screening for fecal occult blood. Minnesota Colon Cancer Control Study. N Engl J Med 1993;328:1365-71.
9. Kronborg O, Fenger C, Olsen J, Jorgensen OD, Sondergaard O. Randomised study of screening for colorectal cancer with faecal-occult-blood test. Lancet 1996;348:1467-71.
10. Hardcastle JD, Chamberlain JO, Robinson MH, et al. Randomised controlled trial of faecal-occult-blood screening for colorectal cancer. Lancet 1996;348:1472-7.
11. Fraser CG, Allison JE, Halloran SP, Young GP. A proposal to standardize reporting units for fecal immunochemical tests for hemoglobin. J Natl Cancer Inst 2012;104:810-4.
12. Quintero E, Castells A, Bujanda L, et al. Colonoscopy versus fecal immunochemical testing in colorectal-cancer screening. N Engl J Med 2012;366:697-706.
13. Selby JV, Friedman GD, Quesenberry CP, Jr., Weiss NS. A case-control study of screening sigmoidoscopy and mortality from colorectal cancer. N Engl J Med 1992;326:653-7.
14. Imperiale TF, Wagner DR, Lin CY, Larkin GN, Rogge JD, Ransohoff DF. Risk of advanced proximal neoplasms in asymptomatic adults according to the distal colorectal findings. N Engl J Med 2000;343:169-74.
15. Jentschura D, Raute M, Winter J, Henkel T, Kraus M, Manegold BC. Complications in endoscopy of the lower gastrointestinal tract. Therapy and prognosis. Surg Endosc 1994;8:672-6.
16. Rex DK, Lehman GA, Ulbright TM, et al. Colonic neoplasia in asymptomatic persons with negative fecal occult blood tests: influence of age, gender, and family history. Am J Gastroenterol 1993;88:825-31.
17. Fork FT. Double contrast enema and colonoscopy in polyp detection. Gut 1981;22:971-7.
18. Rex DK, Weddle RA, Lehman GA, et al. Flexible sigmoidoscopy plus air contrast barium enema versus colonoscopy for suspected lower gastrointestinal bleeding. Gastroenterology 1990;98:855-61.
19. Hawes RH. Does virtual colonoscopy have a major role in population-based screening? Gastrointestinal endoscopy clinics of North America 2002;12:85-91.
20. Galdino GM, Yee J. Carpet lesion on CT colonography: a potential pitfall. AJR Am J Roentgenol 2003;180:1332-4.
21. Sidransky D, Tokino T, Hamilton SR, et al. Identification of ras oncogene mutations in the stool of patients with curable colorectal tumors. Science 1992;256:102-5.
22. Ahlquist DA, Shuber AP. Stool screening for colorectal cancer: evolution from occult blood to molecular markers. Clin Chim Acta 2002;315:157-68.
23. Lengauer C, Kinzler KW, Vogelstein B. Genetic instability in colorectal cancers. Nature 1997;386:623-7.
24. Thibodeau SN, Bren G, Schaid D. Microsatellite instability in cancer of the proximal colon. Science 1993;260:816-9.
25. Issa JP, Ottaviano YL, Celano P, Hamilton SR, Davidson NE, Baylin SB. Methylation of the oestrogen receptor CpG island links ageing and neoplasia in human colon. Nat Genet 1994;7:536-40.
26. Schuebel KE, Chen W, Cope L, et al. Comparing the DNA hypermethylome with gene mutations in human colorectal cancer. PLoS genetics 2007;3:1709-23.
27. Wood LD, Parsons DW, Jones S, et al. The genomic landscapes of human breast and colorectal cancers. Science 2007;318:1108-13.
28. Samowitz WS. Genetic and epigenetic changes in colon cancer. Experimental and molecular pathology 2008;85:64-7.
29. Nosho K, Irahara N, Shima K, et al. Comprehensive biostatistical analysis of CpG island methylator phenotype in colorectal cancer using a large population-based sample. PLoS One 2008;3:e3698.
30. Toyota M, Ohe-Toyota M, Ahuja N, Issa JP. Distinct genetic profiles in colorectal tumors with or without the CpG island methylator phenotype. Proc Natl Acad Sci U S A 2000;97:710-5.
31. Koornstra JJ, de Jong S, Hollema H, de Vries EG, Kleibeuker JH. Changes in apoptosis during the development of colorectal cancer: a systematic review of the literature. Crit Rev Oncol Hematol 2003;45:37-53.
32. Ahlquist DA, Skoletsky JE, Boynton KA, et al. Colorectal cancer screening by detection of altered human DNA in stool: feasibility of a multitarget assay panel. Gastroenterology 2000;119:1219-27.
33. Dong SM, Traverso G, Johnson C, et al. Detecting colorectal cancer in stool with the use of multiple genetic targets. J Natl Cancer Inst 2001;93:858-65.
34. Syngal S, Stoffel E, Chung D, et al. Detection of stool DNA mutations before and after treatment of colorectal neoplasia. Cancer 2006;106:277-83.
35. Tagore KS, Lawson MJ, Yucaitis JA, et al. Sensitivity and specificity of a stool DNA multitarget assay panel for the detection of advanced colorectal neoplasia. Clinical colorectal cancer 2003;3:47-53.
36. 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;351:2704-14.
37. Ahmed FE, James SI, Lysle DT, et al. Improved methods for extracting RNA from exfoliated human colonocytes in stool and RT-PCR analysis. Dig Dis Sci 2004;49:1889-98.
38. Kuusela P, Jalanko H, Roberts P, et al. Comparison of CA 19-9 and carcinoembryonic antigen (CEA) levels in the serum of patients with colorectal diseases. Br J Cancer 1984;49:135-9.
39. Wang FM, Tsai LC, Chang ZN, Han SH, Tsao D. The significance of CA19-9 tumor antigen in the serum of patients with carcinomas. Proceedings of the National Science Council, Republic of China Part B, Life sciences 1985;9:119-25.
40. Kornek G, Depisch D, Temsch EM, Scheithauer W. Comparative analysis of cancer-associated antigen CA-195, CA 19-9 and carcinoembryonic antigen in diagnosis, follow-up and monitoring of response to chemotherapy in patients with gastrointestinal cancer. Journal of cancer research and clinical oncology 1991;117:493-6.
41. Kuusela P, Haglund C, Roberts PJ. Comparison of a new tumour marker CA 242 with CA 19-9, CA 50 and carcinoembryonic antigen (CEA) in digestive tract diseases. Br J Cancer 1991;63:636-40.
42. Meltzer PS. Cancer genomics: small RNAs with big impacts. Nature 2005;435:745-6.
43. Gusev Y, Schmittgen TD, Lerner M, Postier R, Brackett D. Computational analysis of biological functions and pathways collectively targeted by co-expressed microRNAs in cancer. BMC bioinformatics 2007;8 Suppl 7:S16.
44. Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993;75:843-54.
45. Kim VN. Small RNAs: classification, biogenesis, and function. Mol Cells 2005;19:1-15.
46. Rodriguez A, Griffiths-Jones S, Ashurst JL, Bradley A. Identification of mammalian microRNA host genes and transcription units. Genome Res 2004;14:1902-10.
47. van Kouwenhove M, Kedde M, Agami R. MicroRNA regulation by RNA-binding proteins and its implications for cancer. Nat Rev Cancer 2011;11:644-56.
48. Santarpia L, Nicoloso M, Calin GA. MicroRNAs: a complex regulatory network drives the acquisition of malignant cell phenotype. Endocr Relat Cancer 2010;17:F51-75.
49. Filipowicz W, Bhattacharyya SN, Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 2008;9:102-14.
50. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004;116:281-97.
51. Croce CM, Calin GA. miRNAs, cancer, and stem cell division. Cell 2005;122:6-7.
52. Lovat F, Valeri N, Croce CM. MicroRNAs in the Pathogenesis of Cancer. Semin Oncol 2011;38:724-33.
53. Sandhu S, Garzon R. Potential Applications of MicroRNAs in Cancer Diagnosis, Prognosis, and Treatment. Semin Oncol 2011;38:781-7.
54. Marcucci G, Radmacher MD, Mrozek K, Bloomfield CD. MicroRNA expression in acute myeloid leukemia. Curr Hematol Malig Rep 2009;4:83-8.
55. Wang J, Sen S. MicroRNA functional network in pancreatic cancer: from biology to biomarkers of disease. J Biosci 2011;36:481-91.
56. Fanini F, Vannini I, Amadori D, Fabbri M. Clinical Implications of MicroRNAs in Lung Cancer. Semin Oncol 2011;38:776-80.
57. Li SD, Zhang JR, Wang YQ, Wan XP. The role of microRNAs in ovarian cancer initiation and progression. J Cell Mol Med 2010;14:2240-9.
58. Wu WK, Lee CW, Cho CH, et al. MicroRNA dysregulation in gastric cancer: a new player enters the game. Oncogene 2010;29:5761-71.
59. Catto JW, Alcaraz A, Bjartell AS, et al. MicroRNA in prostate, bladder, and kidney cancer: a systematic review. Eur Urol 2011;59:671-81.
60. Negrini M, Gramantieri L, Sabbioni S, Croce CM. microRNA involvement in hepatocellular carcinoma. Anticancer Agents Med Chem 2011;11:500-21.
61. Menon MP, Khan A. Micro-RNAs in thyroid neoplasms: molecular, diagnostic and therapeutic implications. J Clin Pathol 2009;62:978-85.
62. Nikiforova MN, Tseng GC, Steward D, Diorio D, Nikiforov YE. MicroRNA expression profiling of thyroid tumors: biological significance and diagnostic utility. J Clin Endocrinol Metab 2008;93:1600-8.
63. Turchinovich A, Weiz L, Langheinz A, Burwinkel B. Characterization of extracellular circulating microRNA. Nucleic acids research 2011;39:7223-33.
64. Michael MZ, SM OC, van Holst Pellekaan NG, Young GP, James RJ. Reduced accumulation of specific microRNAs in colorectal neoplasia. Molecular cancer research : MCR 2003;1:882-91.
65. Bandres E, Cubedo E, Agirre X, et al. Identification by Real-time PCR of 13 mature microRNAs differentially expressed in colorectal cancer and non-tumoral tissues. Molecular cancer 2006;5:29.
66. Volinia S, Calin GA, Liu CG, et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci U S A 2006;103:2257-61.
67. Schetter AJ, Leung SY, Sohn JJ, et al. MicroRNA expression profiles associated with prognosis and therapeutic outcome in colon adenocarcinoma. JAMA 2008;299:425-36.
68. Monzo M, Navarro A, Bandres E, et al. Overlapping expression of microRNAs in human embryonic colon and colorectal cancer. Cell research 2008;18:823-33.
69. Schmitz KJ, Hey S, Schinwald A, et al. Differential expression of microRNA 181b and microRNA 21 in hyperplastic polyps and sessile serrated adenomas of the colon. Virchows Arch 2009;455:49-54.
70. Arndt GM, Dossey L, Cullen LM, et al. Characterization of global microRNA expression reveals oncogenic potential of miR-145 in metastatic colorectal cancer. BMC Cancer 2009;9:374.
71. Chiang Y, Song Y, Wang Z, et al. Aberrant expression of miR-203 and its clinical significance in gastric and colorectal cancers. J Gastrointest Surg 2011;15:63-70.
72. Wu CW, Ng SS, Dong YJ, et al. Detection of miR-92a and miR-21 in stool samples as potential screening biomarkers for colorectal cancer and polyps. Gut 2012;61:739-45.
73. Slattery ML, Wolff E, Hoffman MD, Pellatt DF, Milash B, Wolff RK. MicroRNAs and colon and rectal cancer: differential expression by tumor location and subtype. Genes Chromosomes Cancer 2011;50:196-206.
74. Chang KH, Miller N, Kheirelseid EA, et al. MicroRNA signature analysis in colorectal cancer: identification of expression profiles in stage II tumors associated with aggressive disease. Int J Colorectal Dis 2011;26:1415-22.
75. Mosakhani N, Sarhadi VK, Borze I, et al. MicroRNA profiling differentiates colorectal cancer according to KRAS status. Genes Chromosomes Cancer 2012;51:1-9.
76. Kanaan Z, Rai SN, Eichenberger MR, et al. Plasma miR-21: a potential diagnostic marker of colorectal cancer. Ann Surg 2012;256:544-51.
77. Slaby O, Svoboda M, Fabian P, et al. Altered expression of miR-21, miR-31, miR-143 and miR-145 is related to clinicopathologic features of colorectal cancer. Oncology 2007;72:397-402.
78. Chang KH, Mestdagh P, Vandesompele J, Kerin MJ, Miller N. MicroRNA expression profiling to identify and validate reference genes for relative quantification in colorectal cancer. BMC Cancer 2010;10:173.
79. Xu XM, Qian JC, Deng ZL, et al. Expression of miR-21, miR-31, miR-96 and miR-135b is correlated with the clinical parameters of colorectal cancer. Oncology letters 2012;4:339-45.
80. Motoyama K, Inoue H, Takatsuno Y, et al. Over- and under-expressed microRNAs in human colorectal cancer. Int J Oncol 2009;34:1069-75.
81. Earle JS, Luthra R, Romans A, et al. Association of microRNA expression with microsatellite instability status in colorectal adenocarcinoma. The Journal of molecular diagnostics : JMD 2010;12:433-40.
82. Wang CJ, Zhou ZG, Wang L, et al. Clinicopathological significance of microRNA-31, -143 and -145 expression in colorectal cancer. Dis Markers 2009;26:27-34.
83. Chen X, Guo X, Zhang H, et al. Role of miR-143 targeting KRAS in colorectal tumorigenesis. Oncogene 2009;28:1385-92.
84. Sarver AL, French AJ, Borralho PM, et al. Human colon cancer profiles show differential microRNA expression depending on mismatch repair status and are characteristic of undifferentiated proliferative states. BMC Cancer 2009;9:401.
85. Faltejskova P, Svoboda M, Srutova K, et al. Identification and functional screening of microRNAs highly deregulated in colorectal cancer. J Cell Mol Med 2012.
86. Hamfjord J, Stangeland AM, Hughes T, et al. Differential expression of miRNAs in colorectal cancer: comparison of paired tumor tissue and adjacent normal mucosa using high-throughput sequencing. PLoS One 2012;7:e34150.
87. Wang YX, Zhang XY, Zhang BF, Yang CQ, Chen XM, Gao HJ. Initial study of microRNA expression profiles of colonic cancer without lymph node metastasis. Journal of digestive diseases 2010;11:50-4.
88. Schepeler T, Reinert JT, Ostenfeld MS, et al. Diagnostic and prognostic microRNAs in stage II colon cancer. Cancer Res 2008;68:6416-24.
89. Diosdado B, van de Wiel MA, Terhaar Sive Droste JS, et al. MiR-17-92 cluster is associated with 13q gain and c-myc expression during colorectal adenoma to adenocarcinoma progression. Br J Cancer 2009;101:707-14.
90. Nishida N, Nagahara M, Sato T, et al. Microarray analysis of colorectal cancer stromal tissue reveals upregulation of two oncogenic miRNA clusters. Clin Cancer Res 2012;18:3054-70.
91. Kulda V, Pesta M, Topolcan O, et al. Relevance of miR-21 and miR-143 expression in tissue samples of colorectal carcinoma and its liver metastases. Cancer genetics and cytogenetics 2010;200:154-60.
92. Nakajima G, Hayashi K, Xi Y, et al. Non-coding MicroRNAs hsa-let-7g and hsa-miR-181b are Associated with Chemoresponse to S-1 in Colon Cancer. Cancer genomics & proteomics 2006;3:317-24.
93. Xi Y, Formentini A, Chien M, et al. Prognostic Values of microRNAs in Colorectal Cancer. Biomarker insights 2006;2:113-21.
94. Wang X, Wang J, Ma H, Zhang J, Zhou X. Downregulation of miR-195 correlates with lymph node metastasis and poor prognosis in colorectal cancer. Med Oncol 2012;29:919-27.
95. Luo H, Zou J, Dong Z, Zeng Q, Wu D, Liu L. Up-regulated miR-17 promotes cell proliferation, tumour growth and cell cycle progression by targeting the RND3 tumour suppressor gene in colorectal carcinoma. The Biochemical journal 2012;442:311-21.
96. 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;127:118-26.
97. Sun K, Wang W, Zeng JJ, Wu CT, Lei ST, Li GX. MicroRNA-221 inhibits CDKN1C/p57 expression in human colorectal carcinoma. Acta pharmacologica Sinica 2011;32:375-84.
98. Balaguer F, Moreira L, Lozano JJ, et al. Colorectal cancers with microsatellite instability display unique miRNA profiles. Clin Cancer Res 2011;17:6239-49.
99. Akao Y, Nakagawa Y, Naoe T. MicroRNAs 143 and 145 are possible common onco-microRNAs in human cancers. Oncol Rep 2006;16:845-50.
100. Liu L, Chen L, Xu Y, Li R, Du X. microRNA-195 promotes apoptosis and suppresses tumorigenicity of human colorectal cancer cells. Biochem Biophys Res Commun 2010;400:236-40.
101. Chiang Y, Song Y, Wang Z, et al. microRNA-192, -194 and -215 are frequently downregulated in colorectal cancer. Experimental and therapeutic medicine 2012;3:560-6.
102. Dai X, Chiang Y, Wang Z, et al. Expression levels of microRNA-375 in colorectal carcinoma. Molecular medicine reports 2012;5:1299-304.
103. Ma Y, Zhang P, Wang F, et al. miR-150 as a potential biomarker associated with prognosis and therapeutic outcome in colorectal cancer. Gut 2012;61:1447-53.
104. Zhang Y, He X, Liu Y, et al. microRNA-320a inhibits tumor invasion by targeting neuropilin 1 and is associated with liver metastasis in colorectal cancer. Oncol Rep 2012;27:685-94.
105. Nie J, Liu L, Zheng W, et al. microRNA-365, down-regulated in colon cancer, inhibits cell cycle progression and promotes apoptosis of colon cancer cells by probably targeting Cyclin D1 and Bcl-2. Carcinogenesis 2012;33:220-5.
106. Yamakuchi M, Yagi S, Ito T, Lowenstein CJ. MicroRNA-22 regulates hypoxia signaling in colon cancer cells. PLoS One 2011;6:e20291.
107. Roy S, Levi E, Majumdar AP, Sarkar FH. Expression of miR-34 is lost in colon cancer which can be re-expressed by a novel agent CDF. Journal of hematology & oncology 2012;5:58.
108. Li XM, Wang AM, Zhang J, Yi H. Down-regulation of miR-126 expression in colorectal cancer and its clinical significance. Med Oncol 2011;28:1054-7.
109. Tang JT, Wang JL, Du W, et al. MicroRNA 345, a methylation-sensitive microRNA is involved in cell proliferation and invasion in human colorectal cancer. Carcinogenesis 2011;32:1207-15.
110. Chen X, Ba Y, Ma L, et al. Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell research 2008;18:997-1006.
111. Ng EK, Chong WW, Jin H, et al. Differential expression of microRNAs in plasma of patients with colorectal cancer: a potential marker for colorectal cancer screening. Gut 2009;58:1375-81.
112. Pu XX, Huang GL, Guo HQ, 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;25:1674-80.
113. Wang B, Zhang Q. The expression and clinical significance of circulating microRNA-21 in serum of five solid tumors. Journal of cancer research and clinical oncology 2012;138:1659-66.
114. Cheng H, Zhang L, Cogdell DE, et al. Circulating plasma MiR-141 is a novel biomarker for metastatic colon cancer and predicts poor prognosis. PLoS One 2011;6:e17745.
115. 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:e44398.
116. Ahmed FE, Jeffries CD, Vos PW, et al. Diagnostic microRNA markers for screening sporadic human colon cancer and active ulcerative colitis in stool and tissue. Cancer genomics & proteomics 2009;6:281-95.
117. Link A, Balaguer F, Shen Y, et al. Fecal MicroRNAs as novel biomarkers for colon cancer screening. Cancer Epidemiol Biomarkers Prev 2010;19:1766-74.
118. Koga Y, Yasunaga M, Takahashi A, et al. MicroRNA expression profiling of exfoliated colonocytes isolated from feces for colorectal cancer screening. Cancer Prev Res (Phila) 2010;3:1435-42.
119. Kalimutho M, Di Cecilia S, Del Vecchio Blanco G, et al. Epigenetically silenced miR-34b/c as a novel faecal-based screening marker for colorectal cancer. Br J Cancer 2011;104:1770-8.
120. Kalimutho M, Del Vecchio Blanco G, Di Cecilia S, et al. Differential expression of miR-144* as a novel fecal-based diagnostic marker for colorectal cancer. Journal of gastroenterology 2011;46:1391-402.
121. Li JM, Zhao RH, Li ST, et al. Down-regulation of fecal miR-143 and miR-145 as potential markers for colorectal cancer. Saudi medical journal 2012;33:24-9.
122. Diaz R, Silva J, Garcia JM, et al. Deregulated expression of miR-106a predicts survival in human colon cancer patients. Genes Chromosomes Cancer 2008;47:794-802.
123. Yantiss RK, Goodarzi M, Zhou XK, et al. Clinical, pathologic, and molecular features of early-onset colorectal carcinoma. Am J Surg Pathol 2009;33:572-82.
124. Schetter AJ, Nguyen GH, Bowman ED, et al. Association of inflammation-related and microRNA gene expression with cancer-specific mortality of colon adenocarcinoma. Clin Cancer Res 2009;15:5878-87.
125. Nielsen BS, Jorgensen S, Fog JU, et al. High levels of microRNA-21 in the stroma of colorectal cancers predict short disease-free survival in stage II colon cancer patients. Clinical & experimental metastasis 2011;28:27-38.
126. Feng YH, Wu CL, Tsao CJ, et al. Deregulated expression of sprouty2 and microRNA-21 in human colon cancer: Correlation with the clinical stage of the disease. Cancer Biol Ther 2011;11:111-21.
127. Nishida N, Yokobori T, Mimori K, et al. MicroRNA miR-125b is a prognostic marker in human colorectal cancer. Int J Oncol 2011;38:1437-43.
128. Shibuya H, Iinuma H, Shimada R, Horiuchi A, Watanabe T. Clinicopathological and prognostic value of microRNA-21 and microRNA-155 in colorectal cancer. Oncology 2010;79:313-20.
129. Iwaya T, Yokobori T, Nishida N, et al. Downregulation of miR-144 is associated with colorectal cancer progression via activation of mTOR signaling pathway. Carcinogenesis 2012.
130. Zhu L, Chen H, Zhou D, et al. MicroRNA-9 up-regulation is involved in colorectal cancer metastasis via promoting cell motility. Med Oncol 2012;29:1037-43.
131. Nishida N, Yamashita S, Mimori K, et al. MicroRNA-10b is a Prognostic Indicator in Colorectal Cancer and Confers Resistance to the Chemotherapeutic Agent 5-Fluorouracil in Colorectal Cancer Cells. Ann Surg Oncol 2012;19:3065-71.
132. Akcakaya P, Ekelund S, Kolosenko I, et al. miR-185 and miR-133b deregulation is associated with overall survival and metastasis in colorectal cancer. Int J Oncol 2011;39:311-8.
133. Karaayvaz M, Pal T, Song B, et al. Prognostic significance of miR-215 in colon cancer. Clinical colorectal cancer 2011;10:340-7.
134. Vickers MM, Bar J, Gorn-Hondermann I, et al. Stage-dependent differential expression of microRNAs in colorectal cancer: potential role as markers of metastatic disease. Clinical & experimental metastasis 2012;29:123-32.
135. Liu K, Li G, Fan C, Zhou X, Wu B, Li J. Increased expression of microRNA-21and its association with chemotherapeutic response in human colorectal cancer. The Journal of international medical research 2011;39:2288-95.
136. Horiuchi A, Iinuma H, Akahane T, Shimada R, Watanabe T. Prognostic significance of PDCD4 expression and association with microRNA-21 in each Dukes' stage of colorectal cancer patients. Oncol Rep 2012;27:1384-92.
137. Weissmann-Brenner A, Kushnir M, Lithwick Yanai G, et al. Tumor microRNA-29a expression and the risk of recurrence in stage II colon cancer. Int J Oncol 2012;40:2097-103.
138. Yamashita S, Yamamoto H, Mimori K, et al. MicroRNA-372 is associated with poor prognosis in colorectal cancer. Oncology 2012;82:205-12.
139. Pichler M, Winter E, Stotz M, et al. Down-regulation of KRAS-interacting miRNA-143 predicts poor prognosis but not response to EGFR-targeted agents in colorectal cancer. Br J Cancer 2012;106:1826-32.
140. Ryan BM, McClary AC, Valeri N, et al. rs4919510 in hsa-mir-608 is associated with outcome but not risk of colorectal cancer. PLoS One 2012;7:e36306.
141. Lin M, Gu J, Eng C, et al. Genetic polymorphisms in MicroRNA-related genes as predictors of clinical outcomes in colorectal adenocarcinoma patients. Clin Cancer Res 2012;18:3982-91.
142. Zhou T, Zhang G, Liu Z, Xia S, Tian H. Overexpression of miR-92a correlates with tumor metastasis and poor prognosis in patients with colorectal cancer. Int J Colorectal Dis 2012.
143. Nishimura J, Handa R, Yamamoto H, et al. microRNA-181a is associated with poor prognosis of colorectal cancer. Oncol Rep 2012;28:2221-6.
144. Wang MJ, Li Y, Wang R, et al. Downregulation of microRNA-124 is an independent prognostic factor in patients with colorectal cancer. Int J Colorectal Dis 2012.