MiR-194 deregulation contributes to colorectal carcinogenesis via targeting AKT2 pathway

Theranostics

Volumn 4, Issue 12, 2014, Pages 1193-1208

  Zhao, Hui Jun ^a   Ren, Lin Lin ^a   Wang, Zhen Hua ^a   Sun, Tian Tian ^a   Yu, Ya Nan ^a   Wang, Ying Chao ^a   Yan, Ting Ting ^a   Zou, Weiping ^b   He, Jie ^c   Zhang, Yaou ^c   Hong, Jie ^a   Fang, Jing Yuan ^a  

^a SHANGHAI UNIVERSITY   (China)

^b UNIVERSITY OF MICHIGAN   (United States)

^c TSINGHUA UNIVERSITY   (China)

Author keywords

AKT2 pathway; Biomarker; Carcinogenesis; Colorectal cancer; miR 194

Indexed keywords

MICRORNA; MIR 194; PHOSPHOINOSITIDE DEPENDENT PROTEIN KINASE 1; PROTEIN KINASE B BETA; UNCLASSIFIED DRUG; X LINKED INHIBITOR OF APOPTOSIS; MIRN194 MICRORNA, HUMAN; MIRN194 MICRORNA, MOUSE; PROTEIN KINASE B;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER SURVIVAL; CARCINOGENESIS; CELL INVASION; CELL VIABILITY; COLORECTAL ADENOMA; COLORECTAL CANCER; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LYMPH NODE METASTASIS; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN TARGETING; TUMOR GROWTH; TUMOR VOLUME; ANIMAL; COLORECTAL TUMOR; DOWN REGULATION; ENZYMOLOGY; FEMALE; GENETICS; METABOLISM; NUDE MOUSE; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; CARCINOGENESIS; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; DOWN-REGULATION; FEMALE; HETEROGRAFTS; HUMANS; MALE; MICE; MICE, NUDE; MICRORNAS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 84907526467     PISSN: None     EISSN: 18387640     Source Type: Journal    
DOI: 10.7150/thno.8712     Document Type: Article

References (44)

1. Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin. 2005; 55: 74-108.
2. Mandel JS, Bond JH, Church TR, Snover DC, Bradley GM, Schuman LM, 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. doi:10.1056/NEJM199305133281901.
3. Yamashita K, Watanabe M. Clinical significance of tumor markers and an emerging perspective on colorectal cancer. Cancer Sci. 2009; 100: 195-9. doi:10.1111/j.1349-7006.2008.01022.x.
4. Pepe MS, Etzioni R, Feng Z, Potter JD, Thompson ML, Thornquist M, et al. Phases of biomarker development for early detection of cancer. J Natl Cancer Inst. 2001; 93: 1054-61.
5. Kim VN. MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol. 2005; 6: 376-85. doi:10.1038/nrm1644.
6. Valencia-Sanchez MA, Liu J, Hannon GJ, Parker R. Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev. 2006; 20: 515-24. doi:10.1101/gad.1399806.
7. Calin GA, Croce CM. MicroRNA signatures in human cancers. Nat Rev Cancer. 2006; 6: 857-66. doi:10.1038/nrc1997.
8. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, et al. MicroRNA expression profiles classify human cancers. Nature. 2005; 435: 834-8. doi:10.1038/nature03702.
9. Lanza G, Ferracin M, Gafa R, Veronese A, Spizzo R, Pichiorri F, et al. mRNA/microRNA gene expression profile in microsatellite unstable colorectal cancer. Mol Cancer. 2007; 6: 54. doi:10.1186/1476-4598-6-54.
10. Schetter AJ, Leung SY, Sohn JJ, Zanetti KA, Bowman ED, Yanaihara N, et al. MicroRNA expression profiles associated with prognosis and therapeutic outcome in colon adenocarcinoma. JAMA. 2008; 299: 425-36. doi:10.1001/jama.299.4.425.
11. Padi SK, Zhang Q, Rustum YM, Morrison C, Guo B. MicroRNA-627 mediates the epigenetic mechanisms of vitamin D to suppress proliferation of human colorectal cancer cells and growth of xenograft tumors in mice. Gastroenterology. 2013; 145: 437-46. doi:10.1053/j.gastro.2013.04.012.
12. Chen MB, Wei MX, Han JY, Wu XY, Li C, Wang J, et al. MicroRNA-451 regulates AMPK/mTORC1 signaling and fascin1 expression in HT-29 colorectal cancer. Cell Signal. 2014; 26: 102-9. doi:10.1016/j.cellsig.2013.07.017.
13. Meng Z, Fu X, Chen X, Zeng S, Tian Y, Jove R, et al. miR-194 is a marker of hepatic epithelial cells and suppresses metastasis of liver cancer cells in mice. Hepatology. 2010; 52: 2148-57. doi:10.1002/hep.23915.
14. Wu X, Liu T, Fang O, Leach LJ, Hu X, Luo Z. miR-194 suppresses metastasis of non-small cell lung cancer through regulating expression of BMP1 and p27. Oncogene. 2013. doi:10.1038/onc.2013.108.
15. Song Y, Zhao F, Wang Z, Liu Z, Chiang Y, Xu Y, et al. Inverse association between miR-194 expression and tumor invasion in gastric cancer. Ann Surg Oncol. 2012; 19 Suppl 3: S509-17. doi:10.1245/s10434-011-1999-2.
16. Pichiorri F, Suh SS, Rocci A, De Luca L, Taccioli C, Santhanam R, et al. Downregulation of p53-inducible microRNAs 192, 194, and 215 impairs the p53/MDM2 autoregulatory loop in multiple myeloma development. Cancer Cell. 2010; 18: 367-81. doi:10.1016/j.ccr.2010.09.005.
17. Chiang Y, Song Y, Wang Z, Liu Z, Gao P, Liang J, et al. microRNA-192, -194 and -215 are frequently downregulated in colorectal cancer. Exp Ther Med. 2012; 3: 560-6. doi:10.3892/etm.2011.436.
18. Sundaram P, Hultine S, Smith LM, Dews M, Fox JL, Biyashev D, et al. p53-responsive miR-194 inhibits thrombospondin-1 and promotes angiogenesis in colon cancers. Cancer Res. 2011; 71: 7490-501. doi:10.1158/0008-5472.CAN-11-1124.
19. Xiong H, Hong J, Du W, Lin YW, Ren LL, Wang YC, et al. Roles of STAT3 and ZEB1 proteins in E-cadherin down-regulation and human colorectal cancer epithelial-mesenchymal transition. J Biol Chem. 2012; 287: 5819-32. doi:M111.295964 [pii] 10.1074/jbc.M111.295964.
20. Christian SL, Sims PV, Gold MR. The B cell antigen receptor regulates the transcriptional activator beta-catenin via protein kinase C-mediated inhibition of glycogen synthase kinase-3. J Immunol. 2002; 169: 758-69.
21. Fodde R, Brabletz T. Wnt/beta-catenin signaling in cancer stemness and malignant behavior. Curr Opin Cell Biol. 2007; 19: 150-8. doi:S0955-0674(07)00021-X [pii] 10.1016/j.ceb.2007.02.007.
22. Moser AR, Pitot HC, Dove WF. A dominant mutation that predisposes to multiple intestinal neoplasia in the mouse. Science. 1990; 247: 322-4.
23. Hino K, Tsuchiya K, Fukao T, Kiga K, Okamoto R, Kanai T, et al. Inducible expression of microRNA-194 is regulated by HNF-1alpha during intestinal epithelial cell differentiation. RNA. 2008; 14: 1433-42. doi:10.1261/rna.810208.
24. Rajput A, Dominguez San Martin I, Rose R, Beko A, Levea C, Sharratt E, et al. Characterization of HCT116 human colon cancer cells in an orthotopic model. J Surg Res. 2008; 147: 276-81. doi:S0022-4804(07)00278-8 [pii] 10.1016/j.jss.2007.04.021.
25. Monnier Y, Farmer P, Bieler G, Imaizumi N, Sengstag T, Alghisi GC, et al. CYR61 and alphaVbeta5 integrin cooperate to promote invasion and metastasis of tumors growing in preirradiated stroma. Cancer Res. 2008; 68: 7323-31. doi:68/18/7323 [pii] 10.1158/0008-5472.CAN-08-0841.
26. Kundu ST, Gosavi P, Khapare N, Patel R, Hosing AS, Maru GB, et al. Plakophilin3 downregulation leads to a decrease in cell adhesion and promotes metastasis. Int J Cancer. 2008; 123: 2303-14. doi:10.1002/ijc.23797.
27. Zhang H, Hao Y, Yang J, Zhou Y, Li J, Yin S, et al. Genome-wide functional screening of miR-23b as a pleiotropic modulator suppressing cancer metastasis. Nat Commun. 2011; 2: 554. doi:ncomms1555 [pii] 10.1038/ncomms1555.
28. Rychahou PG, Jackson LN, Silva SR, Rajaraman S, Evers BM. Targeted molecular therapy of the PI3K pathway: therapeutic significance of PI3K subunit targeting in colorectal carcinoma. Ann Surg. 2006; 243: 833-42; discussion 43-4. doi:10.1097/01.sla.0000220040.66012.a9.
29. Roy HK, Olusola BF, Clemens DL, Karolski WJ, Ratashak A, Lynch HT, et al. AKT proto-oncogene overexpression is an early event during sporadic colon carcinogenesis. Carcinogenesis. 2002; 23: 201-5.
30. Ericson K, Gan C, Cheong I, Rago C, Samuels Y, Velculescu VE, et al. Genetic inactivation of AKT1, AKT2, and PDPK1 in human colorectal cancer cells clarifies their roles in tumor growth regulation. Proc Natl Acad Sci U S A. 2010; 107: 2598-603. doi:10.1073/pnas.0914018107.
31. Rychahou PG, Kang J, Gulhati P, Doan HQ, Chen LA, Xiao SY, et al. Akt2 overexpression plays a critical role in the establishment of colorectal cancer metastasis. Proc Natl Acad Sci U S A. 2008; 105: 20315-20. doi:10.1073/pnas.0810715105.
32. Hemmings BA, Restuccia DF. PI3K-PKB/Akt pathway. Cold Spring Harb Perspect Biol. 2012; 4: a011189. doi:4/9/a011189 [pii] 10.1101/cshperspect.a011189.
33. Dan HC, Sun M, Kaneko S, Feldman RI, Nicosia SV, Wang HG, et al. Akt phosphorylation and stabilization of X-linked inhibitor of apoptosis protein (XIAP). J Biol Chem. 2004; 279: 5405-12. doi:10.1074/jbc.M312044200 M312044200 [pii].
34. He J, Wu J, Xu N, Xie W, Li M, Li J, et al. MiR-210 disturbs mitotic progression through regulating a group of mitosis-related genes. Nucleic Acids Res. 2013; 41: 498-508. doi:gks995 [pii] 10.1093/nar/gks995.
35. Zhang L, Sun S, Zhou J, Liu J, Lv JH, Yu XQ, et al. Knockdown of Akt1 promotes Akt2 upregulation and resistance to oxidative-stress-induced apoptosis through control of multiple signaling pathways. Antioxid Redox Signal. 2011; 15: 1-17. doi:10.1089/ars.2010.3560.
36. Moro L, Arbini AA, Yao JL, di Sant'Agnese PA, Marra E, Greco M. Mitochondrial DNA depletion in prostate epithelial cells promotes anoikis resistance and invasion through activation of PI3K/Akt2. Cell Death Differ. 2009; 16: 571-83. doi:10.1038/cdd.2008.178.
37. Behrens J, von Kries JP, Kuhl M, Bruhn L, Wedlich D, Grosschedl R, et al. Functional interaction of beta-catenin with the transcription factor LEF-1. Nature. 1996; 382: 638-42. doi:10.1038/382638a0.
38. Mills CN, Nowsheen S, Bonner JA, Yang ES. Emerging roles of glycogen synthase kinase 3 in the treatment of brain tumors. Front Mol Neurosci. 2011; 4: 47. doi:10.3389/fnmol.2011.00047.
39. Hino K, Fukao T, Watanabe M. Regulatory interaction of HNF1-alpha to microRNA-194 gene during intestinal epithelial cell differentiation. Nucleic Acids Symp Ser (Oxf). 2007;: 415-6. doi:51/1/415 [pii] 10.1093/nass/nrm208.
40. Krutzfeldt J, Rosch N, Hausser J, Manoharan M, Zavolan M, Stoffel M. MicroRNA-194 is a target of transcription factor 1 (Tcf1, HNF1alpha) in adult liver and controls expression of frizzled-6. Hepatology. 2012; 55: 98-107. doi:10.1002/hep.24658.
41. Bandres E, Cubedo E, Agirre X, Malumbres R, Zarate R, Ramirez N, et al. Identification by Real-time PCR of 13 mature microRNAs differentially expressed in colorectal cancer and non-tumoral tissues. Mol Cancer. 2006; 5: doi:10.1186/1476-4598-5-29.
42. Cummins JM, He Y, Leary RJ, Pagliarini R, Diaz LA, Jr., Sjoblom T, et al. The colorectal microRNAome. Proc Natl Acad Sci U S A. 2006; 103: 3687-92. doi:10.1073/pnas.0511155103.
43. Ahmed FE, Jeffries CD, Vos PW, Flake G, Nuovo GJ, Sinar DR, 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.
44. Link A, Balaguer F, Shen Y, Nagasaka T, Lozano JJ, Boland CR, et al. Fecal MicroRNAs as novel biomarkers for colon cancer screening. Cancer Epidemiol Biomarkers Prev. 2010; 19: 1766-74. doi:10.1158/1055-9965.EPI-10-0027.