Specific microRNA–mRNA Regulatory Network of Colon Cancer Invasion Mediated by Tissue Kallikrein–Related Peptidase 6

Neoplasia (United States)

Volumn 19, Issue 5, 2017, Pages 396-411

  Sells, Earlphia ^a   Pandey, Ritu ^b,c   Chen, Hwudaurw ^b   Skovan, Bethany A ^b   Cui, Haiyan ^b   Ignatenko, Natalia A ^c  

^a The University of Arizona   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA AMIDATING ENZYME; APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3G; CALRETININ; COLECALCIFEROL 24 HYDROXYLASE; DIPEPTIDYL PEPTIDASE IV; HSA MIR 1276; HSA MIR 1278; HSA MIR 1301; HSA MIR 183; HSA MIR 3116 2; HSA MIR 3118 1; HSA MIR 3118 2; HSA MIR 3118 3; HSA MIR 4270; HSA MIR 548 H 4; HSA MIR 548F 3; HSA MIR 648; HSA MIR 718; KALLIKREIN 6; MESSENGER RNA; MICRORNA; MICRORNA 181D; MICRORNA 182; MICRORNA 203; NEUROPILIN 1; PROTEIN FOS; PROTEOCHONDROITIN SULFATE; TOLL LIKE RECEPTOR 3; TRANSCRIPTION FACTOR RUNX2; TRANSFORMING GROWTH FACTOR BETA2; UNCLASSIFIED DRUG; KALLIKREIN; KLK6 PROTEIN, HUMAN; TRANSFORMING GROWTH FACTOR BETA;

3' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOINFORMATICS; CELL DIFFERENTIATION; CELL GROWTH; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; GENE INTERACTION; GENE REGULATORY NETWORK; GENE SILENCING; GENE TARGETING; HCT 116 CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; METASTATIC COLORECTAL CANCER; MOUSE; NONHUMAN; PHENOTYPE; PREDICTION; PRIORITY JOURNAL; PROTEIN SECRETION; REAL TIME POLYMERASE CHAIN REACTION; TRANSIENT TRANSFECTION; TUMOR INVASION; ANIMAL; COLON TUMOR; DRUG SCREENING; GENE EXPRESSION REGULATION; GENE KNOCKDOWN; GENETICS; METABOLISM; METASTASIS; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; COLONIC NEOPLASMS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; GENE REGULATORY NETWORKS; HCT116 CELLS; HUMANS; KALLIKREINS; MICE; MICRORNAS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 85017335981     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1016/j.neo.2017.02.003     Document Type: Article

References (52)

1. [1] Siegel, RL, Miller, KD, Jemal, A, Cancer statistics, 2016. CA Cancer J Clin 66 (2016), 7–30.
2. [2] Valastyan, S, Weinberg, RA, Tumor metastasis: molecular insights and evolving paradigms. Cell 147 (2011), 275–292.
3. [3] Fearon, ER, Molecular genetics of colorectal cancer. Annu Rev Pathol 6 (2011), 479–507.
4. [4] Friedman, RC, Farh, KK, Burge, CB, Bartel, DP, Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19 (2009), 92–105.
5. [5] Leung, AK, Sharp, PA, Function and localization of microRNAs in mammalian cells. Cold Spring Harb Symp Quant Biol 71 (2006), 29–38.
6. [6] Ebert, MS, Sharp, PA, Roles for microRNAs in conferring robustness to biological processes. Cell 149 (2012), 515–524.
7. [7] Esquela-Kerscher, A, Slack, FJ, Oncomirs - microRNAs with a role in cancer. Nat Rev Cancer 6 (2006), 259–269.
8. [8] Hammond, SM, MicroRNAs as oncogenes. Curr Opin Genet Dev 16 (2006), 4–9.
9. [9] Lee, YS, Dutta, A, MicroRNAs: small but potent oncogenes or tumor suppressors. Curr Opin Investig Drugs 7 (2006), 560–564.
10. [10] Nazarov, PV, Reinsbach, SE, Muller, A, Nicot, N, Philippidou, D, Vallar, L, Kreis, S, Interplay of microRNAs, transcription factors and target genes: linking dynamic expression changes to function. Nucleic Acids Res 41 (2013), 2817–2831.
11. [11] Guo, L, Zhao, Y, Yang, S, Zhang, H, Chen, F, Integrative analysis of miRNA-mRNA and miRNA-miRNA interactions. Biomed Res Int, 2014, 2014, 907420.
12. [12] Borgono, CA, Diamandis, EP, The emerging roles of human tissue kallikreins in cancer. Nat Rev Cancer 4 (2004), 876–890.
13. [13] Emami, N, Diamandis, EP, Human tissue kallikreins: a road under construction. Clin Chim Acta 381 (2007), 78–84.
14. [14] Paliouras, M, Borgono, C, Diamandis, EP, Human tissue kallikreins: the cancer biomarker family. Cancer Lett 249 (2007), 61–79.
15. [15] Sotiropoulou, G, Pampalakis, G, Diamandis, EP, Functional roles of human kallikrein-related peptidases. J Biol Chem 284 (2009), 32989–32994.
16. [16] Magklara, A, Mellati, AA, Wasney, GA, Little, SP, Sotiropoulou, G, Becker, GW, Diamandis, EP, Characterization of the enzymatic activity of human kallikrein 6: Autoactivation, substrate specificity, and regulation by inhibitors. Biochem Biophys Res Commun 307 (2003), 948–955.
17. [17] Kim, JT, Song, EY, Chung, KS, Kang, MA, Kim, JW, Kim, SJ, Yeom, YI, Kim, JH, Kim, KH, Lee, HG, Up-regulation and clinical significance of serine protease kallikrein 6 in colon cancer. Cancer 117 (2011), 2608–2619.
18. [18] Ogawa, K, Utsunomiya, T, Mimori, K, Tanaka, F, Inoue, H, Nagahara, H, Murayama, S, Mori, M, Clinical significance of human kallikrein gene 6 messenger RNA expression in colorectal cancer. Clin Cancer Res 11 (2005), 2889–2893.
19. [19] Ohlsson, L, Lindmark, G, Israelsson, A, Palmqvist, R, Oberg, A, Hammarstrom, ML, Hammarstrom, S, Lymph node tissue kallikrein-related peptidase 6 mRNA: a progression marker for colorectal cancer. Br J Cancer 107 (2012), 150–157.
20. [20] Qi, L, Ding, Y, Screening and regulatory network analysis of survival-related genes of patients with colorectal cancer. Sci China Life Sci 57 (2014), 526–531.
21. [21] Henkhaus, RS, Gerner, EW, Ignatenko, NA, Kallikrein 6 is a mediator of K-RAS-dependent migration of colon carcinoma cells. Biol Chem 389 (2008), 757–764.
22. [22] Ignatenko, NA, Zhang, H, Watts, GS, Skovan, BA, Stringer, DE, Gerner, EW, The chemopreventive agent alpha-difluoromethylornithine blocks Ki-ras-dependent tumor formation and specific gene expression in Caco-2 cells. Mol Carcinog 39 (2004), 221–233.
23. [23] Chow, TF, Crow, M, Earle, T, El-Said, H, Diamandis, EP, Yousef, GM, Kallikreins as microRNA targets: an in silico and experimental-based analysis. Biol Chem 389 (2008), 731–738.
24. [24] Gentleman, RC, Carey, VJ, Bates, DM, Bolstad, B, Dettling, M, Dudoit, S, Ellis, B, Gautier, L, Ge, Y, Gentry, J, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol, 5, 2004, R80.
25. [25] Ritchie, ME, Phipson, B, Wu, D, Hu, Y, Law, CW, Shi, W, Smyth, GK, limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res, 43, 2015, e47.
26. [26] Pampalakis, G, Prosnikli, E, Agalioti, T, Vlahou, A, Zoumpourlis, V, Sotiropoulou, G, A tumor-protective role for human kallikrein-related peptidase 6 in breast cancer mediated by inhibition of epithelial-to-mesenchymal transition. Cancer Res 69 (2009), 3779–3787.
27. [27] Betel, D, Wilson, M, Gabow, A, Marks, DS, Sander, C, The microRNA.org resource: targets and expression. Nucleic Acids Res 36 (2008), D149–D153.
28. [28] Betel, D, Koppal, A, Agius, P, Sander, C, Leslie, C, Comprehensive modeling of microRNA targets predicts functional non-conserved and non-canonical sites. Genome Biol, 11, 2010, R90.
29. [29] Attisano, L, Wrana, JL, Signal transduction by the TGF-beta superfamily. Science 296 (2002), 1646–1647.
30. [30] Nieto, MA, The snail superfamily of zinc-finger transcription factors. Nat Rev Mol Cell Biol 3 (2002), 155–166.
31. [31] Moes, M, Le Bechec, A, Crespo, I, Laurini, C, Halavatyi, A, Vetter, G, Del Sol, A, Friederich, E, A novel network integrating a miRNA-203/SNAI1 feedback loop which regulates epithelial to mesenchymal transition. PLoS One, 7, 2012, e35440.
32. [32] Li, Y, Zhao, Z, Xu, C, Zhou, Z, Zhu, Z, You, T, HMGA2 induces transcription factor Slug expression to promote epithelial-to-mesenchymal transition and contributes to colon cancer progression. Cancer Lett 355 (2014), 130–140.
33. [33] Thuault, S, Valcourt, U, Petersen, M, Manfioletti, G, Heldin, CH, Moustakas, A, Transforming growth factor-beta employs HMGA2 to elicit epithelial-mesenchymal transition. J Cell Biol 174 (2006), 175–183.
34. [34] Henkhaus, RS, Roy, UK, Cavallo-Medved, D, Sloane, BF, Gerner, EW, Ignatenko, NA, Caveolin-1-mediated expression and secretion of kallikrein 6 in colon cancer cells. Neoplasia 10 (2008), 140–148.
35. [35] Valastyan, S, Weinberg, RA, MicroRNAs: Crucial multi-tasking components in the complex circuitry of tumor metastasis. Cell Cycle 8 (2009), 3506–3512.
36. [36] Bouyssou, JM, Manier, S, Huynh, D, Issa, S, Roccaro, AM, Ghobrial, IM, Regulation of microRNAs in cancer metastasis. Biochim Biophys Acta 1845 (2014), 255–265.
37. [37] Weng, M, Wu, D, Yang, C, Peng, H, Wang, G, Wang, T, Li, X, Noncoding RNAs in the development, diagnosis, and prognosis of colorectal cancer. Transl Res, 2016.
38. [38] Wang, XF, Shi, ZM, Wang, XR, Cao, L, Wang, YY, Zhang, JX, Yin, Y, Luo, H, Kang, CS, Liu, N, et al. MiR-181d acts as a tumor suppressor in glioma by targeting K-ras and Bcl-2. J Cancer Res Clin Oncol 138 (2012), 573–584.
39. [39] Drucker, KL, Paulsen, AR, Giannini, C, Decker, PA, Blaber, SI, Blaber, M, Uhm, JH, O'Neill, BP, Jenkins, RB, Scarisbrick, IA, Clinical significance and novel mechanism of action of kallikrein 6 in glioblastoma. Neuro Oncol 15 (2013), 305–318.
40. [40] Sidiropoulos, KG, White, NM, Bui, A, Ding, Q, Boulos, P, Pampalakis, G, Khella, H, Samuel, JN, Sotiropoulou, G, Yousef, GM, Kallikrein-related peptidase 5 induces miRNA-mediated anti-oncogenic pathways in breast cancer. Oncoscience 1 (2014), 709–724.
41. [41] Thuault, S, Tan, EJ, Peinado, H, Cano, A, Heldin, CH, Moustakas, A, HMGA2 and Smads co-regulate SNAIL1 expression during induction of epithelial-to-mesenchymal transition. J Biol Chem 283 (2008), 33437–33446.
42. [42] Tran, DD, Corsa, CA, Biswas, H, Aft, RL, Longmore, GD, Temporal and spatial cooperation of Snail1 and Twist1 during epithelial-mesenchymal transition predicts for human breast cancer recurrence. Mol Cancer Res 9 (2011), 1644–1657.
43. [43] Gregory, PA, Bert, AG, Paterson, EL, Barry, SC, Tsykin, A, Farshid, G, Vadas, MA, Khew-Goodall, Y, Goodall, GJ, The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 10 (2008), 593–601.
44. [44] Gregory, PA, Bracken, CP, Smith, E, Bert, AG, Wright, JA, Roslan, S, Morris, M, Wyatt, L, Farshid, G, Lim, YY, et al. An autocrine TGF-beta/ZEB/miR-200 signaling network regulates establishment and maintenance of epithelial-mesenchymal transition. Mol Biol Cell 22 (2011), 1686–1698.
45. [45] Benaich, N, Woodhouse, S, Goldie, SJ, Mishra, A, Quist, SR, Watt, FM, Rewiring of an epithelial differentiation factor, miR-203, to inhibit human squamous cell carcinoma metastasis. Cell Rep 9 (2014), 104–117.
46. [46] Baker, K, Raut, P, Jass, JR, Microsatellite unstable colorectal cancer cell lines with truncating TGFbetaRII mutations remain sensitive to endogenous TGFbeta. J Pathol 213 (2007), 257–265.
47. [47] Wang, X, Liu, X, Li, AY, Chen, L, Lai, L, Lin, HH, Hu, S, Yao, L, Peng, J, Loera, S, et al. Overexpression of HMGA2 promotes metastasis and impacts survival of colorectal cancers. Clin Cancer Res 17 (2011), 2570–2580.
48. [48] White, NM, Youssef, YM, Fendler, A, Stephan, C, Jung, K, Yousef, GM, The miRNA-kallikrein axis of interaction: a new dimension in the pathogenesis of prostate cancer. Biol Chem 393 (2012), 379–389.
49. [49] Sidiropoulos, KG, Ding, Q, Pampalakis, G, White, NM, Boulos, P, Sotiropoulou, G, Yousef, GM, KLK6-regulated miRNA networks activate oncogenic pathways in breast cancer subtypes. Mol Oncol 10 (2016), 993–1007.
50. [50] Gurtan, AM, Sharp, PA, The role of miRNAs in regulating gene expression networks. J Mol Biol 425 (2013), 3582–3600.
51. [51] Locker, GY, Hamilton, S, Harris, J, Jessup, JM, Kemeny, N, Macdonald, JS, Somerfield, MR, Hayes, DF, Bast, RC Jr., ASCO 2006 update of recommendations for the use of tumor markers in gastrointestinal cancer. J Clin Oncol 24 (2006), 5313–5327.
52. [52] Shannon, P, Markiel, A, Ozier, O, Baliga, NS, Wang, JT, Ramage, D, Amin, N, Schwikowski, B, Ideker, T, Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13 (2003), 2498–2504.