In silico screening of alleged miRNAs associated with cell competition: an emerging cellular event in cancer
-
Manish Patel
Abstract
Cell competition is identified as a crucial phenomenon for cancer and organ development. There is a possibility that microRNAs (miRNAs) may play an important role in the regulation of expression of genes involved in cell competition. In silico screening of miRNAs is an effort to abridge, economize and expedite the experimental approaches to identification of potential miRNAs involved in cell competition, as no study has reported involvement of miRNAs in cell competition to date. In this study, we used multiple screening steps as follows: (i) selection of cell competition related genes of Drosophila through a literature survey; (ii) homology study of selected cell competition related genes; (iii) identification of miRNAs that target conserved cell competitionrelated genes through prediction tools; (iv) sequence conservation analysis of identified miRNAs with human genome; (v) identification of conserved cell competition miRNAs using their expression profiles and exploration of roles of their homologous human miRNAs. This study led to the identification of nine potential cell competition miRNAs in the Drosophila genome. Importantly, eighteen human homologs of these nine potential Drosophila miRNAs are well reported for their involvement in different types of cancers. This confirms their probable involvement in cell competition as well, because cell competition is well justified for its involvement in cancer initiation and maintenance.
References
1. Moreno, E. Is cell competition relevant to cancer? Nat. Rev. Cancer 8 (2008) 141-147.Search in Google Scholar
2. de la Cova, C., Abril, M., Bellosta, P., Gallant, P. and Johnston, L.A. Drosophila myc regulates organ size by inducing cell competition. Cell 117 (2004) 107-116.Search in Google Scholar
3. Tamori, Y. and Deng, W.M. Cell competition and its implications for development and cancer. J. Genet. Genomics 38 (2011) 483-495.Search in Google Scholar
4. Baker, N.E. and Li, W. Cell competition and its possible relation to cancer. Cancer Res. 68 (2008) 5505-5507.Search in Google Scholar
5. Wagstaff, L., Kolahgar, G. and Piddini, E. Competitive cell interactions in cancer: a cellular tug of war. Trends Cell Biol. 23 (2013) 160-167.10.1016/j.tcb.2012.11.002Search in Google Scholar PubMed
6. Tamori, Y. and Deng, W.M. Tissue repair through cell competition and compensatory cellular hypertrophy in postmitotic epithelia. Dev. Cell 25 (2013) 350-363.Search in Google Scholar
7. Vincent, J.P., Kolahgar, G., Gagliardi, M. and Piddini, E. Steep differences in wingless signaling trigger Myc-independent competitive cell interactions. Dev. Cell 21 (2011) 366-374.Search in Google Scholar
8. Tyler, D.M., Li, W., Zhuo, N., Pellock, B. and Baker, N.E. Genes affecting cell competition in Drosophila. Genetics 175 (2007) 643-657.Search in Google Scholar
9. Chen, C.L., Schroeder, M.C., Kango-Singh, M., Tao, C. and Halder, G. Tumor suppression by cell competition through regulation of the Hippo pathway. Proc. Natl. Acad. Sci. U. S. A. 109 (2012) 484-489.Search in Google Scholar
10. Moreno, E. and Basler, K. dMyc transforms cells into super-competitors. Cell 117 (2004) 117-129.Search in Google Scholar
11. Graves, H.K., Woodfield, S.E., Yang, C.C., Halder, G. and Bergmann, A. Notch signaling activates Yorkie non-cell autonomously in Drosophila. PLoS One 7 (2012) e37615.10.1371/journal.pone.0037615Search in Google Scholar PubMed PubMed Central
12. Ohsawa, S., Sugimura, K., Takino, K., Xu, T., Miyawaki, A. and Igaki, T. Elimination of oncogenic neighbors by JNK-mediated engulfment in Drosophila. Dev. Cell 20 (2011) 315-328.Search in Google Scholar
13. Grzeschik, N.A., Parsons, L.M. and Richardson, H.E. Lgl, the SWH pathway and tumorigenesis: It's a matter of context & competition! Cell Cycle 9 (2010) 3202-3212.Search in Google Scholar
14. Tamori, Y., Bialucha, C.U., Tian, A.G., Kajita, M., Huang, Y.C., Norman, M., Harrison, N., Poulton, J., Ivanovitch, K., Disch, L., Liu, T., Deng, W.M. and Fujita, Y. Involvement of Lgl and Mahjong/VprBP in cell competition. PLoS Biol. 8 (2010) e1000422.10.1371/journal.pbio.1000422Search in Google Scholar PubMed PubMed Central
15. Li, W. and Baker, N.E. Engulfment is required for cell competition. Cell 129 (2007) 1215-1225.Search in Google Scholar
16. Xiong, H., Qian, J., He, T. and Li, F. Independent transcription of miR-281 in the intron of ODA in Drosophila melanogaster. Biochem. Biophys. Res. Commun. 378 (2009) 883-889.Search in Google Scholar
17. Engelmann, J.C. and Spang, R. A least angle regression model for the prediction of canonical and non-canonical miRNA-mRNA interactions. PLoS One 7 (2012) e40634.10.1371/journal.pone.0040634Search in Google Scholar PubMed PubMed Central
18. Fullaondo, A. and Lee, S.Y. Identification of putative miRNA involved in Drosophila melanogaster immune response. Dev. Comp. Immunol. 36 (2012) 267-273.Search in Google Scholar
19. Huang da, W., Sherman, B.T. and Lempicki, R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4 (2009) 44-57.Search in Google Scholar
20. Huang da, W., Sherman, B.T. and Lempicki, R.A. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37 (2009) 1-13.Search in Google Scholar
21. Shirdel, E.A., Xie, W., Mak, T.W. and Jurisica, I. NAViGaTing the micronome--using multiple microRNA prediction databases to identify signalling pathway-associated microRNAs. PLoS One 6 (2011) e17429.10.1371/journal.pone.0017429Search in Google Scholar PubMed PubMed Central
22. Witkos, T.M., Koscianska, E. and Krzyzosiak, W.J. Practical Aspects of microRNA Target Prediction. Curr. Mol. Med. 11 (2011) 93-109.Search in Google Scholar
23. Ibanez-Ventoso, C., Vora, M. and Driscoll, M. Sequence relationships among C. elegans, D. melanogaster and human microRNAs highlight the extensive conservation of microRNAs in biology. PLoS One 3 (2008) e2818.10.1371/journal.pone.0002818Search in Google Scholar PubMed PubMed Central
24. Thompson, J.D., Higgins, D.G. and Gibson, T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22 (1994) 4673-4680.Search in Google Scholar
25. de Beco, S., Ziosi, M. and Johnston, L.A. New frontiers in cell competition. Dev. Dyn. 241 (2012) 831-841.Search in Google Scholar
26. Yuan, L., Hillman, J.D. and Progulske-Fox, A. Microarray analysis of quorum-sensing-regulated genes in Porphyromonas gingivalis. Infect. Immun. 73 (2005) 4146-4154. Search in Google Scholar
27. Igaki, T., Pastor-Pareja, J.C., Aonuma, H., Miura, M. and Xu, T. Intrinsic tumor suppression and epithelial maintenance by endocytic activation of Eiger/TNF signaling in Drosophila. Dev. Cell 16 (2009) 458-465.Search in Google Scholar
28. Kuranaga, E., Kanuka, H., Igaki, T., Sawamoto, K., Ichijo, H., Okano, H. and Miura, M. Reaper-mediated inhibition of DIAP1-induced DTRAF1 degradation results in activation of JNK in Drosophila. Nat. Cell Biol. 4 (2002) 705-710.Search in Google Scholar
29. Moreno, E., Basler, K. and Morata, G. Cells compete for decapentaplegic survival factor to prevent apoptosis in Drosophila wing development. Nature 416 (2002) 755-759.Search in Google Scholar
30. Suissa, Y., Ziv, O., Dinur, T., Arama, E. and Gerlitz, O. The NAB-Brk signal bifurcates at JNK to independently induce apoptosis and compensatory proliferation. J. Biol. Chem. 286 (2011) 15556-15564.Search in Google Scholar
31. Li, W., You, L., Cooper, J., Schiavon, G., Pepe-Caprio, A., Zhou, L., Ishii, R., Giovannini, M., Hanemann, C.O., Long, S.B., Erdjument-Bromage, H., Zhou, P., Tempst, P. and Giancotti, F.G. Merlin/NF2 suppresses tumorigenesis by inhibiting the E3 ubiquitin ligase CRL4(DCAF1) in the nucleus. Cell 140 (2010) 477-490.Search in Google Scholar
32. Neto-Silva, R.M., de Beco, S. and Johnston, L.A. Evidence for a growthstabilizing regulatory feedback mechanism between Myc and Yorkie, the Drosophila homolog of Yap. Dev. Cell 19 (2010) 507-520.Search in Google Scholar
33. Prober, D.A. and Edgar, B.A. Ras1 promotes cellular growth in the Drosophila wing. Cell 100 (2000) 435-446.Search in Google Scholar
34. Vaccari, T. and Bilder, D. The Drosophila tumor suppressor vps25 prevents nonautonomous overproliferation by regulating notch trafficking. Dev. Cell 9 (2005) 687-698.Search in Google Scholar
35. Giraldez, A.J. and Cohen, S.M. Wingless and Notch signaling provide cell survival cues and control cell proliferation during wing development. Development 130 (2003) 6533-6543.Search in Google Scholar
36. Moberg, K.H., Schelble, S., Burdick, S.K. and Hariharan, I.K. Mutations in erupted, the Drosophila ortholog of mammalian tumor susceptibility gene 101, elicit non-cell-autonomous overgrowth. Dev. Cell 9 (2005) 699-710.Search in Google Scholar
37. Vidal, M., Larson, D.E. and Cagan, R.L. Csk-deficient boundary cells are eliminated from normal Drosophila epithelia by exclusion, migration, and apoptosis. Dev. Cell 10 (2006) 33-44.10.1016/j.devcel.2005.11.007Search in Google Scholar PubMed
38. Rhiner, C., Lopez-Gay, J.M., Soldini, D., Casas-Tinto, S., Martin, F.A., Lombardia, L. and Moreno, E. Flower forms an extracellular code that reveals the fitness of a cell to its neighbors in Drosophila. Dev. Cell 18 (2010) 985-998.Search in Google Scholar
39. Portela, M., Casas-Tinto, S., Rhiner, C., Lopez-Gay, J.M., Dominguez, O., Soldini, D. and Moreno, E. Drosophila SPARC is a self-protective signal expressed by loser cells during cell competition. Dev. Cell 19 (2010) 562-573. Search in Google Scholar
40. Ruby, J.G., Stark, A., Johnston, W.K., Kellis, M., Bartel, D.P. and Lai, E.C. Evolution, biogenesis, expression, and target predictions of a substantially expanded set of Drosophila microRNAs. Genome Res. 17 (2007) 1850-1864.Search in Google Scholar
41. Lai, E.C., Tomancak, P., Williams, R.W. and Rubin, G.M. Computational identification of Drosophila microRNA genes. Genome Biol. 4 (2003) R42.10.1186/gb-2003-4-7-r42Search in Google Scholar PubMed PubMed Central
42. Lim, L.P., Lau, N.C., Weinstein, E.G., Abdelhakim, A., Yekta, S., Rhoades, M.W., Burge, C.B. and Bartel, D.P. The microRNAs of Caenorhabditis elegans. Genes Dev. 17 (2003) 991-1008.Search in Google Scholar
43. Levayer, R. and Moreno, E. Mechanisms of cell competition: themes and variations. J. Cell Biol. 200 (2013) 689-698.10.1083/jcb.201301051Search in Google Scholar PubMed PubMed Central
44. Pandey, U.B. and Nichols, C.D. Human disease models in Drosophila melanogaster and the role of the fly in therapeutic drug discovery. Pharmacol. Rev. 63 (2011) 411-436.Search in Google Scholar
45. Rhiner, C. and Moreno, E. Super competition as a possible mechanism to pioneer precancerous fields. Carcinogenesis 30 (2009) 723-728.Search in Google Scholar
46. Casas-Tinto, S., Torres, M. and Moreno, E. The flower code and cancer development. Clin. Transl. Oncol. 13 (2011) 5-9.Search in Google Scholar
47. Gottardo, F., Liu, C.G., Ferracin, M., Calin, G.A., Fassan, M., Bassi, P., Sevignani, C., Byrne, D., Negrini, M., Pagano, F., Gomella, L.G., Croce, C.M. and Baffa, R. Micro-RNA profiling in kidney and bladder cancers. Urol. Oncol. 25 (2007) 387-392.Search in Google Scholar
48. Wang, X., Tang, S., Le, S.Y., Lu, R., Rader, J.S., Meyers, C. and Zheng, Z.M. Aberrant expression of oncogenic and tumor-suppressive microRNAs in cervical cancer is required for cancer cell growth. PLoS One 3 (2008) e2557.10.1371/journal.pone.0002557Search in Google Scholar PubMed PubMed Central
49. Liu, T., Tang, H., Lang, Y., Liu, M. and Li, X. MicroRNA-27a functions as an oncogene in gastric adenocarcinoma by targeting prohibitin. Cancer Lett. 273 (2009) 233-242.Search in Google Scholar
50. Mertens-Talcott, S.U., Chintharlapalli, S., Li, X. and Safe, S. The oncogenic microRNA-27a targets genes that regulate specificity protein transcription factors and the G2-M checkpoint in MDA-MB-231 breast cancer cells. Cancer Res. 67 (2007) 11001-11011.Search in Google Scholar
51. Guttilla, I.K. and White, B.A. Coordinate regulation of FOXO1 by miR-27a, miR-96, and miR-182 in breast cancer cells. J. Biol. Chem. 284 (2009) 23204-23216.Search in Google Scholar
52. Mu, W., Hu, C., Zhang, H., Qu, Z., Cen, J., Qiu, Z., Li, C., Ren, H., Li, Y., He, X., Shi, X. and Hui, L. miR-27b synergizes with anticancer drugs via p53 activation and CYP1B1 suppression. Cell Res. 25 (2015) 477-495.Search in Google Scholar
53. Li, M., Fu, W., Wo, L., Shu, X., Liu, F. and Li, C. miR-128 and its target genes in tumorigenesis and metastasis. Exp. Cell Res. 319 (2013) 3059-3064.Search in Google Scholar
54. Schraivogel, D., Weinmann, L., Beier, D., Tabatabai, G., Eichner, A., Zhu, J.Y., Anton, M., Sixt, M., Weller, M., Beier, C.P. and Meister, G. CAMTA1 is a novel tumour suppressor regulated by miR-9/9* in glioblastoma stem cells. EMBO J. 30 (2011) 4309-4322. Search in Google Scholar
55. Hsieh, I.S., Chang, K.C., Tsai, Y.T., Ke, J.Y., Lu, P.J., Lee, K.H., Yeh, S.D., Hong, T.M. and Chen, Y.L. MicroRNA-320 suppresses the stem cell-like characteristics of prostate cancer cells by downregulating the Wnt/betacatenin signaling pathway. Carcinogenesis 34 (2013) 530-538.Search in Google Scholar
56. Hong, L., Lai, M., Chen, M., Xie, C., Liao, R., Kang, Y.J., Xiao, C., Hu, W.Y., Han, J. and Sun, P. The miR-17-92 cluster of microRNAs confers tumorigenicity by inhibiting oncogene-induced senescence. Cancer Res. 70 (2010) 8547-8557.Search in Google Scholar
57. Chen, Q., Li, L., Tu, Y., Zheng, L.L., Liu, W., Zuo, X.Y., He, Y.M., Zhang, S.Y., Zhu, W., Cao, J.P., Cui, F.M. and Hou, J. MiR-34a regulates apoptosis in liver cells by targeting the KLF4 gene. Cell. Mol. Biol. Lett. 19 (2014) 52-64.Search in Google Scholar
58. Afanasyeva, E.A., Mestdagh, P., Kumps, C., Vandesompele, J., Ehemann, V., Theissen, J., Fischer, M., Zapatka, M., Brors, B., Savelyeva, L., Sagulenko, V., Speleman, F., Schwab, M. and Westermann, F. MicroRNA miR-885-5p targets CDK2 and MCM5, activates p53 and inhibits proliferation and survival. Cell Death Differ. 18 (2011) 974-984.10.1038/cdd.2010.164Search in Google Scholar PubMed PubMed Central
59. Selcuklu, S.D., Donoghue, M.T., Rehmet, K., de Souza Gomes, M., Fort, A., Kovvuru, P., Muniyappa, M.K., Kerin, M.J., Enright, A.J. and Spillane, C. MicroRNA-9 inhibition of cell proliferation and identification of novel miR-9 targets by transcriptome profiling in breast cancer cells. J. Biol. Chem. 287 (2012) 29516-29528.Search in Google Scholar
60. Sun, Q., Luo, T., Ren, Y., Florey, O., Shirasawa, S., Sasazuki, T., Robinson, D.N. and Overholtzer, M. Competition between human cells by entosis. Cell Res. 24 (2014) 1299-1310. Search in Google Scholar
© University of Wroclaw, Poland
Articles in the same Issue
- How taste works: cells, receptors and gustatory perception
- Non-cooperative immobilization of residual water bound in lyophilized photosynthetic lamellae
- Coexistence of rare variant HbD Punjab [α2β2121(Glu→Gln)] and alpha 3.7 kb deletion in a young boy of Hindu family in West Bengal, India
- Somatic stem cell aging and malignant transformation – impact on therapeutic application
- 1H NMR-based metabolic profiling for evaluating poppy seed rancidity and brewing
- Homology arms of targeting vectors for gene insertions and CRISPR/Cas9 technology: size does not matter; quality control of targeted clones does
- Death domain associated protein (Daxx), a multi-functional protein
- In silico screening of alleged miRNAs associated with cell competition: an emerging cellular event in cancer
- MGL induces nuclear translocation of EndoG and AIF in caspase-independent T cell death
- Cerivastatin represses atherogenic gene expression through the induction of KLF2 via isoprenoid metabolic pathways
- Proteasomes raise the microtubule dynamics in influenza A (H1N1) virus-infected LLC-MK2 cells
- Purinergic signaling and the functioning of the nervous system cells
- The effect of cultureware surfaces on functional and structural components of differentiated 3T3-L1 preadipocytes
- Ramipril inhibits high glucose-stimulated up-regulation of adhesion molecules via the ERK1/2 MAPK signaling pathway in human umbilical vein endothelial cells
- The effect of nicotine on the expressions of the α7 nicotinic receptor gene and Bax and Bcl-2 proteins in the mammary gland epithelial-7 breast cancer cell line and its relationship to drug resistance
- The cloning, expression and purification of recombinant human neuritin from Escherichia coli and the partial analysis of its neurobiological activity
Articles in the same Issue
- How taste works: cells, receptors and gustatory perception
- Non-cooperative immobilization of residual water bound in lyophilized photosynthetic lamellae
- Coexistence of rare variant HbD Punjab [α2β2121(Glu→Gln)] and alpha 3.7 kb deletion in a young boy of Hindu family in West Bengal, India
- Somatic stem cell aging and malignant transformation – impact on therapeutic application
- 1H NMR-based metabolic profiling for evaluating poppy seed rancidity and brewing
- Homology arms of targeting vectors for gene insertions and CRISPR/Cas9 technology: size does not matter; quality control of targeted clones does
- Death domain associated protein (Daxx), a multi-functional protein
- In silico screening of alleged miRNAs associated with cell competition: an emerging cellular event in cancer
- MGL induces nuclear translocation of EndoG and AIF in caspase-independent T cell death
- Cerivastatin represses atherogenic gene expression through the induction of KLF2 via isoprenoid metabolic pathways
- Proteasomes raise the microtubule dynamics in influenza A (H1N1) virus-infected LLC-MK2 cells
- Purinergic signaling and the functioning of the nervous system cells
- The effect of cultureware surfaces on functional and structural components of differentiated 3T3-L1 preadipocytes
- Ramipril inhibits high glucose-stimulated up-regulation of adhesion molecules via the ERK1/2 MAPK signaling pathway in human umbilical vein endothelial cells
- The effect of nicotine on the expressions of the α7 nicotinic receptor gene and Bax and Bcl-2 proteins in the mammary gland epithelial-7 breast cancer cell line and its relationship to drug resistance
- The cloning, expression and purification of recombinant human neuritin from Escherichia coli and the partial analysis of its neurobiological activity
