miR-30 family controls proliferation and differentiation of intestinal epithelial cell models by directing a broad gene expression program that includes SOX9 and the ubiquitin ligase pathway

Journal of Biological Chemistry

Volumn 291, Issue 31, 2016, Pages 15975-15984

  Peck, Bailey C E ^a   Sincavage, John ^b   Feinstein, Sydney ^b   Mah, Amanda T ^b,c   Simmons, James G ^b   Lund, P Kay ^a,b   Sethupathy, Praveen ^a,b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c University of North Carolina at Chapel Hill   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOLOGY; PROTEINS; RNA; TRANSCRIPTION FACTORS;

BIOINFORMATIC ANALYSIS; COLORECTAL ADENOCARCINOMA; IN-DEPTH ANALYSIS; INTESTINAL EPITHELIAL CELLS; LOCKED NUCLEIC ACID; REGULATORY PROGRAM; TRANSCRIPTION FACTOR EXPRESSION; UBIQUITIN LIGASES;

TRANSCRIPTION;

MESSENGER RNA; MICRORNA; MICRORNA 101; MICRORNA 145; MICRORNA 30; MICRORNA 495; TRANSCRIPTION FACTOR HES 1; TRANSCRIPTION FACTOR SOX9; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; MIRN30 MICRORNA, HUMAN; MIRN30D MICRORNA, MOUSE; SOX9 PROTEIN, HUMAN; SOX9 PROTEIN, MOUSE;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; CTNNB1 GENE; DLL4 GENE; DOWN REGULATION; ENZYME ACTIVITY; GENE; GENE EXPRESSION; GENE FUNCTION; HES1 GENE; HOMEOSTASIS; IN VITRO STUDY; INTESTINE EPITHELIUM CELL; LGR4 GENE; MOUSE; NEXT GENERATION SEQUENCING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; RNA ANALYSIS; RNA SEQUENCE; SOX9 GENE; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; CACO-2 CELL LINE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; INTESTINE CELL; MALE; METABOLISM; MUTANT MOUSE STRAIN; PHYSIOLOGY;

ANIMALS; CACO-2 CELLS; CELL DIFFERENTIATION; CELL PROLIFERATION; ENTEROCYTES; GENE EXPRESSION REGULATION; HUMANS; MALE; MICE; MICE, MUTANT STRAINS; MICRORNAS; SOX9 TRANSCRIPTION FACTOR; UBIQUITIN-PROTEIN LIGASES;

EID: 84979776395     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.733733     Document Type: Article

References (60)

1. Tsang, J., Zhu, J., and van Oudenaarden, A. (2007) MicroRNA-mediated feedback and feedforward loops are recurrent network motifs in mammals. Mol. Cell 26, 753-767
2. Herranz, H., and Cohen, S. M. (2010) MicroRNAs and gene regulatory networks: managing the impact of noise in biological systems. Genes Dev. 24, 1339-1344
3. Su, W.-L., Kleinhanz, R. R., and Schadt, E. E. (2011) Characterizing the role of miRNAs within gene regulatory networks using integrative genomics techniques. Mol. Syst. Biol. 7, 490-490
4. McKenna, L. B., Schug, J., Vourekas, A., McKenna, J. B., Bramswig, N. C., Friedman, J. R., and Kaestner, K. H. (2010) MicroRNAs control intestinal epithelial differentiation, architecture, and barrier function. Gastroenterology 139, 1654-1664
5. Ye, D., Guo, S., Al-Sadi, R., and Ma, T. Y. (2011) MicroRNA regulation of intestinal epithelial tight junction permeability. Gastroenterology 141, 1323-1333
6. Dalmasso, G., Nguyen, H. T., Yan, Y., Laroui, H., Charania, M. A., Ayyadurai, S., Sitaraman, S. V., and Merlin, D. (2011) Microbiota modulate host gene expression via microRNAs. PLoS One 6, e19293
7. Liu, S., da Cunha, A. P., Rezende, R. M., Cialic, R., Wei, Z., Bry, L., Comstock, L. E., Gandhi, R., and Weiner, H. L. (2016) The host shapes the gut microbiota via fecal microRNA. Cell Host Microbe 19, 32-43
8. van Rooij, E., Purcell, A. L., and Levin, A. A. (2012) Developing microRNA therapeutics. Circ. Res. 110, 496-507
9. Lee, S., Yoon, D. S., Paik, S., Lee, K.-M., Jang, Y., and Lee, J. W. (2014) microRNA-495 inhibits chondrogenic differentiation in human mesenchymal stem cells by targeting Sox9. Stem Cells Dev. 23, 1798-1808
10. She, Z.-Y., and Yang, W.-X. (2015) SOX family transcription factors involved in diverse cellular events during development. Eur. J. Cell Biol. 94, 547-563
11. Kanai, Y., Hiramatsu, R., Matoba, S., and Kidokoro, T. (2005) From SRY to SOX9: mammalian testis differentiation. J. Biochem. 138, 13-19
12. Mori-Akiyama, Y., Akiyama, H., Rowitch, D. H., and de Crombrugghe, B. (2003) Sox9 is required for determination of the chondrogenic cell lineage in the cranial neural crest. Proc. Natl. Acad. Sci. U.S.A. 100, 9360-9365
13. Nunn, A. C. (2012) The Role of SOX9 in Neural Progenitor Identity, Ph.D. thesis, University College London, London, UK
14. Rockich, B. E., Hrycaj, S. M., Shih, H. P., Nagy, M. S., Ferguson, M. A., Kopp, J. L., Sander, M., Wellik, D. M., and Spence, J. R. (2013) Sox9 plays multiple roles in the lung epithelium during branching morphogenesis. Proc. Natl. Acad. Sci. U.S.A. 110, E4456-E4464
15. Belo, J., Krishnamurthy, M., Oakie, A., and Wang, R. (2013) The role of SOX9 transcription factor in pancreatic and duodenal development. Stem Cells Dev. 22, 2935-2943
16. Bastide, P., Darido, C., Pannequin, J., Kist, R., Robine, S., Marty-Double, C., Bibeau, F., Scherer, G., Joubert, D., Hollande, F., Blache, P., and Jay, P. (2007) Sox9 regulates cell proliferation and is required for Paneth cell differentiation in the intestinal epithelium. J. Cell Biol. 178, 635-648
17. Roche, K. C., Gracz, A. D., Liu, X. F., Newton, V., Akiyama, H., and Magness, S. T. (2015) SOX9 maintains reserve stem cells and preserves radioresistance in mouse small intestine. Gastroenterology 149, 1553-1563
18. Sarkar, A., and Hochedlinger, K. (2013) The sox family of transcription factors: versatile regulators of stem and progenitor cell fate. Cell Stem Cell 12, 15-30
19. Kamachi, Y., and Kondoh, H. (2013) Sox proteins: regulators of cell fate specification and differentiation. Development 140, 4129-4144
20. Gracz, A. D., Ramalingam, S., and Magness, S. T. (2010) Sox9 expression marks a subset of CD24-expressing small intestine epithelial stem cells that form organoids in vitro. Am. J. Physiol. Gastrointest. Liver Physiol. 298, G590-G600
21. Van Landeghem, L., Santoro, M. A., Krebs, A. E., Mah, A. T., Dehmer, J. J., Gracz, A. D., Scull, B. P., McNaughton, K., Magness, S. T., and Lund, P. K. (2012) Activation of two distinct Sox9-EGFP-expressing intestinal stem cell populations during crypt regeneration after irradiation. Am. J. Physiol. Gastrointest. Liver Physiol. 302, G1111-G1132
22. Formeister, E. J., Sionas, A. L., Lorance, D. K., Barkley, C. L., Lee, G. H., and Magness, S. T. (2009) Distinct SOX9 levels differentially mark stem/progenitor populations and enteroendocrine cells of the small intestine epithelium. Am. J. Physiol. Gastrointest. Liver Physiol. 296, G1108-G1118
23. Mah, A. T., Van Landeghem, L., Gavin, H. E., Magness, S. T., and Lund, P. K. (2014) Impact of diet-induced obesity on intestinal stem cells: hyperproliferation but impaired intrinsic function that requires insulin/IGF1. Endocrinology 155, 3302-3314
24. Andres, S. F., Simmons, J. G., Mah, A. T., Santoro, M. A., Van Landeghem, L., and Lund, P. K. (2013) Insulin receptor isoform switching in intestinal stem cells, progenitors, differentiated lineages and tumors: evidence that IR-B limits proliferation. J. Cell Sci. 126, 5645-5656
25. Dynoodt, P., Speeckaert, R., De Wever, O., Chevolet, I., Brochez, L., Lambert, J., and Van Gele, M. (2013) miR-145 overexpression suppresses the migration and invasion of metastatic melanoma cells. Int. J. Oncol. 42, 1443-1451
26. Yu, C.-C., Tsai, L.-L., Wang, M.-L., Yu, C.-H., Lo, W.-L., Chang, Y.-C., Chiou, G.-Y., Chou, M.-Y., and Chiou, S.-H. (2013) miR145 targets the SOX9/ADAM17 axis to inhibit tumor-initiating cells and IL-6-mediated paracrine effects in head and neck cancer. Cancer Res. 73, 3425-3440
27. Martinez-Sanchez, A., Dudek, K. A., and Murphy, C. L. (2012) Regulation of human chondrocyte function through direct inhibition of cartilage master regulator SOX9 by microRNA-145 (miRNA-145). J. Biol. Chem. 287, 916-924
28. Yang, B., Guo, H., Zhang, Y., Chen, L., Ying, D., and Dong, S. (2011) MicroRNA-145 regulates chondrogenic differentiation of mesenchymal stem cells by targeting Sox9. PLoS One 6, e21679
29. Zhang, Y., Guo, X., Xiong, L., Kong, X., Xu, Y., Liu, C., Zou, L., Li, Z., Zhao, J., and Lin, N. (2012) MicroRNA-101 suppresses SOX9-dependent tumorigenicity and promotes favorable prognosis of human hepatocellular carcinoma. FEBS Lett. 586, 4362-4370
30. Lewis, B. P., Burge, C. B., and Bartel, D. P. (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 15-20
31. Grimson, A., Farh, K. K., Johnston, W. K., Garrett-Engele, P., Lim, L. P., and Bartel, D. P. (2007) MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol. Cell 27, 91-105
32. Garcia, D. M., Baek, D., Shin, C., Bell, G. W., Grimson, A., and Bartel, D. P. (2011) Weak seed-pairing stability and high target-site abundance decrease the proficiency of lsy-6 and other microRNAs. Nat. Struct. Mol. Biol. 18, 1139-1146
33. Friedman, R. C., Farh, K. K., Burge, C. B., and Bartel, D. P. (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 19, 92-105
34. Chivukula, R. R., Shi, G., Acharya, A., Mills, E. W., Zeitels, L. R., Anandam, J. L., Abdelnaby, A. A., Balch, G. C., Mansour, J. C., Yopp, A. C., Maitra, A., and Mendell, J. T. (2014) An essential mesenchymal function for miR-143/145 in intestinal epithelial regeneration. Cell 157, 1104-1116
35. Chang, T., Xie, J., Li, H., Li, D., Liu, P., and Hu, Y. (2016) MicroRNA-30a promotes extracellular matrix degradation in articular cartilage via downregulation of Sox9. Cell Prolif. 49, 207-218
36. Robinson, M. D., McCarthy, D. J., and Smyth, G. K. (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139-140
37. Baran-Gale, J., Fannin, E. E., Kurtz, C. L., and Sethupathy, P. (2013) Beta cell 5′-shifted isomiRs are candidate regulatory hubs in type 2 diabetes. PLoS One 8, e73240
38. Kurtz, C. L., Peck, B. C., Fannin, E. E., Beysen, C., Miao, J., Landstreet, S. R., Ding, S., Turaga, V., Lund, P. K., Turner, S., Biddinger, S. B., Vickers, K. C., and Sethupathy, P. (2014) MicroRNA-29 fine-tunes the expression of key FOXA2-activated lipid metabolism genes and is dysregulated in animal models of insulin resistance and diabetes. Diabetes 63, 3141-3148
39. Peck, B. C., Weiser, M., Lee, S. E., Gipson, G. R., Iyer, V. B., Sartor, R. B., Herfarth, H. H., Long, M. D., Hansen, J. J., Isaacs, K. L., Trembath, D. G., Rahbar, R., Sadiq, T. S., Furey, T. S., Sethupathy, P., and Sheikh, S. Z. (2015) MicroRNAs classify different disease behavior phenotypes of Crohn's disease and may have prognostic utility. Inflamm. Bowel Dis. 21, 2178-2187
40. Gene Ontology Consortium (2015) Gene Ontology Consortium: going forward. Nucleic Acids Res. 43, D1049-D1056
41. Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., Harris, M. A., Hill, D. P., Issel-Tarver, L., Kasarskis, A., Lewis, S., et al. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25, 25-29
42. Chen, E. Y., Tan, C. M., Kou, Y., Duan, Q., Wang, Z., Meirelles, G. V., Clark, N. R., and Ma'ayan, A. (2013) Enrichr: interactive and collaborative HTML5 gene list enrichment analysis tool. BMC Bioinformatics 14, 128
43. Hattori, T., Kishino, T., Stephen, S., Eberspaecher, H., Maki, S., Takigawa, M., de Crombrugghe, B., and Yasuda, H. (2013) E6-AP/UBE3A protein acts as a ubiquitin ligase toward SOX9 protein. J. Biol. Chem. 288, 35138-35148
44. Shi, Z., Chiang, C.-I., Mistretta, T.-A., Major, A., and Mori-Akiyama, Y. (2013) SOX9 directly regulates IGFBP-4 in the intestinal epithelium. Am. J. Physiol. Gastrointest. Liver Physiol. 305, G74-G83
45. Mologni, L., Dekhil, H., Ceccon, M., Purgante, S., Lan, C., Cleris, L., Magistroni, V., Formelli, F., and Gambacorti-Passerini, C. B. (2010) Colorectal tumors are effectively eradicated by combined Inhibition of β-catenin, KRAS, and the oncogenic transcription factor ITF2. Cancer Res. 70, 7253-7263
46. He, P., Liang, J., Shao, T., Guo, Y., Hou, Y., and Li, Y. (2015) HDAC5 promotes colorectal cancer cell proliferation by up-regulating DLL4 expression. Int. J. Clin. Exp. Med. 8, 6510-6516
47. Mustata, R. C., Van Loy, T., Lefort, A., Libert, F., Strollo, S., Vassart, G., and Garcia, M.-I. (2011) Lgr4 is required for Paneth cell differentiation and maintenance of intestinal stem cells ex vivo. EMBO Reports 12, 558-564
48. Noah, T. K., Donahue, B., and Shroyer, N. F. (2011) Intestinal development and differentiation. Exp. Cell Res. 317, 2702-2710
49. Van Beers, E. H., Al, R. H., Rings, E. H., Einerhand, A. W., Dekker, J., and Büller, H. A. (1995) Lactase and sucrase-isomaltase gene expression during Caco-2 cell differentiation. Biochem. J. 308, 769-775
50. Hidalgo, I. J., Raub, T. J., and Borchardt, R. T. (1989) Characterization of the human colon carcinoma cell line (Caco-2) as a model system for intestinal epithelial permeability. Gastroenterology 96, 736-749
51. Zweibaum, A., Triadou, N., Kedinger, M., Augeron, C., Robine-Léon, S., Pinto, M., Rousset, M., and Haffen, K. (1983) Sucrase-isomaltase: a marker of foetal and malignant epithelial cells of the human colon. Int. J. Cancer 32, 407-412
52. Agrawal, R., Tran, U., and Wessely, O. (2009) The miR-30 miRNA family regulates Xenopus pronephros development and targets the transcription factor Xlim1/Lhx1. Development 136, 3927-3936
53. Guess, M. G., Barthel, K. K., Harrison, B. C., and Leinwand, L. A. (2015) miR-30 family microRNAs regulate myogenic differentiation and provide negative feedback on the microRNA pathway. PLoS One 10, e0118229-18
54. Wu, T., Zhou, H., Hong, Y., Li, J., Jiang, X., and Huang, H. (2012) miR-30 family members negatively regulate osteoblast differentiation. J. Biol. Chem. 287, 7503-7511
55. Perreault, N., and Beaulieu, J. F. (1996) Use of the dissociating enzyme thermolysin to generate viable human normal intestinal epithelial cell cultures. Exp. Cell Res. 224, 354-364
56. Basuroy, S., Sheth, P., Kuppuswamy, D., Balasubramanian, S., Ray, R. M., and Rao, R. K. (2003) Expression of kinase-inactive c-Src delays oxidative stress-induced disassembly and accelerates calcium-mediated reassembly of tight junctions in the Caco-2 cell monolayer. J. Biol. Chem. 278, 11916-11924
57. Gil-Zamorano, J., Martin, R., Daimiel, L., Richardson, K., Giordano, E., Nicod, N., García-Carrasco, B., Soares, S. M., Iglesias-Gutiérrez, E., Lasunción, M. A., Sala-Vila, A., Ros, E., Ordovás, J. M., Visioli, F., and Dávalos, A. (2014) Docosahexaenoic acid modulates the enterocyte Caco-2 cell expression of microRNAs involved in lipid metabolism. J. Nutr. 144, 575-585
58. Briske-Anderson, M. J., Finley, J. W., and Newman, S. M. (1997) The influence of culture time and passage number on the morphological and physiological development of Caco-2 cells. Proc. Soc. Exp. Biol. Med. 214, 248-257
59. Wang, K., Singh, D., Zeng, Z., Coleman, S. J., Huang, Y., Savich, G. L., He, X., Mieczkowski, P., Grimm, S. A., Perou, C. M., MacLeod, J. N., Chiang, D. Y., Prins, J. F., and Liu, J. (2010) MapSplice: accurate mapping of RNA-seq reads for splice junction discovery. Nucleic Acids Res. 38, e178
60. Li, B., and Dewey, C. N. (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12, 323