Transcription factor hepatocyte nuclear factor-1β (HNF-1β) regulates microRNA-200 expression through a long noncoding RNA

Journal of Biological Chemistry

Volumn 290, Issue 41, 2015, Pages 24793-24805

  Hajarnis, Sachin S ^a   Patel, Vishal ^a   Aboudehen, Karam ^a   Attanasio, Massimo ^a   Cobo Stark, Patricia ^a   Pontoglio, Marco ^b   Igarashi, Peter ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b INSTITUT COCHIN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING SITES; BINS; DISEASE CONTROL; GENE EXPRESSION; GENES; POLYMERASE CHAIN REACTION; RNA; TRANSCRIPTION FACTORS;

CHROMATIN IMMUNOPRECIPITATION; DOMINANT-NEGATIVE MUTANTS; EPITHELIAL-MESENCHYMAL TRANSITION; HEPATOCYTE NUCLEAR FACTORS; LUCIFERASE REPORTER ASSAYS; NEXT-GENERATION SEQUENCING; TISSUE-SPECIFIC GENE EXPRESSION; TRANSCRIPTIONAL TARGETS;

TRANSCRIPTION;

HEPATOCYTE NUCLEAR FACTOR 1BETA; LONG UNTRANSLATED RNA; MICRORNA 200; MICRORNA 200A; MICRORNA 200B; MICRORNA 429; UNCLASSIFIED DRUG; HNF1B PROTEIN, MOUSE; HOMEODOMAIN PROTEIN; MICRORNA; MIRN200 MICRORNA, MOUSE; POLYCYSTIC KIDNEY DISEASE 1 PROTEIN; POLYCYSTIN; REPRESSOR PROTEIN; ZEB2 PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; GENE CLUSTER; GENE EXPRESSION REGULATION; GENE MUTATION; KIDNEY EPITHELIUM; MICROARRAY ANALYSIS; MOUSE; NEXT GENERATION SEQUENCING; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA TRANSCRIPTION; ANIMAL; CYTOLOGY; DEFICIENCY; GENE INACTIVATION; GENETICS; GENOMICS; HELA CELL LINE; HUMAN; KIDNEY; METABOLISM; MUTATION; NUCLEOTIDE SEQUENCE;

ANIMALS; BASE SEQUENCE; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; GENE KNOCKOUT TECHNIQUES; GENOMICS; HELA CELLS; HEPATOCYTE NUCLEAR FACTOR 1-BETA; HOMEODOMAIN PROTEINS; HUMANS; KIDNEY; MICE; MICRORNAS; MUTATION; REPRESSOR PROTEINS; RNA, LONG NONCODING; TRPP CATION CHANNELS;

EID: 84943634487     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.670646     Document Type: Article

References (55)

1. Ott, M. O., Rey-Campos, J., Cereghini, S., and Yaniv, M. (1991) vHNF1 is expressed in epithelial cells of distinct embryonic origin during development and precedes HNF1 expression. Mech. Dev. 36, 47-58
2. Coffinier, C., Barra, J., Babinet, C., and Yaniv, M. (1999) Expression of the vHNF1/HNF1b homeoprotein gene during mouse organogenesis. Mech. Dev. 89, 211-213
3. Mendel, D. B., Hansen, L. P., Graves, M. K., Conley, P. B., and Crabtree, G. R. (1991) HNF-1a and HNF-1b (vHNF-1) share dimerization and homeo domains, but not activation domains, and form heterodimers in vitro. Genes Dev. 5, 1042-1056
4. De Simone, V., De Magistris, L., Lazzaro, D., Gerstner, J., Monaci, P., Nicosia, A., and Cortese, R. (1991) LFB3, a heterodimer-forming homeoprotein of the LFB1 family, is expressed in specialized epithelia. EMBOJ. 10, 1435-1443
5. Bai, Y., Pontoglio, M., Hiesberger, T., Sinclair, A. M., and Igarashi, P. (2002) Regulation of kidney-specific Ksp-cadherin gene promoter by hepatocyte nuclear factor-1β. Am. J. Physiol. Renal Physiol 283, F839-F851
6. Pontoglio, M., Barra, J., Hadchouel, M., Doyen, A., Kress, C., Bach, J. P., Babinet, C., and Yaniv, M. (1996) Hepatocyte nuclear factor 1 inactivation results in hepatic dysfunction, phenylketonuria, and renal Fanconi syndrome. Cell 84, 575-585
7. Sun, Z., and Hopkins, N. (2001) vhnf1, the MODY5 and familial GCKD-associated gene, regulates regional specification of the zebrafish gut, pronephros, and hindbrain. Genes Dev. 15, 3217-3229
8. Wild, W., Pogge Von Strandmann, E., Nastos, A., Senkel, S., Lingott-Frieg, A., Bulman, M., Bingham, C., Ellard, S., Hattersley, A. T., and Ryffel, G. U. (2000) The mutated human gene encoding hepatocyte nuclear factor 1β inhibits kidney formation in developing Xenopus embryos. Proc. Natl. Acad. Sci. U. S. A. 97, 4695-4700
9. Lokmane, L., Heliot, C., Garcia-Villalba, P., Fabre, M., and Cereghini, S. (2010) vHNF1 functions in distinct regulatory circuits to control ureteric bud branching and early nephrogenesis. Development 137, 347-357
10. Massa, F., Garbay, S., Bouvier, R., Sugitani, Y., Noda, T., Gubler, M. C., Heidet, L., Pontoglio, M., and Fischer, E. (2013) Hepatocyte nuclear factor 1β controls nephron tubular development. Development 140, 886-896
11. Igarashi, P., Whyte, D. A., Li, K., and Nagami, G. T. (1996) Cloning and kidney cell-specific activity of the promoter of the murine renal Na-K-C1 cotransporter gene. J. Biol. Chem. 271, 9666-9674
12. Zhang, Y., Wada, J., Yasuhara, A., Iseda, I., Eguchi, J., Fukui, K., Yang, Q., Yamagata, K., Hiesberger, T., Igarashi, P., Zhang, H., Wang, H., Akagi, S., Kanwar, Y. S., and Makino, H. (2007) The role for HNF-1β-targeted collectrin in maintenance of primary cilia and cell polarity in collecting duct cells. PLoS ONE 2, e414
13. Gresh, L., Fischer, E., Reimann, A., Tanguy, M., Garbay, S., Shao, X., Hiesberger, T., Fiette, L., Igarashi, P., Yaniv, M., and Pontoglio, M. (2004) A transcriptional network in polycystic kidney disease. EMBO J. 23, 1657-1668
14. Kikuchi, R., Kusuhara, H., Hattori, N., Shiota, K., Kim, I., Gonzalez, F. J., and Sugiyama, Y. (2006) Regulation of the expression of human organic anion transporter 3 by hepatocyte nuclear factor 1α/β and DNA methylation. Mol. Pharmacol. 70, 887-896
15. Kikuchi, R., Kusuhara, H., Hattori, N., Kim, I., Shiota, K., Gonzalez, F. J., and Sugiyama, Y. (2007) Regulation of tissue-specific expression of the human and mouse urate transporter 1 gene by hepatocyte nuclear factor 1 α/β and DNA methylation. Mol. Pharmacol. 72, 1619-1625
16. Saji, T., Kikuchi, R., Kusuhara, H., Kim, I., Gonzalez, F. J., and Sugiyama, Y. (2008) Transcriptional regulation of human and mouse organic anion transporter 1 by hepatocyte nuclear factor 1 α/β. J. Pharmacol. Exp. Ther. 324, 784-790
17. Jin, L., Kikuchi, R., Saji, T., Kusuhara, H., and Sugiyama, Y. (2012) Regulation of tissue-specific expression of renal organic anion transporters by hepatocyte nuclear factor 1 α/β and DNA methylation. J. Pharmacol. Exp. Ther. 340, 648-655
18. Cheret, C., Doyen, A., Yaniv, M., and Pontoglio, M. (2002) Hepatocyte nuclear factor 1α controls renal expression of the Npt1-Npt4 anionic transporter locus. J. Mol. Biol. 322, 929-941
19. Bingham, C., and Hattersley, A. T. (2004) Renal cysts and diabetes syndrome resulting from mutations in hepatocyte nuclear factor-1 β. Nephrol. Dial. Transplant. 19, 2703-2708
20. Hiesberger, T., Bai, Y., Shao, X., McNally, B. T., Sinclair, A. M., Tian, X., Somlo, S., and Igarashi, P. (2004) Mutation of hepatocyte nuclear factor-1{β} inhibits Pkhd1 gene expression and produces renal cysts in mice. J. Clin. Invest. 113, 814-825
21. Hiesberger, T., Shao, X., Gourley, E., Reimann, A., Pontoglio, M., and Igarashi, P. (2005) Role of the hepatocyte nuclear factor-1β (HNF-1β) C-terminal domain in Pkhd1 (ARPKD) gene transcription and renal cystogenesis. J. Biol. Chem. 280, 10578-10586
22. Boutet, A., De Frutos, C. A., Maxwell, P. H., Mayol, M. J., Romero, J., and Nieto, M. A. (2006) Snail activation disrupts tissue homeostasis and induces fibrosis in the adult kidney. EMBO J. 25, 5603-5613
23. Lee, Y., Jeon, K., Lee, J. T., Kim, S., and Kim, V. N. (2002) MicroRNA maturation: stepwise processing and subcellular localization. EMBO J. 21, 4663-4670
24. Olsen, P. H., and Ambros, V. (1999) The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. Dev. Biol. 216, 671-680
25. Galasso, M., Sana, M. E., and Volinia, S. (2010) Non-coding RNAs: a key to future personalized molecular therapy? Genome Med. 2, 12
26. Patel, V., Williams, D., Hajarnis, S., Hunter, R., Pontoglio, M., Somlo, S., and Igarashi, P. (2013) miR-17∼92 miRNA cluster promotes kidney cyst growth in polycystic kidney disease. Proc. Natl. Acad. Sci. U. S. A. 110, 10765-10770
27. Pandey, P., Brors, B., Srivastava, P. K., Bott, A., Boehn, S. N., Groene, H. J., and Gretz, N. (2008) Microarray-based approach identifies microRNAs and their target functional patterns in polycystic kidney disease. BMC Genomics 9, 624
28. Patel, V., Hajarnis, S., Williams, D., Hunter, R., Huynh, D., and Igarashi, P. (2012) MicroRNAs regulate renal tubule maturation through modulation of Pkd1. J. Am. Soc. Nephrol. 23, 1941-1948
29. Ma, Z., Gong, Y., Patel, V., Karner, C. M., Fischer, E., Hiesberger, T., Carroll, T. J., Pontoglio, M., and Igarashi, P. (2007) Mutations of HNF-1β inhibit epithelial morphogenesis through dysregulation of SOCS-3. Proc. Natl. Acad. Sci. U. S. A. 104, 20386-20391
30. Spaderna, S., Brabletz, T., and Opitz, O. G. (2009) The miR-200 family: central player for gain and loss of the epithelial phenotype. Gastroenterology 136, 1835-1837
31. Cano, A., and Nieto, M. A. (2008) Non-coding RNAs take centre stage in epithelial-to-mesenchymal transition. Trends Cell Biol. 18, 357-359
32. Yoshino, H., Enokida, H., Itesako, T., Tatarano, S., Kinoshita, T., Fuse, M., Kojima, S., Nakagawa, M., and Seki, N. (2013) Epithelial-mesenchymal transition-related microRNA-200s regulate molecular targets and pathways in renal cell carcinoma. J. Hum. Genet. 58, 508-516
33. Duns, G., Van Den Berg, A., Van Dijk, M. C., Van Duivenbode, I., Giezen, C., Kluiver, J., Van Goor, H., Hofstra, R. M., Van Den Berg, E., and Kok, K. (2013) The entire miR-200 seed family is strongly deregulated in clear cell renal cell cancer compared to the proximal tubular epithelial cells of the kidney. Genes Chromosomes Cancer 52, 165-173
34. Rebouissou, S., Vasiliu, V., Thomas, C., Bellanné-Chantelot, C., Bui, H., Chrétien, Y., Timsit, J., Rosty, C., Laurent-Puig, P., Chauveau, D., and Zucman-Rossi, J. (2005) Germline hepatocyte nuclear factor 1α and 1β mutations in renal cell carcinomas. Hum. Mol. Genet. 14, 603-614
35. Marques, A. C., Hughes, J., Graham, B., Kowalczyk, M. S., Higgs, D. R., and Ponting, C. P. (2013) Chromatin signatures at transcriptional start sites separate two equally populated yet distinct classes of intergenic long noncoding RNAs. Genome Biol. 14, R131
36. Flynn, R. A., and Chang, H. Y. (2014) Long noncoding RNAs in cell-fate programming and reprogramming. Cell Stem Cell 14, 752-761
37. Dey, B. K., Pfeifer, K., and Dutta, A. (2014) The H19 long noncoding RNA gives rise to microRNAs miR-675-3p and miR-675-5p to promote skeletal muscle differentiation and regeneration. Genes Dev. 28, 491-501
38. Legnini, I., Morlando, M., Mangiavacchi, A., Fatica, A., and Bozzoni, I. (2014) A feedforward regulatory loop between HuR and the long noncoding RNA linc-MD1 controls early phases of myogenesis. Mol. Cell 53, 506-514
39. Ballarino, M., Cazzella, V., D'Andrea, D., Grassi, L., Bisceglie, L., Cipriano, A., Santini, T., Pinnarò, C., Morlando, M., Tramontano, A., and Bozzoni, I. (2015) Novel Long Noncoding RNAs (lncRNAs) in Myogenesis: a miR-31 Overlapping lncRNA transcript controls myoblast differentiation. Mol. Cell. Biol. 35, 728-736
40. Alvarez, M. L., Khosroheidari, M., Eddy, E., and Kiefer, J. (2013) Role of microRNA 1207-5P and its host gene, the long non-coding RNA Pvt1, as mediators of extracellular matrix accumulation in the kidney: implications for diabetic nephropathy. PLoS ONE 8, e77468
41. Burk, U., Schubert, J., Wellner, U., Schmalhofer, O., Vincan, E., Spaderna, S., and Brabletz, T. (2008) A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep. 9, 582-589
42. Bracken, C. P., Gregory, P. A., Kolesnikoff, N., Bert, A. G., Wang, J., Shannon, M. F., and Goodall, G. J. (2008) A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelialmesenchymal transition. Cancer Res. 68, 7846-7854
43. Pieraccioli, M., Imbastari, F., Antonov, A., Melino, G., and Raschellà, G. (2013) Activation of miR200 by c-Myb depends on ZEB1 expression and miR200 promoter methylation. Cell Cycle 12, 2309-2320
44. Kolesnikoff, N., Attema, J. L., Roslan, S., Bert, A. G., Schwarz, Q. P., Gregory, P. A., and Goodall, G. J. (2014) Specificity protein 1 (Sp1) maintains basal epithelial expression of the miR-200 family: implications for epithelial-mesenchymal transition. J. Biol. Chem. 289, 11194-11205
45. Knouf, E. C., Garg, K., Arroyo, J. D., Correa, Y., Sarkar, D., Parkin, R. K., Wurz, K., O'Briant, K. C., Godwin, A. K., Urban, N. D., Ruzzo, W. L., Gentleman, R., Drescher, C. W., Swisher, E. M., and Tewari, M. (2012) An integrative genomic approach identifies p73 and p63 as activators of miR-200 microRNA family transcription. Nucleic Acids Res. 40, 499-510
46. Gregory, P. A., Bert, A. G., Paterson, E. L., Barry, S. C., Tsykin, A., Farshid, G., Vadas, M. A., Khew-Goodall, Y., and Goodall, G. J. (2008) The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat. Cell Biol. 10, 593-601
47. Vandewalle, C., Comijn, J., De Craene, B., Vermassen, P., Bruyneel, E., Andersen, H., Tulchinsky, E., Van Roy, F., and Berx, G. (2005) SIP1/ZEB2 induces EMT by repressing genes of different epithelial cell-cell junctions. Nucleic Acids Res. 33, 6566-6578
48. Pritchard, L., Sloane-Stanley, J. A., Sharpe, J. A., Aspinwall, R., Lu, W., Buckle, V., Strmecki, L., Walker, D., Ward, C. J., Alpers, C. E., Zhou, J., Wood, W. G., and Harris, P. C. (2000) A human PKD1 transgene generates functional polycystin-1 in mice and is associated with a cystic phenotype. Hum. Mol. Genet. 9, 2617-2627
49. Thivierge, C., Kurbegovic, A., Couillard, M., Guillaume, R., Coté, O., and Trudel, M. (2006) Overexpression of PKD1 causes polycystic kidney disease. Mol. Cell. Biol. 26, 1538-1548
50. Kurbegovic, A., Côté, O., Couillard, M., Ward, C. J., Harris, P. C., and Trudel, M. (2010) Pkd1 transgenic mice: adult model of polycystic kidney disease with extrarenal and renal phenotypes. Hum. Mol. Genet. 19, 1174-1189
51. Rossetti, S., Kubly, V. J., Consugar, M. B., Hopp, K., Roy, S., Horsley, S. W., Chauveau, D., Rees, L., Barratt, T. M., Van't Hoff, W. G., Niaudet, P., Niaudet, W. P., Torres, V. E., and Harris, P. C. (2009) Incompletely penetrant PKD1 alleles suggest a role for gene dosage in cyst initiation in polycystic kidney disease. Kidney Int. 75, 848-855
52. Hopp, K., Ward, C. J., Hommerding, C. J., Nasr, S. H., Tuan, H. F., Gainullin, V. G., Rossetti, S., Torres, V. E., and Harris, P. C. (2012) Functional polycystin-1 dosage governs autosomal dominant polycystic kidney disease severity. J. Clin. Invest. 122, 4257-4273
53. Kent, W. J., Sugnet, C. W., Furey, T. S., Roskin, K. M., Pringle, T. H., Zahler, A. M., and Haussler, D. (2002) The human genome browser at UCSC. Genome Res. 12, 996-1006
54. ENCODE Project Consortium (2012) An integrated encyclopedia of DNA elements in the human genome. Nature 489, 57-74
55. Lin, S., Lin, Y., Nery, J. R., Urich, M. A., Breschi, A., Davis, C. A., Dobin, A., Zaleski, C., Beer, M. A., Chapman, W. C., Gingeras, T. R., Ecker, J. R., and Snyder, M. P. (2014) Comparison of the transcriptional landscapes between human and mouse tissues. Proc. Natl. Acad. Sci. U. S. A. 111, 17224-17229