miR-9 enhances the transactivation of nuclear factor of activated T cells by targeting KPNB1 and DYRK1B

American Journal of Physiology - Cell Physiology

Volumn 308, Issue 9, 2015, Pages C720-C728

  Zeng, Yan ^a   Wang, Yuna ^a   Wu, Zhiqin ^a   Kang, Kang ^a   Peng, Xiao ^a   Peng, Wenda ^a   Qu, Junle ^a   Liu, Lin ^b   Usha Raj, J ^c   Gou, Deming ^a  

^a SHENZHEN UNIVERSITY   (China)

^b OKLAHOMA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

IL 2; Jurkat T cells; miR 9; NFAT

Indexed keywords

CALCINEURIN; DUAL SPECIFICITY TYROSINE PHOSPHORYLATION REGULATED KINASE 1B; INTERLEUKIN 2; IONOMYCIN; KARYOPHERIN; KARYOPHERIN BETA1; MICRORNA 124; MICRORNA 375; MICRORNA 9; PHOSPHOTRANSFERASE; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG; DYRK KINASE; IL2 PROTEIN, HUMAN; KARYOPHERIN BETA; KPNB1 PROTEIN, HUMAN; MICRORNA; MIRN92 MICRORNA, HUMAN; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN SERINE THREONINE KINASE; PROTEIN TYROSINE KINASE;

ARTICLE; BINDING SITE; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVITY; ENZYME MECHANISM; EXPRESSION VECTOR; FEMALE; GENE EXPRESSION; GENE OVEREXPRESSION; GENE TRANSLOCATION; GENETIC TRANSFECTION; HEK293 CELL LINE; HELA CELL LINE; HUMAN; HUMAN CELL; JURKAT CELL LINE; NUCLEOCYTOPLASMIC TRANSPORT; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; REGULATORY MECHANISM; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TRANSACTIVATION; UPREGULATION; ACTIVE TRANSPORT; DRUG EFFECTS; ENZYMOLOGY; GENETICS; LYMPHOCYTE ACTIVATION; METABOLISM; PHOSPHORYLATION; TIME; TRANSCRIPTION INITIATION;

ACTIVE TRANSPORT, CELL NUCLEUS; BETA KARYOPHERINS; HEK293 CELLS; HELA CELLS; HUMANS; INTERLEUKIN-2; IONOMYCIN; JURKAT CELLS; LYMPHOCYTE ACTIVATION; MICRORNAS; NFATC TRANSCRIPTION FACTORS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TETRADECANOYLPHORBOL ACETATE; TIME FACTORS; TRANSCRIPTIONAL ACTIVATION; TRANSFECTION;

EID: 84930841574     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00299.2014     Document Type: Article

References (36)

1. Bazzoni F, Rossato M, Fabbri M, Gaudiosi D, Mirolo M, Mori L, Tamassia N, Mantovani A, Cassatella MA, Locati M. Induction and regulatory function of miR-9 in human monocytes and neutrophils exposed to proinflammatory signals. Proc Natl Acad Sci USA 106: 5282- 5287, 2009.
2. Becker W, Joost HG. Structural and functional characteristics of Dyrk, a novel subfamily of protein kinases with dual specificity. Prog Nucleic Acid Res Mol Biol 62: 1-17, 1999.
3. Becker W, Weber Y, Wetzel K, Eirmbter K, Tejedor FJ, Joost HG. Sequence characteristics, subcellular localization, and substrate specificity of DYRK-related kinases, a novel family of dual specificity protein kinases. J Biol Chem 273: 25893-25902, 1998.
4. da Costa Martins PA, Salic K, Gladka MM, Armand AS, Leptidis S, el Azzouzi H, Hansen A, Coenen-de Roo CJ, Bierhuizen MF, van der Nagel R, van Kuik J, de Weger R, de Bruin A, Condorelli G, Arbones ML, Eschenhagen T, De Windt LJ. MicroRNA-199b targets the nuclear kinase Dyrk1a in an auto-amplification loop promoting calcineurin/NFAT signalling. Nat Cell Biol 12: 1220-1227, 2010.
5. Deng X, Ewton DZ, Friedman E. Mirk/Dyrk1B maintains the viability of quiescent pancreatic cancer cells by reducing levels of reactive oxygen species. Cancer Res 69: 3317-3324, 2009.
6. Dilda F, Gioia G, Pisani L, Restelli L, Lecchi C, Albonico F, Bronzo V, Mortarino M, Ceciliani F. Escherichia coli lipopolysaccharides and Staphylococcus aureus enterotoxin B differentially modulate inflammatory microRNAs in bovine monocytes. Vet J 192: 514-516, 2012.
7. Elyada E, Pribluda A, Goldstein RE, Morgenstern Y, Brachya G, Cojocaru G, Snir-Alkalay I, Burstain I, Haffner-Krausz R, Jung S, Wiener Z, Alitalo K, Oren M, Pikarsky E, Ben-Neriah Y. CKIα ablation highlights a critical role for p53 in invasiveness control. Nature 470: 409-413, 2011.
8. Gwack Y, Sharma S, Nardone J, Tanasa B, Iuga A, Srikanth S, Okamura H, Bolton D, Feske S, Hogan PG, Rao A. A genome-wide Drosophila RNAi screen identifies DYRK-family kinases as regulators of NFAT. Nature 441: 646-650, 2006.
9. Hogan PG, Chen L, Nardone J, Rao A. Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev 17: 2205-2232, 2003.
10. Huntzinger E, Izaurralde E. Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet 12: 99-110, 2011.
11. Jung HJ, Coffinier C, Choe Y, Beigneux AP, Davies BS, Yang SH, Barnes RH 2nd, Hong J, Sun T, Pleasure SJ, Young SG, Fong LG. Regulation of prelamin A but not lamin C by miR-9, a brain-specific microRNA. Proc Natl Acad Sci USA 109: E423-E431, 2012.
12. Kang K, Peng X, Zhang X, Wang Y, Zhang L, Gao L, Weng T, Zhang H, Ramchandran R, Raj JU, Gou D, Liu L. MicroRNA-124 suppresses the transactivation of nuclear factor of activated T cells by targeting multiple genes and inhibits the proliferation of pulmonary artery smooth muscle cells. J Biol Chem 288: 25414-25427, 2013.
13. Kang K, Zhang X, Liu H, Wang Z, Zhong J, Huang Z, Peng X, Zeng Y, Wang Y, Yang Y, Luo J, Gou D. A novel real-time PCR assay of microRNAs using S-Poly(T), a specific oligo(dT) reverse transcription primer with excellent sensitivity and specificity. PLos One 7: e48536, 2012.
14. Krell J, Frampton AE, Jacob J, Pellegrino L, Roca-Alonso L, Zeloof D, Alifrangis C, Lewis JS, Jiao LR, Stebbing J, Castellano L. The clinico-pathologic role of microRNAs miR-9 and miR-151-5p in breast cancer metastasis. Mol Diagn Ther 16: 167-172, 2012.
15. Leucci E, Zriwil A, Gregersen LH, Jensen KT, Obad S, Bellan C, Leoncini L, Kauppinen S, Lund AH. Inhibition of miR-9 de-represses HuR and DICER1 and impairs Hodgkin lymphoma tumour outgrowth in vivo. Oncogene 31: 5081-5089, 2012.
16. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120: 15-20, 2005.
17. Li Q, Lin X, Yang X, Chang J. NFATc4 is negatively regulated in miR-133a-mediated cardiomyocyte hypertrophic repression. Am J Physiol Heart Circ Physiol 298: H1340-H1347, 2010.
18. Li W, Kong LB, Li JT, Guo ZY, Xue Q, Yang T, Meng YL, Jin BQ, Wen WH, Yang AG. MiR-568 inhibits the activation and function of CD4+ T cells and Treg cells by targeting NFAT5. Int Immunol 26: 269-281, 2014.
19. Lin Z, Murtaza I, Wang K, Jiao J, Gao J, Li PF. miR-23a functions downstream of NFATc3 to regulate cardiac hypertrophy. Proc Natl Acad Sci USA 106: 12103-12108, 2009.
20. Liu XK, Lin X, Gaffen SL. Crucial role for nuclear factor of activated T cells in T cell receptor-mediated regulation of human interleukin-17. J Biol Chem 279: 52762-52771, 2004.
21. -ΔΔCT method. Methods 25: 402-408, 2001.
22. Macian F. NFAT proteins: key regulators of T-cell development and function. Nat Rev Immunol 5: 472-484, 2005.
23. Muller MR, Rao A. NFAT, immunity and cancer: a transcription factor comes of age. Nat Rev Immunol 10: 645-656, 2010.
24. Pan MG, Xiong Y, Chen F. NFAT gene family in inflammation and cancer. Curr Mol Med 13: 543-554, 2013.
25. Plaisance V, Abderrahmani A, Perret-Menoud V, Jacquemin P, Lemaigre F, Regazzi R. MicroRNA-9 controls the expression of Granuphilin/ Slp4 and the secretory response of insulin-producing cells. J Biol Chem 281: 26932-26942, 2006.
26. Schonrock N, Humphreys DT, Preiss T, Gotz J. Target gene repression mediated by miRNAs miR-181c and miR-9 both of which are downregulated by amyloid-β. J Mol Neurosci 46: 324-335, 2012.
27. Seddiki N, Phetsouphanh C, Swaminathan S, Xu Y, Rao S, Li J, Sutcliffe EL, Denyer G, Finlayson R, Gelgor L, Cooper DA, Zaunders J, Kelleher AD. The microRNA-9/B-lymphocyte-induced maturation protein-1/IL-2 axis is differentially regulated in progressive HIV infection. Eur J Immunol 43: 510-520, 2013.
28. Sharma S, Findlay GM, Bandukwala HS, Oberdoerffer S, Baust B, Li Z, Schmidt V, Hogan PG, Sacks DB, Rao A. Dephosphorylation of the nuclear factor of activated T cells (NFAT) transcription factor is regulated by an RNA-protein scaffold complex. Proc Natl Acad Sci USA 108: 11381-11386, 2011.
29. Shaw JP, Utz PJ, Durand DB, Toole JJ, Emmel EA, Crabtree GR. Identification of a putative regulator of early T cell activation genes. Science 241: 202-205, 1988.
30. Strom AC, Weis K. Importin-β-like nuclear transport receptors. Genome Biol 2: REVIEWS3008, 2001.
31. Tardif G, Pelletier JP, Fahmi H, Hum D, Zhang Y, Kapoor M, Martel-Pelletier J. NFAT3 and TGF-β/SMAD3 regulate the expression of miR-140 in osteoarthritis. Arthritis Res Ther 15: R197, 2013.
32. + T cells by repressing Blimp-1. Eur J Immunol 42: 2100-2108, 2012.
33. Tsitsiou E, Lindsay MA. microRNAs and the immune response. Curr Opin Pharmacol 9: 514-520, 2009.
34. Venkatesh N, Feng Y, DeDecker B, Yacono P, Golan D, Mitchison T, McKeon F. Chemical genetics to identify NFAT inhibitors: potential of targeting calcium mobilization in immunosuppression. Proc Natl Acad Sci USA 101: 8969-8974, 2004.
35. + T cells. Blood 113: 6648-6657, 2009.
36. Willingham AT, Orth AP, Batalov S, Peters EC, Wen BG, Aza-Blanc P, Hogenesch JB, Schultz PG. A strategy for probing the function of noncoding RNAs finds a repressor of NFAT. Science 309: 1570-1573, 2005.