Redistribution of demethylated RNA helicase A during foot-and-mouth disease virus infection: Role of jumonji c-domain containing protein 6 in RHA demethylation

Virology

Volumn 452-453, Issue , 2014, Pages 1-11

  Lawrence, Paul ^a   Conderino, Joseph S ^a   Rieder, Elizabeth ^a  

^a PLUM ISLAND ANIMAL DISEASE CENTER   (United States)

Author keywords

Arginine demethylation; Foot and mouth disease virus (FMDV); Jumonji C domain containing protein 6 (JMJD6); RNA helicase A (RHA)

Indexed keywords

GLYCINE DERIVATIVE; HISTONE DEMETHYLASE; MONOMER; N OXALYLGLYCINE; RNA HELICASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DEMETHYLATION; FOOT AND MOUTH DISEASE; FOOT AND MOUTH DISEASE VIRUS; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; VIRUS CELL INTERACTION; VIRUS REPLICATION;

ARGININE DEMETHYLATION; FOOT-AND-MOUTH DISEASE VIRUS (FMDV); JUMONJI C-DOMAIN CONTAINING PROTEIN 6 (JMJD6); RNA HELICASE A (RHA);

ANIMALS; CATTLE; CATTLE DISEASES; CELL LINE; CELL NUCLEUS; CRICETINAE; CYTOPLASM; FOOT-AND-MOUTH DISEASE; FOOT-AND-MOUTH DISEASE VIRUS; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; METHYLATION; PROTEIN BINDING; PROTEIN TRANSPORT; RNA HELICASES;

EID: 84892855175     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.12.040     Document Type: Article

References (59)

1. Abdelhaleem M.M., Hameed S., Klassen D., Greenberg A.H. Leukophysin: an RNA helicase A-related molecule identified in cytotoxic T cell granules and vesicles. J. Immunol. 1996, 156:2026-2035.
2. Aratani S., Fujii R., Oishi T., Fujita H., Amano T., Ohshima T., Hagiwara M., Fukamizu A., Nakajima T. Dual roles of RNA helicase A in CREB-dependent transcription. Mol. Cell. Biol. 2001, 21:4460-4469.
3. Bachand F. Protein arginine methyltransferases: from unicellular eukaryotes to humans. Eukaryot. Cell 2007, 6:889-898.
4. Back S.H., Kim Y.K., Kim W.J., Cho S., Oh H.R., Kim J.E., Jang S.K. Translation of polioviral mRNA is inhibited by cleavage of polypyrimidine tract-binding proteins executed by polioviral 3C(pro). J. Virol. 2002, 76:2529-2542.
5. Cammas A., Pileur F., Bonnal S., Lewis S.M., Leveque N., Holcik M., Vagner S. Cytoplasmic relocalization of heterogeneous nuclear ribonucleoprotein A1 controls translation initiation of specific mRNAs. Mol. Biol. Cell 2007, 18:5048-5059.
6. Cao W.M., Murao K., Imachi H., Hiramine C., Abe H., Yu X., Dobashi H., Wong N.C., Takahara J., Ishida T. Phosphatidylserine receptor cooperates with high-density lipoprotein receptor in recognition of apoptotic cells by thymic nurse cells. J. Mol. Endocrinol. 2004, 32:497-505.
7. Chang B., Chen Y., Zhao Y., Bruick R.K. JMJD6 is a histone arginine demethylase. Science 2007, 318:444-447.
8. Chau C.M., Deng Z., Kang H., Lieberman P.M. Cell cycle association of the retinoblastoma protein Rb and the histone demethylase LSD1 with the Epstein-Barr virus latency promoter Cp. J. Virol. 2008, 82:3428-3437.
9. Cho H.S., Suzuki T., Dohmae N., Hayami S., Unoki M., Yoshimatsu M., Toyokawa G., Takawa M., Chen T., Kurash J.K., Field H.I., Ponder B.A., Nakamura Y., Hamamoto R. Demethylation of RB regulator MYPT1 by histone demethylase LSD1 promotes cell cycle progression in cancer cells. Cancer Res. 2011, 71:655-660.
10. Cikala M., Alexandrova O., David C.N., Proschel M., Stiening B., Cramer P., Bottger A. The phosphatidylserine receptor from Hydra is a nuclear protein with potential Fe(II) dependent oxygenase activity. BMC Cell Biol. 2004, 5:26.
11. Cui P., Qin B., Liu N., Pan G., Pei D. Nuclear localization of the phosphatidylserine receptor protein via multiple nuclear localization signals. Exp. Cell Res. 2004, 293:154-163.
12. Esko J.D., Rostand K.S., Weinke J.L. Tumor formation dependent on proteoglycan biosynthesis. Science 1988, 241:1092-1096.
13. Fadok V.A., Bratton D.L., Rose D.M., Pearson A., Ezekewitz R.A., Henson P.M. A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature 2000, 405:85-90.
14. Gardner K.E., Allis C.D., Strahl B.D. Operating on chromatin, a colorful language where context matters. J. Mol. Biol. 2011, 409:36-46.
15. Gu H., Roizman B. Engagement of the lysine-specific demethylase/HDAC1/CoREST/REST complex by herpes simplex virus 1. J. Virol. 2009, 83:4376-4385.
16. Guex N., Peitsch M.C. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 1997, 18:2714-2723.
17. Gustin K.E., Sarnow P. Inhibition of nuclear import and alteration of nuclear pore complex composition by rhinovirus. J. Virol. 2002, 76:8787-8796.
18. Hahn P., Bose J., Edler S., Lengeling A. Genomic structure and expression of Jmjd6 and evolutionary analysis in the context of related JmjC domain containing proteins. BMC Genomics 2008, 9:293.
19. Hahn P., Wegener I., Burrells A., Bose J., Wolf A., Erck C., Butler D., Schofield C.J., Bottger A., Lengeling A. Analysis of Jmjd6 cellular localization and testing for its involvement in histone demethylation. PLoS One 2010, 5:e13769.
20. Hamada S., Kim T.D., Suzuki T., Itoh Y., Tsumoto H., Nakagawa H., Janknecht R., Miyata N. Synthesis and activity of N-oxalylglycine and its derivatives as Jumonji C-domain-containing histone lysine demethylase inhibitors. Bioorg. Med. Chem. Lett. 2009, 19:2852-2855.
21. Han G., Li J., Wang Y., Li X., Mao H., Liu Y., Chen C.D. The hydroxylation activity of Jmjd6 is required for its homo-oligomerization. J. Cell. Biochem. 2012, 113:1663-1670.
22. Hoffmann P.R., deCathelineau A.M., Ogden C.A., Leverrier Y., Bratton D.L., Daleke D.L., Ridley A.J., Fadok V.A., Henson P.M. Phosphatidylserine (PS) induces PS receptor-mediated macropinocytosis and promotes clearance of apoptotic cells. J. Cell Biol. 2001, 155:649-659.
23. Hong S., Cho Y.W., Yu L.R., Yu H., Veenstra T.D., Ge K. Identification of JmjC domain-containing UTX and JMJD3 as histone H3 lysine 27 demethylases. Proc. Natl. Acad. Sci. USA 2007, 104:18439-18444.
24. Huang J., Sengupta R., Espejo A.B., Lee M.G., Dorsey J.A., Richter M., Opravil S., Shiekhattar R., Bedford M.T., Jenuwein T., Berger S.L. p53 is regulated by the lysine demethylase LSD1. Nature 2007, 449:105-108.
25. Kaplan W., Littlejohn T.G. Swiss-PDB viewer (deep view). Brief. Bioinf. 2001, 2:195-197.
26. Karplus K., Barrett C., Hughey R. Hidden Markov models for detecting remote protein homologies. Bioinformatics 1998, 14:846-856.
27. Karplus K., Sjolander K., Barrett C., Cline M., Haussler D., Hughey R., Holm L., Sander C. Predicting protein structure using hidden Markov models. Proteins Suppl. 1997, 1:134-139.
28. Kokura K., Fang J. In vitro histone demethylase assays. Methods Mol. Biol. 2009, 523:249-261.
29. Krause C.D., Yang Z.H., Kim Y.S., Lee J.H., Cook J.R., Pestka S. Protein arginine methyltransferases: evolution and assessment of their pharmacological and therapeutic potential. Pharmacol. Ther. 2007, 113:50-87.
30. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
31. Lawrence P., LaRocco M., Baxt B., Rieder E. Examination of soluble integrin resistant mutants of foot-and-mouth disease virus. Virol. J. 2013, 10:2.
32. Lawrence P., Rieder E. Identification of RNA helicase A as a new host factor in the replication cycle of foot-and-mouth disease virus. J. Virol. 2009, 83:11356-11366.
33. Lawrence P., Schafer E.A., Rieder E. The nuclear protein Sam68 is cleaved by the FMDV 3C protease redistributing Sam68 to the cytoplasm during FMDV infection of host cells. Virology 2012, 425:40-52.
34. Liang Y., Vogel J.L., Narayanan A., Peng H., Kristie T.M. Inhibition of the histone demethylase LSD1 blocks alpha-herpesvirus lytic replication and reactivation from latency. Nat. Med. 2009, 15:1312-1317.
35. Mantri M., Krojer T., Bagg E.A., Webby C.J., Butler D.S., Kochan G., Kavanagh K.L., Oppermann U., McDonough M.A., Schofield C.J. Crystal structure of the 2-oxoglutarate- and Fe(II)-dependent lysyl hydroxylase JMJD6. J. Mol. Biol. 2010, 401:211-222.
36. McBride A.E., Schlegel A., Kirkegaard K. Human protein Sam68 relocalization and interaction with poliovirus RNA polymerase in infected cells. Proc. Natl. Acad. Sci. USA 1996, 93:2296-2301.
37. Mosammaparast N., Shi Y. Reversal of histone methylation: biochemical and molecular mechanisms of histone demethylases. Annu. Rev. Biochem. 2010, 79:155-179.
38. Ng S.S., Yue W.W., Oppermann U., Klose R.J. Dynamic protein methylation in chromatin biology. Cell. Mol. Life Sci. 2009, 66:407-422.
39. Nicholson T.B., Chen T. LSD1 demethylates histone and non-histone proteins. Epigenetics 2009, 4:129-132.
40. Niepmann M., Petersen A., Meyer K., Beck E. Functional involvement of polypyrimidine tract-binding protein in translation initiation complexes with the internal ribosome entry site of foot-and-mouth disease virus. J. Virol. 1997, 71:8330-8339.
41. Ota T., Suzuki Y., Nishikawa T., Otsuki T., Sugiyama T., Irie R., Wakamatsu A., Hayashi K., Sato H., Nagai K., Kimura K., Makita H., Sekine M., Obayashi M., Nishi T., Shibahara T., Tanaka T., Ishii S., Yamamoto J., Saito K., Kawai Y., Isono Y., Nakamura Y., Nagahari K., Murakami K., Yasuda T., Iwayanagi T., Wagatsuma M., Shiratori A., Sudo H., Hosoiri T., Kaku Y., Kodaira H., Kondo H., Sugawara M., Takahashi M., Kanda K., Yokoi T., Furuya T., Kikkawa E., Omura Y., Abe K., Kamihara K., Katsuta N., Sato K., Tanikawa M., Yamazaki M., Ninomiya K., Ishibashi T., Yamashita H., Murakawa K., Fujimori K., Tanai H., Kimata M., Watanabe M., Hiraoka S., Chiba Y., Ishida S., Ono Y., Takiguchi S., Watanabe S., Yosida M., Hotuta T., Kusano J., Kanehori K., Takahashi-Fujii A., Hara H., Tanase T.O., Nomura Y., Togiya S., Komai F., Hara R., Takeuchi K., Arita M., Imose N., Musashino K., Yuuki H., Oshima A., Sasaki N., Aotsuka S., Yoshikawa Y., Matsunawa H., Ichihara T., Shiohata N., Sano S., Moriya S., Momiyama H., Satoh N., Takami S., Terashima Y., Suzuki O., Nakagawa S., Senoh A., Mizoguchi H., Goto Y., Shimizu F., Wakebe H., Hishigaki H., Watanabe T., Sugiyama A., Takemoto M., Kawakami B., Yamazaki M., Watanabe K., Kumagai A., Itakura S., Fukuzumi Y., Fujimori Y., Komiyama M., Tashiro H., Tanigami A., Fujiwara T., Ono T., Yamada K., Fujii Y., Ozaki K., Hirao M., Ohmori Y., Kawabata A., Hikiji T., Kobatake N., Inagaki H., Ikema Y., Okamoto S., Okitani R., Kawakami T., Noguchi S., Itoh T., Shigeta K., Senba T., Matsumura K., Nakajima Y., Mizuno T., Morinaga M., Sasaki M., Togashi T., Oyama M., Hata H., Watanabe M., Komatsu T., Mizushima-Sugano J., Satoh T., Shirai Y., Takahashi Y., Nakagawa K., Okumura K., Nagase T., Nomura N., Kikuchi H., Masuho Y., Yamashita R., Nakai K., Yada T., Nakamura Y., Ohara O., Isogai T., Sugano S. Complete sequencing and characterization of 21,243 full-length human cDNAs. Nat. Genet. 2004, 36:40-45.
42. Rieder E., Bunch T., Brown F., Mason P.W. Genetically engineered foot-and-mouth disease viruses with poly(C) tracts of two nucleotides are virulent in mice. J. Virol. 1993, 67:5139-5145.
43. Rieder E., Henry T., Duque H., Baxt B. Analysis of a foot-and-mouth disease virus type A24 isolate containing an SGD receptor recognition site in vitro and its pathogenesis in cattle. J. Virol. 2005, 79:12989-12998.
44. Sakane N., Kwon H.S., Pagans S., Kaehlcke K., Mizusawa Y., Kamada M., Lassen K.G., Chan J., Greene W.C., Schnoelzer M., Ott M. Activation of HIV transcription by the viral Tat protein requires a demethylation step mediated by lysine-specific demethylase 1 (LSD1/KDM1). PLoS Pathog. 2011, 7:e1002184.
45. Schneider J., Shilatifard A. Histone demethylation by hydroxylation: chemistry in action. ACS Chem. Biol. 2006, 1:75-81.
46. Shi Y., Lan F., Matson C., Mulligan P., Whetstine J.R., Cole P.A., Casero R.A. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 2004, 119:941-953.
47. Shiroki K., Isoyama T., Kuge S., Ishii T., Ohmi S., Hata S., Suzuki K., Takasaki Y., Nomoto A. Intracellular redistribution of truncated La protein produced by poliovirus 3Cpro-mediated cleavage. J. Virol. 1999, 73:2193-2200.
48. Smith W.A., Schurter B.T., Wong-Staal F., David M. Arginine methylation of RNA helicase a determines its subcellular localization. J. Biol. Chem. 2004, 279:22795-22798.
49. Suzuki T., Miyata N. Lysine demethylases inhibitors. J. Med. Chem. 2011, 54:8236-8250.
50. Swaney L.M. A continuous bovine kidney cell line for routine assays of foot-and-mouth disease virus. Vet. Microbiol. 1988, 18:1-14.
51. Swigut T., Wysocka J. H3K27 demethylases, at long last. Cell 2007, 131:29-32.
52. Tibrewal N., Liu T., Li H., Birge R.B. Characterization of the biochemical and biophysical properties of the phosphatidylserine receptor (PS-R) gene product. Mol. Cell. Biochem. 2007, 304:119-125.
53. Trewick S.C., McLaughlin P.J., Allshire R.C. Methylation: lost in hydroxylation?. EMBO Rep. 2005, 6:315-320.
54. Tsukada Y., Fang J., Erdjument-Bromage H., Warren M.E., Borchers C.H., Tempst P., Zhang Y. Histone demethylation by a family of JmjC domain-containing proteins. Nature 2006, 439:811-816.
55. Tsukada Y., Zhang Y. Purification of histone demethylases from HeLa cells. Methods 2006, 40:318-326.
56. Webby C.J., Wolf A., Gromak N., Dreger M., Kramer H., Kessler B., Nielsen M.L., Schmitz C., Butler D.S., Yates J.R., Delahunty C.M., Hahn P., Lengeling A., Mann M., Proudfoot N.J., Schofield C.J., Bottger A. Jmjd6 catalyses lysyl-hydroxylation of U2AF65, a protein associated with RNA splicing. Science 2009, 325:90-93.
57. Xiang Y., Zhu Z., Han G., Lin H., Xu L., Chen C.D. JMJD3 is a histone H3K27 demethylase. Cell Res. 2007, 17:850-857.
58. Yamane K., Toumazou C., Tsukada Y., Erdjument-Bromage H., Tempst P., Wong J., Zhang Y. JHDM2A, a JmjC-containing H3K9 demethylase, facilitates transcription activation by androgen receptor. Cell 2006, 125:483-495.
59. Zakharova L., Dadsetan S., Fomina A.F. Endogenous Jmjd6 gene product is expressed at the cell surface and regulates phagocytosis in immature monocyte-like activated THP-1 cells. J. Cell. Physiol. 2009, 221:84-91.