Dynamics of Human and Viral RNA Methylation during Zika Virus Infection

Cell Host and Microbe

Volumn 20, Issue 5, 2016, Pages 666-673

  Lichinchi, Gianluigi ^a,b   Zhao, Boxuan Simen ^c,d   Wu, Yinga ^a,b   Lu, Zhike ^c,d   Qin, Yue ^a   He, Chuan ^c,d   Rana, Tariq M ^a,b,e  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b BURNHAM INSTITUTE   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

^d UNIVERSITY OF CHICAGO   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

2 O methylation; m6A methylation; methyltransferases; Zika virus

Indexed keywords

HISTONE DEMETHYLASE; MESSENGER RNA; METHYLTRANSFERASE; VIRUS RNA; ALKBH5 PROTEIN, HUMAN; ALKYLATED DNA REPAIR PROTEIN ALKB HOMOLOG 5; ALPHA KETOGLUTARATE DEPENDENT DIOXYGENASE FTO; FTO PROTEIN, HUMAN; METTL14 PROTEIN, HUMAN; METTL3 PROTEIN, HUMAN;

ARTICLE; CELL FUNCTION; CONTROLLED STUDY; DNA MODIFICATION; ENZYME ACTIVITY; GENE SILENCING; GENE TARGETING; HOST CELL; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN MOTIF; RNA BINDING; RNA METHYLATION; RNA STRUCTURE; VIRUS CELL INTERACTION; VIRUS GENE; VIRUS REPLICATION; ZIKA FEVER; CELL LINE; HOST PATHOGEN INTERACTION; METABOLISM; METHYLATION; PHYSIOLOGY; RNA PROCESSING; ZIKA VIRUS;

ALKB HOMOLOG 5, RNA DEMETHYLASE; ALPHA-KETOGLUTARATE-DEPENDENT DIOXYGENASE FTO; CELL LINE; HOST-PATHOGEN INTERACTIONS; HUMANS; METHYLATION; METHYLTRANSFERASES; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, VIRAL; VIRUS REPLICATION; ZIKA VIRUS;

EID: 84994777582     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2016.10.002     Document Type: Article

References (49)

1. Batista, P.J., Molinie, B., Wang, J., Qu, K., Zhang, J., Li, L., Bouley, D.M., Lujan, E., Haddad, B., Daneshvar, K., et al. m(6)A RNA modification controls cell fate transition in mammalian embryonic stem cells. Cell Stem Cell 15 (2014), 707–719.
2. Bokar, J.A., Shambaugh, M.E., Polayes, D., Matera, A.G., Rottman, F.M., Purification and cDNA cloning of the AdoMet-binding subunit of the human mRNA (N6-adenosine)-methyltransferase. RNA 3 (1997), 1233–1247.
3. Brasil, P., Pereira, J.P. Jr., Raja Gabaglia, C., Damasceno, L., Wakimoto, M., Ribeiro Nogueira, R.M., Carvalho de Sequeira, P., Machado Siqueira, A., Abreu de Carvalho, L.M., Cotrim da Cunha, D., et al. Zika virus infection in pregnant women in Rio de Janeiro—preliminary report. N. Engl. J. Med., 2016, 10.1056/NEJMoa1602412.
4. Broutet, N., Krauer, F., Riesen, M., Khalakdina, A., Almiron, M., Aldighieri, S., Espinal, M., Low, N., Dye, C., Zika virus as a cause of neurologic disorders. N. Engl. J. Med. 374 (2016), 1506–1509.
5. Cugola, F.R., Fernandes, I.R., Russo, F.B., Freitas, B.C., Dias, J.L.M., Guimarães, K.P., Benazzato, C., Almeida, N., Pignatari, G.C., Romero, S., et al. The Brazilian Zika virus strain causes birth defects in experimental models. Nature 534 (2016), 267–271, 10.1038/nature18296.
6. Daffis, S., Szretter, K.J., Schriewer, J., Li, J., Youn, S., Errett, J., Lin, T.Y., Schneller, S., Zust, R., Dong, H., et al. 2′-O methylation of the viral mRNA cap evades host restriction by IFIT family members. Nature 468 (2010), 452–456.
7. Dang, J., Tiwari, S.K., Lichinchi, G., Qin, Y., Patil, V.S., Eroshkin, A.M., Rana, T.M., Zika virus depletes neural progenitors in human cerebral organoids through activation of the innate immune receptor TLR3. Cell Stem Cell 19 (2016), 258–265.
8. Dejnirattisai, W., Supasa, P., Wongwiwat, W., Rouvinski, A., Barba-Spaeth, G., Duangchinda, T., Sakuntabhai, A., Cao-Lormeau, V.M., Malasit, P., Rey, F.A., et al. Dengue virus sero-cross-reactivity drives antibody-dependent enhancement of infection with zika virus. Nat. Immunol. 17 (2016), 1102–1108.
9. Dominissini, D., Moshitch-Moshkovitz, S., Schwartz, S., Salmon-Divon, M., Ungar, L., Osenberg, S., Cesarkas, K., Jacob-Hirsch, J., Amariglio, N., Kupiec, M., et al. Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq. Nature 485 (2012), 201–206.
10. Dong, H., Chang, D.C., Hua, M.H., Lim, S.P., Chionh, Y.H., Hia, F., Lee, Y.H., Kukkaro, P., Lok, S.M., Dedon, P.C., Shi, P.Y., 2′-O methylation of internal adenosine by flavivirus NS5 methyltransferase. PLoS Pathog., 8, 2012, e1002642.
11. Driggers, R.W., Ho, C.Y., Korhonen, E.M., Kuivanen, S., Jääskeläinen, A.J., Smura, T., Rosenberg, A., Hill, D.A., DeBiasi, R.L., Vezina, G., et al. Zika virus infection with prolonged maternal viremia and fetal brain abnormalities. N. Engl. J. Med. 374 (2016), 2142–2151.
12. Fauci, A.S., Morens, D.M., Zika virus in the Americas—yet another arbovirus threat. N. Engl. J. Med. 374 (2016), 601–604.
13. Finkel, D., Groner, Y., Methylations of adenosine residues (m6A) in pre-mRNA are important for formation of late simian virus 40 mRNAs. Virology 131 (1983), 409–425.
14. Frayling, T.M., Timpson, N.J., Weedon, M.N., Zeggini, E., Freathy, R.M., Lindgren, C.M., Perry, J.R., Elliott, K.S., Lango, H., Rayner, N.W., et al. A common variant in the FTO gene is associated with body mass index and predisposes to childhood and adult obesity. Science 316 (2007), 889–894.
15. 6A RNA methylation. Nat. Rev. Genet. 15 (2014), 293–306.
16. Fustin, J.M., Doi, M., Yamaguchi, Y., Hida, H., Nishimura, S., Yoshida, M., Isagawa, T., Morioka, M.S., Kakeya, H., Manabe, I., Okamura, H., RNA-methylation-dependent RNA processing controls the speed of the circadian clock. Cell 155 (2013), 793–806.
17. Geula, S., Moshitch-Moshkovitz, S., Dominissini, D., Mansour, A.A., Kol, N., Salmon-Divon, M., Hershkovitz, V., Peer, E., Mor, N., Manor, Y.S., et al. Stem cells. m6A mRNA methylation facilitates resolution of naïve pluripotency toward differentiation. Science 347 (2015), 1002–1006.
18. Hamel, R., Dejarnac, O., Wichit, S., Ekchariyawat, P., Neyret, A., Luplertlop, N., Perera-Lecoin, M., Surasombatpattana, P., Talignani, L., Thomas, F., et al. Biology of Zika virus infection in human skin cells. J. Virol. 89 (2015), 8880–8896.
19. Heymann, D.L., Hodgson, A., Sall, A.A., Freedman, D.O., Staples, J.E., Althabe, F., Baruah, K., Mahmud, G., Kandun, N., Vasconcelos, P.F., et al. Zika virus and microcephaly: why is this situation a PHEIC?. Lancet 387 (2016), 719–721.
20. Hills, S.L., Russell, K., Hennessey, M., Williams, C., Oster, A.M., Fischer, M., Mead, P., Transmission of Zika virus through sexual contact with travelers to areas of ongoing transmission—continental United States, 2016. MMWR Morb. Mortal. Wkly. Rep. 65 (2016), 215–216.
21. Jia, G., Fu, Y., Zhao, X., Dai, Q., Zheng, G., Yang, Y., Yi, C., Lindahl, T., Pan, T., Yang, Y.G., He, C., N6-methyladenosine in nuclear RNA is a major substrate of the obesity-associated FTO. Nat. Chem. Biol. 7 (2011), 885–887.
22. Kane, S.E., Beemon, K., Precise localization of m6A in Rous sarcoma virus RNA reveals clustering of methylation sites: implications for RNA processing. Mol. Cell. Biol. 5 (1985), 2298–2306.
23. Kennedy, E.M., Bogerd, H.P., Kornepati, A.V., Kang, D., Ghoshal, D., Marshall, J.B., Poling, B.C., Tsai, K., Gokhale, N.S., Horner, S.M., Cullen, B.R., Posttranscriptional m(6)A editing of HIV-1 mRNAs enhances viral gene expression. Cell Host Microbe 19 (2016), 675–685.
24. Kroschewski, H., Lim, S.P., Butcher, R.E., Yap, T.L., Lescar, J., Wright, P.J., Vasudevan, S.G., Davidson, A.D., Mutagenesis of the dengue virus type 2 NS5 methyltransferase domain. J. Biol. Chem. 283 (2008), 19410–19421.
25. Krug, R.M., Morgan, M.A., Shatkin, A.J., Influenza viral mRNA contains internal N6-methyladenosine and 5′-terminal 7-methylguanosine in cap structures. J. Virol. 20 (1976), 45–53.
26. Lazear, H.M., Govero, J., Smith, A.M., Platt, D.J., Fernandez, E., Miner, J.J., Diamond, M.S., A mouse model of Zika virus pathogenesis. Cell Host Microbe 19 (2016), 720–730.
27. Li, C., Xu, D., Ye, Q., Hong, S., Jiang, Y., Liu, X., Zhang, N., Shi, L., Qin, C.F., Xu, Z., Zika virus disrupts neural progenitor development and leads to microcephaly in mice. Cell Stem Cell 19 (2016), 120–126.
28. Lichinchi, G., Gao, S., Saletore, Y., Gonzalez, G.M., Bansal, V., Wang, Y., Mason, C.E., Rana, T.M., Dynamics of the human and viral m(6)A RNA methylomes during HIV-1 infection of T cells. Nat. Microbiol., 1, 2016, 16011.
29. Liu, J., Yue, Y., Han, D., Wang, X., Fu, Y., Zhang, L., Jia, G., Yu, M., Lu, Z., Deng, X., et al. A METTL3-METTL14 complex mediates mammalian nuclear RNA N6-adenosine methylation. Nat. Chem. Biol. 10 (2014), 93–95.
30. Liu, N., Dai, Q., Zheng, G., He, C., Parisien, M., Pan, T., N(6)-methyladenosine-dependent RNA structural switches regulate RNA-protein interactions. Nature 518 (2015), 560–564.
31. Meyer, K.D., Saletore, Y., Zumbo, P., Elemento, O., Mason, C.E., Jaffrey, S.R., Comprehensive analysis of mRNA methylation reveals enrichment in 3′ UTRs and near stop codons. Cell 149 (2012), 1635–1646.
32. Meyer, K.D., Patil, D.P., Zhou, J., Zinoviev, A., Skabkin, M.A., Elemento, O., Pestova, T.V., Qian, S.B., Jaffrey, S.R., 5′ UTR m(6)A promotes cap-independent translation. Cell 163 (2015), 999–1010.
33. Mlakar, J., Korva, M., Tul, N., Popović, M., Poljšak-Prijatelj, M., Mraz, J., Kolenc, M., Resman Rus, K., Vesnaver Vipotnik, T., Fabjan Vodušek, V., et al. Zika virus associated with microcephaly. N. Engl. J. Med. 374 (2016), 951–958.
34. Petersen, L.R., Jamieson, D.J., Powers, A.M., Honein, M.A., Zika virus. N. Engl. J. Med. 374 (2016), 1552–1563.
35. Ping, X.L., Sun, B.F., Wang, L., Xiao, W., Yang, X., Wang, W.J., Adhikari, S., Shi, Y., Lv, Y., Chen, Y.S., et al. Mammalian WTAP is a regulatory subunit of the RNA N6-methyladenosine methyltransferase. Cell Res. 24 (2014), 177–189.
36. Sarno, M., Sacramento, G.A., Khouri, R., do Rosário, M.S., Costa, F., Archanjo, G., Santos, L.A., Nery, N. Jr., Vasilakis, N., Ko, A.I., de Almeida, A.R., Zika virus infection and stillbirths: a case of hydrops fetalis, hydranencephaly and fetal demise. PLoS Negl. Trop. Dis., 10, 2016, e0004517.
37. Schwartz, S., Mumbach, M.R., Jovanovic, M., Wang, T., Maciag, K., Bushkin, G.G., Mertins, P., Ter-Ovanesyan, D., Habib, N., Cacchiarelli, D., et al. Perturbation of m6A writers reveals two distinct classes of mRNA methylation at internal and 5′ sites. Cell Rep. 8 (2014), 284–296.
38. Squires, J.E., Patel, H.R., Nousch, M., Sibbritt, T., Humphreys, D.T., Parker, B.J., Suter, C.M., Preiss, T., Widespread occurrence of 5-methylcytosine in human coding and non-coding RNA. Nucleic Acids Res. 40 (2012), 5023–5033.
39. Tang, H., Hammack, C., Ogden, S.C., Wen, Z., Qian, X., Li, Y., Yao, B., Shin, J., Zhang, F., Lee, E.M., et al. Zika virus infects human cortical neural progenitors and attenuates their growth. Cell Stem Cell 18 (2016), 587–590.
40. Tirumuru, N., Zhao, B.S., Lu, W., Lu, Z., He, C., Wu, L., N(6)-methyladenosine of HIV-1 RNA regulates viral infection and HIV-1 Gag protein expression. eLife, 5, 2016, 10.7554/eLife.15528.
41. Wang, X., Lu, Z., Gomez, A., Hon, G.C., Yue, Y., Han, D., Fu, Y., Parisien, M., Dai, Q., Jia, G., et al. N6-methyladenosine-dependent regulation of messenger RNA stability. Nature 505 (2014), 117–120.
42. Wang, Y., Li, Y., Toth, J.I., Petroski, M.D., Zhang, Z., Zhao, J.C., N6-methyladenosine modification destabilizes developmental regulators in embryonic stem cells. Nat. Cell Biol. 16 (2014), 191–198.
43. Wang, X., Zhao, B.S., Roundtree, I.A., Lu, Z., Han, D., Ma, H., Weng, X., Chen, K., Shi, H., He, C., N(6)-methyladenosine modulates messenger RNA translation efficiency. Cell 161 (2015), 1388–1399.
44. Xu, C., Wang, X., Liu, K., Roundtree, I.A., Tempel, W., Li, Y., Lu, Z., He, C., Min, J., Structural basis for selective binding of m6A RNA by the YTHDC1 YTH domain. Nat. Chem. Biol. 10 (2014), 927–929.
45. Yi, C., Pan, T., Cellular dynamics of RNA modification. Acc. Chem. Res. 44 (2011), 1380–1388.
46. Zhang, B., Dong, H., Zhou, Y., Shi, P.Y., Genetic interactions among the West Nile virus methyltransferase, the RNA-dependent RNA polymerase, and the 5′ stem-loop of genomic RNA. J. Virol. 82 (2008), 7047–7058.
47. Zhao, X., Yang, Y., Sun, B.F., Shi, Y., Yang, X., Xiao, W., Hao, Y.J., Ping, X.L., Chen, Y.S., Wang, W.J., et al. FTO-dependent demethylation of N6-methyladenosine regulates mRNA splicing and is required for adipogenesis. Cell Res. 24 (2014), 1403–1419.
48. Zheng, G., Dahl, J.A., Niu, Y., Fedorcsak, P., Huang, C.M., Li, C.J., Vågbø, C.B., Shi, Y., Wang, W.L., Song, S.H., et al. ALKBH5 is a mammalian RNA demethylase that impacts RNA metabolism and mouse fertility. Mol. Cell 49 (2013), 18–29.
49. Zhou, J., Wan, J., Gao, X., Zhang, X., Jaffrey, S.R., Qian, S.B., Dynamic m(6)A mRNA methylation directs translational control of heat shock response. Nature 526 (2015), 591–594.