Structural basis for 2'-5'-oligoadenylate binding and enzyme activity of a viral RNase L antagonist

Journal of Virology

Volumn 89, Issue 13, 2015, Pages 6633-6645

  Ogden, Kristen M ^a   Hu, Liya ^b   Jha, Babal K ^c   Sankaran, Banumathi ^d   Weiss, Susan R ^e   Silverman, Robert H ^c   Patton, John T ^a   Venkataram Prasad, B V ^b  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c LERNER RESEARCH INSTITUTE   (United States)

^d LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2',5' OLIGOADENYLIC ACID; 2H PHOSPHOESTERASE; A KINASE ANCHORING PROTEIN 7; CARRIER PROTEINS AND BINDING PROTEINS; PHOSPHATASE; PROTEIN VP3; UNCLASSIFIED DRUG; VIRUS PROTEIN; 2',5'-OLIGOADENYLATE; 2'-PHOSPHODIESTERASE; ADENINE NUCLEOTIDE; CAPSID PROTEIN; EXORIBONUCLEASE; OLIGORIBONUCLEOTIDE; PROTEIN BINDING; VP3 PROTEIN, ROTAVIRUS;

ALPHA HELIX; ARTICLE; BETA SHEET; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME STRUCTURE; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF; ROTAVIRUS A; ROTAVIRUS B; CHEMISTRY; ENZYMOLOGY; METABOLISM; PROTEIN CONFORMATION; ROTAVIRUS; X RAY CRYSTALLOGRAPHY;

ROTAVIRUS; ROTAVIRUS A; ROTAVIRUS B;

ADENINE NUCLEOTIDES; CAPSID PROTEINS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; EXORIBONUCLEASES; OLIGORIBONUCLEOTIDES; PROTEIN BINDING; PROTEIN CONFORMATION; ROTAVIRUS;

EID: 84930887195     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00701-15     Document Type: Article

References (46)

1. Goubau D, Deddouche S, Reis e Sousa C. 2013. Cytosolic sensing of viruses. Immunity 38:855-869. http://dx.doi.org/10.1016/j.immuni.2013.05.007.
2. Li XL, Ezelle HJ, Hsi TY, Hassel BA. 2011. A central role for RNA in the induction and biological activities of type 1 interferons. Wiley Interdiscip Rev RNA 2:58-78. http://dx.doi.org/10.1002/wrna.32.
3. Chakrabarti A, Jha BK, Silverman RH. 2011. New insights into the role of RNase L in innate immunity. J Interferon Cytokine Res 31:49-57. http://dx.doi.org/10.1089/jir.2010.0120.
4. Silverman RH. 2007. Viral encounters with 2'5'-oligoadenylate synthetase and RNase L during the interferon antiviral response. J Virol 81: 12720-12729. http://dx.doi.org/10.1128/JVI.01471-07.
5. Silverman RH, Weiss SR. 2014. Viral phosphodiesterases that antagonize double-stranded RNA signaling to RNase L by degrading 2-5A. J Interferon Cytokine Res 34:455-463. http://dx.doi.org/10.1089/jir.2014.0007.
6. Zhang R, Jha BK, Ogden KM, Dong B, Zhao L, Elliott R, Patton JT, Silverman RH, Weiss SR. 2013. Homologous 2'5'-phosphodiesterases from disparate RNA viruses antagonize antiviral innate immunity. Proc Natl Acad Sci U S A 110:13114-13119. http://dx.doi.org/10.1073/pnas.1306917110.
7. Zhao L, Jha BK, Wu A, Elliott R, Ziebuhr J, Gorbalenya AE, Silverman RH, Weiss SR. 2012. Antagonism of the interferon-induced OAS-RNase L pathway by murine coronavirus ns2 protein is required for virus replication and liver pathology. Cell Host Microbe 11:607-616. http://dx.doi .org/10.1016/j.chom.2012.04.011.
8. Desselberger U. 2014. Rotaviruses. Virus Res 190:75-96. http://dx.doi .org/10.1016/j.virusres.2014.06.016.
9. Anonymous. 2013. Rotavirus vaccines WHO position paper: January 2013-recommendations. Vaccine 31:6170-6171. http://dx.doi.org/10.1016/j.vaccine.2013.05.037.
10. Matthijnssens J, Otto PH, Ciarlet M, Desselberger U, Van Ranst M, Johne R. 2012. VP6-sequence-based cutoff values as a criterion for rotavirus species demarcation. Arch Virol 157:1177-1182. http://dx.doi.org/10.1007/s00705-012-1273-3.
11. Feng N, Yasukawa LL, Sen A, Greenberg HB. 2013. Permissive replication of homologous murine rotavirus in the mouse intestine is primarily regulated by VP4 and NSP1. J Virol 87:8307-8316. http://dx.doi.org/10.1128/JVI.00619-13.
12. Hoshino Y, Saif LJ, Kang SY, Sereno MM, Chen WK, Kapikian AZ. 1995. Identification of group A rotavirus genes associated with virulence of a porcine rotavirus and host range restriction of a human rotavirus in the gnotobiotic piglet model. Virology 209:274-280.
13. Wang W, Donnelly B, Bondoc A, Mohanty SK, McNeal M, Ward R, Sestak K, Zheng S, Tiao G. 2011. The rhesus rotavirus gene encoding VP4 is a major determinant in the pathogenesis of biliary atresia in newborn mice. J Virol 85:9069-9077. http://dx.doi.org/10.1128/JVI.02436-10.
14. Ogden KM, Snyder MJ, Dennis AF, Patton JT. 2014. Predicted structure and domain organization of rotavirus capping enzyme and innate immune antagonist VP3. J Virol 88:9072-9085. http://dx.doi.org/10.1128/JVI.00923-14.
15. Mazumder R, Iyer LM, Vasudevan S, Aravind L. 2002. Detection of novel members, structure-function analysis and evolutionary classification of the 2H phosphoesterase superfamily. Nucleic Acids Res 30:5229-5243. http://dx.doi.org/10.1093/nar/gkf645.
16. Hofmann A, Tarasov S, Grella M, Ruvinov S, Nasr F, Filipowicz W, Wlodawer A. 2002. Biophysical characterization of cyclic nucleotide phosphodiesterases. Biochem Biophys Res Commun 291:875-883. http://dx.doi.org/10.1006/bbrc.2002.6527.
17. Hofmann A, Zdanov A, Genschik P, Ruvinov S, Filipowicz W, Wlodawer A. 2000. Structure and mechanism of activity of the cyclic phosphodiesterase of Appr >p, a product of the tRNA splicing reaction. EMBO J 19:6207-6217. http://dx.doi.org/10.1093/emboj/19.22.6207.
18. Gusho E, Zhang R, Jha BK, Thornbrough JM, Dong B, Gaughan C, Elliott R, Weiss SR, Silverman RH. 2014. Murine AKAP7 has a 2'5'- phosphodiesterase domain that can complement an inactive murine coronavirus ns2 gene. mBio 5(4):e01312-14. http://dx.doi.org/10.1128/mBio .01312-14.
19. Zhao L, Birdwell LD, Wu A, Elliott R, Rose KM, Phillips JM, Li Y, Grinspan J, Silverman RH, Weiss SR. 2013. Cell-type-specific activation of the oligoadenylate synthetase-RNase L pathway by a murine coronavirus. J Virol 87:8408-8418. http://dx.doi.org/10.1128/JVI.00769-13.
20. Gold MG, Smith FD, Scott JD, Barford D. 2008. AKAP18 contains a phosphoesterase domain that binds AMP. J Mol Biol 375:1329-1343. http://dx.doi.org/10.1016/j.jmb.2007.11.037.
21. Huang H, Zeqiraj E, Dong B, Jha BK, Duffy NM, Orlicky S, Thevakumaran N, Talukdar M, Pillon MC, Ceccarelli DF, Wan LC, Juang YC, Mao DY, Gaughan C, Brinton MA, Perelygin AA, Kourinov I, Guarne A, Silverman RH, Sicheri F. 2014. Dimeric structure of pseudokinase RNase L bound to 2-5A reveals a basis for interferon-induced antiviral activity. Mol Cell 53:221-234. http://dx.doi.org/10.1016/j.molcel.2013.12.025.
22. Jha BK, Polyakova I, Kessler P, Dong B, Dickerman B, Sen GC, Silverman RH. 2011. Inhibition of RNase L and RNA-dependent protein kinase (PKR) by sunitinib impairs antiviral innate immunity. J Biol Chem 286:26319-26326. http://dx.doi.org/10.1074/jbc.M111.253443.
23. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AG, McCoy A, McNicholas SJ, Murshudov GN, Pannu NS, Potterton EA, Powell HR, Read RJ, Vagin A, Wilson KS. 2011. Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr 67:235-242. http://dx.doi.org/10.1107/S0907444910045749.
24. Evans P. 2006. Scaling and assessment of data quality. Acta Crystallogr D Biol Crystallogr 62:72-82. http://dx.doi.org/10.1107/S0907444905036693.
25. Sheldrick GM. 2010. Experimental phasing with SHELXC/D/E: combining chain tracing with density modification. Acta Crystallogr D Biol Crystallogr 66:479-485. http://dx.doi.org/10.1107/S0907444909038360.
26. Morris RJ, Perrakis A, Lamzin VS. 2003. ARP/wARP and automatic interpretation of protein electron density maps. Methods Enzymol 374: 229-244. http://dx.doi.org/10.1016/S0076-6879(03)74011-7.
27. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66:486-501. http://dx.doi.org/10.1107/S0907444910007493.
28. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH. 2010. PHENIX: a comprehensive Pythonbased system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66:213-221. http://dx.doi.org/10.1107/S0907444909052925.
29. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. 2007. Phaser crystallographic software. J Appl Crystallogr 40: 658-674. http://dx.doi.org/10.1107/S0021889807021206.
30. Wallace AC, Laskowski RA, Thornton JM. 1995. LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng 8:127-134. http://dx.doi.org/10.1093/protein/8.2.127.
31. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. 2004. UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25:1605-1612. http://dx.doi.org/10.1002/jcc.20084.
32. Thakur CS, Xu Z, Wang Z, Novince Z, Silverman RH. 2005. A convenient and sensitive fluorescence resonance energy transfer assay for RNase L and 2'5' oligoadenylates. Methods Mol Med 116:103-113. http://dx.doi .org/10.1385/1-59259-939-7:103.
33. Sali A, Blundell TL. 1993. Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234:779-815.
34. Brandmann T, Jinek M. 10 March 2015. Crystal structure of the C-terminal 2'5'-phosphodiesterase domain of group A rotavirus protein VP3. Proteins http://dx.doi.org/10.1002/prot.24794.
35. Phan TG, Vo NP, Boros A, Pankovics P, Reuter G, Li OT, Wang C, Deng X, Poon LL, Delwart E. 2013. The viruses of wild pigeon droppings. PLoS One 8:e72787. http://dx.doi.org/10.1371/journal.pone.0072787.
36. Johnston MI, Hearl WG. 1987. Purification and characterization of a 2'-phosphodiesterase from bovine spleen. J Biol Chem 262:8377-8382.
37. Kubota K, Nakahara K, Ohtsuka T, Yoshida S, Kawaguchi J, Fujita Y, Ozeki Y, Hara A, Yoshimura C, Furukawa H, Haruyama H, Ichikawa K, Yamashita M, Matsuoka T, Iijima Y. 2004. Identification of 2'- phosphodiesterase, which plays a role in the 2-5A system regulated by interferon. J Biol Chem 279:37832-37841. http://dx.doi.org/10.1074/jbc .M400089200.
38. Schmidt A, Chernajovsky Y, Shulman L, Federman P, Berissi H, Revel M. 1979. An interferon-induced phosphodiesterase degrading (2'-5') oligoisoadenylate and the C-C-A terminus of tRNA. Proc Natl Acad Sci U S A 76:4788-4792.
39. 32P-labelled derivatives of ppp(A2'p)nA. Eur J Biochem 115:79-85.
40. Myllykoski M, Raasakka A, Lehtimaki M, Han H, Kursula I, Kursula P. 2013. Crystallographic analysis of the reaction cycle of 2'3'-cyclic nucleotide 3'-phosphodiesterase, a unique member of the 2H phosphoesterase family. J Mol Biol 425:4307-4322. http://dx.doi.org/10.1016/j.jmb.2013.06.012.
41. Remus BS, Jacewicz A, Shuman S. 2014. Structure and mechanism of E. coli RNA 2'3'-cyclic phosphodiesterase. RNA 20:1697-1705. http://dx .doi.org/10.1261/rna.046797.114.
42. Attoui H, Becnel J, Belaganahalli S, Bergoin M, Brussaard CP, Chappell JD, Ciarlet M, del Vas M, Dermody TS, Dormitzer PR, Duncan R, Fang Q, Graham R, Guglielmi KM, Harding RM, Hillman B, Makkay A, Marzachì C, Matthijnssens J, Mertens PPC, Milne RG, Mohd Jaafar F, Mori H, Noordeloos AA, Omura T, Patton JT, Rao S, Maan M, Stoltz D, Suzuki N, Upadhyaya NM, Wei C, Zhou H. 2012. Family Reoviridae, p 541-637. In King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (ed). 2011. Virus taxonomy: classification and nomenclature of viruses. Ninth report of the International Committee on Taxonomy of Viruses. Academic Press, San Diego, CA.
43. Langland JO, Pettiford S, Jiang B, Jacobs BL. 1994. Products of the porcine group C rotavirus NSP3 gene bind specifically to double-stranded RNA and inhibit activation of the interferon-induced protein kinase PKR. J Virol 68:3821-3829.
44. Morelli M, Ogden KM, Patton JT. 25 February 2015. Silencing the alarms: innate immune antagonism by rotavirus NSP1 and VP3. Virology http://dx.doi.org/10.1016/j.virol.2015.01.006.
45. Di Tommaso P, Moretti S, Xenarios I, Orobitg M, Montanyola A, Chang JM, Taly JF, Notredame C. 2011. T-Coffee: a web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension. Nucleic Acids Res 39:W13-W17. http://dx.doi.org/10.1093/nar/gkr245.
46. Kemena C, Notredame C. 2009. Upcoming challenges for multiple sequence alignment methods in the high-throughput era. Bioinformatics 25:2455-2465. http://dx.doi.org/10.1093/bioinformatics/btp452.