Structural basis for lack of ADP-ribosyltransferase activity in poly(ADP-ribose) polymerase-13/zinc finger antiviral protein

Journal of Biological Chemistry

Volumn 290, Issue 12, 2015, Pages 7336-7344

  Karlberg, Tobias ^a   Klepsch, Mirjam ^a   Thorsell, Ann Gerd ^a   Andersson, C David ^b   Linusson, Anna ^b   Schüler, Herwig ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYST ACTIVITY; CHAINS; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; MAMMALS; MOLECULAR DYNAMICS; PROTEINS; RNA;

ADP-RIBOSYLTRANSFERASE; ANTIVIRAL PROTEIN; BIOCHEMICAL ANALYSIS; CONSENSUS SEQUENCE; MOLECULAR DYNAMICS SIMULATIONS; POLY(ADP-RIBOSE) POLYMERASE; STRUCTURAL REQUIREMENTS; THREE-DIMENSIONAL ALIGNMENTS;

X RAY CRYSTALLOGRAPHY;

NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 12; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 13; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 15; UNCLASSIFIED DRUG; VIRUS PROTEIN; ZINC FINGER PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE;

ARTICLE; BINDING SITE; CHEMICAL ANALYSIS; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME STRUCTURE; HUMAN; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN DOMAIN; SIMULATION; SITE DIRECTED MUTAGENESIS; X RAY CRYSTALLOGRAPHY; AMINO ACID SEQUENCE; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR GENETICS; SEQUENCE HOMOLOGY;

MAMMALIA;

ADP RIBOSE TRANSFERASES; AMINO ACID SEQUENCE; CRYSTALLOGRAPHY, X-RAY; HUMANS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NAD; POLY(ADP-RIBOSE) POLYMERASES; SEQUENCE HOMOLOGY, AMINO ACID; ZINC FINGERS;

EID: 84925310791     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.630160     Document Type: Article

References (53)

1. Gao, G., Guo, X., and Goff, S. P. (2002) Inhibition of retroviral RNA production by ZAP, a CCCH-type zinc finger protein. Science 297, 1703-1706
2. Zhu, Y., and Gao, G. (2008) ZAP-mediated mRNA degradation. RNA Biol. 5, 65-67
3. Bick, M. J., Carroll, J. W., Gao, G., Goff, S. P., Rice, C. M., and MacDonald, M. R. (2003) Expression of the zinc-finger antiviral protein inhibits alpha-virus replication. J. Virol. 77, 11555-11562
4. Müller, S., Möller, P., Bick, M. J., Wurr, S., Becker, S., Günther, S., and Kümmerer, B. M. (2007) Inhibition of filovirus replication by the zinc finger antiviral protein. J. Virol. 81, 2391-2400
5. Guo, X., Carroll, J. W., Macdonald, M. R., Goff, S. P., and Gao, G. (2004) The zinc finger antiviral protein directly binds to specific viral mRNAs through the CCCH zinc finger motifs. J. Virol. 78, 12781-12787
6. Chen, S., Xu, Y., Zhang, K., Wang, X., Sun, J., Gao, G., and Liu, Y. (2012) Structure of N-terminal domain of ZAP indicates how a zinc-finger protein recognizes complex RNA. Nat. Struct. Mol. Biol. 19, 430-435
7. Guo, X., Ma, J., Sun, J., and Gao, G. (2007) The zinc-finger antiviral protein recruits the RNA processing exosome to degrade the target mRNA. Proc. Natl. Acad. Sci. U.S.A. 104, 151-156
8. Chen, G., Guo, X., Lv, F., Xu, Y., and Gao, G. (2008) p72 DEAD box RNA helicase is required for optimal function of the zinc-finger antiviral protein. Proc. Natl. Acad. Sci. U.S.A. 105, 4352-4357
9. Hayakawa, S., Shiratori, S., Yamato, H., Kameyama, T., Kitatsuji, C., Kashigi, F., Goto, S., Kameoka, S., Fujikura, D., Yamada, T., Mizutani, T., Kazumata, M., Sato, M., Tanaka, J., Asaka, M., Ohba, Y., Miyazaki, T., Imamura, M., and Takaoka, A. (2011) ZAPS is a potent stimulator of signaling mediated by the RNA helicase RIG-I during antiviral responses. Nat. Immunol. 12, 37-44
10. Kerns, J. A., Emerman, M., and Malik, H. S. (2008) Positive selection and increased antiviral activity associated with the PARP-containing isoform of human zinc-finger antiviral protein. PLoS Genet. 4, e21
11. Cagliani, R., Guerini, F. R., Fumagalli, M., Riva, S., Agliardi, C., Galimberti, D., Pozzoli, U., Goris, A., Dubois, B., Fenoglio, C., Forni, D., Sanna, S., Zara, I., Pitzalis, M., Zoledziewska, M., Cucca, F., Marini, F., Comi, G. P., Scarpini, E., Bresolin, N., Clerici, M., and Sironi, M. (2012) A trans-specific polymorphism in ZC3HAV1 is maintained by long-standing balancing selection and may confer susceptibility to multiple sclerosis. Mol. Biol. Evol. 29, 1599-1613
12. Jeong, M. S., Kim, E. J., and Jang, S. B. (2010) Expression and RNA-binding of human zinc-finger antiviral protein. Biochem. Biophys. Res. Commun. 396, 696-702
13. Todorova, T., Bock, F. J., and Chang, P. (2014) PARP13 regulates cellular mRNA post-transcriptionally and functions as a pro-apoptotic factor by destabilizing TRAILR4 transcript. Nat. Commun. 5, 5362
14. Leung, A. K., Vyas, S., Rood, J. E., Bhutkar, A., Sharp, P. A., and Chang, P. (2011) Poly(ADP-ribose) regulates stress responses and microRNA activity in the cytoplasm. Mol. Cell 42, 489-499
15. Hottiger, M. O., Hassa, P. O., Lüscher, B., Schüler, H., and Koch-Nolte, F. (2010) Toward a unified nomenclature for mammalian ADP-ribosyltransferases. Trends Biochem. Sci. 35, 208-219
16. Marsischky, G. T., Wilson, B. A., and Collier, R. J. (1995) Role of glutamic acid 988 of human poly-ADP-ribose polymerase in polymer formation: evidence for active-site similarities to the ADP-ribosylating toxins. J. Biol. Chem. 270, 3247-3254
17. Ruf, A., Mennissier de Murcia, J., de Murcia, G., and Schulz, G. E. (1996) Structure of the catalytic fragment of poly(AD-ribose) polymerase from chicken. Proc. Natl. Acad. Sci. U.S.A. 93, 7481-7485
18. Gibson, B. A., and Kraus, W. L. (2012) New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. Nat. Rev. Mol. Cell Biol. 13, 411-424
19. Vyas, S., Matic, I., Uchima, L., Rood, J., Zaja, R., Hay, R. T., Ahel, I., and Chang, P. (2014) Family-wide analysis of poly(ADP-ribose) polymerase activity. Nat. Commun. 5, 4426
20. Otto, H., Reche, P. A., Bazan, F., Dittmar, K., Haag, F., and Koch-Nolte, F. (2005) In silico characterization of the family of PARP-like poly(ADP-ribosyl) transferases (pARTs). BMC Genomics 6, 139
21. Kleine, H., Poreba, E., Lesniewicz, K., Hassa, P. O., Hottiger, M. O., Litchfield, D. W., Shilton, B. H., and Lüscher, B. (2008) Substrate-assisted catalysis by PARP10 limits its activity to mono-ADP-Ribosylation. Mol. Cell 32, 57-69
22. Aguiar, R. C., Yakushijin, Y., Kharbanda, S., Salgia, R., Fletcher, J. A., and Shipp, M. A. (2000) BAL is a novel risk-related gene in diffuse large B-cell lymphomas that enhances cellular migration. Blood 96, 4328-4334
23. Aguiar, R. C., Takeyama, K., He, C., Kreinbrink, K., and Shipp, M. A. (2005) B-aggressive lymphoma family proteins have unique domains that modulate transcription and exhibit poly(ADP-ribose) polymerase activity. J. Biol. Chem. 280, 33756-33765
24. Leung, A., Todorova, T., Ando, Y., and Chang, P. (2012) Poly(ADP-ribose) regulates post-transcriptional gene regulation in the cytoplasm. RNA Biol. 9, 542-548
25. Gileadi, O., Burgess-Brown, N. A., Colebrook, S. M., Berridge, G., Savitsky, P., Smee, C. E., Loppnau, P., Johansson, C., Salah, E., and Pantic, N. H. (2008) High throughput production of recombinant human proteins for crystallography. Methods Mol. Biol. 426, 221-246
26. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
27. Adams, P. D., Grosse-Kunstleve, R. W., Hung, L. W., Ioerger, T. R., Mc-Coy, A. J., Moriarty, N. W., Read, R. J., Sacchettini, J. C., Sauter, N. K., and Terwilliger, T. C. (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 58, 1948-1954
28. Murshudov, G. N., Skubák, P., Lebedev, A. A., Pannu, N. S., Steiner, R. A., Nicholls, R. A., Winn, M. D., Long, F., and Vagin, A. A. (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67, 355-367
29. Terwilliger, T. C., and Berendzen, J. (1999) Automated MAD and MIR structure solution. Acta Crystallogr. D Biol. Crystallogr. 55, 849-861
30. Bricogne, G., Blanc, E., Brandl, M., Flensburg, C., Keller, P., Paciorek, W., Roversi, P., Smart, O. S., Vonrhein, C., and Womack, T. O. (2011) BUSTER, version 2.11.1. Ed., Global Phasing Ltd., Cambridge, UK
31. Kabsch, W. (2010) XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132
32. Vagin, A., and Teplyakov, A. (2000) An approach to multi-copy search in molecular replacement. Acta Crystallogr. D Biol. Crystallogr. 56, 1622-1624
33. Langer, G., Cohen, S. X., Lamzin, V. S., and Perrakis, A. (2008) Automated macromolecular model building for x-ray crystallography using ARP/wARP version 7. Nat. Protoc. 3, 1171-1179
34. Karlberg, T., Thorsell, A. G., Kallas, Å., and Schüler, H. (2012) Crystal structure of human ADP-ribose transferase ARTD15/PARP16 reveals a novel putative regulatory domain. J. Biol. Chem. 287, 24077-24081
35. Halgren, T. A. (1999) MMFF VI. MMFF94s option for energy minimization studies. J. Comput. Chem. 20, 720-729
36. Chemical Computing Group Inc. (2011) Molecular Operating Environment (MOE), 2011.10, Montreal, Quebec, Canada
37. Case, D. A., Darden, T. A., Cheatham III, T. E., Simmerling, C. L., W. J., Duke, R. E., Luo, R. C., Walker, R. C., Zhang, W., Merz, K. M., Roberts, B., Hayik, S., Roitberg, A., Seabra, G., Swails, J., Goetz, A. W., Kolossváry, I., Wong, K. F., Paesani, F., Vanicek, J., Wolf, R. M., Liu, J., Wu, X., Brozell, S. R., Steinbrecher, T., Gohlke, H., Cai, Q., Ye, X., Wang, J., Hsieh, M.-J., Cui, G., Roe, D. R., Mathews, D. H., Seetin, M. G., Salomon-Ferrer, R., Sagui, C., Babin, V., Luchko, T., Gusarov, S., Kovalenko, A., and Kollman, P. A. (2012) AMBER 12, University of California, San Francisco
38. Darden, T., York, D., and Pedersen, L. (1993) Particle mesh Ewald: an N. Log(N) method for Ewald sums in large systems. J. Chem. Phys. 98, 10089-10092
39. Hornak, V., Abel, R., Okur, A., Strockbine, B., Roitberg, A., and Simmerling, C. (2006) Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins 65, 712-725
40. Pastor, R. W., Brooks, B. R., and Szabo, A. (1988) An analysis of the accuracy of Langevin and molecular dynamics algorithms. Mol. Phys. 65, 1409-1419
41. Laurie, A. T., and Jackson, R. M. (2005) Q-SiteFinder: an energy-based method for the prediction of protein-ligand binding sites. Bioinformatics 21, 1908-1916
42. Blanke, S. R., Huang, K., Wilson, B. A., Papini, E., Covacci, A., and Collier, R. J. (1994) Active-site mutations of the diphtheria toxin catalytic domain: role of histidine-21 in nicotinamide adenine dinucleotide binding and ADP-ribosylation of elongation factor 2. Biochemistry 33, 5155-5161
43. 3 domain of human poly(ADP-ribose) polymerase-1 (PARP-1) functions in both DNA-dependent poly(ADP-ribose) synthesis activity and chromatin compaction. J. Biol. Chem. 285, 18877-18887
44. Ruf, A., Rolli, V., de Murcia, G., and Schulz, G. E. (1998) The mechanism of the elongation and branching reaction of poly(ADP-ribose) polymerase as derived from crystal structures and mutagenesis. J. Mol. Biol. 278, 57-65
45. Karlberg, T., Hammarström, M., Schütz, P., Svensson, L., and Schüler, H. (2010) Crystal structure of the catalytic domain of human PARP2 in complex with PARP inhibitor ABT-888. Biochemistry 49, 1056-1058
46. Lehtiö, L., Jemth, A. S., Collins, R., Loseva, O., Johansson, A., Markova, N., Hammarström, M., Flores, A., Holmberg-Schiavone, L., Weigelt, J., Helleday, T., Schüler, H., and Karlberg, T. (2009) Structural basis for inhibitor specificity in human poly(ADP-ribose) polymerase-3. J. Med. Chem. 52, 3108-3111
47. Wahlberg, E., Karlberg, T., Kouznetsova, E., Markova, N., Macchiarulo, A., Thorsell, A. G., Pol, E., Frostell, Å., Ekblad, T., Öncü, D., Kull, B., Robertson, G. M., Pellicciari, R., Schüler, H., and Weigelt, J. (2012) Family-wide chemical profiling and structural analysis of PARP and tankyrase inhibitors. Nat. Biotechnol. 30, 283-288
48. Andersson, C. D., Karlberg, T., Ekblad, T., Lindgren, A. E., Thorsell, A. G., Spjut, S., Uciechowska, U., Niemiec, M. S., Wittung-Stafshede, P., Weigelt, J., Elofsson, M., Schüler, H., and Linusson, A. (2012) Discovery of ligands for ADP-ribosyltransferases via docking-based virtual screening. J. Med. Chem. 55, 7706-7718
49. Bell, C. E., and Eisenberg, D. (1996) Crystal structure of diphtheria toxin bound to nicotinamide adenine dinucleotide. Biochemistry 35, 1137-1149
50. Karlberg, T., Markova, N., Johansson, I., Hammarström, M., Schütz, P., Weigelt, J., and Schüler, H. (2010) Structural basis for the interaction between tankyrase-2 and a potent Wnt-signaling inhibitor. J. Med. Chem. 53, 5352-5355
51. Gouet, P., Courcelle, E., Stuart, D. I., and Metoz, F. (1999) ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15, 305-308
52. Engh, R. A., and Huber, R. (1991) Accurate bond and angle parameters for x-ray protein-structure refinement. Acta Crystallogr. A 47, 392-400
53. Chen, V. B., Arendall, W. B., 3rd, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D. Biol. Crystallogr 66, 12-21