The role of phosphodiesterase 12 (PDE12) as a negative regulator of the innate immune response and the discovery of antiviral inhibitors

Journal of Biological Chemistry

Volumn 290, Issue 32, 2015, Pages 19681-19696

  Wood, Edgar R ^a   Bledsoe, Randy ^a   Chai, Jing ^a   Daka, Philias ^a   Deng, Hongfeng ^a   Ding, Yun ^a   Harris Gurley, Sarah ^a   Kryn, Luz Helena ^a   Nartey, Eldridge ^a   Nichols, James ^a   Nolte, Robert T ^b   Prabhu, Ninad ^a   Rise, Cecil ^a   Sheahan, Timothy ^a   Shotwell, J Brad ^a   Smith, Danielle ^a   Tai, Vince ^a   Taylor, J David ^a   Tomberlin, Ginger ^a   Wang, Liping ^b   Wisely, Bruce ^a   You, Shihyun ^a   Xia, Bing ^a   Dickson, Hamilton ^a   more..

^a GLAXOSMITHKLINE   (United States)

^b Department of Chemical Sciences ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CELLS; CRYSTAL STRUCTURE; CYTOLOGY; DATA STORAGE EQUIPMENT; ENZYMES; ESTERS; GENES; NUCLEIC ACIDS; OLIGONUCLEOTIDES; RNA; TRANSCRIPTION;

ANTIVIRAL ACTIVITIES; DNA-ENCODED CHEMICAL LIBRARIES; ENCEPHALOMYOCARDITIS VIRUS; INNATE IMMUNE RESPONSE; NEGATIVE REGULATORS; RESPIRATORY SYNCYTIAL VIRUS; STRUCTURE ACTIVITY RELATIONSHIPS; TRANSCRIPTION ACTIVATORS;

VIRUSES;

ANTIVIRUS AGENT; INTERFERON; PHOSPHODIESTERASE; PHOSPHODIESTERASE 12; PHOSPHODIESTERASE INHIBITOR; POLYINOSINIC POLYCYTIDYLIC ACID; UNCLASSIFIED DRUG; 2',5' OLIGOADENYLATE SYNTHETASE; 2',5'-OLIGOADENYLATE; 2-5A-DEPENDENT RIBONUCLEASE; ADENINE NUCLEOTIDE; ALPHA INTERFERON; EXORIBONUCLEASE; MOLECULAR LIBRARY; OLIGORIBONUCLEOTIDE; PDE12 PROTEIN, HUMAN; RECOMBINANT PROTEIN; RIBONUCLEASE;

ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG POTENCY; DRUG SCREENING; DRUG SELECTIVITY; ENCEPHALOMYOCARDITIS VIRUS; ENZYME INHIBITION; GENE; GENE INACTIVATION; HUMAN; HUMAN CELL; HUMAN RESPIRATORY SYNCYTIAL VIRUS; HUMAN RHINOVIRUS; IMMUNOREGULATION; INNATE IMMUNITY; NONHUMAN; PDE12 GENE; PRIORITY JOURNAL; STRUCTURE ACTIVITY RELATION; VIRUS RESISTANCE; ANTAGONISTS AND INHIBITORS; CHEMICAL STRUCTURE; CHEMISTRY; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETICS; HELA CELL LINE; IMMUNOLOGY; METABOLISM; MOLECULAR LIBRARY; PHARMACOLOGY; RHINOVIRUS; SIGNAL TRANSDUCTION; SYNTHESIS; X RAY CRYSTALLOGRAPHY;

ENCEPHALOMYOCARDITIS VIRUS; HUMAN RHINOVIRUS SP.; RESPIRATORY SYNCYTIAL VIRUS;

2',5'-OLIGOADENYLATE SYNTHETASE; ADENINE NUCLEOTIDES; ANTIVIRAL AGENTS; CRYSTALLOGRAPHY, X-RAY; ENCEPHALOMYOCARDITIS VIRUS; ENDORIBONUCLEASES; ESCHERICHIA COLI; EXORIBONUCLEASES; GENE EXPRESSION REGULATION; GENE KNOCKOUT TECHNIQUES; HELA CELLS; HUMANS; IMMUNITY, INNATE; INTERFERON-ALPHA; MODELS, MOLECULAR; OLIGORIBONUCLEOTIDES; POLY I-C; RECOMBINANT PROTEINS; RESPIRATORY SYNCYTIAL VIRUSES; RHINOVIRUS; SIGNAL TRANSDUCTION; SMALL MOLECULE LIBRARIES; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84939200371     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.653113     Document Type: Article

References (52)

1. Lou, Z., Sun, Y., and Rao, Z. (2014) Current progress in antiviral strategies. Trends Pharmacol. Sci. 35, 86-102
2. Li, X.-L., Ezelle, H. J., Hsi, T. Y., and Hassel, B. A. (2011) A central role for RNA in the induction and biological activities of type 1 interferons. Wiley Interdiscip. Rev. RNA 2, 58-78
3. Sadler, A. J., and Williams, B. R. (2008) Interferon-inducible antiviral effectors. Nat. Rev. Immunol. 8, 559-568
4. Silverman, R. H. (2007) Viral encounters with 2′,5′-oligoadenylate synthetase and RNase L during the interferon antiviral response. J. Virol. 81, 12720-12729
5. Ezelle, H. J., and Hassel, B. A. (2012) Pathologic effects of RNase-L dysregulation in immunity and proliferative control. Front. Biosci. 4, 767-786
6. Williams, B. R., Kerr, I. M., Gilbert, C. S., White, C. N., and Ball, L. A. (1978) Synthesis and breakdown of pppA2′p5′A2′p5′ A and transient inhibition of protein synthesis in extracts from interferon-treated and control cells. Eur. J. Biochem. 92, 455-462
7. Torrence, P. F., Imai, J., and Johnston, M. I. (1983) Assay of 2′,5′-oligoadenylate phosphodiesterase activity in mouse L-cell extracts. Anal. Biochem. 129, 103-110
8. Drappier, M., Sorgeloos, F., and Michiels, T. (2014) The OAS/RNase L pathway and its inhibition by viruses. Virologie 18, 1026-1036
9. Han, J.-Q., Townsend, H. L., Jha, B. K., Paranjape, J. M., Silverman, R. H., and Barton, D. J. (2007) A phylogenetically conserved RNA structure in the poliovirus open reading frame inhibits the antiviral endoribonuclease RNase L. J. Virol. 81, 5561-5572
10. Sorgeloos, F., Jha, B. K., Silverman, R. H., and Michiels, T. (2013) Evasion of antiviral Innate immunity by Theiler's virus L∗protein through direct inhibition of RNase L. PLoS Pathog. 9, e1003474
11. Min, J.-Y., and Krug, R. M. (2006) The primary function of RNA binding by the influenza A virus NS1 protein in infected cells: Inhibiting the 2′-5′oligoA synthetase/RNase L pathway. Proc. Natl. Acad. Sci. U.S.A. 103, 7100-7105
12. Zhang, R., Jha, B. K., Ogden, K. M., Dong, B., Zhao, L., Elliott, R., Patton, J. T., Silverman, R. H., and Weiss, S. R. (2013) Homologous 2′,5′-phosphodiesterases from disparate RNA viruses antagonize antiviral innate immunity. Proc. Natl. Acad. Sci. U.S.A. 110, 13114-13119
13. Zhao, L., Jha, B. K., Wu, A., Elliott, R., Ziebuhr, J., Gorbalenya, A. E., Silverman, R. H., and Weiss, S. R. (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
14. Silverman, R. H., and Weiss, S. R. (2014) Viral phosphodiesterases that antagonize double-stranded RNA signaling to RNase L by degrading 2-5A. J. Interferon Cytokine Res. 34, 455-463
15. Mazumder, R., Iyer, L. M., Vasudevan, S., and Aravind, L. (2002) Detection of novel members, structure-function analysis and evolutionary classification of the 2H phosphoesterase superfamily. Nucleic Acids Res. 30, 5229-5243
16. Gusho, E., Zhang, R., Jha, B. K., Thornbrough, J. M., Dong, B., Gaughan, C., Elliott, R., Weiss, S. R., and Silverman, R. H. (2014) Murine AKAP7 has a 2,5-phosphodiesterase domain that can complement an inactive murine coronavirus ns2 gene. mBio 5, e01312-14
17. 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., and 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
18. Goldstrohm, A. C., and Wickens, M. (2008) Multifunctional deadenylase complexes diversify mRNA control. Nat. Rev. Mol. Cell Biol. 9, 337-344
19. Poulsen, J. B., Andersen, K. R., Kjær, K. H., Vestergaard, A. L., Justesen, J., and Martensen, P. M. (2012) Characterization of human phosphodiesterase 12 and identification of a novel 2′-5′ oligoadenylate nuclease-The ectonucleotide pyrophosphatase/phosphodiesterase 1. Biochimie 94, 1098-1107
20. Gaj, T., Gersbach, C. A., and Barbas, C. F., 3rd (2013) ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol. 31, 397-405
21. Elbahesh, H., Jha, B. K., Silverman, R. H., Scherbik, S. V., and Brinton, M. A. (2011) The Flvr-encoded murine oligoadenylate synthetase 1b (Oas1b) suppresses 2-5A synthesis in intact cells. Virology 409, 262-270
22. Miklos, A. E., Hughes, R. A., and Ellington, A. D. (2012) Design and assembly of large synthetic DNA constructs. Curr. Protoc. Mol. Biol. Chapter 3, Unit 3.23
23. Einhauer, A., and Jungbauer, A. (2001) The FLAG(trademark) peptide, a versatile fusion tag for the purification of recombinant proteins. J. Biochem. Biophys. Methods 49, 455-465
24. Parks, T. D., Leuther, K. K., Howard, E. D., Johnston, S. A., and Dougherty, W. G. (1994) Release of proteins and peptides from fusion proteins using a recombinant plant virus proteinase. Anal. Biochem. 216, 413-417
25. Kay, B. K., Thai, S., and Volgina, V. V. (2009) High-throughput biotinylation of proteins. Methods Mol. Biol. 498, 185-196
26. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326
27. McCoy, A. J. (2007) Solving structures of protein complexes by molecular replacement with Phaser. Acta Crystallogr. D Biol. Crystallogr. 63, 32-41
28. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L.-W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., et al. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
29. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
30. Smart, O. S., Womack, T. O., Flensburg, C., Keller, P., Paciorek, W., Sharff, A., Vonrhein, C., and Bricogne, G. (2012) Exploiting structure similarity in refinement: Automated NCS and target-structure restraints in BUSTER. Acta Crystallogr. D Biol. Crystallogr. 68, 368-380
31. Winn, M. D., Ballard, C. C., Cowtan, K. D., Dodson, E. J., Emsley, P., Evans, P. R., Keegan, R. M., Krissinel, E. B., Leslie, A. G., McCoy, A., McNicholas, S. J., Murshudov, G. N., Pannu, N. S., Potterton, E. A., Powell, H. R., et al. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242
32. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255
33. Deng, H., O'Keefe, H., Davie, C. P., Lind, K. E., Acharya, R. A., Franklin, G. J., Larkin, J., Matico, R., Neeb, M., Thompson, M. M., Lohr, T., Gross, J. W., Centrella, P. A., O'Donovan, G. K., Bedard, K. L., et al. (2012) Discovery of highly potent and selective small molecule ADAMTS-5 inhibitors that inhibit human cartilage degradation via encoded library technology (ELT). J. Med. Chem. 55, 7061-7079
34. Disch, J. S., Evindar, G., Chiu, C. H., Blum, C. A., Dai, H., Jin, L., Schuman, E., Lind, K. E., Belyanskaya, S. L., Deng, J., Coppo, F., Aquilani, L., Graybill, T. L., Cuozzo, J. W., Lavu, S., et al. (2013) Discovery of thieno[3,2-d]-pyrimidine-6-carboxamides as potent inhibitors of SIRT1, SIRT2, and SIRT3. J. Med. Chem. 56, 3666-3679
35. Morin, B., Rabah, N., Boretto-Soler, J., Tolou, H., Alvarez, K., and Canard, B. (2010) High yield synthesis, purification and characterisation of the RNase L activators 5′-triphosphate 2′-5′-oligoadenylates. Antiviral Res. 87, 345-352
36. Copeland, R. A. (2000) Enzymes: A Practical Introduction to Structure, Mechanism and Data Analysis, 2nd Ed., John Wiley and Sons, New York
37. Zhang, W., Zhao, Y., Guo, Y., and Ye, K. (2012) Plant actin-binding protein SCAB1 is dimeric actin cross-linker with atypical pleckstrin homology domain. J. Biol. Chem. 287, 11981-11990
38. Wang, H., Morita, M., Yang, X., Suzuki, T., Yang, W., Wang, J., Ito, K., Wang, Q., Zhao, C., Bartlam, M., Yamamoto, T., and Rao, Z. (2010) Crystal structure of the human CNOT6L nuclease domain reveals strict poly(A) substrate specificity. EMBO J. 29, 2566-2576
39. Clark, M. A., Acharya, R. A., Arico-Muendel, C. C., Belyanskaya, S. L., Benjamin, D. R., Carlson, N. R., Centrella, P. A., Chiu, C. H., Creaser, S. P., Cuozzo, J. W., Davie, C. P., Ding, Y., Franklin, G. J., Franzen, K. D., Gefter, M. L., et al. (2009) Design, synthesis and selection of DNA-encoded small-molecule libraries. Nat. Chem. Biol. 5, 647-654
40. Thalji, R. K., McAtee, J. J., Belyanskaya, S., Brandt, M., Brown, G. D., Costell, M. H., Ding, Y., Dodson, J. W., Eisennagel, S. H., Fries, R. E., Gross, J. W., Harpel, M. R., Holt, D. A., Israel, D. I., Jolivette, L. J., et al. (2013) Discovery of 1-(1,3,5-triazin-2-yl)piperidine-4-carboxamides as inhibitors of soluble epoxide hydrolase. Bioorg. Med. Chem. Lett. 23, 3584-3588
41. Rorbach, J., Nicholls, T. J., and Minczuk, M. (2011) PDE12 removes mitochondrial RNA poly(A) tails and controls translation in human mitochondria. Nucleic Acids Res. 39, 7750-7763
42. Poulsen, J. B., Andersen, K. R., Kjær, K. H., Durand, F., Faou, P., Vestergaard, A. L., Talbo, G. H., Hoogenraad, N., Brodersen, D. E., Justesen, J., and Martensen, P. M. (2011) Human 2′-phosphodiesterase localizes to the mitochondrial matrix with a putative function in mitochondrial RNA turnover. Nucleic Acids Res. 39, 3754-3770
43. Lugnier, C. (2006) Cyclic nucleotide phosphodiesterase (PDE) superfamily: a new target for the development of specific therapeutic agents. Pharmacol. Ther. 109, 366-398
44. Mol, C. D., Izumi, T., Mitra, S., and Tainer, J. A. (2000) DNA-bound structures and mutants reveal abasic DNA binding by APE1 DNA repair and coordination. Nature 403, 451-456
45. Kjær, K. H., Pahus, J., Hansen, M. F., Poulsen, J. B., Christensen, E. I., Justesen, J., and Martensen, P. M. (2014) Mitochondrial localization of the OAS1 p46 isoform associated with a common single nucleotide polymorphism. BMC Cell Biol. 15, 33
46. Le Roy, F., Silhol, M., Salehzada, T., and Bisbal, C. (2007) Regulation of mitochondrial mRNA stability by RNase L is translation-dependent and controls IFNα-induced apoptosis. Cell Death Differ. 14, 1406-1413
47. Domingo-Gil E., and Esteban, M. (2006) Role of mitochondria in apoptosis induced by the 2-5A system and mechanisms involved. Apoptosis 11, 725-738
48. Lin, R.-J., Yu, H.-P., Chang, B.-L., Tang, W.-C., Liao, C.-L., and Lin, Y.-G. (2009) Distinct antiviral roles for human 2′,5′-oligoadenylate synthetase family members against dengue virus infection. J. Immunol. 183, 8035-8043
49. Flodström-Tullberg, M., Hultcrantz, M., Stotland, A., Maday, A., Tsai, D., Fine, C., Williams, B., Silverman, R., and Sarvetnick, N. (2005) RNase L and double-stranded RNA-dependent protein kinase exert complementary roles in islet cell defense during coxsackievirus infection. J. Immunol. 174, 1171-1177
50. Zhou, A., Paranjape, J., Brown, T. L., Nie, H., Naik, S., Dong, B., Chang, A., Trapp, B., Fairchild, R., Colmenares, C., and Silverman, R. H. (1997) Interferon action and apoptosis are defective in mice devoid of 2′,5′-oligoadenylate-dependent RNase L. EMBO J. 16, 6355-6363
51. Samuel, M. A., Whitby, K., Keller, B. C., Marri, A., Barchet, W., Williams, B. R., Silverman, R. H., Gale, M., Jr., and Diamond, M. S. (2006) PKR and RNase L contribute to protection against lethal West Nile virus infection by controlling early viral spread in the periphery and replication in neurons. J. Virol. 80, 7009-7019
52. Scherbik, S. V., Paranjape, J. M., Stockman, B. M., Silverman, R. H., and Brinton, M. A. (2006) RNase L plays a role in the antiviral response to West Nile virus. J. Virol. 80, 2987-2999