An Intrinsically Disordered Region of the DNA Repair Protein Nbs1 Is a Species-Specific Barrier to Herpes Simplex Virus 1 in Primates

Cell Host and Microbe

Volumn 20, Issue 2, 2016, Pages 178-188

  Lou, Dianne I ^a,g   Kim, Eui Tae ^b   Meyerson, Nicholas R ^c   Pancholi, Neha J ^b,d   Mohni, Kareem N ^e   Enard, David ^f   Petrov, Dmitri A ^f   Weller, Sandra K ^e   Weitzman, Matthew D ^b   Sawyer, Sara L ^a,c  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^c UNIVERSITY OF COLORADO   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^f STANFORD UNIVERSITY   (United States)

^g VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INFECTED CELL PROTEIN 8; INTRINSICALLY DISORDERED PROTEIN; NIBRIN; PHOSPHONOACETIC ACID; VIRAL PROTEIN; CELL CYCLE PROTEIN; DNA LIGASE; IMMEDIATE EARLY PROTEIN; NBN PROTEIN, HUMAN; NUCLEAR PROTEIN; PROTEIN BINDING; UBIQUITIN PROTEIN LIGASE; VMW110 PROTEIN, HUMAN HERPESVIRUS 1;

ANIMAL CELL; APE; ARTICLE; CONTROLLED STUDY; DNA REPAIR; GENE EXPRESSION; HERPES SIMPLEX VIRUS 1; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MOLECULAR PHYLOGENY; NIJMEGEN BREAKAGE SYNDROME; NONHUMAN; PRIMATE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIRAL PLAQUE ASSAY; VIRUS CELL INTERACTION; ANIMAL; CELL LINE; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; PROTEIN ANALYSIS; PROTEIN DOMAIN; SEQUENCE HOMOLOGY; VIRUS LOAD; VIRUS REPLICATION;

ANIMALS; CELL CYCLE PROTEINS; CELL LINE; DNA REPAIR ENZYMES; HERPESVIRUS 1, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMEDIATE-EARLY PROTEINS; NUCLEAR PROTEINS; PRIMATES; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPPING; SEQUENCE HOMOLOGY, AMINO ACID; UBIQUITIN-PROTEIN LIGASES; VIRAL LOAD; VIRUS REPLICATION;

EID: 84991666896     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2016.07.003     Document Type: Article

References (63)

1. Balasubramanian, N., Bai, P., Buchek, G., Korza, G., Weller, S.K., Physical interaction between the herpes simplex virus type 1 exonuclease, UL12, and the DNA double-strand break-sensing MRN complex. J. Virol. 84 (2010), 12504–12514.
2. Barnes, K.J., Garner, M.M., Wise, A.G., Persiani, M., Maes, R.K., Kiupel, M., Herpes simplex encephalitis in a captive black howler monkey (Alouatta caraya). J. Vet. Diagn. Invest. 28 (2016), 76–78.
3. Boutell, C., Everett, R.D., Regulation of alphaherpesvirus infections by the ICP0 family of proteins. J. Gen. Virol. 94 (2013), 465–481.
4. Brown, C.J., Johnson, A.K., Daughdrill, G.W., Comparing models of evolution for ordered and disordered proteins. Mol. Biol. Evol. 27 (2010), 609–621.
5. Chapman, J.R., Taylor, M.R.G., Boulton, S.J., Playing the end game: DNA double-strand break repair pathway choice. Mol. Cell 47 (2012), 497–510.
6. Chaurushiya, M.S., Lilley, C.E., Aslanian, A., Meisenhelder, J., Scott, D.C., Landry, S., Ticau, S., Boutell, C., Yates, J.R. 3rd, Schulman, B.A., et al. Viral E3 ubiquitin ligase-mediated degradation of a cellular E3: viral mimicry of a cellular phosphorylation mark targets the RNF8 FHA domain. Mol. Cell 46 (2012), 79–90.
7. Chayavichitsilp, P., Buckwalter, J.V., Krakowski, A.C., Friedlander, S.F., Herpes simplex. Pediatr. Rev. 30 (2009), 119–129, quiz 130.
8. Choe, H., Jemielity, S., Abraham, J., Radoshitzky, S.R., Farzan, M., Transferrin receptor 1 in the zoonosis and pathogenesis of New World hemorrhagic fever arenaviruses. Curr. Opin. Microbiol. 14 (2011), 476–482.
9. Ciccia, A., Elledge, S.J., The DNA damage response: making it safe to play with knives. Mol. Cell 40 (2010), 179–204.
10. Demogines, A., Abraham, J., Choe, H., Farzan, M., Sawyer, S.L., Dual host-virus arms races shape an essential housekeeping protein. PLoS Biol., 11, 2013, e1001571.
11. Desai-Mehta, A., Cerosaletti, K.M., Concannon, P., Distinct functional domains of nibrin mediate Mre11 binding, focus formation, and nuclear localization. Mol. Cell. Biol. 21 (2001), 2184–2191.
12. Dosztányi, Z., Csizmok, V., Tompa, P., Simon, I., IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content. Bioinformatics 21 (2005), 3433–3434.
13. Elde, N.C., Child, S.J., Geballe, A.P., Malik, H.S., Protein kinase R reveals an evolutionary model for defeating viral mimicry. Nature 457 (2009), 485–489.
14. Enard, D., Cai, L., Gwennap, C., Petrov, D.A., Viruses are a dominant driver of protein adaptation in mammals. eLife, 5, 2016, e12469.
15. Evans, J.D., Hearing, P., Relocalization of the Mre11-Rad50-Nbs1 complex by the adenovirus E4 ORF3 protein is required for viral replication. J. Virol. 79 (2005), 6207–6215.
16. Everett, R.D., Dynamic response of IFI16 and promyelocytic leukemia nuclear body components to herpes simplex virus 1 infection. J. Virol. 90 (2015), 167–179.
17. Everett, R.D., Murray, J., ND10 components relocate to sites associated with herpes simplex virus type 1 nucleoprotein complexes during virus infection. J. Virol. 79 (2005), 5078–5089.
18. Everett, R.D., Rechter, S., Papior, P., Tavalai, N., Stamminger, T., Orr, A., PML contributes to a cellular mechanism of repression of herpes simplex virus type 1 infection that is inactivated by ICP0. J. Virol. 80 (2006), 7995–8005.
19. Everett, R.D., Parada, C., Gripon, P., Sirma, H., Orr, A., Replication of ICP0-null mutant herpes simplex virus type 1 is restricted by both PML and Sp100. J. Virol. 82 (2008), 2661–2672.
20. Garber, D.A., Beverley, S.M., Coen, D.M., Demonstration of circularization of herpes simplex virus DNA following infection using pulsed field gel electrophoresis. Virology 197 (1993), 459–462.
21. Gilardi, K.V.K., Oxford, K.L., Gardner-Roberts, D., Kinani, J.-F., Spelman, L., Barry, P.A., Cranfield, M.R., Lowenstine, L.J., Human herpes simplex virus type 1 in confiscated gorilla. Emerg. Infect. Dis. 20 (2014), 1883–1886.
22. Glass, M., Everett, R.D., Components of promyelocytic leukemia nuclear bodies (ND10) act cooperatively to repress herpesvirus infection. J. Virol. 87 (2013), 2174–2185.
23. Heldstab, A., Rüedi, D., Sonnabend, W., Deinhardt, F., Spontaneous generalized Herpesvirus hominis infection of a lowland gorilla (Gorilla gorilla gorilla). J. Med. Primatol. 10 (1981), 129–135.
24. Kaelber, J.T., Demogines, A., Harbison, C.E., Allison, A.B., Goodman, L.B., Ortega, A.N., Sawyer, S.L., Parrish, C.R., Evolutionary reconstructions of the transferrin receptor of Caniforms supports canine parvovirus being a re-emerged and not a novel pathogen in dogs. PLoS Pathog., 8, 2012, e1002666.
25. Kailasan, S., Agbandje-McKenna, M., Parrish, C.R., Parvovirus family conundrum: what makes a killer?. Annu Rev Virol 2 (2015), 425–450.
26. Kerr, S.A., Jackson, E.L., Lungu, O.I., Meyer, A.G., Demogines, A., Ellington, A.D., Georgiou, G., Wilke, C.O., Sawyer, S.L., Computational and functional analysis of the virus-receptor interface reveals host range trade-offs in new world arenaviruses. J. Virol. 89 (2015), 11643–11653.
27. Kik, M.J.L., Bos, J.H., Groen, J., Dorrestein, G.M., Herpes simplex infection in a juvenile orangutan (Pongo pygmaeus pygmaeus). J. Zoo Wildl. Med. 36 (2005), 131–134.
28. Kirmaier, A., Wu, F., Newman, R.M., Hall, L.R., Morgan, J.S., O'Connor, S., Marx, P.A., Meythaler, M., Goldstein, S., Buckler-White, A., et al. TRIM5 suppresses cross-species transmission of a primate immunodeficiency virus and selects for emergence of resistant variants in the new species. PLoS Biol., 8, 2010, e1000462.
29. Knipe, D.M., Senechek, D., Rice, S.A., Smith, J.L., Stages in the nuclear association of the herpes simplex virus transcriptional activator protein ICP4. J. Virol. 61 (1987), 276–284.
30. Kraakman-van der Zwet, M., Overkamp, W.J., Friedl, A.A., Klein, B., Verhaegh, G.W., Jaspers, N.G., Midro, A.T., Eckardt-Schupp, F., Lohman, P.H., Zdzienicka, M.Z., Immortalization and characterization of Nijmegen Breakage syndrome fibroblasts. Mutat. Res. 434 (1999), 17–27.
31. Lakdawala, S.S., Schwartz, R.A., Ferenchak, K., Carson, C.T., McSharry, B.P., Wilkinson, G.W., Weitzman, M.D., Differential requirements of the C terminus of Nbs1 in suppressing adenovirus DNA replication and promoting concatemer formation. J. Virol. 82 (2008), 8362–8372.
32. Landolfi, J.A., Wellehan, J.F.X., Johnson, A.J., Kinsel, M.J., Fatal human herpesvirus type 1 infection in a white-handed gibbon (Hylobates lar). J. Vet. Diagn. Invest. 17 (2005), 369–371.
33. Lees-Miller, S.P., Long, M.C., Kilvert, M.A., Lam, V., Rice, S.A., Spencer, C.A., Attenuation of DNA-dependent protein kinase activity and its catalytic subunit by the herpes simplex virus type 1 transactivator ICP0. J. Virol. 70 (1996), 7471–7477.
34. Li, H., Baskaran, R., Krisky, D.M., Bein, K., Grandi, P., Cohen, J.B., Glorioso, J.C., Chk2 is required for HSV-1 ICP0-mediated G2/M arrest and enhancement of virus growth. Virology 375 (2008), 13–23.
35. Lilley, C.E., Carson, C.T., Muotri, A.R., Gage, F.H., Weitzman, M.D., DNA repair proteins affect the lifecycle of herpes simplex virus 1. Proc. Natl. Acad. Sci. USA 102 (2005), 5844–5849.
36. Lilley, C.E., Chaurushiya, M.S., Boutell, C., Everett, R.D., Weitzman, M.D., The intrinsic antiviral defense to incoming HSV-1 genomes includes specific DNA repair proteins and is counteracted by the viral protein ICP0. PLoS Pathog., 7, 2011, e1002084.
37. Livingston, C.M., DeLuca, N.A., Wilkinson, D.E., Weller, S.K., Oligomerization of ICP4 and rearrangement of heat shock proteins may be important for herpes simplex virus type 1 prereplicative site formation. J. Virol. 82 (2008), 6324–6336.
38. Lukashchuk, V., Everett, R.D., Regulation of ICP0-null mutant herpes simplex virus type 1 infection by ND10 components ATRX and hDaxx. J. Virol. 84 (2010), 4026–4040.
39. Mätz-Rensing, K., Jentsch, K.D., Rensing, S., Langenhuyzen, S., Verschoor, E., Niphuis, H., Kaup, F.J., Fatal Herpes simplex infection in a group of common marmosets (Callithrix jacchus). Vet. Pathol. 40 (2003), 405–411.
40. Meyerson, N.R., Sawyer, S.L., Two-stepping through time: mammals and viruses. Trends Microbiol. 19 (2011), 286–294.
41. Mocarski, E.S., Comparative analysis of herpesvirus-common proteins. Arvin, A., Campadelli-Fiume, G., Mocasarski, E., Moore, P.S., Roizman, B., Whitely, R., Yamanishi, K., (eds.) Human Herpesviruses: Biology, Therapy, and Immunoprophylaxis, 2007, Cambridge University Press, 1–28.
42. Mohan, A., Oldfield, C.J., Radivojac, P., Vacic, V., Cortese, M.S., Dunker, A.K., Uversky, V.N., Analysis of molecular recognition features (MoRFs). J. Mol. Biol. 362 (2006), 1043–1059.
43. Mohni, K.N., Mastrocola, A.S., Bai, P., Weller, S.K., Heinen, C.D., DNA mismatch repair proteins are required for efficient herpes simplex virus 1 replication. J. Virol. 85 (2011), 12241–12253.
44. Mootnick, A.R., Reingold, M., Holshuh, H.J., Mirkovic, R.R., Isolation of a herpes simplex virus type 1-like agent from the brain of a mountain agile gibbon (Hylobates agilis agilis) with encephalitis. J. Zoo Wildl. Med. 29 (1998), 61–64.
45. Müller, S., Hollatz, M., Wienberg, J., Chromosomal phylogeny and evolution of gibbons (Hylobatidae). Hum. Genet. 113 (2003), 493–501.
46. 2: database of disordered protein predictions. Nucleic Acids Res. 41 (2013), D508–D516.
47. Parkinson, J., Lees-Miller, S.P., Everett, R.D., Herpes simplex virus type 1 immediate-early protein vmw110 induces the proteasome-dependent degradation of the catalytic subunit of DNA-dependent protein kinase. J. Virol. 73 (1999), 650–657.
48. Poffenberger, K.L., Roizman, B., A noninverting genome of a viable herpes simplex virus 1: presence of head-to-tail linkages in packaged genomes and requirements for circularization after infection. J. Virol. 53 (1985), 587–595.
49. Randall, R.E., Dinwoodie, N., Intranuclear localization of herpes simplex virus immediate-early and delayed-early proteins: evidence that ICP 4 is associated with progeny virus DNA. J. Gen. Virol. 67 (1986), 2163–2177.
50. Sawyer, S.L., Elde, N.C., A cross-species view on viruses. Curr. Opin. Virol. 2 (2012), 561–568.
51. Sawyer, S.L., Wu, L.I., Emerman, M., Malik, H.S., Positive selection of primate TRIM5alpha identifies a critical species-specific retroviral restriction domain. Proc. Natl. Acad. Sci. USA 102 (2005), 2832–2837.
52. Schrenzel, M.D., Osborn, K.G., Shima, A., Klieforth, R.B., Maalouf, G.A., Naturally occurring fatal herpes simplex virus 1 infection in a family of white-faced saki monkeys (Pithecia pithecia pithecia). J. Med. Primatol. 32 (2003), 7–14.
53. Schumacher, A.J., Mohni, K.N., Kan, Y., Hendrickson, E.A., Stark, J.M., Weller, S.K., The HSV-1 exonuclease, UL12, stimulates recombination by a single strand annealing mechanism. PLoS Pathog., 8, 2012, e1002862.
54. Sharp, P.M., Origins of human virus diversity. Cell 108 (2002), 305–312.
55. Shirata, N., Kudoh, A., Daikoku, T., Tatsumi, Y., Fujita, M., Kiyono, T., Sugaya, Y., Isomura, H., Ishizaki, K., Tsurumi, T., Activation of ataxia telangiectasia-mutated DNA damage checkpoint signal transduction elicited by herpes simplex virus infection. J. Biol. Chem. 280 (2005), 30336–30341.
56. Smith, S., Reuven, N., Mohni, K.N., Schumacher, A.J., Weller, S.K., Structure of the herpes simplex virus 1 genome: manipulation of nicks and gaps can abrogate infectivity and alter the cellular DNA damage response. J. Virol. 88 (2014), 10146–10156.
57. Stracker, T.H., Carson, C.T., Weitzman, M.D., Adenovirus oncoproteins inactivate the Mre11-Rad50-NBS1 DNA repair complex. Nature 418 (2002), 348–352.
58. Strang, B.L., Stow, N.D., Circularization of the herpes simplex virus type 1 genome upon lytic infection. J. Virol. 79 (2005), 12487–12494.
59. Taylor, T.J., Knipe, D.M., Proteomics of herpes simplex virus replication compartments: association of cellular DNA replication, repair, recombination, and chromatin remodeling proteins with ICP8. J. Virol. 78 (2004), 5856–5866.
60. Tischer, B.K., Osterrieder, N., Herpesviruses—a zoonotic threat?. Vet. Microbiol. 140 (2010), 266–270.
61. Wertheim, J.O., Smith, M.D., Smith, D.M., Scheffler, K., Kosakovsky Pond, S.L., Evolutionary origins of human herpes simplex viruses 1 and 2. Mol. Biol. Evol. 31 (2014), 2356–2364.
62. Wilkinson, D.E., Weller, S.K., Recruitment of cellular recombination and repair proteins to sites of herpes simplex virus type 1 DNA replication is dependent on the composition of viral proteins within prereplicative sites and correlates with the induction of the DNA damage response. J. Virol. 78 (2004), 4783–4796.
63. Williams, R.S., Dodson, G.E., Limbo, O., Yamada, Y., Williams, J.S., Guenther, G., Classen, S., Glover, J.N.M., Iwasaki, H., Russell, P., Tainer, J.A., Nbs1 flexibly tethers Ctp1 and Mre11-Rad50 to coordinate DNA double-strand break processing and repair. Cell 139 (2009), 87–99.