SAMHD1 restricts herpes simplex virus 1 in macrophages by limiting DNA replication

Journal of Virology

Volumn 87, Issue 23, 2013, Pages 12949-12956

  Kim, Eui Tae ^a   White, Tommy E ^b   Brandariz Núñez, Alberto ^b   Diaz Griffero, Felipe ^b   Weitzman, Matthew D ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEOSIDE TRIPHOSPHATE TRIPHOSPHOHYDROLASE; PHOSPHATASE; PROTEIN SAMHD1; UNCLASSIFIED DRUG; VIRUS DNA; VIRUS PROTEIN;

ARTICLE; CONTROLLED STUDY; DNA REPLICATION; ENZYME ACTIVITY; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; GENETIC TRANSDUCTION; HERPES SIMPLEX VIRUS 1; IMMUNOBLOTTING; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; VIRUS GENE; VIRUS GENOME; VIRUS REPLICATION; VIRUS STRAIN;

CELL LINE; DNA REPLICATION; DOWN-REGULATION; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; MACROPHAGES; MONOMERIC GTP-BINDING PROTEINS; VIRUS REPLICATION;

EID: 84887133253     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02291-13     Document Type: Article

References (49)

1. Bieniasz PD. 2004. Intrinsic immunity:a front-line defense against viral attack. Nat. Immunol. 5:1109-1115.
2. Hatziioannou T, Bieniasz PD. 2011. Antiretroviral restriction factors. Curr. Opin. Virol. 1:526-532.
3. Blanco-Melo D, Venkatesh S, Bieniasz PD. 2012. Intrinsic cellular defenses against human immunodeficiency viruses. Immunity 37:399-411.
4. Harris RS, Hultquist JF, Evans DT. 2012. The restriction factors of human immunodeficiency virus. J. Biol. Chem. 287:40875-40883.
5. Wolf D, Goff SP. 2008. Host restriction factors blocking retroviral replication. Annu. Rev. Genet. 42:143-163.
6. Sheehy AM, Gaddis NC, Choi JD, Malim MH. 2002. Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418:646-650.
7. Neil SJ, Zang T, Bieniasz PD. 2008. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451:425-430.
8. Laguette N, Sobhian B, Casartelli N, Ringeard M, Chable-Bessia C, Segeral E, Yatim A, Emiliani S, Schwartz O, Benkirane M. 2011. SAMHD1 is the dendritic-and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx. Nature 474:654-657.
9. Hrecka K, Hao C, Gierszewska M, Swanson SK, Kesik-Brodacka M, Srivastava S, Florens L, Washburn MP, Skowronski J. 2011. Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature 474:658-661.
10. Rossini G, Cerboni C, Santoni A, Landini MP, Landolfo S, Gatti D, Gribaudo G, Varani S. 2012. Interplay between human cytomegalovirus and intrinsic/innate host responses:a complex bidirectional relationship. Mediators Inflamm. 2012:607276.
11. Tavalai N, Stamminger T. 2011. Intrinsic cellular defense mechanisms targeting human cytomegalovirus. Virus Res. 157:128-133.
12. Weitzman MD, Ornelles DA. 2005. Inactivating intracellular antiviral responses during adenovirus infection. Oncogene 24:7686-7696.
13. Everett RD, Chelbi-Alix MK. 2007. PML and PML nuclear bodies:implications in antiviral defence. Biochimie 89:819-830.
14. Orzalli MH, DeLuca NA, Knipe DM. 2012. Nuclear IFI16 induction of IRF-3 signaling during herpesviral infection and degradation of IFI16 by the viral ICP0 protein. Proc. Natl. Acad. Sci. U.S.A. 109:E3008-E3017.
15. Kerur N, Veettil MV, Sharma-Walia N, Bottero V, Sadagopan S, Otageri P, Chandran B. 2011. IFI16 acts as a nuclear pathogen sensor to induce the inflammasome in response to Kaposi sarcoma-associated herpesvirus infection. Cell Host Microbe 9:363-375.
16. Lilley CE, Chaurushiya MS, Boutell C, Everett RD, Weitzman MD. 2011. The intrinsic antiviral defense to incoming HSV-1 genomes includes specificDNArepair proteins and is counteracted by the viral protein ICP0. PLoS Pathog. 7:e1002084. doi:10.1371/journal.ppat.1002084.
17. Geoffroy MC, Chelbi-Alix MK. 2011. Role of promyelocytic leukemia protein in host antiviral defense. J. Interferon Cytokine Res. 31:145-158.
18. Chin KC, Cresswell P. 2001. Viperin (cig5), an IFN-inducible antiviral protein directly induced by human cytomegalovirus. Proc. Natl. Acad. Sci. U.S.A. 98:15125-15130.
19. Suspene R, Aynaud MM, Koch S, Pasdeloup D, Labetoulle M, Gaertner B, Vartanian JP, Meyerhans A, Wain-Hobson S. 2011. Genetic editing of herpes simplex virus 1 and Epstein-Barr herpesvirus genomes by human APOBEC3 cytidine deaminases in culture and in vivo. J. Virol. 85:7594-7602.
20. Pardieu C, Vigan R, Wilson SJ, Calvi A, Zang T, Bieniasz P, Kellam P, Towers GJ, Neil SJ. 2010. The RING-CH ligase K5 antagonizes restriction of KSHV and HIV-1 particle release by mediating ubiquitin-dependent endosomal degradation of tetherin. PLoS Pathog. 6:e1000843. doi:10.1371 /journal.ppat.1000843.
21. Gramberg T, Kahle T, Bloch N, Wittmann S, Mullers E, Daddacha W, Hofmann H, Kim B, Lindemann D, Landau NR. 2013. Restriction of diverse retroviruses by SAMHD1. Retrovirology 10:26.
22. White TE, Brandariz-Nunez A, Valle-Casuso JC, Amie S, Nguyen L, Kim B, Brojatsch J, Diaz-Griffero F. 2013. Contribution of SAM and HD domains to retroviral restriction mediated by human SAMHD1. Virology 436:81-90.
23. Arduino PG, Porter SR. 2008. Herpes simplex virus type 1 infection: overview on relevant clinico-pathological features. J. Oral Pathol. Med. 37:107-121.
24. Kennedy PG, Steiner I. 2013. Recent issues in herpes simplex encephalitis. J. Neurovirol. 19:346-350.
25. Held K, Derfuss T. 2011. Control of HSV-1 latency in human trigeminal ganglia-current overview. J. Neurovirol. 17:518-527.
26. Weller SK, Coen DM. 2012. Herpes simplex viruses:mechanisms of DNA replication. Cold Spring Harb. Perspect. Biol. 4:a013011.
27. Ellermann-Eriksen S. 2005. Macrophages and cytokines in the early defence against herpes simplex virus. Virol. J. 2:59.
28. Laguette N, Benkirane M. 2012. How SAMHD1 changes our view of viral restriction. Trends Immunol. 33:26-33.
29. Luban J. 2012. Innate immune sensing of HIV-1 by dendritic cells. Cell Host Microbe 12:408-418.
30. Pan X, Baldauf HM, Keppler OT, Fackler OT. 2013. Restrictions to HIV-1 replication in resting CD4 T lymphocytes. Cell Res. 23:876-885.
31. Lim ES, Fregoso OI, McCoy CO, Matsen FA, Malik HS, Emerman M. 2012. The ability of primate lentiviruses to degrade the monocyte restriction factorSAMHD1preceded the birth of the viral accessory protein Vpx. Cell Host Microbe 11:194-204.
32. Rice GI, Bond J, Asipu A, Brunette RL, Manfield IW, Carr IM, Fuller JC, Jackson RM, Lamb T, Briggs TA, Ali M, Gornall H, Couthard LR, Aeby A, Attard-Montalto SP, Bertini E, Bodemer C, Brockmann K, Brueton LA, Corry PC, Desguerre I, Fazzi E, Cazorla AG, Gener B, Hamel BC, Heiberg A, Hunter M, van der Knaap MS, Kumar R, Lagae L, Landrieu PG, Lourenco CM, Marom D, McDermott MF, van der Merwe W, Orcesi S, Prendiville JS, Rasmussen M, Shalev SA, Soler DM, Shinawi M, Spiegel R, Tan TY, Vanderver A, Wakeling EL, Wassmer E, Whittaker E, Lebon P, Stetson DB, Bonthron DT, Crow YJ. 2009. Mutations involved in Aicardi-Goutieres syndrome implicate SAMHD1 as regulator of the innate immune response. Nat. Genet. 41:829-832.
33. Goldstone DC, Ennis-Adeniran V, Hedden JJ, Groom HC, Rice GI, Christodoulou E, Walker PA, Kelly G, Haire LF, Yap MW, de Carvalho LP, Stoye JP, Crow YJ, Taylor IA, Webb M. 2011. HIV-1 restriction factor SAMHD1 is a deoxynucleoside triphosphate triphosphohydrolase. Nature 480:379-382.
34. Amie SM, Noble E, Kim B. 2013. Intracellular nucleotide levels and the control of retroviral infections. Virology 436:247-254.
35. Kim B, Nguyen LA, Daddacha W, Hollenbaugh JA. 2012. Tight interplay among SAMHD1 protein level, cellular dNTP levels, and HIV-1 proviral DNA synthesis kinetics in human primary monocyte-derived macrophages. J. Biol. Chem. 287:21570-21574.
36. Beloglazova N, Flick R, Tchigvintsev A, Brown G, Popovic A, Nocek B, Yakunin AF. 2013. Nuclease activity of the human SAMHD1 protein implicated in the Aicardi-Goutieres syndrome and HIV-1 restriction. J. Biol. Chem. 288:8101-8110.
37. Lahouassa H, Daddacha W, Hofmann H, Ayinde D, Logue EC, Dragin L, Bloch N, Maudet C, Bertrand M, Gramberg T, Pancino G, Priet S, Canard B, Laguette N, Benkirane M, Transy C, Landau NR, Kim B, Margottin-Goguet F. 2012. SAMHD1 restricts the replication of human immunodeficiency virus type 1 by depleting the intracellular pool of deoxynucleoside triphosphates. Nat. Immunol. 13:223-228.
38. Baldauf HM, Pan X, Erikson E, Schmidt S, Daddacha W, Burggraf M, Schenkova K, Ambiel I, Wabnitz G, Gramberg T, Panitz S, Flory E, Landau NR, Sertel S, Rutsch F, Lasitschka F, Kim B, Konig R, Fackler OT, Keppler OT. 2012. SAMHD1 restricts HIV-1 infection in resting CD4(+) T cells. Nat. Med. 18:1682-1687.
39. Berger A, Sommer AF, Zwarg J, Hamdorf M, Welzel K, Esly N, Panitz S, Reuter A, Ramos I, Jatiani A, Mulder LC, Fernandez-Sesma A, Rutsch F, Simon V, Konig R, Flory E. 2011. SAMHD1-deficient CD14+ cells from individuals with Aicardi-Goutieres syndrome are highly susceptible to HIV-1 infection. PLoS Pathog. 7:e1002425. doi:10.1371/journal .ppat.1002425.
40. Sunseri N, O'Brien M, Bhardwaj N, Landau NR. 2011. Human immunodeficiency virus type 1 modified to package simian immunodeficiency virus Vpx efficiently infects macrophages and dendritic cells. J. Virol. 85: 6263-6274.
41. Hollenbaugh JA, Gee P, Baker J, Daly MB, Amie SM, Tate J, Kasai N, Kanemura Y, Kim DH, Ward BM, Koyanagi Y, Kim B. 2013. Host factor SAMHD1 restricts DNA viruses in nondividing myeloid cells. PLoS Pathog. 9:e1003481. doi:10.1371/journal.ppat.1003481.
42. White TE, Brandariz-Nunez A, Valle-Casuso JC, Amie S, Nguyen LA, Kim B, Tuzova M, Diaz-Griffero F. 2013. The retroviral restriction ability of SAMHD1, but not its deoxynucleotide triphosphohydrolase activity, is regulated by phosphorylation. Cell Host Microbe 13:441-451.
43. Everett RD, Cross A, Orr A. 1993. A truncated form of herpes simplex virus type 1 immediate-early protein Vmw110 is expressed in a cell type dependent manner. Virology 197:751-756.
44. Cribier A, Descours B, Valadao AL, Laguette N, Benkirane M. 2013. Phosphorylation of SAMHD1 by cyclin A2/CDK1 regulates its restriction activity toward HIV-1. Cell Rep. 3:1036-1043.
45. Goncalves A, Karayel E, Rice GI, Bennett KL, Crow YJ, Superti-Furga G, Burckstummer T. 2012. SAMHD1 is a nucleic-acid binding protein that is mislocalized due to Aicardi-Goutieres syndrome-associated mutations. Hum. Mutat. 33:1116-1122.
46. Schoggins JW, Wilson SJ, Panis M, Murphy MY, Jones CT, Bieniasz P, Rice CM. 2011. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472:481-485.
47. Kirchhoff F. 2010. Immune evasion and counteraction of restriction factors by HIV-1 and other primate lentiviruses. Cell Host Microbe 8:55-67.
48. Brandariz-Nunez A, Valle-Casuso JC, White TE, Laguette N, Benkirane M, Brojatsch J, Diaz-Griffero F. 2012. Role of SAMHD1 nuclear localization in restriction of HIV-1 and SIVmac. Retrovirology 9:49.
49. Goodrum F, Caviness K, Zagallo P. 2012. Human cytomegalovirus persistence. Cell Microbiol. 14:644-655.