SAMHD1-deficient CD14+ cells from individuals with Aicardi-Goutières syndrome are highly susceptible to HIV-1 infection

PLoS Pathogens

Volumn 7, Issue 12, 2011, Pages

  Berger, André ^a   Sommer, Andreas F R ^a   Zwarg, Jenny ^a   Hamdorf, Matthias ^a   Welzel, Karin ^a   Esly, Nicole ^a   Panitz, Sylvia ^a   Reuter, Andreas ^a   Ramos, Irene ^b   Jatiani, Asavari ^b   Mulder, Lubbertus C F ^b   Fernandez Sesma, Ana ^b   Rutsch, Frank ^c   Simon, Viviana ^b   König, Renate ^a,d   Flory, Egbert ^a  

^a PAUL EHRLICH INSTITUT   (Germany)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^d BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD14 ANTIGEN; CHEMOKINE; CYTOKINE; HUMAN IMMUNODEFICIENCY VIRUS PROTEINASE; INTERFERON; SAMHD1 PROTEIN; UNCLASSIFIED DRUG; MONOMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; SAMHD1 PROTEIN, HUMAN;

AICARDI GOUTIERES SYNDROME; ARTICLE; CELL STRAIN HEK293; CELL SUBPOPULATION; CYTOKINE RELEASE; GENETIC ASSOCIATION; GENETIC TRANSFECTION; HELA CELL; HOMOZYGOSITY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; INFECTION SENSITIVITY; NONSENSE MUTATION; PERIPHERAL BLOOD MONONUCLEAR CELL; PLASMID; PROTEIN DEFECT; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; SINGLE NUCLEOTIDE POLYMORPHISM; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; UBIQUITINATION; VIRUS PARTICLE; VIRUS REPLICATION; BONE MARROW CELL; CELL SEPARATION; CONFOCAL MICROSCOPY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENETIC PREDISPOSITION; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOBLOTTING; IMMUNOPRECIPITATION; METABOLISM; MISSENSE MUTATION; NERVOUS SYSTEM MALFORMATION; NEUROLOGIC DISEASE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TANDEM MASS SPECTROMETRY; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2;

ANTIGENS, CD14; AUTOIMMUNE DISEASES OF THE NERVOUS SYSTEM; CELL SEPARATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENETIC PREDISPOSITION TO DISEASE; HIV INFECTIONS; HIV-1; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MICROSCOPY, CONFOCAL; MONOMERIC GTP-BINDING PROTEINS; MUTATION, MISSENSE; MYELOID CELLS; NERVOUS SYSTEM MALFORMATIONS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TANDEM MASS SPECTROMETRY; TRANSFECTION;

EID: 84855272511     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002425     Document Type: Article

References (46)

1. Sonza S, Maerz A, Deacon N, Meanger J, Mills J, et al. (1996) Human immunodeficiency virus type 1 replication is blocked prior to reverse transcription and integration in freshly isolated peripheral blood monocytes. J Virol 70: 3863-3869.
2. Neil S, Martin F, Ikeda Y, Collins M, (2001) Postentry restriction to human immunodeficiency virus-based vector transduction in human monocytes. J Virol 75: 5448-5456 10.1128/JVI.75.12.5448-5456.2001 [doi].
3. Kaushik R, Zhu X, Stranska R, Wu Y, Stevenson M, (2009) A cellular restriction dictates the permissivity of nondividing monocytes/macrophages to lentivirus and gammaretrovirus infection. Cell Host Microbe 6: 68-80.
4. Negre D, Mangeot PE, Duisit G, Blanchard S, Vidalain PO, et al. (2000) Characterization of novel safe lentiviral vectors derived from simian immunodeficiency virus (SIVmac251) that efficiently transduce mature human dendritic cells. Gene Ther 7: 1613-1623 10.1038/sj.gt.3301292 [doi].
5. Fujita M, Otsuka M, Nomaguchi M, Adachi A, (2010) Multifaceted activity of HIV Vpr/Vpx proteins: the current view of their virological functions. Rev Med Virol 20: 68-76.
6. Goujon C, Arfi V, Pertel T, Luban J, Lienard J, et al. (2008) Characterization of simian immunodeficiency virus SIVSM/human immunodeficiency virus type 2 Vpx function in human myeloid cells. J Virol 82: 12335-12345.
7. Yu XF, Yu QC, Essex M, Lee TH, (1991) The vpx gene of simian immunodeficiency virus facilitates efficient viral replication in fresh lymphocytes and macrophage. J Virol 65: 5088-5091.
8. Hirsch VM, Sharkey ME, Brown CR, Brichacek B, Goldstein S, et al. (1998) Vpx is required for dissemination and pathogenesis of SIV(SM) PBj: evidence of macrophage-dependent viral amplification. Nat Med 4: 1401-1408.
9. Berger A, Munk C, Schweizer M, Cichutek K, Schule S, et al. (2010) Interaction of Vpx and apolipoprotein B mRNA-editing catalytic polypeptide 3 family member A (APOBEC3A) correlates with efficient lentivirus infection of monocytes. J Biol Chem 285: 12248-12254.
10. Schule S, Kloke BP, Kaiser JK, Heidmeier S, Panitz S, et al. (2009) Restriction of HIV-1 replication in monocytes is abolished by Vpx of SIVsmmPBj. PLoS One 4: e7098.
11. Goujon C, Jarrosson-Wuilleme L, Bernaud J, Rigal D, Darlix JL, et al. (2006) With a little help from a friend: increasing HIV transduction of monocyte-derived dendritic cells with virion-like particles of SIV(MAC). Gene Ther 13: 991-994.
12. Gramberg T, Sunseri N, Landau NR, (2010) Evidence for an activation domain at the amino terminus of simian immunodeficiency virus Vpx. J Virol 84: 1387-1396.
13. Accola MA, Bukovsky AA, Jones MS, Gottlinger HG, (1999) A conserved dileucine-containing motif in p6(gag) governs the particle association of Vpx and Vpr of simian immunodeficiency viruses SIV(mac) and SIV(agm). J Virol 73: 9992-9999.
14. Strebel K, Luban J, Jeang KT, (2009) Human cellular restriction factors that target HIV-1 replication. BMC Med 7 48. 1741-7015-7-48 [pii];10.1186/1741-7015-7-48 [doi].
15. Wolf D, Goff SP, (2008) Host restriction factors blocking retroviral replication. Annu Rev Genet 42: 143-163 10.1146/annurev.genet.42.110807.091704 [doi].
16. Bergamaschi A, Ayinde D, David A, Le Rouzic E, Morel M, et al. (2009) The human immunodeficiency virus type 2 Vpx protein usurps the CUL4A-DDB1 DCAF1 ubiquitin ligase to overcome a postentry block in macrophage infection. J Virol 83: 4854-4860.
17. Sharova N, Wu Y, Zhu X, Stranska R, Kaushik R, et al. (2008) Primate lentiviral Vpx commandeers DDB1 to counteract a macrophage restriction. PLoS Pathog 4: e1000057.
18. Goujon C, Riviere L, Jarrosson-Wuilleme L, Bernaud J, Rigal D, et al. (2007) SIVSM/HIV-2 Vpx proteins promote retroviral escape from a proteasome-dependent restriction pathway present in human dendritic cells. Retrovirology 4: 2.
19. Hrecka K, Hao C, Gierszewska M, Swanson SK, Kesik-Brodacka M, et al. (2011) Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature 474: 658-661 nature10195 [pii];10.1038/nature10195 [doi].
20. Laguette N, Sobhian B, Casartelli N, Ringeard M, Chable-Bessia C, et al. (2011) SAMHD1 is the dendritic- and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx. Nature 474: 654-657 nature10117 [pii];10.1038/nature10117 [doi].
21. Crow YJ, Livingston JH, (2008) Aicardi-Goutieres syndrome: an important Mendelian mimic of congenital infection. Dev Med Child Neurol 50: 410-416 DMCN02062 [pii];10.1111/j.1469-8749.2008.02062.x [doi].
22. Lee-Kirsch MA, (2010) Nucleic acid metabolism and systemic autoimmunity revisited. Arthritis Rheum 62: 1208-1212 10.1002/art.27372 [doi].
23. Dussaix E, Lebon P, Ponsot G, Huault G, Tardieu M, (1985) Intrathecal synthesis of different alpha-interferons in patients with various neurological diseases. Acta Neurol Scand 71: 504-509.
24. Yan N, Regalado-Magdos AD, Stiggelbout B, Lee-Kirsch MA, Lieberman J, (2010) The cytosolic exonuclease TREX1 inhibits the innate immune response to human immunodeficiency virus type 1. Nat Immunol 11: 1005-1013 ni.1941 [pii];10.1038/ni.1941 [doi].
25. Rice GI, Bond J, Asipu A, Brunette RL, Manfield IW, et al. (2009) Mutations involved in Aicardi-Goutieres syndrome implicate SAMHD1 as regulator of the innate immune response. Nat Genet 41: 829-832 ng.373 [pii];10.1038/ng.373 [doi].
26. du MM, Nurnberg P, Crow YJ, Rutsch F, (2011) Cerebral vasculopathy is a common feature in Aicardi-Goutieres syndrome associated with SAMHD1 mutations. Proc Natl Acad Sci USA 108 1104699108 [pii];10.1073/pnas.1104699108 [doi].
27. Ramesh V, Bernardi B, Stafa A, Garone C, Franzoni E, et al. (2010) Intracerebral large artery disease in Aicardi-Goutieres syndrome implicates SAMHD1 in vascular homeostasis. Dev Med Child Neurol 52: 725-732 DMCN3727 [pii];10.1111/j.1469-8749.2010.03727.x [doi].
28. Thiele H, du MM, Barczyk K, George C, Schwindt W, et al. (2010) Cerebral arterial stenoses and stroke: novel features of Aicardi-Goutieres syndrome caused by the Arg164X mutation in SAMHD1 are associated with altered cytokine expression. Hum Mutat 31: E1836-E1850 10.1002/humu.21357 [doi].
29. Xin B, Jones S, Puffenberger EG, Hinze C, Bright A, et al. (2011) Homozygous mutation in SAMHD1 gene causes cerebral vasculopathy and early onset stroke. Proc Natl Acad Sci USA 108: 5372-5377 1014265108 [pii];10.1073/pnas.1014265108 [doi].
30. Srivastava S, Swanson SK, Manel N, Florens L, Washburn MP, et al. (2008) Lentiviral Vpx accessory factor targets VprBP/DCAF1 substrate adaptor for cullin 4 E3 ubiquitin ligase to enable macrophage infection. PLoS Pathog 4: e1000059.
31. Wiskerchen M, Muesing MA, (1995) Human immunodeficiency virus type 1 integrase: effects of mutations on viral ability to integrate, direct viral gene expression from unintegrated viral DNA templates, and sustain viral propagation in primary cells. J Virol 69: 376-386.
32. Feinberg MB, Jarrett RF, Aldovini A, Gallo RC, Wong-Staal F, (1986) HTLV-III expression and production involve complex regulation at the levels of splicing and translation of viral RNA. Cell 46: 807-817 0092-8674(86)90062-0 [pii].
33. Munoz C, Misset B, Fitting C, Bleriot JP, Carlet J, et al. (1991) Dissociation between plasma and monocyte-associated cytokines during sepsis. Eur J Immunol 21: 2177-2184 10.1002/eji.1830210928 [doi].
34. de Bont ES, Kimpen JL, Tamminga RY, Niemarkt AE, de Leij LH, et al. (2000) Intrinsic capacity of monocytes to produce cytokines ex vivo in patients with acute lymphoblastic leukaemia. Cytokine 12: 1723-1726 10.1006/cyto.2000.0776 [doi];S1043-4666(00)90776-2 [pii].
35. Kaiser SE, Riley BE, Shaler TA, Trevino RS, Becker CH, et al. (2011) Protein standard absolute quantification (PSAQ) method for the measurement of cellular ubiquitin pools. Nat Methods 8: 691-696 nmeth.1649 [pii];10.1038/nmeth.1649 [doi].
36. Qiao F, Bowie JU, (2005) The many faces of SAM. Sci STKE 2005:re7. stke.2862005re7 [pii];10.1126/stke.2862005re7 [doi].
37. Oberstrass FC, Lee A, Stefl R, Janis M, Chanfreau G, et al. (2006) Shape-specific recognition in the structure of the Vts1p SAM domain with RNA. Nat Struct Mol Biol 13: 160-167 nsmb1038 [pii];10.1038/nsmb1038 [doi].
38. Zimmerman MD, Proudfoot M, Yakunin A, Minor W, (2008) Structural insight into the mechanism of substrate specificity and catalytic activity of an HD-domain phosphohydrolase: the 5′-deoxyribonucleotidase YfbR from Escherichia coli. J Mol Biol 378: 215-226 S0022-2836(08)00233-7 [pii];10.1016/j.jmb.2008.02.036 [doi].
39. Aravind L, Koonin EV, (1998) The HD domain defines a new superfamily of metal-dependent phosphohydrolases. Trends Biochem Sci 23: 469-472 S0968-0004(98)01293-6 [pii].
40. Oussenko IA, Sanchez R, Bechhofer DH, (2002) Bacillus subtilis YhaM, a member of a new family of 3′-to-5′ exonucleases in gram-positive bacteria. J Bacteriol 184: 6250-6259.
41. Neil S, Bieniasz P, (2009) Human immunodeficiency virus, restriction factors, and interferon. J Interferon Cytokine Res 29: 569-580 10.1089/jir.2009.0077 [doi].
42. Uchil PD, Quinlan BD, Chan WT, Luna JM, Mothes W, (2008) TRIM E3 ligases interfere with early and late stages of the retroviral life cycle. PLoS Pathog 4 07-PLPA-RA-0403 [pii];10.1371/journal.ppat.0040016 [doi].
43. Berger G, Durand S, Fargier G, Nguyen XN, Cordeil S, et al. (2011) APOBEC3A Is a Specific Inhibitor of the Early Phases of HIV-1 Infection in Myeloid Cells. PLoS Pathog 7: e1002221.
44. Arhel N, (2010) Revisiting HIV-1 uncoating. Retrovirology 7 96. 1742-4690-7-96 [pii];10.1186/1742-4690-7-96 [doi].
45. Connor RI, Chen BK, Choe S, Landau NR, (1995) Vpr is required for efficient replication of human immunodeficiency virus type-1 in mononuclear phagocytes. Virology 206: 935-944 S0042-6822(85)71016-1 [pii];10.1006/viro.1995.1016 [doi].
46. Rodriguez-Madoz JR, Belicha-Villanueva A, Bernal-Rubio D, Ashour J, Ayllon J, et al. (2010) Inhibition of the type I interferon response in human dendritic cells by dengue virus infection requires a catalytically active NS2B3 complex. J Virol 84: 9760-9774 JVI.01051-10 [pii];10.1128/JVI.01051-10 [doi].