Complement-Opsonized HIV-1 Overcomes Restriction in Dendritic Cells

PLoS Pathogens

Volumn 11, Issue 6, 2015, Pages

  Posch, Wilfried ^a   Steger, Marion ^a   Knackmuss, Ulla ^a   Blatzer, Michael ^a   Baldauf, Hanna Mari ^b   Doppler, Wolfgang ^a   White, Tommy E ^c   Hörtnagl, Paul ^a   Diaz Griffero, Felipe ^c   Lass Flörl, Cornelia ^a   Hackl, Hubert ^a   Moris, Arnaud ^d,e,f   Keppler, Oliver T ^b   Wilflingseder, Doris ^a  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b GOETHE UNIVERSITY   (Germany)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^d SORBONNE UNIVERSITÉ   (France)

^e Assistance publique Hôpitaux de Paris   (France)

^f PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 ANTIGEN; CD83 ANTIGEN; CD86 ANTIGEN; CHEMOKINE RECEPTOR CCR7; GAG PROTEIN; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HLA DR ANTIGEN; INTERFERON; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; ROSCOVITINE; SAM DOMAIN AND HD DOMAIN-CONTAINING PROTEIN 1; STAT1 PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA; COMPLEMENT;

ANTIGEN EXPRESSION; ANTIVIRAL ACTIVITY; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL MATURATION; CELLULAR IMMUNITY; DENDRITIC CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN IMMUNODEFICIENCY VIRUS 2 INFECTION; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; OPSONIZATION; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; VIRUS REPLICATION; WESTERN BLOTTING; IMMUNOLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

CD4-POSITIVE T-LYMPHOCYTES; COMPLEMENT SYSTEM PROTEINS; DENDRITIC CELLS; HIV INFECTIONS; HIV-1; HUMANS; VIRUS REPLICATION;

EID: 84936763308     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005005     Document Type: Article

References (61)

1. Fernandez NC, Lozier A, Flament C, Ricciardi-Castagnoli P, Bellet D, Suter M, et al. Dendritic cells directly trigger NK cell functions: cross-talk relevant in innate anti-tumor immune responses in vivo. Nat Med. 1999;5(4):405–11. 10202929
2. Steinman RM, Hemmi H, Dendritic cells: translating innate to adaptive immunity. Curr Top Microbiol Immunol. 2006;311:17–58. 17048704
3. Steinman RM, Decisions about dendritic cells: past, present, and future. Annu Rev Immunol. 2012;30:1–22. doi: 10.1146/annurev-immunol-100311-102839 22136168
4. Manel N, Hogstad B, Wang Y, Levy DE, Unutmaz D, Littman DR, A cryptic sensor for HIV-1 activates antiviral innate immunity in dendritic cells. Nature. 2010;467(7312):214–7. doi: 10.1038/nature09337 20829794
5. Wu L, KewalRamani VN, Dendritic-cell interactions with HIV: infection and viral dissemination. Nat Rev Immunol. 2006;6(11):859–68. 17063186
6. Stoiber H, Soederholm A, Wilflingseder D, Gusenbauer S, Hildgartner A, Dierich MP, Complement and antibodies: a dangerous liaison in HIV infection? Vaccine. 2008;26 Suppl 8:I79–85. 19388170
7. Wilflingseder D, Banki Z, Garcia E, Pruenster M, Pfister G, Muellauer B, et al. IgG opsonization of HIV impedes provirus formation in and infection of dendritic cells and subsequent long-term transfer to T cells. J Immunol. 2007;178(12):7840–8. 17548622
8. Ebenbichler CF, Thielens NM, Vornhagen R, Marschang P, Arlaud GJ, Dierich MP, Human immunodeficiency virus type 1 activates the classical pathway of complement by direct C1 binding through specific sites in the transmembrane glycoprotein gp41. J Exp Med. 1991;174(6):1417–24. 1744579
9. Pruenster M, Wilflingseder D, Banki Z, Ammann CG, Muellauer B, Meyer M, et al. C-type lectin-independent interaction of complement opsonized HIV with monocyte-derived dendritic cells. Eur J Immunol. 2005;35(9):2691–8. 16094691
10. Mehlhop E, Whitby K, Oliphant T, Marri A, Engle M, Diamond MS, Complement activation is required for induction of a protective antibody response against West Nile virus infection. J Virol. 2005;79(12):7466–77. 15919902
11. Da Costa XJ, Brockman MA, Alicot E, Ma M, Fischer MB, Zhou X, et al. Humoral response to herpes simplex virus is complement-dependent. Proc Natl Acad Sci U S A. 1999;96(22):12708–12. 10535987
12. Kopf M, Abel B, Gallimore A, Carroll M, Bachmann MF, Complement component C3 promotes T-cell priming and lung migration to control acute influenza virus infection. Nat Med. 2002;8(4):373–8. 11927943
13. Verschoor A, Brockman MA, Knipe DM, Carroll MC, Cutting edge: myeloid complement C3 enhances the humoral response to peripheral viral infection. J Immunol. 2001;167(5):2446–51. 11509581
14. Suresh M, Molina H, Salvato MS, Mastellos D, Lambris JD, Sandor M, Complement component 3 is required for optimal expansion of CD8 T cells during a systemic viral infection. J Immunol. 2003;170(2):788–94. 12517942
15. Goujon C, Jarrosson-Wuilleme L, Bernaud J, Rigal D, Darlix JL, Cimarelli A, With a little help from a friend: increasing HIV transduction of monocyte-derived dendritic cells with virion-like particles of SIV(MAC). Gene therapy. 2006;13(12):991–4. 16525481
16. Manel N, Littman DR, Hiding in plain sight: how HIV evades innate immune responses. Cell. 2011;147(2):271–4. doi: 10.1016/j.cell.2011.09.010 22000008
17. Laguette N, Sobhian B, Casartelli N, Ringeard M, Chable-Bessia C, Segeral E, et al. SAMHD1 is the dendritic- and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx. Nature. 2011;474(7353):654–7. doi: 10.1038/nature10117 21613998
18. Hrecka K, Hao C, Gierszewska M, Swanson SK, Kesik-Brodacka M, Srivastava S, et al. Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature. 2011;474(7353):658–61. doi: 10.1038/nature10195 21720370
19. Baldauf HM, Pan X, Erikson E, Schmidt S, Daddacha W, Burggraf M, et al. SAMHD1 restricts HIV-1 infection in resting CD4(+) T cells. Nat Med. 2012;18(11):1682–7. doi: 10.1038/nm.2964 22972397
20. White TE, Brandariz-Nunez A, Valle-Casuso JC, Amie S, Nguyen L, Kim B, et al. Contribution of SAM and HD domains to retroviral restriction mediated by human SAMHD1. Virology. 2013;436(1):81–90. doi: 10.1016/j.virol.2012.10.029 23158101
21. Cribier A, Descours B, Valadao AL, Laguette N, Benkirane M, Phosphorylation of SAMHD1 by cyclin A2/CDK1 regulates its restriction activity toward HIV-1. Cell reports. 2013;3(4):1036–43. doi: 10.1016/j.celrep.2013.03.017 23602554
22. Welbourn S, Dutta SM, Semmes OJ, Strebel K, Restriction of virus infection but not catalytic dNTPase activity is regulated by phosphorylation of SAMHD1. J Virol. 2013;87(21):11516–24. doi: 10.1128/JVI.01642-13 23966382
23. Ryoo J, Choi J, Oh C, Kim S, Seo M, Kim SY, et al. The ribonuclease activity of SAMHD1 is required for HIV-1 restriction. Nat Med. 2014.
24. Banki Z, Posch W, Ejaz A, Oberhauser V, Willey S, Gassner C, et al. Complement as an endogenous adjuvant for dendritic cell-mediated induction of retrovirus-specific CTLs. PLoS Pathog. 2010;6(4):e1000891. doi: 10.1371/journal.ppat.1000891 20442876
25. Berger A, Sommer AF, Zwarg J, Hamdorf M, Welzel K, Esly N, et al. SAMHD1-deficient CD14+ cells from individuals with Aicardi-Goutieres syndrome are highly susceptible to HIV-1 infection. PLoS Pathog. 2011;7(12):e1002425. doi: 10.1371/journal.ppat.1002425 22174685
26. Descours B, Cribier A, Chable-Bessia C, Ayinde D, Rice G, Crow Y, et al. SAMHD1 restricts HIV-1 reverse transcription in quiescent CD4(+) T-cells. Retrovirology. 2012;9:87. doi: 10.1186/1742-4690-9-87 23092122
27. St Gelais C, de Silva S, Hach JC, White TE, Diaz-Griffero F, Yount JS, et al. Identification of Cellular Proteins Interacting with the Retroviral Restriction Factor SAMHD1. J Virol. 2014;88(13):7689.
28. Pauls E, Ruiz A, Badia R, Permanyer M, Gubern A, Riveira-Munoz E, et al. Cell Cycle Control and HIV-1 Susceptibility Are Linked by CDK6-Dependent CDK2 Phosphorylation of SAMHD1 in Myeloid and Lymphoid Cells. J Immunol. 2014;193(4):1988–97. doi: 10.4049/jimmunol.1400873 25015816
29. Chauveau L, Puigdomenech I, Ayinde D, Roesch F, Porrot F, Bruni D, et al. HIV-2 infects resting CD4+ T cells but not monocyte-derived dendritic cells. Retrovirology. 2015;12(1):2.
30. Duvall MG, Lore K, Blaak H, Ambrozak DA, Adams WC, Santos K, et al. Dendritic cells are less susceptible to human immunodeficiency virus type 2 (HIV-2) infection than to HIV-1 infection. J Virol. 2007;81(24):13486–98. 17913821
31. Rasaiyaah J, Tan CP, Fletcher AJ, Price AJ, Blondeau C, Hilditch L, et al. HIV-1 evades innate immune recognition through specific cofactor recruitment. Nature. 2013;503(7476):402–5. doi: 10.1038/nature12769 24196705
32. Posch W, Cardinaud S, Hamimi C, Fletcher A, Muhlbacher A, Loacker K, et al. Antibodies attenuate the capacity of dendritic cells to stimulate HIV-specific cytotoxic T lymphocytes. J Allergy Clin Immunol. 2012;130(6):1368–74 e2. doi: 10.1016/j.jaci.2012.08.025 23063584
33. Stoiber H, Pinter C, Siccardi AG, Clivio A, Dierich MP, Efficient destruction of human immunodeficiency virus in human serum by inhibiting the protective action of complement factor H and decay accelerating factor (DAF, CD55). J Exp Med. 1996;183(1):307–10. 8551237
34. Frank I, Stoiber H, Godar S, Stockinger H, Steindl F, Katinger HW, et al. Acquisition of host cell-surface-derived molecules by HIV-1. AIDS. 1996;10(14):1611–20. 8970680
35. Stoiber H, Thielens NM, Ebenbichler C, Arlaud GJ, Dierich MP, The envelope glycoprotein of HIV-1 gp120 and human complement protein C1q bind to the same peptides derived from three different regions of gp41, the transmembrane glycoprotein of HIV-1, and share antigenic homology. Eur J Immunol. 1994;24(2):294–300. 7507842
36. Doncel GF, Joseph T, Thurman AR, Role of semen in HIV-1 transmission: inhibitor or facilitator? Am J Reprod Immunol. 2011;65(3):292–301. doi: 10.1111/j.1600-0897.2010.00931.x 21087339
37. Willey S, Aasa-Chapman MM, Humoral immunity to HIV-1: neutralisation and antibody effector functions. Trends Microbiol. 2008;16(12):596–604. doi: 10.1016/j.tim.2008.08.008 18964020
38. Posch W, Pfaller K, Lass-Florl C, Wilflingseder D, The viral make-up makes a world of difference. AIDS Res Hum Retroviruses. 2014;30(7):642–3. doi: 10.1089/aid.2014.0061 24984236
39. Bloch N, O'Brien M, Norton TD, Polsky SB, Bhardwaj N, Landau NR, HIV Type 1 Infection of Plasmacytoid and Myeloid Dendritic Cells Is Restricted by High Levels of SAMHD1 and Cannot be Counteracted by Vpx. AIDS Res Hum Retroviruses. 2013.
40. Puigdomenech I, Casartelli N, Porrot F, Schwartz O, SAMHD1 restricts HIV-1 cell-to-cell transmission and limits immune detection in monocyte-derived dendritic cells. J Virol. 2013;87(5):2846–56. doi: 10.1128/JVI.02514-12 23269793
41. Brandariz-Nunez A, Valle-Casuso JC, White TE, Laguette N, Benkirane M, Brojatsch J, et al. Role of SAMHD1 nuclear localization in restriction of HIV-1 and SIVmac. Retrovirology. 2012;9:49. doi: 10.1186/1742-4690-9-49 22691373
42. Sze A, Olagnier D, Lin R, van Grevenynghe J, Hiscott J, SAMHD1 host restriction factor: a link with innate immune sensing of retrovirus infection. J Mol Biol. 2013;425(24):4981–94. doi: 10.1016/j.jmb.2013.10.022 24161438
43. Bajtay Z, Speth C, Erdei A, Dierich MP, Cutting edge: productive HIV-1 infection of dendritic cells via complement receptor type 3 (CR3, CD11b/CD18). J Immunol. 2004;173(8):4775–8. 15470016
44. Bouhlal H, Chomont N, Requena M, Nasreddine N, Saidi H, Legoff J, et al. Opsonization of HIV with complement enhances infection of dendritic cells and viral transfer to CD4 T cells in a CR3 and DC-SIGN-dependent manner. J Immunol. 2007;178(2):1086–95. 17202372
45. Tjomsland V, Ellegard R, Kjolhede P, Wodlin NB, Hinkula J, Lifson JD, et al. Blocking of integrins inhibits HIV-1 infection of human cervical mucosa immune cells with free and complement-opsonized virions. Eur J Immunol. 2013;43(9):2361–72. doi: 10.1002/eji.201243257 23686382
46. Moris A, Nobile C, Buseyne F, Porrot F, Abastado JP, Schwartz O, DC-SIGN promotes exogenous MHC-I-restricted HIV-1 antigen presentation. Blood. 2004;103(7):2648–54. 14576049
47. Turville SG, Santos JJ, Frank I, Cameron PU, Wilkinson J, Miranda-Saksena M, et al. Immunodeficiency virus uptake, turnover, and 2-phase transfer in human dendritic cells. Blood. 2004;103(6):2170–9. 14630806
48. Nobile C, Petit C, Moris A, Skrabal K, Abastado JP, Mammano F, et al. Covert human immunodeficiency virus replication in dendritic cells and in DC-SIGN-expressing cells promotes long-term transmission to lymphocytes. J Virol. 2005;79(9):5386–99. 15827153
49. Ellegard R, Crisci E, Burgener A, Sjowall C, Birse K, Westmacott G, et al. Complement Opsonization of HIV-1 Results in Decreased Antiviral and Inflammatory Responses in Immature Dendritic Cells via CR3. J Immunol. 2014;193(9):4590–601. doi: 10.4049/jimmunol.1401781 25252956
50. Sato M, Suemori H, Hata N, Asagiri M, Ogasawara K, Nakao K, et al. Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-alpha/beta gene induction. Immunity. 2000;13(4):539–48. 11070172
51. Su B, Lederle A, Laumond G, Ducloy C, Schmidt S, Decoville T, et al. Broadly neutralizing antibody VRC01 prevents HIV-1 transmission from plasmacytoid dendritic cells to CD4 T lymphocytes. J Virol. 2014;88(18):10975–81. doi: 10.1128/JVI.01748-14 24965460
52. Su B, Biedma ME, Lederle A, Peressin M, Lambotin M, Proust A, et al. Dendritic cell-lymphocyte cross talk downregulates host restriction factor SAMHD1 and stimulates HIV-1 replication in dendritic cells. J Virol. 2014;88(9):5109–21. doi: 10.1128/JVI.03057-13 24574390
53. Tjomsland V, Ellegard R, Burgener A, Mogk K, Che KF, Westmacott G, et al. Complement opsonization of HIV-1 results in a different intracellular processing pattern and enhanced MHC class I presentation by dendritic cells. Eur J Immunol. 2013;43(6):1470–83. doi: 10.1002/eji.201242935 23526630
54. Moris A, Pajot A, Blanchet F, Guivel-Benhassine F, Salcedo M, Schwartz O, Dendritic cells and HIV-specific CD4+ T cells: HIV antigen presentation, T-cell activation, and viral transfer. Blood. 2006;108(5):1643–51. 16675708
55. Rodriguez-Plata MT, Urrutia A, Cardinaud S, Buzon MJ, Izquierdo-Useros N, Prado JG, et al. HIV-1 capture and antigen presentation by dendritic cells: enhanced viral capture does not correlate with better T cell activation. J Immunol. 2012;188(12):6036–45. doi: 10.4049/jimmunol.1200267 22581857
56. Geuenich S, Goffinet C, Venzke S, Nolkemper S, Baumann I, Plinkert P, et al. Aqueous extracts from peppermint, sage and lemon balm leaves display potent anti-HIV-1 activity by increasing the virion density. Retrovirology. 2008;5:27. doi: 10.1186/1742-4690-5-27 18355409
57. Sunseri N, O'Brien M, Bhardwaj N, Landau NR, Human immunodeficiency virus type 1 modified to package Simian immunodeficiency virus Vpx efficiently infects macrophages and dendritic cells. J Virol. 2011;85(13):6263–74. doi: 10.1128/JVI.00346-11 21507971
58. Purtscher M, Trkola A, Gruber G, Buchacher A, Predl R, Steindl F, et al. A broadly neutralizing human monoclonal antibody against gp41 of human immunodeficiency virus type 1. AIDS Res Hum Retroviruses. 1994;10(12):1651–8. 7888224
59. Garcia E, Pion M, Pelchen-Matthews A, Collinson L, Arrighi JF, Blot G, et al. HIV-1 trafficking to the dendritic cell-T-cell infectious synapse uses a pathway of tetraspanin sorting to the immunological synapse. Traffic. 2005;6(6):488–501. 15882445
60. Bustin SA, Benes V, Nolan T, Pfaffl MW, Quantitative real-time RT-PCR—a perspective. J Mol Endocrinol. 2005;34(3):597–601. 15956331
61. Casartelli N, Guivel-Benhassine F, Bouziat R, Brandler S, Schwartz O, Moris A, The antiviral factor APOBEC3G improves CTL recognition of cultured HIV-infected T cells. J Exp Med. 2010;207(1):39–49. doi: 10.1084/jem.20091933 20038599