HIV/SIV Infection Primes Monocytes and Dendritic Cells for Apoptosis


Subversion or exacerbation of antigen-presenting cells (APC) death modulates host/pathogen equilibrium. We demonstrated during in vitro differentiation of monocyte-derived macrophages and monocyte-derived dendritic cells (DCs) that HIV sensitizes the cells to undergo apoptosis in response to TRAIL and FasL, respectively. In addition, we found that HIV-1 increased the levels of pro-apoptotic Bax and Bak molecules and decreased the levels of anti-apoptotic Mcl-1 and FLIP proteins. To assess the relevance of these observations in the context of an experimental model of HIV infection, we investigated the death of APC during pathogenic SIV-infection in rhesus macaques (RMs). We demonstrated increased apoptosis, during the acute phase, of both peripheral blood DCs and monocytes (CD14+) from SIV+RMs, associated with a dysregulation in the balance of pro- and anti-apoptotic molecules. Caspase-inhibitor and death receptors antagonists prevented apoptosis of APCs from SIV+RMs. Furthermore, increased levels of FasL in the sera of pathogenic SIV+RMs were detected, compared to non-pathogenic SIV infection of African green monkey. We suggest that inappropriate apoptosis of antigen-presenting cells may contribute to dysregulation of cellular immunity early in the process of HIV/SIV infection.


Vyšlo v časopise: HIV/SIV Infection Primes Monocytes and Dendritic Cells for Apoptosis. PLoS Pathog 7(6): e32767. doi:10.1371/journal.ppat.1002087
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002087

Souhrn

Subversion or exacerbation of antigen-presenting cells (APC) death modulates host/pathogen equilibrium. We demonstrated during in vitro differentiation of monocyte-derived macrophages and monocyte-derived dendritic cells (DCs) that HIV sensitizes the cells to undergo apoptosis in response to TRAIL and FasL, respectively. In addition, we found that HIV-1 increased the levels of pro-apoptotic Bax and Bak molecules and decreased the levels of anti-apoptotic Mcl-1 and FLIP proteins. To assess the relevance of these observations in the context of an experimental model of HIV infection, we investigated the death of APC during pathogenic SIV-infection in rhesus macaques (RMs). We demonstrated increased apoptosis, during the acute phase, of both peripheral blood DCs and monocytes (CD14+) from SIV+RMs, associated with a dysregulation in the balance of pro- and anti-apoptotic molecules. Caspase-inhibitor and death receptors antagonists prevented apoptosis of APCs from SIV+RMs. Furthermore, increased levels of FasL in the sera of pathogenic SIV+RMs were detected, compared to non-pathogenic SIV infection of African green monkey. We suggest that inappropriate apoptosis of antigen-presenting cells may contribute to dysregulation of cellular immunity early in the process of HIV/SIV infection.


Zdroje

1. GordonSTaylorPR 2005 Monocyte and macrophage heterogeneity. Nat Rev Immunol 5 953 964

2. LusterADAlonRvon AndrianUH 2005 Immune cell migration in inflammation: present and future therapeutic targets. Nat Immunol 6 1182 1190

3. GeissmannFManzMGJungSSiewekeMHMeradM 2010 Development of monocytes, macrophages, and dendritic cells. Science 327 656 661

4. PalframanRTJungSChengGWeningerWLuoY 2001 Inflammatory chemokine transport and presentation in HEV: a remote control mechanism for monocyte recruitment to lymph nodes in inflamed tissues. J Exp Med 194 1361 1373

5. LeonBLopez-BravoMArdavinC 2007 Monocyte-derived dendritic cells formed at the infection site control the induction of protective T helper 1 responses against Leishmania. Immunity 26 519 531

6. LeonBArdavinC 2008 Monocyte migration to inflamed skin and lymph nodes is differentially controlled by L-selectin and PSGL-1. Blood 111 3126 3130

7. HoDDRotaTRHirschMS 1986 Infection of monocyte/macrophages by human T lymphotropic virus type III. J Clin Invest 77 1712 1715

8. McElrathMJSteinmanRMCohnZA 1991 Latent HIV-1 infection in enriched populations of blood monocytes and T cells from seropositive patients. J Clin Invest 87 27 30

9. MeyaardLSchuitemakerHMiedemaF 1993 T-cell dysfunction in HIV infection: anergy due to defective antigen-presenting cell function? Immunol Today 14 161 164

10. MeltzerMSSkillmanDRHooverDLHansonBDTurpinJA 1990 Macrophages and the human immunodeficiency virus. Immunol Today 11 217 223

11. EnnenJSeippINorleySGKurthR 1990 Decreased accessory cell function of macrophages after infection with human immunodeficiency virus type 1 in vitro. Eur J Immunol 20 2451 2456

12. Granelli-PipernoAGolebiowskaATrumpfhellerCSiegalFPSteinmanRM 2004 HIV-1-infected monocyte-derived dendritic cells do not undergo maturation but can elicit IL-10 production and T cell regulation. Proc Natl Acad Sci U S A 101 7669 7674

13. Smed-SorensenALoreKWalther-JallowLAnderssonJSpetzAL 2004 HIV-1-infected dendritic cells up-regulate cell surface markers but fail to produce IL-12 p70 in response to CD40 ligand stimulation. Blood 104 2810 2817

14. TaoufikYLantzOWallonCCharlesADussaixE 1997 Human immunodeficiency virus gp120 inhibits interleukin-12 secretion by human monocytes: an indirect interleukin-10-mediated effect. Blood 89 2842 2848

15. HurtrelBPetitFArnoultDMuller-TrutwinMSilvestriG 2005 Apoptosis in SIV infection. Cell Death Differ 12 Suppl 1 979 990

16. EstaquierJIdziorekTZouWEmilieDFarberCM 1995 T helper type 1/T helper type 2 cytokines and T cell death: preventive effect of interleukin 12 on activation-induced and CD95 (FAS/APO-1)-mediated apoptosis of CD4+ T cells from human immunodeficiency virus-infected persons. J Exp Med 182 1759 1767

17. KatsikisPDWunderlichESSmithCAHerzenbergLA 1995 Fas antigen stimulation induces marked apoptosis of T lymphocytes in human immunodeficiency virus-infected individuals. J Exp Med 181 2029 2036

18. FinkelTHTudor-WilliamsGBandaNKCottonMFCurielT 1995 Apoptosis occurs predominantly in bystander cells and not in productively infected cells of HIV- and SIV-infected lymph nodes. Nat Med 1 129 134

19. EstaquierJTanakaMSudaTNagataSGolsteinP 1996 Fas-mediated apoptosis of CD4+ and CD8+ T cells from human immunodeficiency virus-infected persons: differential in vitro preventive effect of cytokines and protease antagonists. Blood 87 4959 4966

20. MuellerYMDe RosaSCHuttonJAWitekJRoedererM 2001 Increased CD95/Fas-induced apoptosis of HIV-specific CD8(+) T cells. Immunity 15 871 882

21. ArnoultDPetitFLelievreJDLecossierDHanceA 2003 Caspase-dependent and -independent T-cell death pathways in pathogenic simian immunodeficiency virus infection: relationship to disease progression. Cell Death Differ 10 1240 1252

22. MonceauxVEstaquierJFevrierMCumontMCRiviereY 2003 Extensive apoptosis in lymphoid organs during primary SIV infection predicts rapid progression towards AIDS. AIDS 17 1585 1596

23. SilvestriGSodoraDLKoupRAPaiardiniMO'NeilSP 2003 Nonpathogenic SIV infection of sooty mangabeys is characterized by limited bystander immunopathology despite chronic high-level viremia. Immunity 18 441 452

24. LiQDuanLEstesJDMaZMRourkeT 2005 Peak SIV replication in resting memory CD4+ T cells depletes gut lamina propria CD4+ T cells. Nature 434 1148 1152

25. ViolletLMonceauxVPetitFHo Tsong FangRCumontMC 2006 Death of CD4+ T cells from lymph nodes during primary SIVmac251 infection predicts the rate of AIDS progression. J Immunol 177 6685 6694

26. EstaquierJLelievreJDPetitFBrunnerTMoutouh-De ParsevalL 2002 Effects of antiretroviral drugs on human immunodeficiency virus type 1-induced CD4(+) T-cell death. J Virol 76 5966 5973

27. LelievreJDPetitFArnoultDAmeisenJCEstaquierJ 2005 Interleukin 7 increases human immunodeficiency virus type 1 LAI-mediated Fas-induced T-cell death. J Virol 79 3195 3199

28. ManganDFWahlSM 1991 Differential regulation of human monocyte programmed cell death (apoptosis) by chemotactic factors and pro-inflammatory cytokines. J Immunol 147 3408 3412

29. ManganDFWelchGRWahlSM 1991 Lipopolysaccharide, tumor necrosis factor-alpha, and IL-1 beta prevent programmed cell death (apoptosis) in human peripheral blood monocytes. J Immunol 146 1541 1546

30. KitajimaTCaceres-DittmarGTapiaFJJesterJBergstresserPR 1996 T cell-mediated terminal maturation of dendritic cells: loss of adhesive and phagocytotic capacities. J Immunol 157 2340 2347

31. PerlmanHPagliariLJGeorganasCManoTWalshK 1999 FLICE-inhibitory protein expression during macrophage differentiation confers resistance to fas-mediated apoptosis. J Exp Med 190 1679 1688

32. RescignoMPiguetVValzasinaBLensSZublerR 2000 Fas engagement induces the maturation of dendritic cells (DCs), the release of interleukin (IL)-1beta, and the production of interferon gamma in the absence of IL-12 during DC-T cell cognate interaction: a new role for Fas ligand in inflammatory responses. J Exp Med 192 1661 1668

33. LeverkusMWalczakHMcLellanAFriesHWTerbeckG 2000 Maturation of dendritic cells leads to up-regulation of cellular FLICE-inhibitory protein and concomitant down-regulation of death ligand-mediated apoptosis. Blood 96 2628 2631

34. IrmlerMThomeMHahneMSchneiderPHofmannK 1997 Inhibition of death receptor signals by cellular FLIP. Nature 388 190 195

35. KienerPADavisPMStarlingGCMehlinCKlebanoffSJ 1997 Differential induction of apoptosis by Fas-Fas ligand interactions in human monocytes and macrophages. J Exp Med 185 1511 1516

36. KikuchiHIizukaRSugiyamaSGonGMoriH 1996 Monocytic differentiation modulates apoptotic response to cytotoxic anti-Fas antibody and tumor necrosis factor alpha in human monoblast U937 cells. J Leukoc Biol 60 778 783

37. Dang-VuAPPisetskyDSWeinbergJB 1987 Functional alterations of macrophages in autoimmune MRL-lpr/lpr mice. J Immunol 138 1757 1761

38. MarriottHMBingleCDReadRCBraleyKEKroemerG 2005 Dynamic changes in Mcl-1 expression regulate macrophage viability or commitment to apoptosis during bacterial clearance. J Clin Invest 115 359 368

39. DesagherSMartinouJC 2000 Mitochondria as the central control point of apoptosis. Trends Cell Biol 10 369 377

40. KeaneJBalcewicz-SablinskaMKRemoldHGChuppGLMeekBB 1997 Infection by Mycobacterium tuberculosis promotes human alveolar macrophage apoptosis. Infect Immun 65 298 304

41. KremerLEstaquierJBrandtEAmeisenJCLochtC 1997 Mycobacterium bovis Bacillus Calmette Guerin infection prevents apoptosis of resting human monocytes. Eur J Immunol 27 2450 2456

42. OddoMRennoTAttingerABakkerTMacDonaldHR 1998 Fas ligand-induced apoptosis of infected human macrophages reduces the viability of intracellular Mycobacterium tuberculosis. J Immunol 160 5448 5454

43. OrlofskyASomogyiRDWeissLMPrystowskyMB 1999 The murine antiapoptotic protein A1 is induced in inflammatory macrophages and constitutively expressed in neutrophils. J Immunol 163 412 419

44. YrlidUWickMJ 2000 Salmonella-induced apoptosis of infected macrophages results in presentation of a bacteria-encoded antigen after uptake by bystander dendritic cells. J Exp Med 191 613 624

45. Servet-DelpratCVidalainPOAzocarOLe DeistFFischerA 2000 Consequences of Fas-mediated human dendritic cell apoptosis induced by measles virus. J Virol 74 4387 4393

46. AkaridKArnoultDMicic-PolianskiJSifJEstaquierJ 2004 Leishmania major-mediated prevention of programmed cell death induction in infected macrophages is associated with the repression of mitochondrial release of cytochrome c. J Leukoc Biol 76 95 103

47. GuptaMSpiropoulouCRollinPE 2007 Ebola virus infection of human PBMCs causes massive death of macrophages, CD4 and CD8 T cell sub-populations in vitro. Virology 364 45 54

48. HouWSoEYKimBS 2007 Role of dendritic cells in differential susceptibility to viral demyelinating disease. PLoS Pathog 3 e124

49. RescignoMMartinoMSutherlandCLGoldMRRicciardi-CastagnoliP 1998 Dendritic cell survival and maturation are regulated by different signaling pathways. J Exp Med 188 2175 2180

50. AshanyDSavirABhardwajNElkonKB 1999 Dendritic cells are resistant to apoptosis through the Fas (CD95/APO-1) pathway. J Immunol 163 5303 5311

51. KoppiTATough-BementTLewinsohnDMLynchDHAldersonMR 1997 CD40 ligand inhibits Fas/CD95-mediated apoptosis of human blood-derived dendritic cells. Eur J Immunol 27 3161 3165

52. OuaazFArronJZhengYChoiYBegAA 2002 Dendritic cell development and survival require distinct NF-kappaB subunits. Immunity 16 257 270

53. SwinglerSMannAMZhouJSwinglerCStevensonM 2007 Apoptotic killing of HIV-1-infected macrophages is subverted by the viral envelope glycoprotein. PLoS Pathog 3 1281 1290

54. CuiMHuangYZhaoYZhengJ 2008 Transcription factor FOXO3a mediates apoptosis in HIV-1-infected macrophages. J Immunol 180 898 906

55. PacanowskiJKahiSBailletMLebonPDeveauC 2001 Reduced blood CD123+ (lymphoid) and CD11c+ (myeloid) dendritic cell numbers in primary HIV-1 infection. Blood 98 3016 3021

56. KamgaIKahiSDeveliogluLLichtnerMMaranonC 2005 Type I interferon production is profoundly and transiently impaired in primary HIV-1 infection. J Infect Dis 192 303 310

57. DonaghyHPozniakAGazzardBQaziNGilmourJ 2001 Loss of blood CD11c(+) myeloid and CD11c(–) plasmacytoid dendritic cells in patients with HIV-1 infection correlates with HIV-1 RNA virus load. Blood 98 2574 2576

58. FeldmanSSteinDAmruteSDennyTGarciaZ 2001 Decreased interferon-alpha production in HIV-infected patients correlates with numerical and functional deficiencies in circulating type 2 dendritic cell precursors. Clin Immunol 101 201 210

59. GrassiFHosmalinAMcIlroyDCalvezVDebreP 1999 Depletion in blood CD11c-positive dendritic cells from HIV-infected patients. AIDS 13 759 766

60. BarronMABlyveisNPalmerBEMaWhinneySWilsonCC 2003 Influence of plasma viremia on defects in number and immunophenotype of blood dendritic cell subsets in human immunodeficiency virus 1-infected individuals. J Infect Dis 187 26 37

61. ChehimiJCampbellDEAzzoniLBachellerDPapasavvasE 2002 Persistent decreases in blood plasmacytoid dendritic cell number and function despite effective highly active antiretroviral therapy and increased blood myeloid dendritic cells in HIV-infected individuals. J Immunol 168 4796 4801

62. BrownKNTrichelABarratt-BoyesSM 2007 Parallel loss of myeloid and plasmacytoid dendritic cells from blood and lymphoid tissue in simian AIDS. J Immunol 178 6958 6967

63. BrownKNWijewardanaVLiuXBarratt-BoyesSM 2009 Rapid influx and death of plasmacytoid dendritic cells in lymph nodes mediate depletion in acute simian immunodeficiency virus infection. PLoS Pathog 5 e1000413

64. MeyersJHJustementJSHallahanCWBlairETSunYA 2007 Impact of HIV on cell survival and antiviral activity of plasmacytoid dendritic cells. PLoS ONE 2 e458

65. HasegawaALiuHLingBBordaJTAlvarezX 2009 The level of monocyte turnover predicts disease progression in the macaque model of AIDS. Blood 114 2917 2925

66. AlhetheelAYakubtsovYAbdkaderKSantNDiaz-MitomaF 2008 Amplification of the signal transducer and activator of transcription I signaling pathway and its association with apoptosis in monocytes from HIV-infected patients. AIDS 22 1137 1144

67. GiriMSNebozyhnMRaymondAGekongeBHancockA 2009 Circulating monocytes in HIV-1-infected viremic subjects exhibit an antiapoptosis gene signature and virus- and host-mediated apoptosis resistance. J Immunol 182 4459 4470

68. DeeksSGKitchenCMLiuLGuoHGasconR 2004 Immune activation set point during early HIV infection predicts subsequent CD4+ T-cell changes independent of viral load. Blood 104 942 947

69. MonceauxVViolletLPetitFHo Tsong FangRCumontMC 2005 CD8+ T cell dynamics during primary simian immunodeficiency virus infection in macaques: relationship of effector cell differentiation with the extent of viral replication. J Immunol 174 6898 6908

70. CumontMCDiopOVaslinBElbimCViolletL 2008 Early divergence in lymphoid tissue apoptosis between pathogenic and nonpathogenic simian immunodeficiency virus infections of nonhuman primates. J Virol 82 1175 1184

71. ElbimCMonceauxVFrancoisSHurtrelBGougerot-PocidaloMA 2009 Increased neutrophil apoptosis in chronically SIV-infected macaques. Retrovirology 6 29

72. SchuitemakerHKootstraNAFouchierRAHooibrinkBMiedemaF 1994 Productive HIV-1 infection of macrophages restricted to the cell fraction with proliferative capacity. EMBO J 13 5929 5936

73. GartnerSMarkovitsPMarkovitzDMKaplanMHGalloRC 1986 The role of mononuclear phagocytes in HTLV-III/LAV infection. Science 233 215 219

74. GendelmanHEOrensteinJMMartinMAFerruaCMitraR 1988 Efficient isolation and propagation of human immunodeficiency virus on recombinant colony-stimulating factor 1-treated monocytes. J Exp Med 167 1428 1441

75. PernoCFYarchoanRCooneyDAHartmanNRWebbDS 1989 Replication of human immunodeficiency virus in monocytes. Granulocyte/macrophage colony-stimulating factor (GM-CSF) potentiates viral production yet enhances the antiviral effect mediated by 3′-azido-2′3′-dideoxythymidine (AZT) and other dideoxynucleoside congeners of thymidine. J Exp Med 169 933 951

76. TomkowiczBLeeCRavynVCheungRPtasznikA 2006 The Src kinase Lyn is required for CCR5 signaling in response to MIP-1beta and R5 HIV-1 gp120 in human macrophages. Blood 108 1145 1150

77. CheungRRavynVWangLPtasznikACollmanRG 2008 Signaling mechanism of HIV-1 gp120 and virion-induced IL-1beta release in primary human macrophages. J Immunol 180 6675 6684

78. SappMEngelmayerJLarssonMGranelli-PipernoASteinmanR 1999 Dendritic cells generated from blood monocytes of HIV-1 patients are not infected and act as competent antigen presenting cells eliciting potent T-cell responses. Immunol Lett 66 121 128

79. ArnoultDPetitFLelievreJDEstaquierJ 2003 Mitochondria in HIV-1-induced apoptosis. Biochem Biophys Res Commun 304 561 574

80. PeterMEBuddRCDesbaratsJHedrickSMHueberAO 2007 The CD95 receptor: apoptosis revisited. Cell 129 447 450

81. MaurerUCharvetCWagmanASDejardinEGreenDR 2006 Glycogen synthase kinase-3 regulates mitochondrial outer membrane permeabilization and apoptosis by destabilization of MCL-1. Mol Cell 21 749 760

82. OpfermanJTIwasakiHOngCCSuhHMizunoS 2005 Obligate role of anti-apoptotic MCL-1 in the survival of hematopoietic stem cells. Science 307 1101 1104

83. DominaAMVranaJAGregoryMAHannSRCraigRW 2004 MCL1 is phosphorylated in the PEST region and stabilized upon ERK activation in viable cells, and at additional sites with cytotoxic okadaic acid or taxol. Oncogene 23 5301 5315

84. HerrantMJacquelAMarchettiSBelhaceneNColosettiP 2004 Cleavage of Mcl-1 by caspases impaired its ability to counteract Bim-induced apoptosis. Oncogene 23 7863 7873

85. HanJGoldsteinLAGastmanBRFroelichCJYinXM 2004 Degradation of Mcl-1 by granzyme B: implications for Bim-mediated mitochondrial apoptotic events. J Biol Chem 279 22020 22029

86. ZhuTMuthuiDHolteSNickleDFengF 2002 Evidence for human immunodeficiency virus type 1 replication in vivo in CD14(+) monocytes and its potential role as a source of virus in patients on highly active antiretroviral therapy. J Virol 76 707 716

87. ChoiYKWheltonKMMlechickBMurphey-CorbMAReinhartTA 2003 Productive infection of dendritic cells by simian immunodeficiency virus in macaque intestinal tissues. J Pathol 201 616 628

88. EstaquierJIdziorekTde BelsFBarre-SinoussiFHurtrelB 1994 Programmed cell death and AIDS: significance of T-cell apoptosis in pathogenic and nonpathogenic primate lentiviral infections. Proc Natl Acad Sci U S A 91 9431 9435

89. ChehimiJPapasavvasETomescuCGekongeBAbdulhaqqS 2010 Inability of plasmacytoid dendritic cells to directly lyse HIV-infected autologous CD4+ T cells despite induction of tumor necrosis factor-related apoptosis-inducing ligand. J Virol 84 2762 2773

90. Campillo-GimenezLCumontMCFayMKaredHMonceauxV 2010 AIDS progression is associated with the emergence of IL-17-producing cells early after simian immunodeficiency virus infection. J Immunol 184 984 992

91. Campillo-GimenezLLaforgeMFayMBrusselACumontMC 2010 Nonpathogenesis of simian immunodeficiency virus infection is associated with reduced inflammation and recruitment of plasmacytoid dendritic cells to lymph nodes, not to lack of an interferon type I response, during the acute phase. J Virol 84 1838 1846

92. HerbeuvalJPNilssonJBoassoAHardyAWVaccariM 2009 HAART reduces death ligand but not death receptors in lymphoid tissue of HIV-infected patients and simian immunodeficiency virus-infected macaques. AIDS 23 35 40

93. MuellerCCorazzaNTrachsel-LosethSEugsterHPBuhler-JungoM 1999 Noncleavable transmembrane mouse tumor necrosis factor-alpha (TNFalpha) mediates effects distinct from those of wild-type TNFalpha in vitro and in vivo. J Biol Chem 274 38112 38118

94. BorrowPEvansCFOldstoneMB 1995 Virus-induced immunosuppression: immune system-mediated destruction of virus-infected dendritic cells results in generalized immune suppression. J Virol 69 1059 1070

95. Fugier-VivierIServet-DelpratCRivaillerPRissoanMCLiuYJ 1997 Measles virus suppresses cell-mediated immunity by interfering with the survival and functions of dendritic and T cells. J Exp Med 186 813 823

96. ShanMKlassePJBanerjeeKDeyAKIyerSP 2007 HIV-1 gp120 mannoses induce immunosuppressive responses from dendritic cells. PLoS Pathog 3 e169

97. AmeisenJCEstaquierJIdziorekTDe BelsF 1995 The relevance of apoptosis to AIDS pathogenesis. Trends Cell Biol 5 27 32

98. EstaquierJAmeisenJC 1997 A role for T-helper type-1 and type-2 cytokines in the regulation of human monocyte apoptosis. Blood 90 1618 1625

99. BarcelliniWRizzardiGPMarriottJBFainCShattockRJ 1996 Interleukin-10-induced HIV-1 expression is mediated by induction of both membrane-bound tumour necrosis factor (TNF)-alpha and TNF receptor type 1 in a promonocytic cell line. Aids 10 835 842

100. SozzaniSGhezziSIannoloGLuiniWBorsattiA 1998 Interleukin 10 increases CCR5 expression and HIV infection in human monocytes. J Exp Med 187 439 444

101. AlterGKavanaghDRihnSLuteijnRBrooksD 2010 IL-10 induces aberrant deletion of dendritic cells by natural killer cells in the context of HIV infection. J Clin Invest 120 1905 1913

102. BrooksDGWalshKBElsaesserHOldstoneMB 2010 IL-10 directly suppresses CD4 but not CD8 T cell effector and memory responses following acute viral infection. Proc Natl Acad Sci U S A 107 3018 3023

103. AmeisenJCEstaquierJIdziorekT 1994 From AIDS to parasite infection: pathogen-mediated subversion of programmed cell death as a mechanism for immune dysregulation. Immunol Rev 142 9 51

104. ClericiMSarinACoffmanRLWynnTABlattSP 1994 Type 1/type 2 cytokine modulation of T-cell programmed cell death as a model for human immunodeficiency virus pathogenesis. Proc Natl Acad Sci U S A 91 11811 11815

105. EstaquierJZaundersJJ 2010 Cytokines and the pathogenesis of HIV infection. Eur Cytokine Netw 21 195 196

106. KwonDSKaufmannDE 2010 Protective and detrimental roles of IL-10 in HIV pathogenesis. Eur Cytokine Netw 21 208 214

107. EstaquierJBloyCCoralloFPeronCAmeisenJC 1998 The immunomodulating glycoprotein extract from Klebsiella pneumoniae RU 41740 exerts a suppressive effect on human monocyte death by apoptosis. Immunopharmacology 39 157 164

108. FahyRJDoseffAIWewersMD 1999 Spontaneous human monocyte apoptosis utilizes a caspase-3-dependent pathway that is blocked by endotoxin and is independent of caspase-1. J Immunol 163 1755 1762

109. StockingerSMaternaTStoiberDBayrLSteinbornR 2002 Production of type I IFN sensitizes macrophages to cell death induced by Listeria monocytogenes. J Immunol 169 6522 6529

110. LehnerMFelzmannTClodiKHolterW 2001 Type I interferons in combination with bacterial stimuli induce apoptosis of monocyte-derived dendritic cells. Blood 98 736 742

111. BrenchleyJMPriceDASchackerTWAsherTESilvestriG 2006 Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 12 1365 1371

112. DurudasAMilushJMChenHLEngramJCSilvestriG 2009 Elevated levels of innate immune modulators in lymph nodes and blood are associated with more-rapid disease progression in simian immunodeficiency virus-infected monkeys. J Virol 83 12229 12240

113. HosakaNOyaizuNKaplanMHYagitaHPahwaS 1998 Membrane and soluble forms of Fas (CD95) and Fas ligand in peripheral blood mononuclear cells and in plasma from human immunodeficiency virus-infected persons. J Infect Dis 178 1030 1039

114. SilvestrisFCamardaGCafforioPDammaccoF 1998 Upregulation of Fas ligand secretion in non-lymphopenic stages of HIV-1 infection. AIDS 12 1103 1104

115. HerbeuvalJPHardyAWBoassoAAndersonSADolanMJ 2005 Regulation of TNF-related apoptosis-inducing ligand on primary CD4+ T cells by HIV-1: role of type I IFN-producing plasmacytoid dendritic cells. Proc Natl Acad Sci U S A 102 13974 13979

116. Gasper-SmithNCrossmanDMWhitesidesJFMensaliNOttingerJS 2008 Induction of plasma (TRAIL), TNFR-2, Fas ligand, and plasma microparticles after human immunodeficiency virus type 1 (HIV-1) transmission: implications for HIV-1 vaccine design. J Virol 82 7700 7710

117. Ziegler-HeitbrockLAncutaPCroweSDalodMGrauV 2010 Nomenclature of monocytes and dendritic cells in blood. Blood 116 74 80

118. PetitFArnoultDViolletLEstaquierJ 2003 Intrinsic and extrinsic pathways signaling during HIV-1 mediated cell death. Biochimie 85 795 811

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Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

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