Immune suppression by myeloid cells in HIV infection: New targets for immunotherapy

Open AIDS Journal

Volumn 8, Issue 1, 2015, Pages 66-78

  Mehraj, Vikram ^a   Jenabian, Mohammad Ali ^b   Vyboh, Kishanda ^a   Routy, Jean Pierre ^a  

^a MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b UNIVERSITÉ DU QUÉBEC À MONTRÉAL   (Canada)

Author keywords

Dendritic cells (DCs); HIV; Immunotherapy; Macrophages; Monocytes; Myeloid derived suppressor cells; Neutrophils

Indexed keywords

ALPHA INTERFERON; CD14 ANTIGEN; CD15 ANTIGEN; CD16 ANTIGEN; CD4 ANTIGEN; CD57 ANTIGEN; CD68 ANTIGEN; CD8 ANTIGEN; CHEMOKINE RECEPTOR CCR5; GAMMA INTERFERON; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 15; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 6; KYNURENINE; L SELECTIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; PROGRAMMED DEATH 1 RECEPTOR; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TRYPTOPHAN; TUMOR NECROSIS FACTOR ALPHA; UNINDEXED DRUG;

ARTICLE; BONE MARROW CELL; CELL CYCLE REGULATION; CELL PROLIFERATION; CLINICAL TRIAL (TOPIC); COXIELLA BURNETII; CYTOMEGALOVIRUS; DENDRITIC CELL; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNIZATION; IMMUNOLOGICAL SYNAPSE; IMMUNOSUPPRESSIVE TREATMENT; IMMUNOTHERAPY; IN SITU HYBRIDIZATION; MACROPHAGE; MONOCYTE; NEUTROPENIA; NEUTROPHIL; PATHOGENESIS; PERSISTENT VIRUS INFECTION; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; STAPHYLOCOCCUS AUREUS; VACCINATION; VIRUS TRANSMISSION;

EID: 84923351469     PISSN: None     EISSN: 18746136     Source Type: Journal    
DOI: 10.2174/1874613601408010066     Document Type: Article

References (138)

1. Maartens G, Celum C, Lewin SR. HIV infection: epidemiology, pathogenesis, treatment, and prevention. Lancet 2014; 384(9939): 258-71.
2. UNAIDS report on the global AIDS epidemic 2013. Geneva, Switzerland: UNAIDS, 2013 November. Report No.: ISBN 978-92-9253-032-7 Contract No.: JC2502/1/E.
3. Royce RA, Sena A, Cates W, Jr., Cohen MS. Sexual transmission of HIV. N Engl J Med 1997; 336(15): 1072-8.
4. Deeks SG, Autran B, Berkhout B, et al. Towards an HIV cure: a global scientific strategy. Nat Rev Immunol 2012; 12(8): 607-14.
5. Deeks SG, Lewin SR, Havlir DV. The end of AIDS: HIV infection as a chronic disease. Lancet 2013; 382(9903): 1525-33.
6. Aggarwal A, McAllery S, Turville SG. Revising the Role of Myeloid cells in HIV Pathogenesis. Curr HIV/AIDS Rep 2013; 10(1): 3-11.
7. Schlaepfer E, Rochat MA, Duo L, Speck RF. Triggering TLR2, -3, -4, -5, and -8 Reinforces the restrictive nature of M1- and M2-Polarized Macrophages to HIV. J Virol 2014; 88(17): 9769-81.
8. Bowers NL, Helton ES, Huijbregts RP, Goepfert PA, Heath SL, Hel Z. Immune suppression by neutrophils in HIV-1 infection: role of PD-L1/PD-1 pathway. PLoS Pathog 2014; 10(3): e1003993.
9. Anzinger JJ, Butterfield TR, Angelovich TA, Crowe SM, Palmer CS. Monocytes as regulators of inflammation and HIV-related comorbidities during cART. J Immunol Res 2014; 2014: 11.
10. Katsura Y. Redefinition of lymphoid progenitors. Nat Rev Immunol 2002; 2(2): 127-32.
11. Mogensen TH. Pathogen recognition and inflammatory signaling in innate immune defenses. Clin Microbiol Rev 2009; 22(2): 240-73, Table of Contents.
12. Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 2010; 11(5): 373-84.
13. Chang JJ, Lacas A, Lindsay RJ, et al. Differential regulation of toll-like receptor pathways in acute and chronic HIV-1 infection. AIDS 2012; 26(5): 533-41.
14. Cohen OJ, Kinter A, Fauci AS. Host factors in the pathogenesis of HIV disease. Immunologic Rev 1997; 159: 31-48.
15. Ahmad A, Ahmad R, Iannello A, Toma E, Morisset R, Sindhu ST. IL-15 and HIV infection: lessons for immunotherapy and vaccination. Curr HIV Res 2005; 3(3): 261-70.
16. Collman RG, Perno CF, Crowe SM, Stevenson M, Montaner LJ. HIV and cells of macrophage/dendritic lineage and other non-T cell reservoirs: new answers yield new questions. J Leukocyte Biol 2003; 74(5): 631-4.
17. Dion ML, Poulin JF, Bordi R, et al. HIV infection rapidly induces and maintains a substantial suppression of thymocyte proliferation. Immunity 2004; 21(6): 757-68.
18. Alimonti JB, Ball TB, Fowke KR. Mechanisms of CD4+ T lymphocyte cell death in human immunodeficiency virus infection and AIDS. J Gen Virol 2003; 84(Pt 7): 1649-61.
19. Doitsh G, Galloway NL, Geng X, et al. Cell death by pyroptosis drives CD4 T-cell depletion in HIV-1 infection. Nature 2014; 505(7484): 509-14.
20. Kepp O, Galluzzi L, Zitvogel L, Kroemer G. Pyroptosis - a cell death modality of its kind? Eur J Immunol 2010; 40(3): 627-30.
21. Kedzierska K, Crowe SM. Cytokines and HIV-1: interactions and clinical implications. Antiviral Chem Chemother 2001; 12(3): 133-50.
22. Wolbers M, Babiker A, Sabin C, et al. Pretreatment CD4 cell slope and progression to AIDS or death in HIV-infected patients initiating antiretroviral therapy--the CASCADE collaboration: a collaboration of 23 cohort studies. PLoS Med 2010; 7(2): e1000239.
23. Brenchley JM, Schacker TW, Ruff LE, et al. CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med 2004; 200(6): 749-59.
24. Bixler SL, Mattapallil JJ. Loss and dysregulation of Th17 cells during HIV infection. Clin Dev Immunol 2013; 2013: 852418.
25. Brenchley JM, Douek DC. HIV infection and the gastrointestinal immune system. Mucosal Immunol 2008; 1(1): 23-30.
26. Zeng M, Southern PJ, Reilly CS, et al. Lymphoid tissue damage in HIV-1 infection depletes naive T cells and limits T cell reconstitution after antiretroviral therapy. PLoS Pathog 2012; 8(1): e1002437.
27. Paiardini M, Muller-Trutwin M. HIV-associated chronic immune activation. Immunol Rev 2013; 254(1): 78-101.
28. Mandl JN, Barry AP, Vanderford TH, et al. Divergent TLR7 and TLR9 signaling and type I interferon production distinguish pathogenic and nonpathogenic AIDS virus infections. Nat Med 2008; 14(10): 1077-87.
29. Marchetti G, Tincati C, Silvestri G. Microbial translocation in the pathogenesis of HIV infection and AIDS. Clin Microbiol Rev 2013; 26(1): 2-18.
30. Lederman MM, Funderburg NT, Sekaly RP, Klatt NR, Hunt PW. Residual immune dysregulation syndrome in treated HIV infection. Adv Immunol 2013; 119: 51-83.
31. Deeks SG, Tracy R, Douek DC. Systemic effects of inflammation on health during chronic HIV infection. Immunity 2013; 39(4): 633-45.
32. Nordell AD, McKenna M, Borges AH, Duprez D, Neuhaus J, Neaton JD. Severity of cardiovascular disease outcomes among patients with HIV is related to markers of inflammation and coagulation. J Am Heart Assoc 2014; 3(3): e000844.
33. Buzon MJ, Massanella M, Llibre JM, et al. HIV-1 replication and immune dynamics are affected by raltegravir intensification of HAART-suppressed subjects. Nat Med 2010; 16(4): 460-5.
34. Dalgleish AG, Beverley PC, Clapham PR, Crawford DH, Greaves MF, Weiss RA. The CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus. Nature 1984; 312(5996): 763-7.
35. Kuller LH, Tracy R, Belloso W, et al. Inflammatory and coagulation biomarkers and mortality in patients with HIV infection. PLoS Med 2008; 5(10): e203.
36. Sandler NG, Wand H, Roque A, et al. Plasma levels of soluble CD14 independently predict mortality in HIV infection. J Infect Dis 2011; 203(6): 780-90.
37. Brenchley JM, Price DA, Schacker TW, et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 2006; 12(12): 1365-71.
38. Fournier BM, Parkos CA. The role of neutrophils during intestinal inflammation. Mucosal Immunol 2012; 5(4): 354-66.
39. Deeks SG. HIV infection, inflammation, immunosenescence, and aging. Annu Rev Med 2011; 62: 141-55.
40. Sereti I, Estes JD, Thompson WL, et al. Decreases in colonic and systemic inflammation in chronic HIV infection after IL-7 administration. PLoS Pathog 2014; 10(1): e1003890.
41. Godin-Ethier J, Hanafi LA, Piccirillo CA, Lapointe R. Indoleamine 2,3-dioxygenase expression in human cancers: clinical and immunologic perspectives. Clinical cancer research. J Am Assoc Cancer Res 2011; 17(22): 6985-91.
42. Neurauter G, Zangerle R, Widner B, Quirchmair G, Sarcletti M, Fuchs D. Effective antiretroviral therapy reduces degradation of tryptophan in patients with HIV-1 infection. Adv Exp Med Biol 2003; 527: 317-23.
43. Miwa N, Hayakawa S, Miyazaki S, et al. IDO expression on decidual and peripheral blood dendritic cells and monocytes/macrophages after treatment with CTLA-4 or interferon-gamma increase in normal pregnancy but decrease in spontaneous abortion. Mol Hum Reprod 2005; 11(12): 865-70.
44. Jenabian MA, Patel M, Kema I, et al. Distinct tryptophan catabolism and Th17/Treg balance in HIV progressors and elite controllers. PLoS One 2013; 8(10): e78146.
45. Critchfield JW, Lemongello D, Walker DH, et al. Multifunctional human immunodeficiency virus (HIV) gag-specific CD8+ T-cell responses in rectal mucosa and peripheral blood mononuclear cells during chronic HIV type 1 infection. J Virol 2007; 81(11): 5460-71.
46. Khaitan A, Unutmaz D. Revisiting immune exhaustion during HIV infection. Curr HIV/AIDS Rep 2011; 8(1): 4-11.
47. Breton G, Chomont N, Takata H, et al.Programmed death-1 is a marker for abnormal distribution of naive/memory T cell subsets in HIV-1 infection. J Immunol 2013; 191(5): 2194-204.
48. Day CL, Kaufmann DE, Kiepiela P, et al. PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature 2006; 443(7109): 350-4.
49. Brenchley JM, Karandikar NJ, Betts MR, et al.Expression of CD57 defines replicative senescence and antigen-induced apoptotic death of CD8+ T cells. Blood 2003; 101(7): 2711-20.
50. Said EA, Dupuy FP, Trautmann L, et al. Programmed death-1-induced interleukin-10 production by monocytes impairs CD4+ T cell activation during HIV infection. Nat Med 2010; 16(4): 452-9.
51. Gartner S, Markovits P, Markovitz DM, Kaplan MH, Gallo RC, Popovic M. The role of mononuclear phagocytes in HTLVIII/LAV infection. Science 1986; 233(4760): 215-9.
52. Ho DD, Rota TR, Hirsch MS. Infection of monocyte/macrophages by human T lymphotropic virus type III. J Clin Invest 1986; 77(5): 1712-5.
53. Shen R, Richter HE, Clements RH, et al. Macrophages in vaginal but not intestinal mucosa are monocyte-like and permissive to human immunodeficiency virus type 1 infection. J Virol 2009; 83(7): 3258-67.
54. Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol 2005; 5(12): 953-64.
55. Itano AA, Jenkins MK. Antigen presentation to naive CD4 T cells in the lymph node. Nat Immunol 2003; 4(8): 733-9.
56. Mege JL, Mehraj V, Capo C. Macrophage polarization and bacterial infections. Curr Opin Infect Dis 2011; 24(3): 230-4.
57. Mehraj V, Textoris J, Ben Amara A, et al. Monocyte responses in the context of Q fever: from a static polarized model to a kinetic model of activation. J Infect Dis 2013; 208(6): 942-51.
58. Pollard JW. Trophic macrophages in development and disease. Nat Rev Immunol 2009; 9(4): 259-70.
59. Orkin SH, Zon LI. Hematopoiesis: an evolving paradigm for stem cell biology. Cell 2008; 132(4): 631-44.
60. Enzan H. Electron microscopic studies of macrophages in early human yolk sacs. Acta Pathol Jpn 1986; 36(1): 49-64.
61. Ginhoux F, Jung S. Monocytes and macrophages: developmental pathways and tissue homeostasis. Nat Rev Immunol 2014; 14(6): 392-404.
62. Naito M, Yamamura F, Nishikawa S, Takahashi K. Development, differentiation, and maturation of fetal mouse yolk sac macrophages in cultures. J Leuk Biol 1989; 46(1): 1-10.
63. Ginhoux F, Greter M, Leboeuf M, et al. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 2010; 330(6005): 841-5.
64. Katsumoto A, Lu H, Miranda AS, Ransohoff RM. Ontogeny and functions of central nervous system macrophages. J Immunol 2014; 193(6): 2615-21.
65. Schulz C, Perdiguero GE, Chorro L, et al. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 2012; 336(6077): 86-90.
66. Iannello A, Boulassel MR, Samarani S, et al. HIV-1 causes an imbalance in the production of interleukin-18 and its natural antagonist in HIV-infected individuals: implications for enhanced viral replication. J Infect Dis 2010; 201(4): 608-17.
67. Cassol E, Cassetta L, Alfano M, Poli G. Macrophage polarization and HIV-1 infection. J Leuko Biol 2010; 87(4): 599-608.
68. Cassol E, Cassetta L, Rizzi C, Alfano M, Poli G. M1 and M2a polarization of human monocyte-derived macrophages inhibits HIV-1 replication by distinct mechanisms. J Immunol 2009; 182(10): 6237-46.
69. Gobeil LA, Lodge R, Tremblay MJ. Differential HIV-1 endocytosis and susceptibility to virus infection in human macrophages correlate with cell activation status. J Virol 2012; 86(19): 10399-407.
70. Alexaki A, Liu Y, Wigdahl B. Cellular reservoirs of HIV-1 and their role in viral persistence. Curr HIV Res 2008; 6(5): 388-400.
71. Koppensteiner H, Brack-Werner R, Schindler M. Macrophages and their relevance in Human Immunodeficiency Virus Type I infection. Retrovirology 2012; 9: 82.
72. Harrold SM, Wang G, McMahon DK, et al. Recovery of replication-competent HIV type 1-infected circulating monocytes from individuals receiving antiretroviral therapy. AIDS Res Hum Retrovir 2002; 18(6): 427-34.
73. Innocenti P, Ottmann M, Morand P, Leclercq P, Seigneurin JM. HIV-1 in blood monocytes: frequency of detection of proviral DNA using PCR and comparison with the total CD4 count. AIDS Res Hum Retrovir 1992; 8(2): 261-8.
74. Livingstone WJ, Moore M, Innes D, Bell JE, Simmonds P. Frequent infection of peripheral blood CD8-positive Tlymphocytes with HIV-1. Edinburgh Heterosexual Transmission Study Group. Lancet 1996; 348(9028): 649-54.
75. Patterson BK, Carlo DJ, Kaplan MH, Marecki M, Pawha S, Moss RB. Cell-associated HIV-1 messenger RNA and DNA in T-helper cell and monocytes in asymptomatic HIV-1-infected subjects on HAART plus an inactivated HIV-1 immunogen. AIDS 1999; 13(13): 1607-11.
76. Patterson BK, McCallister S, Schutz M, et al.Persistence of intracellular HIV-1 mRNA correlates with HIV-1-specific immune responses in infected subjects on stable HAART. AIDS 2001; 15(13): 1635-41.
77. McElrath MJ, Steinman RM, Cohn ZA. Latent HIV-1 infection in enriched populations of blood monocytes and T cells from seropositive patients. J Clin Invest 1991; 87(1): 27-30.
78. Ellery PJ, Tippett E, Chiu YL, et al. The CD16+ monocyte subset is more permissive to infection and preferentially harbors HIV-1 in vivo. J Immunol 2007; 178(10): 6581-9.
79. Berger A, Sommer AF, Zwarg J, 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.
80. Ryoo J, Choi J, Oh C, et al. The ribonuclease activity of SAMHD1 is required for HIV-1 restriction. Nat Med 2014; 20(8): 936-41.
81. MacDonald KP, Munster DJ, Clark GJ, Dzionek A, Schmitz J, Hart DN. Characterization of human blood dendritic cell subsets. Blood 2002; 100(13): 4512-20.
82. Schuitemaker H, Kootstra NA, Koppelman MH, et al. Proliferation-dependent HIV-1 infection of monocytes occurs during differentiation into macrophages. J Clin Invest 1992; 89(4): 1154-60.
83. Crowe S, Zhu T, Muller WA. The contribution of monocyte infection and trafficking to viral persistence, and maintenance of the viral reservoir in HIV infection. J Leuko Biol 2003; 74(5): 635-41.
84. Brew BJ, Chan P. Update on HIV Dementia and HIV-Associated Neurocognitive Disorders. Curr Neurol Neurosci Rep 2014; 14(8): 468.
85. Pu H, Tian J, Flora G, et al. HIV-1 Tat protein upregulates inflammatory mediators and induces monocyte invasion into the brain. Mol Cell Neurosci 2003; 24(1): 224-37.
86. Ancuta P, Liu KY, Misra V, et al. Transcriptional profiling reveals developmental relationship and distinct biological functions of CD16+ and CD16- monocyte subsets. BMC Genomics 2009; 10: 403.
87. Niedecken H, Lutz G, Bauer R, Kreysel HW. Langerhans cell as primary target and vehicle for transmission of HIV. Lancet 1987; 2(8557): 519-20.
88. Wu L, KewalRamani VN. Dendritic-cell interactions with HIV: infection and viral dissemination. Nat Rev Immunol 2006; 6(11): 859-68.
89. Lambert AA, Gilbert C, Richard M, Beaulieu AD, Tremblay MJ. The C-type lectin surface receptor DCIR acts as a new attachment factor for HIV-1 in dendritic cells and contributes to trans- and cisinfection pathways. Blood 2008; 112(4): 1299-307.
90. Rinaldo CR. HIV-1 trans infection of CD4(+) T cells by professional antigen presenting cells. Scientifica 2013; 2013: 164203.
91. Steinman RM, Inaba K. Myeloid dendritic cells. J Leuko Biol 1999; 66(2): 205-8.
92. Vyas JM, Van der Veen AG, Ploegh HL. The known unknowns of antigen processing and presentation. Nat Rev Immunol 2008; 8(8): 607-18.
93. Fontaine J, Coutlee F, Tremblay C, Routy JP, Poudrier J, Roger M. HIV infection affects blood myeloid dendritic cells after successful therapy and despite nonprogressing clinical disease. J Infect Dis 2009; 199(7): 1007-18.
94. Chaudhry A, Das SR, Hussain A, et al. The Nef protein of HIV-1 induces loss of cell surface costimulatory molecules CD80 and CD86 in APCs. J Immunol 2005; 175(7): 4566-74.
95. Granelli-Piperno A, Golebiowska A, Trumpfheller C, Siegal FP, Steinman RM. 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 USA 2004; 101(20): 7669-74.
96. Popov S, Chenine AL, Gruber A, Li PL, Ruprecht RM. Long-term productive human immunodeficiency virus infection of CD1asorted myeloid dendritic cells. J Virol 2005; 79(1): 602-8.
97. Levine AM, Karim R, Mack W, et al. Neutropenia in human immunodeficiency virus infection: data from the women's interagency HIV study. Arch Intern Med 2006; 166(4): 405-10.
98. Cloke T, Munder M, Bergin P, et al.Phenotypic alteration of neutrophils in the blood of HIV seropositive patients. PLoS One 2013; 8(9): e72034.
99. Vecchiarelli A, Monari C, Palazzetti B, Bistoni F, Casadevall A. Dysregulation in IL-12 secretion by neutrophils from HIV-infected patients. Clin Exp Immunol 2000; 121(2): 311-9.
100. Kolaczkowska E, Kubes P. Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol 2013; 13(3): 159-75.
101. McNab FW, Berry MP, Graham CM, et al.Programmed death ligand 1 is over-expressed by neutrophils in the blood of patients with active tuberculosis. Eur J Immunol 2011; 41(7): 1941-7.
102. Furci L, Sironi F, Tolazzi M, Vassena L, Lusso P. Alpha-defensins block the early steps of HIV-1 infection: interference with the binding of gp120 to CD4. Blood 2007; 109(7): 2928-35.
103. Demirkhanyan LH, Marin M, Padilla-Parra S, et al.Multifaceted mechanisms of HIV-1 entry inhibition by human alpha-defensin. J Biol Chem 2012; 287(34): 28821-38.
104. Defer MC, Dugas B, Picard O, Damais C. Impairment of circulating lactoferrin in HIV-1 infection. Cell Mol Biol (Noisy-legrand) 1995; 41(3): 417-21.
105. D'Agostino C, Lichtner M, Mastroianni CM, et al. In vivo release of alpha-defensins in plasma, neutrophils and CD8 T-lymphocytes of patients with HIV infection. Curr HIV Res 2009; 7(6): 650-5.
106. Yang D, Chen Q, Chertov O, Oppenheim JJ. Human neutrophil defensins selectively chemoattract naive T and immature dendritic cells. J Leuk Biol 2000; 68(1): 9-14.
107. Mohan T, Sharma C, Bhat AA, Rao DN. Modulation of HIV peptide antigen specific cellular immune response by synthetic alpha- and beta-defensin peptides. Vaccine 2013; 31(13): 1707-16.
108. Brinkmann V, Reichard U, Goosmann C, et al. Neutrophil extracellular traps kill bacteria. Science 2004; 303(5663): 1532-5.
109. Gabali AM, Anzinger JJ, Spear GT, Thomas LL. Activation by inflammatory stimuli increases neutrophil binding of human immunodeficiency virus type 1 and subsequent infection of lymphocytes. J Virol 2004; 78(19): 10833-6.
110. Casulli S, Elbim C. Interactions between human immunodeficiency virus type 1 and polymorphonuclear neutrophils. J Innate Immun 2014; 6(1): 13-20.
111. Kamp VM, Pillay J, Lammers JW, Pickkers P, Ulfman LH, Koenderman L. Human suppressive neutrophils CD16bright/CD62Ldim exhibit decreased adhesion. J Leuk Biol 2012; 92(5): 1011-20.
112. Cloke T, Munder M, Taylor G, Muller I, Kropf P. Characterization of a novel population of low-density granulocytes associated with disease severity in HIV-1 infection. PLoS One 2012; 7(11): e48939.
113. Beyrau M, Bodkin JV, Nourshargh S. Neutrophil heterogeneity in health and disease: a revitalized avenue in inflammation and immunity. Open Biol 2012; 2(11): 120134.
114. Tsuda Y, Takahashi H, Kobayashi M, Hanafusa T, Herndon DN, Suzuki F. Three different neutrophil subsets exhibited in mice with different susceptibilities to infection by methicillin-resistant Staphylococcus aureus. Immunity 2004; 21(2): 215-26.
115. Sica A, Mantovani A. Macrophage plasticity and polarization: in vivo veritas. J Clin Invest 2012; 122(3): 787-95.
116. McDonald B, Urrutia R, Yipp BG, Jenne CN, Kubes P. Intravascular neutrophil extracellular traps capture bacteria from the bloodstream during sepsis. Cell Host Microbe 2012; 12(3): 324-33.
117. Hahn S, Giaglis S, Chowdhury CS, Hosli I, Hasler P. Modulation of neutrophil NETosis: interplay between infectious agents and underlying host physiology. Semin Immunopathol 2013; 35(4): 439-53.
118. Guimaraes-Costa AB, Nascimento MT, Froment GS, et al.Leishmania amazonensis promastigotes induce and are killed by neutrophil extracellular traps. Proc Natl Acad Sci USA 2009; 106(16): 6748-53.
119. Saitoh T, Komano J, Saitoh Y, et al. Neutrophil extracellular traps mediate a host defense response to human immunodeficiency virus-1. Cell Host Microbe 2012; 12(1): 109-16.
120. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009; 9(3): 162-74.
121. Qin A, Cai W, Pan T, et al.Expansion of monocytic myeloidderived suppressor cells dampens T cell function in HIV-1-seropositive individuals. J Virol 2013; 87(3): 1477-90.
122. Rodriguez PC, Ernstoff MS, Hernandez C, et al. Arginase Iproducing myeloid-derived suppressor cells in renal cell carcinoma are a subpopulation of activated granulocytes. Cancer Res 2009; 69(4): 1553-60.
123. De Santo C, Salio M, Masri SH, et al. Invariant NKT cells reduce the immunosuppressive activity of influenza A virus-induced myeloid-derived suppressor cells in mice and humans. J Clin Invest 2008; 118(12): 4036-48.
124. Chen S, Akbar SM, Abe M, Hiasa Y, Onji M. Immunosuppressive functions of hepatic myeloid-derived suppressor cells of normal mice and in a murine model of chronic hepatitis B virus. Clin Exp Immunol 2011; 166(1): 134-42.
125. Pilon-Thomas S, Mackay A, Vohra N, Mule JJ. Blockade of programmed death ligand 1 enhances the therapeutic efficacy of combination immunotherapy against melanoma. J Immunol 2010; 184(7): 3442-9.
126. Velu V, Titanji K, Zhu B, et al. Enhancing SIV-specific immunity in vivo by PD-1 blockade. Nature 2009; 458(7235): 206-10.
127. Lu W, Wu X, Lu Y, Guo W, Andrieu JM. Therapeutic dendriticcell vaccine for simian AIDS. Nat Med 2003; 9(1): 27-32.
128. Garcia F, Routy JP. Challenges in dendritic cells-based therapeutic vaccination in HIV-1 infection Workshop in dendritic cell-based vaccine clinical trials in HIV-1. Vaccine 2011; 29(38): 6454-63.
129. Routy JP, Nicolette C. Arcelis AGS-004 dendritic cell-based immunotherapy for HIV infection. Immunotherapy 2010; 2(4): 467-76.
130. Routy JP, Boulassel MR, Yassine-Diab B, et al. Immunologic activity and safety of autologous HIV RNA-electroporated dendritic cells in HIV-1 infected patients receiving antiretroviral therapy. Clin Immunol 2010; 134(2): 140-7.
131. Garcia F, Climent N, Guardo AC, et al. A dendritic cell-based vaccine elicits T cell responses associated with control of HIV-1 replication. Sci Translat Med 2013; 5(166): 166ra2.
132. Sperber K, Quraishi H, Kalb TH, Panja A, Stecher V, Mayer L. Selective regulation of cytokine secretion by hydroxychloroquine: inhibition of interleukin 1 alpha (IL-1-alpha) and IL-6 in human monocytes and T cells. J Rheumatol 1993; 20(5): 803-8.
133. Naarding MA, Baan E, Pollakis G, Paxton WA. Effect of chloroquine on reducing HIV-1 replication in vitro and the DCSIGN mediated transfer of virus to CD4+ T-lymphocytes. Retrovirology 2007; 4: 6.
134. Savarino A, Gennero L, Chen HC, et al. Anti-HIV effects of chloroquine: mechanisms of inhibition and spectrum of activity. AIDS 2001; 15(17): 2221-9.
135. Sperber K, Louie M, Kraus T, et al. Hydroxychloroquine treatment of patients with human immunodeficiency virus type 1. Clin Therap 1995; 17(4): 622-36.
136. Sperber K, Chiang G, Chen H, et al. Comparison of hydroxychloroquine with zidovudine in asymptomatic patients infected with human immunodeficiency virus type 1. Clin Therap 1997; 19(5): 913-23.
137. Routy JP, Angel J, Patel M, et al. Assessment of chloroquine as a modulator of immune activation to improve CD4 recovery in immune nonresponding HIV-infected patients receiving antiretroviral therapy. HIV Med 2014; [Epub ahead of print].
138. Rappocciolo G, Jais M, Piazza P, et al. Alterations in cholesterol metabolism restrict HIV-1 trans infection in nonprogressors. MBio 2014; 5(3): e01031-13.