The lungs as anatomical reservoirs of HIV infection

Reviews in Medical Virology

Volumn 24, Issue 1, 2014, Pages 35-54

  Costiniuk, Cecilia T ^a,b   Jenabian, Mohammad Ali ^c,d  

^a AFRICA HEALTH RESEARCH INSTITUTE   (South Africa)

^b UNIVERSITY OF OTTAWA   (Canada)

^c MCGILL UNIVERSITY   (Canada)

^d MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DIDANOSINE; ZIDOVUDINE;

CLINICAL TRIAL (TOPIC); EVIDENCE BASED MEDICINE; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; LUNG; MIXED INFECTION; REVIEW; SMOKING; VIRUS CARRIER; VIRUS ENTRY; VIRUS LOAD; VIRUS RESISTANCE;

DISEASE RESERVOIRS; HIV INFECTIONS; HIV-1; HUMANS; LUNG; MACROPHAGES, ALVEOLAR; VIRUS LATENCY;

EID: 84892485342     PISSN: 10529276     EISSN: 10991654     Source Type: Journal    
DOI: 10.1002/rmv.1772     Document Type: Review

References (150)

1. Chun TW, Davey RT, Ostrowski M, Justement S, Engel D, Mullins JI, Fauci AS. Relationship between pre-existing viral reservoirs and the re-emergence of plasma viremia after discontinuation of highly active anti-retroviral therapy. Nature Medicine 2000; 6(7): 757-761.
2. Colin L, Van Lint C. Molecular control of HIV-1 postintegration latency: implications for the development of new therapeutic strategies. Retrovirology 2009; 6: 111.
3. Chomont N, El-far M, Ancuta P, et al. HIV reservoir size and persistence are driven by T cell survival and homeostatic proliferation. Nature Medicine 2009; 15(8): 893-900.
4. Redel L, Le Douce V, Cherrier T, et al. HIV-1 regulation of latency in the monocyte-macrophage lineage and in CD4+ T lymphocytes. Journal of Leukocyte Biology 2010; 87(4): 575-588.
5. Keele BF, Tazi L, Gartner S, et al. Characterization of the follicular dendritic cell reservoir of human immunodeficiency virus type 1. Journal of Virology 2008; 82(11): 5548-5561.
6. Eisele E, Siliciano RF. Redefining the viral reservoirs that prevent HIV-1 eradication. Immunity 2012; 37(3): 377-388.
7. Almodovar, S, Knight R, Allshouse AA, et al. Human immunodeficiency virus nef signature sequences are associated with pulmonary hypertension. AIDS Research and Human Retroviruses 2012; 28(6): 607-618.
8. Hull MW, Phillips P, Montaner JS. Changing global epidemiology of pulmonary manifestations of HIV/AIDS. Chest 2008; 134(6): 1287-1298.
9. Clarke JR, Israel-Biet D. Interactions between opportunistic micro-organisms and HIV in the lung. Thorax 1996; 51(9): 875-877.
10. Tsukita S, Yamazaki Y, Katsuno T, Tamura A, Tsukita S. Tight junction-based epithelial microenvironment and cell proliferation. Oncogene 2008; 27(55): 6930-6938.
11. Sato, S, Kiyono H. The mucosal immune system of the respiratory tract. Current Opinion in Virology 2012; 2(3): 225-232.
12. Ryu JH, Kim CH, Yoon JH. Innate immune responses of the airway epithelium. Molecules and Cells 2010; 30(3): 173-183.
13. Kiyono H, Fukuyama S. NALT- versus Peyer's-patch-mediated mucosal immunity. Nature Reviews Immunology 2004; 4(9): 699-710.
14. Moyron-Quiroz JE, Rangel-Moreno J, Kusser K, et al. Role of inducible bronchus associated lymphoid tissue (iBALT) in respiratory immunity. Nature Medicine 2004; 10(9): 927-934.
15. Wu, HY, Russell MW. Nasal lymphoid tissue, intranasal immunization, and compartmentalization of the common mucosal immune system. Immunologic Research 1997; 16(2): 187-201.
16. Chan YR, Chen K, Duncan SR, et al. Patients with cystic fibrosis have inducible IL-17+IL-22+ memory cells in lung draining lymph nodes. Journal of Allergy and Clinical Immunology 2013; 131(4): 1117-1129, 1129 e1-5.
17. Condon TV, Sawyer RT, Fenton MJ, Riches DW. Lung dendritic cells at the innate-adaptive immune interface. Journal of Leukocyte Biology 2011; 90(5): 883-895.
18. Hammad H, Lambrecht BN. Dendritic cells and airway epithelial cells at the interface between innate and adaptive immune responses. Allergy 2011; 66(5): 579-587.
19. Vermaelen KY, Carro-Muino I, Lambrecht BN, Pauwels RA. Specific migratory dendritic cells rapidly transport antigen from the airways to the thoracic lymph nodes. Journal of Experimental Medicine 2001; 193(1): 51-60.
20. Bals R. Epithelial antimicrobial peptides in host defense against infection. Respiratory Research 2000; 1(3): 141-150.
21. Crapo JD, Harmsen AG, Sherman MP, Musson RA. Pulmonary immunobiology and inflammation in pulmonary diseases. American Journal of Respiratory and Critical Care Medicine 2000; 162(5): 1983-1986.
22. Jeffery PK. The origins of secretions in the lower respiratory tract. European Journal of Respiratory Diseases. Supplement 1987; 153: 34-42.
23. Bowdish DM, Davidson DJ, Hancock RE. Immunomodulatory properties of defensins and cathelicidins. Current Topics in Microbiology and Immunology 2006; 306: 27-66.
24. Wright JR. Immunomodulatory functions of surfactant. Physiological Reviews 1997; 77(4): 931-962.
25. Proebstl D, Voisin MB, Woodfin A, et al. Pericytes support neutrophil subendothelial cell crawling and breaching of venular walls in vivo. Journal of Experimental Medicine 2012; 209(6): 1219-1234.
26. Hasenberg M, Stegemann-Koniszewski S, Gunzer M. Cellular immune reactions in the lung. Immunology Reviews 2013; 251(1): 189-214.
27. Soehnlein O, Lindbom L, Weber C. Mechanisms underlying neutrophil-mediated monocyte recruitment. Blood 2009; 114(21): 4613-4623.
28. Scapini P, Lapinet-Vera JA, Gasperini S, Calzetti F, Bazzoni F, Cassatella MA. The neutrophil as a cellular source of chemokines. Immunology Reviews 2000; 177: 195-203.
29. Burns AR, Smith CW, Walker DC. Unique structural features that influence neutrophil emigration into the lung. Physiological Reviews 2003; 83(2): 309-336.
30. Holt PG, Robinson BW, Reid M, et al. Extraction of immune and inflammatory cells from human lung parenchyma: evaluation of an enzymatic digestion procedure. Clinical and Experimental Immunology 1986; 66(1): 188-200.
31. Augustin A, Kubo RT, Sim GK. Resident pulmonary lymphocytes expressing the gamma/delta T-cell receptor. Nature 1989; 340(6230): 239-241.
32. Wolber FM, Curtis JL, Milik AM, et al. Lymphocyte recruitment and the kinetics of adhesion receptor expression during the pulmonary immune response to particulate antigen. American Journal of Pathology 1997; 151(6): 1715-1727.
33. Campbell DJ, Koch MA. Phenotypical and functional specialization of FOXP3+ regulatory T cells. Nature Reviews Immunology 2011; 11(2): 119-130.
34. Sather BD, Treuting P, Perdue N, Miazgomicz M, Fontenot JD, Rudensky AY, Campbell DJ. Altering the distribution of Foxp3(+) regulatory T cells results in tissue-specific inflammatory disease. Journal of Experimental Medicine 2007; 204(6): 1335-1347.
35. Cerutti A. The regulation of IgA class switching. Nature Reviews Immunology 2008; 8(6): 421-434.
36. Mestecky J, McGhee JR. Immunoglobulin A (IgA): molecular and cellular interactions involved in IgA biosynthesis and immune response. Advances in Immunology 1987; 40: 153-245.
37. Gerhard W, Mozdzanowska K, Furchner M, Washko G, Maiese K. Role of the B-cell response in recovery of mice from primary influenza virus infection. Immunology Reviews 1997; 159: 95-103.
38. Takeuchi O, Akira S. Innate immunity to virus infection. Immunology Reviews 2009; 227(1): 75-86.
39. Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell 2010; 140(6): 805-820.
40. Mason MJ, Gillett NA, Bice DE. Comparison of systemic and local immune responses after multiple pulmonary antigen exposures. Regional Immunology 1989; 2(3): 149-157.
41. Pabst R, Tschernig T. Lymphocytes in the lung: an often neglected cell. Numbers, characterization and compartmentalization. Anatomy and Embryology (Berlin) 1995; 192(4): 293-299.
42. Weissman DN, Bice DE, Crowell RE, Schuyler MR. Intrapulmonary antigen deposition in the human lung: local responses. American Journal of Respiratory Cell and Molecular Biology 1994; 11(5): 607-614.
43. Barber SA, Gama L, Li M, et al. Longitudinal analysis of simian immunodeficiency virus (SIV) replication in the lungs: compartmentalized regulation of SIV. The Journal of Infectious Diseases 2006; 194(7): 931-938.
44. Clarke JR, Mitchell DM, Coker RJ, Israel-Biet D. Is the lung important as a privileged site for the human immunodeficiency virus? Thorax 1998; 53(2): 81-82.
45. Tavares Marques MA, Alves V, Duque V, Botelho MF. Deep lung-cellular reaction to HIV. Revista Portuguesa de Pneumologia 2007; 13(2): 175-212.
46. Worgall S, Connor R, Kaner RJ, Fenamore E, Sheridan K, Singh R, Crystal RG. Expression and use of human immunodeficiency virus type 1 coreceptors by human alveolar macrophages. Journal of Virology 1999; 73(7): 5865-5874.
47. Agostini C, Trentin L, Zambello R, et al. Release of granulocyte-macrophage colony-stimulating factor by alveolar macrophages in the lung of HIV-1-infected patients. A mechanism accounting for macrophage and neutrophil accumulation. The Journal of Immunology 1992; 149(10): 3379-3385.
48. Burri, PH. Development and growth of the human lung. Comprehensive Physiology, 2011: 1-46.
49. Bohnet S, Braun J, Dalhoff K. Intercellular adhesion molecule-1 (ICAM-1) is upregulated on alveolar macrophages from AIDS patients. The European Respiratory Journal 1994; 7(2): 229-234.
50. Stevenson M, Gendelman HE. Cellular and viral determinants that regulate HIV-1 infection in macrophages. Journal of Leukocyte Biology 1994; 56(3): 278-288.
51. Thornton DJ, Rousseau K, McGuckin MA. Structure and function of the polymeric mucins in airways mucus. Annual Review of Physiology 2008; 70: 459-486.
52. de Heer HJ, Hammad H, Kool M, Lambrecht BN. Dendritic cell subsets and immune regulation in the lung. Seminars in Immunology 2005; 17(4): 295-303.
53. Descombes P, Schibler U. A liver-enriched transcriptional activator protein, LAP, and a transcriptional inhibitory protein, LIP, are translated from the same mRNA. Cell 1991; 67(3): 569-579.
54. Torre D, Speranza F, Martegani R. Impact of highly active antiretroviral therapy on organ-specific manifestations of HIV-1 infection. HIV Medicine 2005; 6(2): 66-78.
55. Feikin DR, Feldman C, Schuchat A, Janoff EN. Global strategies to prevent bacterial pneumonia in adults with HIV disease. The Lancet Infectious Diseases 2004; 4(7): 445-455.
56. Autran B, Mayaud CM, Raphael M, et al. Evidence for a cytotoxic T-lymphocyte alveolitis in human immunodeficiency virus-infected patients. AIDS 1988; 2(3): 179-183.
57. Guillon JM, Denis M, Fouret P, Plata F, Mayaud CM, Akoun GM. Human immunodeficiency virus-related lymphocytic alveolitis. Chest 1988; 94(6): 1264-1270.
58. Twigg III HL, Weiden M, Valentine F, et al. Effect of highly active antiretroviral therapy on viral burden in the lungs of HIV-infected subjects. The Journal of Infectious Diseases 2008; 197(1): 109-116.
59. Autran B, Plata F, Guillon JM, Joly P, Mayaud C, Debre P. HIV-specific cytotoxic T lymphocytes directed against alveolar macrophages in HIV-infected patients. Research in Virology 1990; 141(2): 131-136.
60. Autran B, Sadat-Sowti B, Hadida F, et al. HIV-specific cytotoxic T lymphocytes against alveolar macrophages: specificities and downregulation. Research in Virology 1991; 142(2-3): 113-118.
61. Plata F, Autran B, Martins LP, et al. AIDS virus-specific cytotoxic T lymphocytes in lung disorders. Nature 1987; 328(6128): 348-351.
62. Agostini C, Semenzato G. Immunologic effects of HIV in the lung. Clinics in Chest Medicine 1996; 17(4): 633-645.
63. Agostini C, Zambello R, Trentin L, et al. Gamma delta T cell receptor subsets in the lung of patients with HIV-1 infection. Cellular Immunology 1994; 153(1): 194-205.
64. Agostini C, Zambello R, Trentin L, Semenzato G. T lymphocytes with gamma/delta T-cell receptors in patients with AIDS and Pneumocystis carinii pneumonia. AIDS 1995; 9(2): 203-204.
65. Kagi MK, Fierz W, Grob PJ, Russi EW. High proportion of gamma-delta T cell receptor positive T cells in bronchoalveolar lavage and peripheral blood of HIV-infected patients with Pneumocystis carinii pneumonias. Respiration 1993; 60(3): 170-177.
66. Agostini C, Chilosi M, Zambello R, Trentin L, Semenzato G. Pulmonary immune cells in health and disease: lymphocytes. The European Respiratory Journal 1993; 6(9): 1378-1401.
67. Yearsley MM, Diaz PT, Knoell D, Nuovo GJ. Correlation of HIV-1 detection and histology in AIDS-associated emphysema. Diagnostic Molecular Pathology 2005; 14(1): 48-52.
68. Agostini C, Zambello R, Trentin L, et al. Prognostic significance of the evaluation of bronchoalveolar lavage cell populations in patients with HIV-1 infection and pulmonary involvement. Chest 1991; 100(6): 1601-1606.
69. Twigg HL 3rd, Soliman DM. Role of alveolar macrophage-T cell adherence in accessory cell function in human immunodeficiency virus-infected individuals. American Journal of Respiratory Cell and Molecular Biology 1994; 11(2): 138-146.
70. Rubbo PA, Tuaillon E, Bollore K, et al. The potential impact of CD4+ T cell activation and enhanced Th1/Th2 cytokine ratio on HIV-1 secretion in the lungs of individuals with advanced AIDS and active pulmonary infection. Clinical Immunology 2011; 139(2): 142-154.
71. Jambo KC, Sepako E, Fullerton DG, et al. Bronchoalveolar CD4+ T cell responses to respiratory antigens are impaired in HIV-infected adults. Thorax 2011; 66(5): 375-382.
72. Schaefer TM, Fuller CL, Basu S, et al. Increased expression of interferon-inducible genes in macaque lung tissues during simian immunodeficiency virus infection. Microbes and Infection 2006; 8(7): 1839-1850.
73. Hoffenbach A, Langlade-Demoyen P, Dadaglio G, et al. Unusually high frequencies of HIV-specific cytotoxic T lymphocytes in humans. The Journal of Immunology 1989; 142(2): 452-462.
74. Agostini C, Poletti V, Zambello R, et al. Phenotypical and functional analysis of bronchoalveolar lavage lymphocytes in patients with HIV infection. The American Review of Respiratory Disease 1988; 138(6): 1609-1615.
75. Agostini C, Zambello R, Trentin L, et al. Cytotoxic events taking place in the lung of patients with HIV-1 infection. Evidence of an intrinsic defect of the major histocompatibility complex-unrestricted killing partially restored by the incubation with rIL-2. The American Review of Respiratory Disease 1990; 142(3): 516-522.
76. Clerici M, Shearer GM. A TH1→TH2 switch is a critical step in the etiology of HIV infection. Immunology Today 1993; 14(3): 107-111.
77. Young KR Jr., Rankin JA, Naegel GP, Paul ES, Reynolds HY. Bronchoalveolar lavage cells and proteins in patients with the acquired immunodeficiency syndrome. An immunologic analysis. Annals of Internal Medicine 1985; 103(4): 522-533.
78. Plouffe JF, Breiman RF, Facklam RR. Bacteremia with Streptococcus pneumoniae. Implications for therapy and prevention. Franklin County Pneumonia Study Group. JAMA 1996; 275(3): 194-198.
79. Janoff EN, Breiman RF, Daley CL, Hopewell PC. Pneumococcal disease during HIV infection. Epidemiologic, clinical, and immunologic perspectives. Annals of Internal Medicine 1992; 117(4): 314-324.
80. Twigg HL 3rd, Spain BA, Soliman DM, Bowen LK, Heidler KM, Wilkes DS. Impaired IgG production in the lungs of HIV-infected individuals. Cellular Immunology 1996; 170(1): 127-133.
81. Steffen M, Reinecker HC, Petersen J, Doehn C, Pfluger I, Voss A, Raedler A. Differences in cytokine secretion by intestinal mononuclear cells, peripheral blood monocytes and alveolar macrophages from HIV-infected patients. Clinical and Experimental Immunology 1993; 91(1): 30-36.
82. Trentin L, Garbisa S, Zambello R, et al. Spontaneous production of interleukin-6 by alveolar macrophages from human immunodeficiency virus type 1-infected patients. The Journal of Infectious Diseases 1992; 166(4): 731-737.
83. Denis, M, Ghadirian E. Dysregulation of interleukin 8, interleukin 10, and interleukin 12 release by alveolar macrophages from HIV type 1-infected subjects. AIDS Research and Human Retroviruses 1994; 10(12): 1619-1627.
84. Gordon SB, Jarman ER, Kanyanda S, et al. Reduced interleukin-8 response to Streptococcus pneumoniae by alveolar macrophages from adults with HIV/AIDS. AIDS 2005; 19(11): 1197-1200.
85. Koziel H, Kruskal BA, Ezekowitz RA, Rose RM. HIV impairs alveolar macrophage mannose receptor function against Pneumocystis carinii. Chest 1993; 103(2 Suppl): 111S-112S.
86. Koziel H, Li X, Armstrong MY, Richards FF, Rose RM. Alveolar macrophages from human immunodeficiency virus-infected persons demonstrate impaired oxidative burst response to Pneumocystis carinii in vitro. American Journal of Respiratory Cell and Molecular Biology 2000; 23(4): 452-459.
87. Lipman MC, Johnson MA, Poulter LW. Functionally relevant changes occur in HIV-infected individuals' alveolar macrophages prior to the onset of respiratory disease. AIDS 1997; 11(6): 765-772.
88. Twigg HL, Soliman DM, Day RB, Knox KS, Anderson RJ, Wilkes DS, Schnizlein-Bick CT. Lymphocytic alveolitis, bronchoalveolar lavage viral load, and outcome in human immunodeficiency virus infection. American Journal of Respiratory and Critical Care Medicine 1999; 159(5 Pt 1): 1439-1444.
89. Koziel H, Kim S, Reardon C, Li X, Garland R, Pinkston P, Kornfeld H. Enhanced in vivo human immunodeficiency virus-1 replication in the lungs of human immunodeficiency virus-infected persons with Pneumocystis carinii pneumonia. American Journal of Respiratory and Critical Care Medicine 1999; 160(6): 2048-2055.
90. Chayt KJ, Harper ME, Marselle LM, et al. Detection of HTLV-III RNA in lungs of patients with AIDS and pulmonary involvement. JAMA 1986; 256(17): 2356-2359.
91. Nakata K, Weiden M, Harkin T, Ho D, Rom WN. Low copy number and limited variability of proviral DNA in alveolar macrophages from HIV-1-infected patients: evidence for genetic differences in HIV-1 between lung and blood macrophage populations. Molecular Medicine 1995; 1(7): 744-757.
92. Rose RM, Krivine DA, Pinkston P, Gillis JM, Huang A, Hammer SM. Frequent identification of HIV-1 DNA in bronchoalveolar lavage cells obtained from individuals with the acquired immunodeficiency syndrome. The American Review of Respiratory Disease 1991; 143(4 Pt 1): 850-854.
93. Linnemann CC Jr., Baughman RP, Frame PT, Floyd R. Recovery of human immunodeficiency virus and detection of p24 antigen in bronchoalveolar lavage fluid from adult patients with AIDS. Chest 1989; 96(1): 64-67.
94. Jeffrey AA, Israel-Biet D, Andrieu JM, Even P, Venet A. HIV isolation from pulmonary cells derived from bronchoalveolar lavage. Clinical and Experimental Immunology 1991; 84(3): 488-492.
95. Israel-Biet D, Cadranel J, Even P. Human immunodeficiency virus production by alveolar lymphocytes is increased during Pneumocystis carinii pneumonia. The American Review of Respiratory Disease 1993; 148(5): 1308-1312.
96. Tan J, Sattentau QJ. The HIV-1-containing macrophage compartment: a perfect cellular niche? Trends in Microbiology, 2013.
97. Jorajuria S, Dereuddre-Bosquet N, Becher F, et al. ATP binding cassette multidrug transporters limit the anti-HIV activity of zidovudine and indinavir in infected human macrophages. Antiviral Therapy 2004; 9(4): 519-528.
98. Semenzato G, Agostini C, Ometto L, Zambello R, Trentin L, Chieco-Bianchi L, De Rossi A. CD8+ T lymphocytes in the lung of acquired immunodeficiency syndrome patients harbor human immunodeficiency virus type 1. Blood 1995; 85(9): 2308-2314.
99. Horiike M, Iwami S, Kodama M, et al. Lymph nodes harbor viral reservoirs that cause rebound of plasma viremia in SIV-infected macaques upon cessation of combined antiretroviral therapy. Virology 2012; 423(2): 107-118.
100. Clarke JR, Gates AJ, Coker RJ, Douglass JA, Williamson JD, Mitchell DM. HIV-1 proviral DNA copy number in peripheral blood leucocytes and bronchoalveolar lavage cells of AIDS patients. Clinical and Experimental Immunology 1994; 96(2): 182-186.
101. Alimohammadi A, Coker R, Miller R, Mitchell D, Williamson J, Clarke J. Genotypic variants of HIV-1 from peripheral blood and lungs of AIDS patients. AIDS 1997; 11(6): 831-832.
102. van't Wout AB, Ran RJ, Kuiken CL, Kootstra NA, Pals ST, Schuitemaker H. Analysis of the temporal relationship between human immunodeficiency virus type 1 quasispecies in sequential blood samples and various organs obtained at autopsy. Journal of Virology 1998; 72(1): 488-496.
103. Collins KR, Quinones-Mateu ME, Wu M, et al. Human immunodeficiency virus type 1 (HIV-1) quasispecies at the sites of Mycobacterium tuberculosis infection contribute to systemic HIV-1 heterogeneity. Journal of Virology 2002; 76(4): 1697-1706.
104. Itescu S, Simonelli PF, Winchester RJ, Ginsberg HS. Human immunodeficiency virus type 1 strains in the lungs of infected individuals evolve independently from those in peripheral blood and are highly conserved in the C-terminal region of the envelope V3 loop. Proceedings of the National Academy of Sciences of the United States of America 1994; 91(24): 11378-11382.
105. Singh A, Besson G, Mobasher A, Collman RG. Patterns of chemokine receptor fusion cofactor utilization by human immunodeficiency virus type 1 variants from the lungs and blood. Journal of Virology 1999; 73(8): 6680-6690.
106. Didierlaurent A, Goulding J, Hussell T. The impact of successive infections on the lung microenvironment. Immunology 2007; 122(4): 457-465.
107. Jensen BN, Lisse IM, Gerstoft J, Borgeskov S, Skinhoj P. Cellular profiles in bronchoalveolar lavage fluid of HIV-infected patients with pulmonary symptoms: relation to diagnosis and prognosis. AIDS 1991; 5(5): 527-533.
108. Rando RF, Srinivasan A, Feingold J, Gonczol E, Plotkin S. Characterization of multiple molecular interactions between human cytomegalovirus (HCMV) and human immunodeficiency virus type 1 (HIV-1). Virology 1990; 176(1): 87-97.
109. Nakata K, Rom WN, Honda Y, Condos R, Kanegasaki S, Cao Y, Weiden W. Mycobacterium tuberculosis enhances human immunodeficiency virus-1 replication in the lung. American Journal of Respiratory and Critical Care Medicine 1997; 155(3): 996-1003.
110. Lebargy F, Branellec A, Deforges L, Bignon J, Bernaudin JF. HIV-1 in human alveolar macrophages from infected patients is latent in vivo but replicates after in vitro stimulation. American Journal of Respiratory Cell and Molecular Biology 1994; 10(1): 72-78.
111. Marchetti G, Cozzi-Lepri A, Merlini E, et al. Microbial translocation predicts disease progression of HIV-infected antiretroviral-naive patients with high CD4+ cell count. AIDS 2011; 25(11): 1385-1394.
112. Kadoki M, Choi BI, Iwakura Y. The mechanism of LPS-induced HIV type I activation in transgenic mouse macrophages. International Immunology 2010; 22(6): 469-478.
113. Mathys JM, Melanson SM, Schiffer-Alberts DJ, Ioannidis JP, Koziel H, Skolnik PR. NF-kappa B modulates TNF-alpha production by alveolar macrophages in asymptomatic HIV-seropositive individuals. The Journal of Immunology 2000; 164(3): 1588-1594.
114. Zhang J, Zhu J, Imrich A, Cushion M, Kinane TB, Koziel H. Pneumocystis activates human alveolar macrophage NF-kappaB signaling through mannose receptors. Infection and Immunity 2004; 72(6): 3147-3160.
115. Ablashi DV, Bernbaum J, DiPaolo JA. Human herpes virus 6 as a potential pathogen. Trends in Microbiology 1995; 3(8): 324-327.
116. Ieong MH, Reardon CC, Levitz SM, Kornfeld H. Human immunodeficiency virus type 1 infection of alveolar macrophages impairs their innate fungicidal activity. American Journal of Respiratory and Critical Care Medicine 2000; 162(3 Pt 1): 966-970.
117. Corbett EL, Watt CJ, Walker N, Maher D, Williams BG, Raviglione MC, Dye C. The growing burden of tuberculosis: global trends and interactions with the HIV epidemic. Archives of Internal Medicine 2003; 163(9): 1009-1021.
118. Zhang YH, Nakata K, Weiden M, Rom WN. Mycobacterium tuberculosis enhances human immunodeficiency virus-1 replication by transcriptional activation at the long terminal repeat. Journal of Clinical Investigation 1995; 95(5): 2324-2331.
119. Rosas-Taraco AG, Revol A, Salinas-Carmona MC, Rendon A, Caballero-Olin G, Arce-Mendoza A. Mycobacterium tuberculosis upregulates coreceptors CCR5 and CXCR4 while HIV modulates CD14 favoring concurrent infection. Aids Research and Human Retroviruses 2006; 22(1): 45-51.
120. Briken V, Porcelli SA, Besra GS, Kremer L. Mycobacterial lipoarabinomannan and related lipoglycans: from biogenesis to modulation of the immune response. Molecular Microbiology 2004; 53(2): 391-403.
121. Marshall MM, McCormack MC, Kirk GD. Effect of cigarette smoking on HIV acquisition, progression, and mortality. AIDS Education and Prevention 2009; 21(3 Suppl): 28-39.
122. Monforte A, Abrams D, Pradier C, et al. HIV-induced immunodeficiency and mortality from AIDS-defining and non-AIDS-defining malignancies. AIDS 2008; 22(16): 2143-2153.
123. Thomassen MJ, Barna BP, Wiedermann HP, Fermer M, Ahmad M. Human alveolar macrophage function: differences between smokers and nonsmokers. Journal of Leukocyte Biology 1988; 44(5): 313-318.
124. Wieslander E, Linden M, Hakansson L, et al. Human alveolar macrophages from smokers have an impaired capacity to secrete LTB4 but not other chemotactic factors. European Journal of Respiratory Diseases 1987; 71(4): 263-272.
125. Brown GP, Iwamoto GK, Monick MM, Hunninghake GW. Cigarette smoking decreases interleukin 1 release by human alveolar macrophages. The American Journal of Physiology 1989; 256(2 Pt 1): C260-C264.
126. Soliman DM, Twigg HL 3rd. Cigarette smoking decreases bioactive interleukin-6 secretion by alveolar macrophages. The American Journal of Physiology 1992; 263(4 Pt 1): L471-L478.
127. Elssner A, Carter JE, Yunger T, Wewers MD. HIV-1 infection does not impair human alveolar macrophage phagocytic function unless combined with cigarette smoking. Chest 2004; 125(3): 1071-1076.
128. Abbud RA, Finegan CK, Guay CA, Rich EA. Enhanced production of human immunodeficiency virus type 1 by in vitro-infected alveolar macrophages from otherwise healthy cigarette smokers. The Journal of Infectious Diseases 1995; 172(3): 859-863.
129. Ballester LY, Capo-Velez CM, Garcia-Beltran WF. Up-regulation of the neuronal nicotinic receptor alpha7 by HIV glycoprotein 120: potential implications for HIV-associated neurocognitive disorder. The Journal of Biological Chemistry 2012; 287(5): 3079-3086.
130. Rock RB, Gekker G, Aravalli RN, Hu S, Sheng WS, Peterson PK. Potentiation of HIV-1 expression in microglial cells by nicotine: involvement of transforming growth factor-beta 1. Journal of Neuroimmune Pharmacology 2008; 3(3): 143-149.
131. Baldwin GC, Tashkin DP, Buckley DM, Park AN, Dubinett SM, Roth MD. Marijuana and cocaine impair alveolar macrophage function and cytokine production. American Journal of Respiratory and Critical Care Medicine 1997; 156(5): 1606-1613.
132. Baldwin GC, Buckley DM, Roth MD, Kleerup EC, Tashkin DP. Acute activation of circulating polymorphonuclear neutrophils following in vivo administration of cocaine. A potential etiology for pulmonary injury. Chest 1997; 111(3): 698-705.
133. Ives NJ, Gazzard BG, Easterbrook PJ. The changing pattern of AIDS-defining illnesses with the introduction of highly active antiretroviral therapy (HAART) in a London clinic. The Journal of Infection 2001; 42(2): 134-139.
134. Kohli R, Lo Y, Homel P, et al. Bacterial pneumonia, HIV therapy, and disease progression among HIV-infected women in the HIV epidemiologic research (HER) study. Clinical Infectious Diseases 2006; 43(1): 90-98.
135. Atkins M, Strappe P, Kaye S, et al. Quantitative differences in the distribution of zidovudine resistance mutations in multiple post-mortem tissues from AIDS patients. Journal of Medical Virology 1998; 55(2): 138-146.
136. Bray DH, Squire SB, Kawana A, Johnson MA, Poulter LW. Antiretroviral treatment reverses HIV-induced reduction in the expression of surface antigens on alveolar macrophages in AIDS patients. Clinical and Experimental Immunology 1993; 91(1): 13-17.
137. Twigg HL, Schnizlein-Bick CT, Weiden M, et al. Measurement of antiretroviral drugs in the lungs of HIV-infected patients. HIV Therapy 2010; 4(2): 247-251.
138. Kolls JK. CD4(+) T-cell subsets and host defense in the lung. Immunology Reviews 2013; 252(1): 156-163.
139. Berman MA, Sandborg CI, Calabia BJ, Andrew BS, Friou GJ. Interleukin 1 inhibitor masks high interleukin 1 production in acquired immunodeficiency syndrome (AIDS). Clinical Immunology and Immunopathology 1987; 42(1): 133-140.
140. Twigg HL 3rd, Iwamoto GK, and Soliman DM. Role of cytokines in alveolar macrophage accessory cell function in HIV-infected individuals. The Journal of Immunology 1992; 149(4): 1462-1469.
141. Lipschik GY, Doerfler ME, Kovacs JA, et al. Leukotriene B4 and interleukin-8 in human immunodeficiency virus-related pulmonary disease. Chest 1993; 104(3): 763-769.
142. Murray HW, Gellene RA, Libby DM, Rothermel CD, Rubin BY. Activation of tissue macrophages from AIDS patients: in vitro response of AIDS alveolar macrophages to lymphokines and interferon-gamma. The Journal of Immunology 1985; 135(4): 2374-2377.
143. White DA, Gellene DA, Gupta S, Cunningham-Rundles C, Stover DE. Pulmonary cell populations in the immunosuppressed patient. Bronchoalveolar lavage findings during episodes of pneumonitis. Chest 1985; 88(3): 352-359.
144. Fahy RJ, Diaz PT, Hart J, Wewers MD. BAL and serum IgG levels in healthy asymptomatic HIV-infected patients. Chest 2001; 119(1): 196-203.
145. Clarke JR, Fleming J, Donegan K, Moss FM, Nieman R, Williamson JD, Mitchell DM. Detection of HIV-1 in human lung macrophages using the polymerase chain reaction. AIDS 1990; 4(11): 1133-1136.
146. Clarke JR, Williamson JD, Mitchell DM. Comparative study of the isolation of human immunodeficiency virus from the lung and peripheral blood of AIDS patients. Journal of Medical Virology 1993; 39(3): 196-199.
147. Sierra-Madero JG, Toossi Z, Hom DL, Finegan CK, Hoenig E, Rich EA. Relationship between load of virus in alveolar macrophages from human immunodeficiency virus type 1-infected persons, production of cytokines, and clinical status. The Journal of Infectious Diseases 1994; 169(1): 18-27.
148. Pinkston P, Pelletier N, Arena C, Schock J, Garland R, Rose RM. Quantitative culture of HIV-1 from bronchoalveolar lavage cells. American Journal of Respiratory and Critical Care Medicine 1995; 152(1): 254-259.
149. Lewin SR, Kirihara J, Sonza S, Irving L, Mills J, Crowe SM. HIV-1 DNA and mRNA concentrations are similar in peripheral blood monocytes and alveolar macrophages in HIV-1-infected individuals. AIDS 1998; 12(7): 719-727.
150. White NC, Weiden M, Valentine F, et al. Different resistance mutations can be detected simultaneously in the blood and the lung of HIV-1 infected individuals on antiretroviral therapy. Journal of Medical Virology 2004; 72(3): 352-357.