Small alveolar macrophages are infected preferentially by HIV and exhibit impaired phagocytic function

Mucosal Immunology

Volumn 7, Issue 5, 2014, Pages 1116-1126

  Jambo, K C ^a,b   Banda, D H ^a   Kankwatira, A M ^a   Sukumar, N ^c   Allain, T J ^d   Heyderman, R S ^a,b,d   Russell, D G ^c   Mwandumba, H C ^a,b,d  

^a UNIVERSITY OF MALAWI   (Malawi)

^b LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

^c Cornell University ^*  (United States)

^d Queen Elizabeth Central Hospital campus   (Malawi)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE IMMUNITY; ADULT; ARTICLE; CELL SIZE; CELL SPECIFICITY; CLINICAL ARTICLE; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; FEMALE; HEALTH STATUS; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; IN VIVO STUDY; INFECTION SENSITIVITY; INNATE IMMUNITY; LARGE ALVEOLAR MACROPHAGE; LOWER RESPIRATORY TRACT INFECTION; LUNG ALVEOLUS MACROPHAGE; LUNG LAVAGE; MACROPHAGE FUNCTION; MALE; PHAGOCYTE DYSFUNCTION; PHAGOCYTOSIS; PHENOTYPE; PRIORITY JOURNAL; PROSPECTIVE STUDY; PROTEIN DEGRADATION; SMALL ALVEOLAR MACROPHAGE; VIRUS CARRIER; ACCESSORY CELL; ANTIGEN EXPRESSION; ASYMPTOMATIC INFECTION; CD4 LYMPHOCYTE COUNT; CD4+ T LYMPHOCYTE; FLOW CYTOMETRY; FLUORESCENCE IN SITU HYBRIDIZATION; IMMUNE RESPONSE; INCIDENCE; LYMPHOCYTE SUBPOPULATION; RISK FACTOR; SMALL LUNG ALVEOLUS MACROPHAGE; SMOKING; IMMUNOLOGY; MIDDLE AGED; VIROLOGY; YOUNG ADULT;

ALPHA INTEGRIN; CD14 ANTIGEN; CD16 ANTIGEN; CD71 ANTIGEN; GLYCOPROTEIN P 15095; INTERLEUKIN 3; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MANNOSE RECEPTOR; TRANSFERRIN RECEPTOR;

ADULT; BRONCHOALVEOLAR LAVAGE; CELL SIZE; FEMALE; FLOW CYTOMETRY; HIV-1; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; MACROPHAGES, ALVEOLAR; MALE; MIDDLE AGED; PHAGOCYTOSIS; YOUNG ADULT;

EID: 84904869329     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2013.127     Document Type: Article

References (50)

1. Cameron, P, Pope,M, Granelli-Piperno, A & Steinman, R.M. Dendritic cells and the replication of HIV-1. J. Leukoc. Biol. 59, 158-171 (1996).
2. Douek, D.C. et al. HIV preferentially infects HIV-specific CD4+ T cells. Nature 417, 95-98 (2002).
3. Innocenti, P, Ottmann, M, Morand, P, Leclercq, P & Seigneurin, J.M. HIV-1 in blood monocytes: frequency of detection of proviral DNA using PCR and comparison with the total CD4 count. AIDS Res. Hum. Retroviruses 8, 261-268 (1992).
4. Betts, M.R., Gray, C.M., Cox, J.H. & Ferrari, G. Antigen-specific T-cellmediated immunity after HIV-1 infection: implications for vaccine control of HIV development. Expert Rev. Vaccines 5, 505-516 (2006).
5. Streeck, H & Nixon, D.F. T cell immunity in acute HIV-1 infection. J. Infect. Dis. 202 (Suppl 2), S302-S308 (2010).
6. Collman, R.G., Perno, C.F., Crowe, S.M., Stevenson, M & Montaner, L.J. HIV and cells of macrophage/dendritic lineage and other non-T cell reservoirs: new answers yield new questions. J. Leukoc. Biol. 74, 631-634 (2003).
7. Gordon, S.B. & Read, R.C.Macrophage defences against respiratory tract infections. Br. Med. Bull. 61, 45-61 (2002).
8. Garratt, L.W., Wright, A.K., Ranganathan, S.C., Grigg, J & Sly, P.D. on behalf of AREST CF. Small macrophages are present in early childhood respiratory disease. J. Cyst. Fibros. 11, 201-208 (2012).
9. Wright, A.K. et al. Pivotal advance: expansion of small sputum macrophages in CF: failure to express MARCO and mannose receptors. J. Leukoc. Biol. 86, 479-489 (2009).
10. Russell, D.G., Vanderven,B.C., Glennie, S,Mwandumba,H& Heyderman, R.S. The macrophage marches on its phagosome: dynamic assays of phagosome function. Nat. Rev. Immunol. 9, 594-600 (2009).
11. Marti-Lliteras, P. et al. Nontypeable Haemophilus influenzae clearance by alveolar macrophages is impaired by exposure to cigarette smoke. Infect. Immun. 77, 4232-4242 (2009).
12. Berenson, C.S. et al. Impaired alveolar macrophage response to Haemophilus antigens in chronic obstructive lung disease. Am. J. Respir. Crit. Care Med. 174, 31-40 (2006).
13. Hirschtick, R.E. et al. Bacterial pneumonia in persons infected with the human immunodeficiency virus. Pulmonary Complications of HIV Infection Study Group. N. Engl. J. Med. 333, 845-851 (1995).
14. Sonnenberg, P, Glynn, J.R., Fielding, K, Murray, J, Godfrey-Faussett, P & Shearer, S. How soon after infection with HIV does the risk of tuberculosis start to increase?Aretrospective cohort study in South African gold miners. J. Infect. Dis. 191, 150-158 (2005).
15. Park, I.W., Koziel, H, Hatch, W, Li, X, Du, B & Groopman, J.E. CD4 receptor-dependent entry of human immunodeficiency virus type-1 env-pseudotypes into CCR5-, CCR3-, and CXCR4-expressing human alveolar macrophages is preferentially mediated by the CCR5 coreceptor. Am. J. Respir. Cell Mol. Biol. 20, 864-871 (1999).
16. Musher, D.M., Watson, D.A., Nickeson, D, Gyorkey, F, Lahart, C & Rossen, R.D. The effect of HIV infection on phagocytosis and killing of Staphylococcus aureus by human pulmonary alveolar macrophages. Am. J. Med. Sci. 299, 158-163 (1990).
17. Tachado, S.D., Zhang, J, Zhu, J, Patel, N & Koziel, H. HIV impairs TNF-alpha release in response to Toll-like receptor 4 stimulation in human macrophages in vitro. Am. J. Respir. Cell Mol. Biol. 33, 610-621 (2005).
18. Elssner, A, Carter, J.E., Yunger, T.M. & Wewers, M.D. HIV-1 infection does not impair human alveolar macrophage phagocytic function unless combined with cigarette smoking. Chest 125, 1071-1076 (2004).
19. Gordon, S.B. et al. Opsonic phagocytosis of Streptococcus pneumoniae by alveolar macrophages is not impaired in human immunodeficiency virus-infected Malawian adults. J. Infect. Dis. 184, 1345-1349 (2001).
20. Mwandumba, H.C. et al. Mycobacterium tuberculosis resides in nonacidified vacuoles in endocytically competent alveolar macrophages from patients with tuberculosis and HIV infection. J. Immunol. 172, 4592-4598 (2004).
21. Kedzierska, K, Azzam, R, Ellery, P, Mak, J, Jaworowski, A & Crowe, S.M. Defective phagocytosis by human monocyte/macrophages following HIV- 1 infection: underlying mechanisms and modulation by adjunctive cytokine therapy. J. Clin. Virol. 26, 247-263 (2003).
22. Koziel, H. et al. Reduced binding and phagocytosis of Pneumocystis carinii by alveolar macrophages from persons infected with HIV-1 correlates with mannose receptor downregulation. J. Clin. Invest. 102, 1332-1344 (1998).
23. Wehle, K, Schirmer, M, Dunnebacke-Hinz, J, Kupper, T & Pfitzer, P. Quantitative differences in phagocytosis and degradation of Pneumocystis carinii by alveolar macrophages in AIDS and non-HIV patients in vivo. Cytopathology 4, 231-236 (1993).
24. Mazzolini, J, Herit, F, Bouchet, J, Benmerah, A, Benichou, S & Niedergang, F. Inhibition of phagocytosis in HIV-1-infected macrophages relies on Nefdependent alteration of focal delivery of recycling compartments. Blood 115, 4226-4236 (2010).
25. Gordon, M.A., Gordon, S.B., Musaya, L, Zijlstra, E.E., Molyneux, M.E. & Read, R.C. Primary macrophages from HIV-infected adults show dysregulated cytokine responses to Salmonella, but normal internalization and killing. AIDS 21, 2399-2408 (2007).
26. Reardon, C.C., Kim, S.J., Wagner, R.P., Koziel, H & Kornfeld, H. Phagocytosis and growth inhibition of Cryptococcus neoformans by human alveolar macrophages: effects of HIV-1 infection. AIDS 10, 613-618 (1996).
27. Shellito, J.E. Failure of host defenses in human immunodeficiency virus. Semin. Respir. Crit. Care Med. 25, 73-84 (2004).
28. Shults, K, Flye-Blakemore, L, Patterson, B.K. & Elbeik, T. Analysis of multiple cell reservoirs expressing unspliced HIV-1 gag-pol mRNA in patients on antiretroviral therapy. Future Virol. 7, 819-832 (2012).
29. Shao, L & Sperber, K. Impaired regulation of HLA-DR expression in human immunodeficiency virus-infected monocytes. Clin. Diagn. Lab. Immunol. 9, 739-746 (2002).
30. Ancuta, P. et al. CD16+ monocytes exposed to HIV promote highly efficient viral replication upon differentiation into macrophages and interaction with T cells. Virology 344, 267-276 (2006).
31. Ellery, P.J. et al. The CD16+ monocyte subset is more permissive to infection and preferentially harbors HIV-1 in vivo. J. Immunol. 178, 6581-6589 (2007).
32. Pilling, D, Fan, T, Huang, D, Kaul, B & Gomer, R.H. Identification of markers that distinguish monocyte-derived fibrocytes from monocytes, macrophages, and fibroblasts. PLoS One 4, e7475 (2009).
33. Wahlstrom, J, Berlin, M, Skold, C.M.,Wigzell, H, Eklund, A & Grunewald, J. Phenotypic analysis of lymphocytes and monocytes/macrophages in peripheral blood and bronchoalveolar lavage fluid from patients with pulmonary sarcoidosis. Thorax 54, 339-346 (1999).
34. Lay, J.C., Alexis, N.E., Zeman, K.L., Peden, D.B. & Bennett, W.D. In vivo uptake of inhaled particles by airway phagocytes is enhanced in patients with mild asthma compared with normal volunteers. Thorax 64, 313-320 (2009).
35. Bowden, D.H. The alveolar macrophage. Environ. Health Perspect. 55, 327-341 (1984).
36. Landsman, L & Jung, S. Lung macrophages serve as obligatory intermediate between blood monocytes and alveolar macrophages. J. Immunol. 179, 3488-3494 (2007).
37. Lebargy, F, Branellec, A, Deforges, L, Bignon, J & Bernaudin, J.F. HIV-1 in human alveolar macrophages from infected patients is latent in vivo but replicates after in vitro stimulation. Am. J. Respir. Cell Mol. Biol. 10, 72-78 (1994).
38. Nakata, K, Weiden, M, Harkin, T, Ho,D& Rom,W.N. 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. Mol. Med. 1, 744-757 (1995).
39. Aderem, A & Underhill, D.M. Mechanisms of phagocytosis in macrophages. Annu. Rev. Immunol. 17, 593-623 (1999).
40. Yates, R.M., Hermetter, A, Taylor, G.A. & Russell, D.G. Macrophage activation downregulates the degradative capacity of the phagosome. Traffic 8, 241-250 (2007).
41. Twigg, H.L. 3rd et al. Production of interferon-gamma by lung lymphocytes in HIV-infected individuals. Am. J. Physiol. 276, L256-L262 (1999).
42. Buhl, R. et al. Activation of alveolar macrophages in asymptomatic HIVinfected individuals. J. Immunol. 150, 1019-1028 (1993).
43. Wahlström, J, Berlin, M, Sköld,C.M.,Wigzell, H, Eklund, A & Grunewald, J. Phenotypic analysis of lymphocytes and monocytes/macrophages in peripheral blood and bronchoalveolar lavage fluid from patients with pulmonary sarcoidosis. Thorax 54, 339-346 (1999).
44. Kalsdorf, B. et al. HIV-1 infection impairs the bronchoalveolar T-cell response to mycobacteria. Am. J. Respir.Crit. Care Med. 180, 1262-1270 (2009).
45. Jambo, K.C. et al. Bronchoalveolar CD4+ T cell responses to respiratory antigens are impaired in HIV-infected adults. Thorax 66, 375-382 (2011).
46. Lewin, S.R., Kirihara, J, Sonza, S, Irving, L, Mills, J & Crowe, S.M. HIV-1 DNA and mRNA concentrations are similar in peripheral blood monocytes and alveolar macrophages in HIV-1-infected individuals. AIDS 12, 719-727 (1998).
47. Meltzer, M.S. et al. Macrophages and the human immunodeficiency virus. Immunol. Today 11, 217-223 (1990).
48. Gordon, S.B. et al. Inhaled delivery of 23-valent pneumococcal polysaccharide vaccine does not result in enhanced pulmonary mucosal immunoglobulin responses. Vaccine 26, 5400-5406 (2008).
49. Mwandumba, H.C. et al. Alveolar macrophages from HIV-infected patients with pulmonary tuberculosis retain the capacity to respond to stimulation by lipopolysaccharide. Microbes Infect. 9, 1053-1060 (2007).
50. Raj, A, van den Bogaard, P, Rifkin, S.A., van Oudenaarden, A & Tyagi, S. Imaging individual mRNA molecules using multiple singly labeled probes. Nat. Methods 5, 877-879 (2008).