Reduced binding and phagocytosis of Pneumocystis carinii by alveolar macrophages from persons infected with HIV-1 correlates with mannose receptor downregulation

Journal of Clinical Investigation

Volumn 102, Issue 7, 1998, Pages 1332-1344

  Koziel, Henry ^a   Eichbaum, Quentin ^b   Kruskal, Benjamin A ^b   Pinkston, Paula ^a   Rogers, Rick A ^c   Armstrong, Martine Y K ^d   Richards, Frank F ^d   Rose, Richard M ^e   Ezekowitz, R Alan B ^b  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e Stem Cells Inc   (United States)

Author keywords

Alveolar macrophages; HIV 1; Innate immunity; Mannose receptor; P. carinii

Indexed keywords

CD4 ANTIGEN; MANNOSE RECEPTOR; MESSENGER RNA;

ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; ENDOCYTOSIS; FEMALE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; LUNG ALVEOLUS MACROPHAGE; MACROPHAGE FUNCTION; MALE; NONHUMAN; OPPORTUNISTIC INFECTION; PHAGOCYTOSIS; PNEUMOCYSTIS PNEUMONIA; PRIORITY JOURNAL; RECEPTOR BINDING; RESPIRATORY TRACT INFECTION; VIRUS INFECTION;

EID: 0032189102     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI560     Document Type: Article

References (68)

1. Murray, J., and J. Mills. 1990. Pulmonary infectious complications of human immunodeficiency virus infection. Part I. Am. Rev. Respir. Dis. 141:1356-1372.
2. Wallace, J.M., N.I. Hansen, L. Lavange, J. Glassroth, B.L. Browdy, M.J. Rosen, P.A. Kvale, B.T. Mangura, L.B. Reichman, P.C. Hopewell, and the Pulmonary Complications of H.I.V. Group. 1997. Respiratory disease trends in the Pulmonary Complications of HIV Infection Study cohort. Am. J. Respir. Crit. Care Med. 155:72-80.
3. Phair, J., A. Munoz, R. Detels, R. Kaslow, C. Rinaldo, and A. Saah. 1990. The risk of Pneumocystis carinii pneumonia among men infected with human immunodeficiency virus type 1. N. Engl. J. Med. 322:161-165.
4. Masur, H., F.P. Ognibene, R. Yarchoan, J.H. Shelhamer, B.F. Baird, W. Travis, A.F. Suffredini, L. Deyton, J.A. Kovacs, J. Falloon, et al. 1989. CD4 counts as predictors of opportunistic pneumonias in human immunodeficiency virus (HIV) infection. Ann. Intern. Med. 111:223-231.
5. Shellito, J.E., V.V. Suzara, W. Blumenfeld, J.M. Beck, H.J. Steger, and T.H. Ermak. 1990. A new model of Pneumocystis carinii infection in mice selectively depleted of helper T lymphocytes. J. Clin. Invest. 85:1686-1693.
6. + cells in resistance to Pneumocystis carinii pneumonia in mice. J. Exp. Med. 172:937-945.
7. Roths, J.B., J.D. Marshall, R.D. Allen, G.A. Carlson, and C.L. Sidman. 1990. Spontaneous Pneumocystis carinii pneumonia in immunodeficient mutant scid mice. Am. J. Pathol. 136:1173-1186.
8. Fels, A., and Z. Cohn. 1986. The alveolar macrophage. J. Appl. Physiol. 60:353-369.
9. Limper, A.H., J.S. Hoyte, and J.E. Standing. 1997. The role of alveolar macrophages in Pneumocystis carinii degradation and clearance from the lung. J. Clin. Invest. 99:2110-2117.
10. Barton, E., and W. Campbell. 1969. Pneumocystis carinii in lungs of rats treated with cortisone acetate. Am. J. Pathol. 54:209-236.
11. + lymphocyte-depleted mice given aerosols of heat-treated Escherichia coli. J. Exp. Med. 176:881-886.
12. Ezekowitz, R.A.B., D.J. Williams, H. Koziel, M.Y.K. Armstong, A. Warner, F.F. Richards, and R.M. Rose. 1991. Uptake of Pneumocystis carinii mediated by the macrophage mannose receptor. Nature. 351:155-158.
13. Hidalgo, H.A., R.J. Helmke, V.F. German, and J.A. Mangos. 1992 Pneumocystis carinii induces an oxidative burst in alveolar macrophages. Infect. Immun. 60:1-7.
14. Masur, H., and T.C. Jones. 1978. The interaction in vitro of Pneumocystis carinii with macrophages and L cells. J. Exp. Med. 147:157-170.
15. von Behren, L.A., and E.L. Pesanti. 1978. Uptake and degradation of Pneumocystis carinii by macrophages in vitro. Am. Rev. Respir. Dis. 118:1051-1059.
16. Pottratz, S.T., J. Paulsrud, J.S. Smith, and W.J. Martin. 1991. Pneumocystis carinii attachment to cultured lung cells by Pneumocystis gp120, a fibronectin binding protein. J. Clin. Invest. 88:403-407.
17. Forte, M., M. Rahelu, C. Stubberfield, L. Tomkins, A. Pithie, and D. Kumararatne. 1991. In-vitro interaction of human macrophages with Pneumocystis carinii. Int. J. Exp. Pathol. 72:589-598.
18. Taylor, M.B., M. Phillips, and C.S.F. Easmon. 1992. Opsonophagocytosis of Pneumocystis carinii. J. Med. Microbiol. 36:223-228.
19. Ezekowitz, R.A.B., K. Sastry, P. Bailly, and A. Warner. 1990. Molecular characterization of the human macrophage mannose receptor. Demonstration of multiple carbohydrate recognition-like domains and phagocytosis of yeasts in Cos-1 cells. J. Exp. Med. 172:1785-1794.
20. Stahl, P.D. 1990. The macrophage mannose receptor: current status. Am. J. Respir. Cell Mol. Biol. 2:317-318.
21. Taylor, M.E., J.T. Conary, M.R. Lennartz, P.D. Stahl, and K. Drickamer. 1990. Primary structure of the mannose receptor contains multiple motifs resembling carbohydrate-recognition domains. J. Biol. Chem. 265:12156-12162.
22. Radding, J.A., M.Y.K. Armstrong, E. Ullu, and F.F. Richards. 1989. Identification and isolation of a major cell surface glycoprotein of Pneumocystis carinii. Infect. Immun. 57:2149-2157.
23. O'Riordan, D.M., J.E. Standing, and A.H. Limper. 1995. Pneumocystis carinii glycoprotein A binds macrophage mannose receptors. Infect. Immun. 63: 779-784.
24. Ezekowitz, R.A.B. 1992. The mannose receptor and phagocytosis. In Mononuclear Phagocytes. Rv. Furth, editor. Kluwer Academic Publishers, The Netherlands. 208-213.
25. Ofek, I., J. Goldhar, Y. Keisari, and N. Sharon. 1995. Nonopsonic phagocytosis of microorganisms. Annu. Rev. Microbiol. 49:239-276.
26. Fearon, D.T., and R.M. Locksley. 1996. The instructive role of innate immunity in the acquired immune response. Science. 272:50-54.
27. Salahuddin, S.Z., R.M. Rose, J.E. Groopman, P.D. Markham, and R.C. Gallo. 1986. Human T lymphotropic virus type III infection of human alveolar macrophages. Blood. 68:281-284.
28. Smith, P.D., K. Ohura, H. Masur, H.C. Lane, A.S. Fauci, and S.M. Wahl. 1984. Monocyte function in the acquired immune deficiency syndrome. Defective chemotaxis. J. Clin. Invest. 74:2121-2128.
29. Belsito, D., M. Sanchez, R. Baer, F. Valentine, and G. Thorbecke. 1984. Reduced Langerhans cell Ia antigen and ATPase activity in patients with the acquired immunodeficiency syndrome. N. Engl. J. Med. 310:1279-1282.
30. Roy, S., L. Fitz-Gibbon, L. Poulin, and M. Wainberg. 1988. Infection of human monocyte/macrophages by HIV-1: effect on secretion of IL-1 activity. Immunology. 64:233-239.
31. Bender, B., M. Frank, T. Lawley, W. Smith, C. Brinkman, and T. Quinn. 1985. Defective reticuloendothelial system Fc-receptor function in patients with acquired immunodeficiency syndrome. J. Infect. Dis. 152:409-412.
32. Holmskov, U., R. Malhotra, R.B. Sim, and J.C. Jensenius. 1994. Collectins: collagenous C-type lectins of the innate immune defense system. Immunol. Today. 15:67-74.
33. Sastry, K., and R.A.B. Ezekowitz. 1993. Collectins: pattern recognition molecules involved in first line host defense. Curr. Opin. Immunol. 5:59-66.
34. Hunninghake, G., J. Gadek, O. Kawanami, V. Ferrans, and R. Crystal. 1979. Inflammatory and immune processes in the human lung in health and disease: evaluation by bronchoalveolar lavage. Am. J. Pathol. 97:149-206.
35. Armstrong, M.Y.K, and F.F. Richards. 1989. Propagation and purification of rat Pneumocystis carinii in short-term cell culture. J. Prolozool. 36:24S-27S.
36. Armstrong, M.Y.K., and M.T. Cushion. 1993. Animal models. In Pneumocystis carinii Pneumonia. 2nd ed. P.D. Walzer, editor. Marcel Dekker, Inc., New York. 182-187.
37. Williams, D.J., J.A. Radding, A. Dell, K.-H. Khoo, M.E. Rogers, F.F. Richards, and M.Y.K. Armstrong. 1991. Glucan synthesis in Pneumocystis carinii. J. Protozool. 38:427-437.
38. Armstrong, M.Y.K., H. Koziel, R.M. Rose, C. Arena, and F.F. Richards. 1991. Indicators of Pneumocystis carinii viability in short-term culture. J. Protozool. 38:88S-90S.
39. Morganelli, P.M., R.A. Rogers, T.J. Kitzmiller, and A. Bergeron. 1995. Enhanced metabolism of LDL aggregates mediated by specific human monocyte IgG Fc receptors. J. Lipid Res. 36:714-724.
40. Greenspan, P., E.P. Mayer, and S.D. Fowler. 1987. Nile red: a selective fluorescent stain for intracellular lipid droplets. J. Cell biol. 100:965-972.
41. Nicholson, J.D.A., and S.W. Browning. 1994. Ability of OptiLyse lysing/ fixing reagents to inactivate HIV-infected H9 cells in whole blood. J. Immunol. Methods. 168:283-284.
42. Hoppe, C., and Y. Lee. 1983. The binding and processing of mannosebovine serum albumin derivatives by rabbit alveolar macrophages. J. Biol. Chem. 258:14193-14199.
43. Ezekowitz, R.A.B., J. Austyn, P.D. Stahl, and S. Gordon. 1981. Surface properties of Bacillus Calmette-Guerin activated mouse macrophages. Reduced expression of mannose-specific endocytosis, Fc receptors and antigen F4/ 80 accompanies induction of Ia. J. Exp. Med. 154:60-76.
44. Stahl, P., P.H. Schleshinger, E. Sigardson, J.S. Rodman, and Y.C. Lee. 1980. Receptor-mediated pinocytosis of mannose glycoconjugates by macrophages: characterization and evidence for receptor recycling. Cell. 19:207-215.
45. O'Riordan, T.G., R.P. Baughman, M.N. Dohn, and G.C. Smaldone. 1994. Lobar pentamidine levels and Pneumocystis carinii pneumonia following aerosolized pentamidine. Chest. 105:53-56.
46. Young, L.S. 1982. Trimethoprim-sulfamethoxazole in the treatment of adults with pneumonia due to Pneumocystis carinii. Rev. Infect. Dis. 4:608-613.
47. Yarchoan, R., R.W. Klecker, K.J. Weinhold, P.D. Markham, H.K. Lyerly, D.T. Durack, E. Gelman, S.N. Lehrman, R.M. Blum, and D.W. Barry. 1986. Administration of 3-azido-3-deoxythymidine, an inhibitor of HTLV-III/ LAV replication, to patients with AIDS or AIDS-related complex. Lancet. 1: 575-580.
48. Bensson, R., A. Sanfridson, J. Ottinger, C. Doyle, and B. Cullen. 1993. Downregulation of cell-surface CD4 expression by simian immunodeficiency virus Nef prevents super infection. J. Exp. Med. 177:1561-1566.
49. Willey, R., F. Maldarelli, M. Martin, and K. Strebel. 1992. HIV-1 vpu protein induces rapid degradation of CD4. J. Virol. 66:7193-7200.
50. Kerkau, T., I. Bacik, J.R. Bennink, J. W. Yewdell, T. Hunig, A. Schimpl, and U. Schubert. 1997. The human immunodeficiency virus type 1 (HIV-1) Vpu protein interferes with an early step in the biosynthesis of major histocompatibility complex (MHC) class I molecules. J. Exp. Med. 185:1295-1305.
51. Lu, W., and D. Israel-Biet. 1993. Virion concentration in bronchoalveolar lavage fluids of HIV-infected patients. Lancet. 342:298.
52. Nakata, K., W.N. Rom, Y. Honda, R. Condos, S. Kanegasaki, Y. Cao, and M. Weiden. 1997. Mycobacterium tuberculosis enhances human immunodeficiency virus-1 replication in the lung. Am. J. Respir. Crit. Care Med. 155: 996-1003.
53. Larkin, M., R. Childs, and T. Matthews. 1989. Oligosaccharide-mediated interactions of the envelope gp120 of HIV-1 that are dependent on CD4 recognition. AIDS. 3:793-798.
54. Berton, G., and S. Gordon. 1983. Modulation of macrophage mannosylspecific receptors by cultivation on immobilized zymosan. Effects on superoxide-anion release and phagocytosis. Immunology. 49:705-715.
55. Fan, J., H.Z. Bass, and J.L. Fahey. 1993. Elevated IFN-γ and decreased IL-2 gene expression are associated with HIV infection. J. Immunol. 151:5031-5040.
56. Buhl, R., H.A. Jaffe, K.J. Holroyd, Z. Borok, J.H. Roum, A. Mastrangeli, F.B. Wells, M. Kirby, C. Saltini, and R.G. Crystal. 1993. Activation of alveolar macrophages in asymptomatic HIV-infected individuals. J. Immunol. 150:1019-1028.
57. Harris, N., M. Super, M. Rits, G. Chang, and R.A.B. Ezekowitz. 1992. Characterization of the murine macrophage mannose receptor: demonstration that the downregulation of receptor expression mediated by interferon-γ occurs at the level of transcription. Blood. 80:2363-2373.
58. Marodi, L., S. Schreiber, D.C. Anderson, R.P. MacDermott, H.M. Korchak, and R.B.J. Johnston. 1993. Enhancement of macrophage candidacidal activity by Interferon-γ. Increased phagocytosis, killing, and calcium signal mediated by a decreased number of mannose receptors. J. Clin. Invest. 91:2596-2601.
59. Raveh, D., B.A. Kruskal, J. Farland, and R.A. Ezekowitz. 1998. Th1 and Th2 cytokines cooperate to stimulate mannose-receptor-mediated phagocytosis. J. Leukoc. Biol. 64:108-113.
60. Shepherd, V.L., R. Abdolrasulnia, M. Garrett, and H.B. Cowan. 1990. Down-regulation of mannose receptor activity in macrophages after treatment with lipopolysaccharide and phorbol esters. J. Immunol. 145:1530-1536.
61. Shepherd, V.L., M.G. Konish, and P. Stahl. 1985. Dexamethasone increases expression of mannose receptors and decreases extracellular lysosomal enzyme accumulation in macrophages. J. Biol. Chem. 260:160-164.
62. Pottratz, S.T., and W.J. Martin. 1990. Mechanism of Pneumocystis carinii attachment to cultured rat alveolar macrophages. J. Clin. Invest. 86:1678-1683.
63. Neese, L.W., J.E. Standing, E.J. Olson, M. Castro, and A.H. Limper. 1994. Vitronectin, fibronectin, and gp120 antibody enhance macrophage release of TNF-α in response to Pneumocystis carinii. J. Immunol. 152:4549-4556.
64. Williams, M.D., J.R. Wright, K.L March, and W.J. Martin, II. 1997. Human surfactant protein A enhances attachment of Pneumocystis carinii to rat alveolar macrophages. Am. J. Respir. Cell Mol. Biol. 14:232-238.
65. O'Riordan, D., J. Standing, K. Kwon, D. Chang, E. Crouch, and A. Limper. 1995. Surfactant protein D interacts with Pneumocystis carinii and mediates organism adherence to alveolar macrophages. J. Clin. Invest. 95:2699-2710.
66. Bermudez, L.E., L.S. Young, and H. Enkel. 1991. Interaction of Mycobacterium avium complex with human macrophages: roles of membrane receptors and serum proteins. Infect. Immun. 59:1697-1702.
67. Bolanos, B., and T.G. Mitchell. 1989. Phagocytosis and killing of Cryptococcus neoformans by rat alveolar macrophages in the absence of serum. J. Leukoc. Biol. 46:521-528.
68. Schlesinger, L.S. 1993. Macrophage phagocytosis of virulent but not attenuated strains of Mycobacterium tuberculosis is mediated by mannose receptors in addition to complement receptors. J. Immunol. 150:2920-2930.