Home LiteratureArticle Details
PMID: 10799594 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Involvement of the mannose receptor in infection of macrophages by influenza virus.

Journal of virology ·Vol. 74 ·No. 11 ·2000-06-00 ·Pages 5190-7

Reading PC, Miller JL, Anders EM

Abstract

Influenza viruses A/PR/8/34 (PR8; H1N1), A/Aichi/68 X-31 (HKx31; H3N2), and A/Beijing/89 X-109 (BJx109; H3N2) show marked differences in their ability to infect murine macrophages, including resident alveolar and peritoneal macrophages as well as the macrophage-derived cell line J774. The hierarchy in infectivity of the viruses (PR8 < HKx31 < BJx109) resembles that of their reactivity with mannose-binding lectins of the collectin family. Since the macrophage mannose receptor recognizes the same spectrum of monosaccharides as the collectins do, we investigated the possible involvement of this receptor in infection of macrophages by influenza virus. In competitive binding studies, the binding of (125)I-labeled mannosylated bovine serum albumin to macrophages was inhibited by the purified hemagglutinin and neuraminidase (HANA) glycoproteins of influenza virus but not by HANA that had been treated with periodate to oxidize its oligosaccharide side chains. The inhibitory activity of HANA from the three strains of virus differed markedly and correlated with the infectivity of each virus for macrophages. Infection of macrophages, but not MDCK cells, by influenza virus was inhibited by yeast mannan. A variant line of J774 cells, J774E, which expresses elevated levels of the mannose receptor, was more readily infected than J774, and the sensitivity of J774E cells to infection was greatly reduced by culture in the presence of D-mannose, which down-modulated mannose receptor expression. Together, the data implicate the mannose receptor as a major endocytic receptor in the infectious entry of influenza virus, and perhaps other enveloped viruses, into murine macrophages.

MeSH Terms
Animals Cell Line Cells, Cultured Dogs Hemagglutinin Glycoproteins, Influenza Virus/metabolism Humans Influenza A virus/metabolism,physiology Lectins, C-Type Macrophages, Alveolar/cytology,metabolism,virology Macrophages, Peritoneal/cytology,metabolism,virology Mannans/metabolism Mannose Receptor Mannose-Binding Lectins Mice Mice, Inbred BALB C Mice, Inbred C57BL N-Acetylneuraminic Acid/metabolism Neuraminidase/metabolism Receptors, Cell Surface/metabolism
Chemicals
Hemagglutinin Glycoproteins, Influenza Virus Lectins, C-Type Mannans Mannose Receptor Mannose-Binding Lectins Receptors, Cell Surface Neuraminidase N-Acetylneuraminic Acid
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Reading P C
Department of Microbiology and Immunology, University of Melbourne, Parkville, Victoria 3052, Australia.
Miller J L
Anders E M
References (50)
50 references, click to expand
  1. Mannose receptor.
    Int Rev Cytol. 1992;137B:221-44 PMID: 1478821
  2. Analysis of the restriction to the growth of nonegg-adapted human influenza virus in eggs.
    Virology. 1993 Oct;196(2):660-5 PMID: 8372439
  3. Comparison of 10 influenza A (H1N1 and H3N2) haemagglutinin sequences obtained directly from clinical specimens to those of MDCK cell- and egg-grown viruses.
    J Gen Virol. 1993 Nov;74 ( Pt 11):2513-8 PMID: 8245870
  4. Role of macrophage cytokines in influenza A virus infections.
    Immunobiology. 1993 Nov;189(3-4):340-55 PMID: 8125516
  5. Complement-dependent neutralization of influenza virus by a serum mannose-binding lectin.
    J Gen Virol. 1994 Mar;75 ( Pt 3):615-22 PMID: 8126457
  6. Collectins: collagenous C-type lectins of the innate immune defense system.
    Immunol Today. 1994 Feb;15(2):67-74 PMID: 8155265
  7. The asialoglycoprotein receptor is a potential liver-specific receptor for Marburg virus.
    J Gen Virol. 1995 Feb;76 ( Pt 2):393-9 PMID: 7844558
  8. Infection of cells by varicella zoster virus: inhibition of viral entry by mannose 6-phosphate and heparin.
    Proc Natl Acad Sci U S A. 1995 Apr 11;92(8):3546-50 PMID: 7724595
  9. Role of mannose-6-phosphate receptors in herpes simplex virus entry into cells and cell-to-cell transmission.
    J Virol. 1995 Jun;69(6):3517-28 PMID: 7745699
  10. Target cell membrane sialic acid modulates both binding and fusion activity of influenza virus.
    Biochim Biophys Acta. 1995 Jun 14;1236(2):323-30 PMID: 7794972
  11. Identification of a 40-kDa cell surface sialoglycoprotein with the characteristics of a major influenza C virus receptor in a Madin-Darby canine kidney cell line.
    J Biol Chem. 1995 Jul 28;270(30):17815-22 PMID: 7629082
  12. Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products.
    J Exp Med. 1995 Aug 1;182(2):389-400 PMID: 7629501
  13. Nonopsonic phagocytosis of microorganisms.
    Annu Rev Microbiol. 1995;49:239-76 PMID: 8561460
  14. Biosynthesis and processing of the mannose receptor in human macrophages.
    J Biol Chem. 1989 Feb 5;264(4):2385-90 PMID: 2914913
  15. The macrophage mannose receptor: current status.
    Am J Respir Cell Mol Biol. 1990 Apr;2(4):317-8 PMID: 2182080
  16. Bovine and mouse serum beta inhibitors of influenza A viruses are mannose-binding lectins.
    Proc Natl Acad Sci U S A. 1990 Jun;87(12):4485-9 PMID: 2162043
  17. Antibodies to HA and NA augment uptake of influenza A viruses into cells via Fc receptor entry.
    Virology. 1991 May;182(1):211-9 PMID: 2024464
  18. Binding of tissue-type plasminogen activator by the mannose receptor.
    J Biol Chem. 1991 Jul 25;266(21):13931-5 PMID: 1906888
  19. Structural requirements for high affinity binding of complex ligands by the macrophage mannose receptor.
    J Biol Chem. 1993 Jan 5;268(1):399-404 PMID: 8416946
  20. Delayed activation of the mannose receptor following synthesis. Requirement for exit from the endoplasmic reticulum.
    J Biol Chem. 1996 Nov 29;271(48):30736-40 PMID: 8940052
  21. The mannose receptor delivers lipoglycan antigens to endosomes for presentation to T cells by CD1b molecules.
    Immunity. 1997 Feb;6(2):187-97 PMID: 9047240
  22. Sendai virus efficiently infects cells via the asialoglycoprotein receptor and requires the presence of cleaved F0 precursor proteins for this alternative route of cell entry.
    J Virol. 1997 Jul;71(7):5481-6 PMID: 9188621
  23. The mannose receptor functions as a high capacity and broad specificity antigen receptor in human dendritic cells.
    Eur J Immunol. 1997 Sep;27(9):2417-25 PMID: 9341788
  24. Collectin-mediated antiviral host defense of the lung: evidence from influenza virus infection of mice.
    J Virol. 1997 Nov;71(11):8204-12 PMID: 9343171
  25. Alveolar macrophages regulate the induction of primary cytotoxic T-lymphocyte responses during influenza virus infection.
    J Virol. 1997 Dec;71(12):9450-7 PMID: 9371606
  26. Mechanisms of anti-influenza activity of surfactant proteins A and D: comparison with serum collectins.
    Am J Physiol. 1997 Dec;273(6 Pt 1):L1156-66 PMID: 9435570
  27. The mannose receptor is a pattern recognition receptor involved in host defense.
    Curr Opin Immunol. 1998 Feb;10(1):50-5 PMID: 9523111
  28. The mannose receptor mediates induction of IFN-alpha in peripheral blood dendritic cells by enveloped RNA and DNA viruses.
    J Immunol. 1998 Sep 1;161(5):2391-9 PMID: 9725235
  29. Potential role of the mannose receptor in antigen transport.
    Immunol Lett. 1999 Jan;65(1-2):9-13 PMID: 10065620
  30. Membrane fusion by surrogate receptor-bound influenza haemagglutinin.
    Virology. 1999 May 10;257(2):415-23 PMID: 10329552
  31. Virus infection activates IL-1 beta and IL-18 production in human macrophages by a caspase-1-dependent pathway.
    J Immunol. 1999 Jun 15;162(12):7322-9 PMID: 10358182
  32. THE PREPARATION OF I-131-LABELLED HUMAN GROWTH HORMONE OF HIGH SPECIFIC RADIOACTIVITY.
    Biochem J. 1963 Oct;89:114-23 PMID: 14097352
  33. Fractionation of glycopeptides by affinity column chromatography on concanavalin A-sepharose.
    J Biochem. 1975 Oct;78(4):687-96 PMID: 1213987
  34. Host defense mechanisms against influenza virus: interaction of influenza virus with murine macrophages in vitro.
    Infect Immun. 1978 Dec;22(3):758-62 PMID: 569645
  35. Structural determinants of concanavalin A specificity for oligosaccharides.
    J Biol Chem. 1979 Apr 10;254(7):2400-7 PMID: 85625
  36. Host cell- and virus strain-dependent differences in oligosaccharides of hemagglutinin glycoproteins of influenza A viruses.
    Virology. 1979 May;95(1):8-23 PMID: 442545
  37. Receptor-mediated pinocytosis of mannose glycoconjugates by macrophages: characterization and evidence for receptor recycling.
    Cell. 1980 Jan;19(1):207-15 PMID: 6766809
  38. Gene composition of high-yielding influenza vaccine strains obtained by recombination.
    J Infect Dis. 1980 Mar;141(3):362-5 PMID: 7365284
  39. Antigenic drift between the haemagglutinin of the Hong Kong influenza strains A/Aichi/2/68 and A/Victoria/3/75.
    Nature. 1980 Aug 21;286(5775):771-6 PMID: 7402351
  40. Interaction of influenza virus with mouse macrophages.
    Infect Immun. 1981 Feb;31(2):751-7 PMID: 6260676
  41. Surface properties of bacillus Calmette-Guérin-activated mouse macrophages. Reduced expression of mannose-specific endocytosis, Fc receptors, and antigen F4/80 accompanies induction of Ia.
    J Exp Med. 1981 Jul 1;154(1):60-76 PMID: 7019381
  42. Nucleotide sequence of the haemagglutinin gene of a human influenza virus H1 subtype.
    Nature. 1981 Jul 2;292(5818):72-5 PMID: 7278968
  43. Infectious entry pathway of influenza virus in a canine kidney cell line.
    J Cell Biol. 1981 Dec;91(3 Pt 1):601-13 PMID: 7328111
  44. Selective diminution of the binding of mannose by murine macrophages in the late stages of activation.
    J Biol Chem. 1982 May 10;257(9):5129-35 PMID: 7040394
  45. The antigenic structure of the influenza virus A/PR/8/34 hemagglutinin (H1 subtype).
    Cell. 1982 Dec;31(2 Pt 1):417-27 PMID: 6186384
  46. The binding and processing of mannose-bovine serum albumin derivatives by rabbit alveolar macrophages. Effect of the sugar density.
    J Biol Chem. 1983 Dec 10;258(23):14193-9 PMID: 6643476
  47. An alternative route of infection for viruses: entry by means of the asialoglycoprotein receptor of a Sendai virus mutant lacking its attachment protein.
    Proc Natl Acad Sci U S A. 1985 Feb;82(4):978-82 PMID: 2983337
  48. Differential infection of receptor-modified host cells by receptor-specific influenza viruses.
    Virus Res. 1985 Sep;3(2):165-79 PMID: 4060886
  49. Generation of macrophage variants with 5-azacytidine: selection for mannose receptor expression.
    J Leukoc Biol. 1987 Nov;42(5):485-90 PMID: 2445884
  50. Antibody-mediated growth of influenza A NWS virus in macrophagelike cell line P388D1.
    J Virol. 1988 Jan;62(1):20-6 PMID: 3334744
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
2000-06-00
Pages
5190-7
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC110872
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]