Collectin-mediated antiviral host defense of the lung: evidence from influenza virus infection of mice

Collagenous lectins (collectins) present in mammalian serum and pulmonary fluids bind to influenza virus and display antiviral activity in vitro, but their role in vivo has yet to be determined. We have used early and late isolates of H3N2 subtype influenza viruses that differ in their degree of glycosylation to examine the relationship between sensitivity to murine serum and pulmonary lectins in vitro and the ability of a virus to replicate in the respiratory tract of mice. A marked inverse correlation was found between these two parameters. Early H3 isolates (1968 to 1972) bear 7 potential glycosylation sites on hemagglutinin (HA), whereas later strains carry 9 or 10. Late isolates were shown to be much more sensitive than early strains to neutralization by the mouse serum mannose-binding lectin (MBL) and rat lung surfactant protein D (SP-D) and bound greater levels of these lectins in enzyme-linked immunosorbent assays and Western blot analyses. They also replicated very poorly in mouse lungs compared to the earlier strains. Growth in the lungs was greatly enhanced, however, if saccharide inhibitors of the collectins were included in the virus inoculum. The level of SP-D in bronchoalveolar lavage fluids increased on influenza virus infection. MBL was absent from lavage fluids of normal mice but could be detected in fluids from mice 3 days after infection with the virulent strain A/PR/8/34 (H1N1). The results implicate SP-D and possibly MBL as important components of the innate defense of the respiratory tract against influenza virus and indicate that the degree or pattern of glycosylation of a virus can be an important factor in its virulence.

[1]  L. Simonsen,et al.  The impact of influenza epidemics on mortality: introducing a severity index. , 1997, American journal of public health.

[2]  B. Benaissa-Trouw,et al.  Surfactant protein A, but not surfactant protein D, is an opsonin for influenza A virus phagocytosis by rat alveolar macrophages , 1997, European journal of immunology.

[3]  Malcolm W. Turner Mannose-binding lectin: the pluripotent molecule of the innate immune system. , 1996, Immunology today.

[4]  S. Hawgood,et al.  Localization and Developmental Expression of Surfactant Proteins D and A in the Respiratory Tract of the Mouse , 1996, Pediatric Research.

[5]  J. Jensenius,et al.  Neutrophil deactivation by influenza A viruses: mechanisms of protection after viral opsonization with collectins and hemagglutination-inhibiting antibodies. , 1996, Blood.

[6]  S. Abe,et al.  Decreased contents of surfactant proteins A and D in BAL fluids of healthy smokers. , 1996, Chest.

[7]  P. Reading,et al.  A serum mannose-binding lectin mediates complement-dependent lysis of influenza virus-infected cells. , 1995, Biochemical and biophysical research communications.

[8]  A. Trkola,et al.  Mucosal model of immunization against human immunodeficiency virus type 1 with a chimeric influenza virus , 1995, Journal of virology.

[9]  M. Turner,et al.  Mannose binding protein gene mutations associated with unusual and severe infections in adults , 1995, The Lancet.

[10]  M. Harmsen,et al.  Interactions of surfactant protein A with influenza A viruses: binding and neutralization. , 1995, The Journal of infectious diseases.

[11]  S. Thiel,et al.  Binding of human collectins (SP-A and MBP) to influenza virus. , 1994, The Biochemical journal.

[12]  Hansjörg Hoppe,et al.  Collectins — soluble proteins containing collagenous regions and lectin domains — and their roles in innate immunity , 1994, Protein science : a publication of the Protein Society.

[13]  K. Hartshorn,et al.  Evidence for a protective role of pulmonary surfactant protein D (SP-D) against influenza A viruses. , 1994, The Journal of clinical investigation.

[14]  A. Persson,et al.  Recombinant pulmonary surfactant protein D. Post-translational modification and molecular assembly. , 1994, The Journal of biological chemistry.

[15]  S. Thiel,et al.  Mannan‐Binding Protein and Bovine Conglutinin Mediate Enhancement of Herpes Simplex Virus Type 2 Infection in Mice , 1994, Scandinavian journal of immunology.

[16]  P. Reading,et al.  Complement-dependent neutralization of influenza virus by a serum mannose-binding lectin. , 1994, The Journal of general virology.

[17]  J. Jensenius,et al.  Collectins: collagenous C-type lectins of the innate immune defense system. , 1994, Immunology today.

[18]  S. Thiel,et al.  Purification and Characterization of Mannan‐Binding Protein from Mouse Serum , 1994, Scandinavian journal of immunology.

[19]  K. Hartshorn,et al.  Conglutinin acts as an opsonin for influenza A viruses. , 1993, Journal of immunology.

[20]  N. Cox,et al.  Comparison of 10 influenza A (H1N1 and H3N2) haemagglutinin sequences obtained directly from clinical specimens to those of MDCK cell- and egg-grown viruses. , 1993, The Journal of general virology.

[21]  S. Thiel,et al.  Complement activation upon binding of mannan‐binding protein to HIV envelope glycoproteins , 1993, AIDS.

[22]  K. Hartshorn,et al.  Human mannose-binding protein functions as an opsonin for influenza A viruses. , 1993, The Journal of clinical investigation.

[23]  A. Persson,et al.  Surfactant protein D: subcellular localization in nonciliated bronchiolar epithelial cells. , 1992, The American journal of physiology.

[24]  D. Jackson,et al.  Two distinct serum mannose-binding lectins function as beta inhibitors of influenza virus: identification of bovine serum beta inhibitor as conglutinin , 1992, Journal of virology.

[25]  E. Crouch,et al.  Interactions of surfactant protein D with bacterial lipopolysaccharides. Surfactant protein D is an Escherichia coli-binding protein in bronchoalveolar lavage. , 1992, The Journal of clinical investigation.

[26]  J. Lélias,et al.  Molecular characterization of the mouse mannose-binding proteins. The mannose-binding protein A but not C is an acute phase reactant. , 1991, Journal of immunology.

[27]  R. Levinsky,et al.  Molecular basis of opsonic defect in immunodeficient children , 1991, The Lancet.

[28]  N. Cox,et al.  Antigenic and genetic variation in influenza A (H1N1) virus isolates recovered from a persistently infected immunodeficient child , 1991, Journal of virology.

[29]  R. Webster,et al.  Measurement of anti-influenza neuraminidase antibody using a peroxidase-linked lectin and microtitre plates coated with natural substrates. , 1990, Journal of immunological methods.

[30]  S. Thiel,et al.  Human leukocyte C1q receptor binds other soluble proteins with collagen domains , 1990, The Journal of experimental medicine.

[31]  D. Jackson,et al.  Bovine and mouse serum beta inhibitors of influenza A viruses are mannose-binding lectins. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[32]  S. Thiel,et al.  ASSOCIATION OF LOW LEVELS OF MANNAN-BINDING PROTEIN WITH A COMMON DEFECT OF OPSONISATION , 1989, The Lancet.

[33]  Kenneth Reid,et al.  Structures and functions associated with the group of mammalian lectins containing collagen‐like sequences , 1989, FEBS letters.

[34]  J. Groopman,et al.  A human serum mannose-binding protein inhibits in vitro infection by the human immunodeficiency virus , 1989, The Journal of experimental medicine.

[35]  エゼコウィッツ、レイモンド・アラン・ブライアン Human mannose binding protein , 1988 .

[36]  K. Nakajima,et al.  Location on the evolutionary tree of influenza H3 haemagglutinin genes of Japanese strains isolated during 1985–6 season , 1988, Epidemiology and Infection.

[37]  C. M. Deom,et al.  Host cell-mediated selection of a mutant influenza A virus that has lost a complex oligosaccharide from the tip of the hemagglutinin. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[38]  W. J. Bean,et al.  Molecular changes in A/Chicken/Pennsylvania/83 (H5N2) influenza virus associated with acquisition of virulence. , 1986, Virology.

[39]  C. Naeve,et al.  Mutations in the hemagglutinin receptor-binding site can change the biological properties of an influenza virus , 1984, Journal of virology.

[40]  I. Wilson,et al.  A carbohydrate side chain on hemagglutinins of Hong Kong influenza viruses inhibits recognition by a monoclonal antibody. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[41]  N. Cox,et al.  Antigenic drift in influenza virus H3 hemagglutinin from 1968 to 1980: multiple evolutionary pathways and sequential amino acid changes at key antigenic sites , 1983, Journal of virology.

[42]  G. Air,et al.  Sequence of the hemagglutinin gene of influenza virus A/Memphis/1/71 and previously uncharacterized monoclonal antibody-derived variants. , 1983, Virology.

[43]  J. Yewdell,et al.  The antigenic structure of the influenza virus A/PR/8/34 hemagglutinin (H1 subtype) , 1982, Cell.

[44]  L. Brown,et al.  Antigenic determinants of influenza virus hemagglutinin--IX. The carbohydrate side chains from an Asian strain. , 1982, Molecular immunology.

[45]  C. Ward,et al.  Amino acid sequence and oligosaccharide distribution of the haemagglutinin from an early Hong Kong influenza virus variant A/Aichi/2/68 (X-31). , 1981, The Biochemical journal.

[46]  I. Wilson,et al.  Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 Å resolution , 1981, Nature.

[47]  L. Brown,et al.  Antigenic determinants of influenza virus hemagglutinin. VII. The carbohydrate side chains of A/Memphis/102/72 hemagglutinin heavy chain which cross-react with host antigen. , 1981, Virology.

[48]  D. Huylebroeck,et al.  Antigenic drift between the haemagglutinin of the Hong Kong influenza strains A/Aichi/2/68 and A/Victoria/3/75 , 1980, Nature.

[49]  G. Schild,et al.  Related studies of a recombinant influenza-virus vaccine. I. Derivation and characterization of virus and vaccine. , 1971, The Journal of infectious diseases.

[50]  R. Webster,et al.  Antiviral Activity of Antiserum Specific for an Influenza Virus Neuraminidase , 1968, Journal of virology.

[51]  P. Reading,et al.  Changes in the hemagglutinin molecule of influenza type A (H3N2) virus associated with increased virulence for mice , 1997, Archives of Virology.

[52]  L. Kinnunen,et al.  Evolution of the HA1 domain of human influenza A (H1N1) virus: loss of glycosylation sites and occurrence of herald and conserved strains. , 1995, The Journal of general virology.

[53]  J. Paulson,et al.  The N2 neuraminidase of human influenza virus has acquired a substrate specificity complementary to the hemagglutinin receptor specificity. , 1991, Virology.

[54]  E. D. Kilbourne Future influenza vaccines and the use of genetic recombinants. , 1969, Bulletin of the World Health Organization.

[55]  J. Schulman The role of antineuraminidase antibody in immunity to influenza virus infection. , 1969, Bulletin of the World Health Organization.

[56]  D. Jackson,et al.  Two Distinct Serum Mannose-Binding Lectins Function as Inhibitors of Influenza Virus : Identification of Bovine Serum Inhibitor as Conglutinin , 2022 .