Critical role for cross-linking of trimeric lectin domains of surfactant protein D in antiviral activity against influenza A virus

Biochemical Journal

Volumn 412, Issue 2, 2008, Pages 323-329

  Tecle, Tesfaldet ^a   White, Mitchell R ^a   Sorensen, Grith ^b   Gantz, Donald ^a   Kacak, Nilgun ^a   Holmskov, Uffe ^b   Smith, Kelly ^c   Crouch, Erika C ^c   Hartshorn, Kevan L ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Collectin; Influenza A virus; Lectin; Neutrophil; Surfactant protein D

Indexed keywords

BINDING SITES; CARBOHYDRATES; CROSSLINKING; ENZYME INHIBITION; LIGANDS; SURFACE ACTIVE AGENTS; VIRUSES;

COLLECTIN; INFLUENZA A VIRUS; LECTIN; NEUTROPHIL; SURFACTANT PROTEIN D;

PROTEINS;

MONOCLONAL ANTIBODY; SURFACTANT PROTEIN D;

AMINO TERMINAL SEQUENCE; ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; CROSS LINKING; INFLUENZA VIRUS A; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; VIRUS NEUTRALIZATION;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIVIRAL AGENTS; CELL LINE; HUMANS; INFLUENZA A VIRUS; LECTINS; MICE; NEURAMINIDASE; NEUTROPHILS; PROTEIN STRUCTURE, TERTIARY; PULMONARY SURFACTANT-ASSOCIATED PROTEIN D; RATS; RESPIRATORY BURST; VIRAL PROTEINS;

INFLUENZA A VIRUS;

EID: 44449126306     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20071663     Document Type: Article

References (30)

1. Hartshorn, K. L., Crouch, E. C., White, M. R., Eggleton, P., Tauber, A. I., Chang, D. and Sastry, K. (1994) Evidence for a protective role of pulmonary surfactant protein D (SP-D) against influenza A viruses. J. Clin. Invest. 94, 311-319
2. LeVine, A. M., Whitsett, J. A., Hartshorn, K. L., Crouch, E. C. and Korfhagen, T. R. (2001) Surfactant protein D enhances clearance of influenza A virus from the lung in vivo. J. Immunol. 167, 5868-5873
3. Atochina, E. N., Gow, A. J., Beck, J. M., Haczku, A., Inch, A., Kadire, H., Tomer, Y., Davis, C., Preston, A. M., Poulain, F. et al. (2004) Delayed clearance of pneumocystis carinii infection, increased inflammation, and altered nitric oxide metabolism in lungs of surfactant protein-D knockout mice. J. Infect. Dis. 189, 1528-1539
4. Giannoni, E., Sawa, T., Allen, L., Wiener-Kronish, J. and Hawgood, S. (2006) Surfactant proteins A and D enhance pulmonary clearance of Pseudomonas aeruginosa. Am. J. Respir. Cell Mol. Biol. 34, 704-710
5. Hawgood, S., Brown, C., Edmondson, J., Stumbaugh, A., Allen, L., Goerke, J., Clark, H. and Poulain, F. (2004) Pulmonary collectins modulate strain-specific influenza a virus infection and host responses. J. Virol. 78, 8565-8572
6. Jounblat, R., Clark, H., Eggleton, P., Hawgood, S., Andrew, P. W. and Kadioglu, A. (2005) The role of surfactant protein D in the colonisation of the respiratory tract and onset of bacteraemia during pneumococcal pneumonia. Respir. Res. 6, 126
7. Crouch, E., McDonald, B., Smith, K., Roberts, M., Mealy, T., Seaton, B. and Head, J. (2007) Critical role of Arg/Lys343 in the species-dependent recognition of phosphatidylinositol by pulmonary surfactant protein D. Biochemistry 46, 5160-5169
8. Clark, H., Palaniyar, N., Hawgood, S. and Reid, K. B. M. (2003) A recombinant fragment of human surfactant protein D reduces alveolar macrophage apoptosis and pro-inflammatory cytokines in mice developing pulmonary emphysema. Ann. N. Y. Acad. Sci. 1010, 113-116
9. Knudsen, L., Ochs, M., Mackay, R., Townsend, P., Deb, R., Muhlfeld, C., Richter, J., Gilbert, F., Hawgood, S., Reid, K. and Clark, H. (2007) Truncated recombinant human SP-D attenuates emphysema and type II cell changes in SP-D deficient mice. Respir. Res. 8, 70
10. Strong, P., Reid, K. and Clark, H. (2002) Intranasal delivery of a truncated recombinant human SP-D is effective at down-regulating allergic hypersensitivity in mice sensitized to allergens of Aspergillus fumigatus. Clin. Exp. Immunol. 130, 19-24
11. Hickling, T. P., Bright, H., Wing, K., Gower, D., Martin, S. L., Sim, R. B. and Malhotra, R. (1999) A recombinant trimeric surfactant protein D carbohydrate recognition domain inhibits respiratory syncytial virus infection in vitro and in vivo. Eur. J. Immunol. 29, 3478-3484
12. Crouch, E. C., Smith, K., McDonald, B., Briner, D., Linders, B., McDonald, J., Holmskov, U., Head, J. and Hartshorn, K. (2006) Species differences in the carbohydrate binding preferences of surfactant protein D. Am. J. Respir. Cell Mol. Biol. 35, 84-94
13. Crouch, E., Tu, Y., Briner, D., McDonald, B., Smith, K., Holmskov, U. and Hartshorn, K. (2005) Ligand specificity of human surfactant protein D: expression of a mutant trimeric collectin that shows enhanced interactions with influenza A virus. J. Biol. Chem. 280, 17046-17056
14. Hartshorn, K., Chang, D., Rust, K., White, M., Heuser, J. and Crouch, E. (1996) Interactions of recombinant human pulmonary surfactant protein D and SPD multimers with influenza A. Am. J. Physiol. 271, L753-L762
15. Ohya, M., Nishitani, C., Sano, H., Yamada, C., Mitsuzawa, H., Shimizu, T., Saito, T., Smith, K., Crouch, E. and Kuroki, Y. (2006) Human pulmonary surfactant protein D binds the extracellular domains of Toll-like receptors 2 and 4 through the carbohydrate recognition domain by a mechanism different from its binding to phosphatidylinositol and lipopolysaccharide. Biochemistry 45, 8657-8664
16. Madsen, J., Kliem, A., Tornoe, I., Skjolt, K., Koch, C. and Holmskov, U. (2000) Localization of lung surfactant protein D on mucosal surfaces in human tissues. J. Immunol. 164, 5866-5870
17. White, M. R., Crouch, E., van Eijk, M., Hartshorn, M., Pemberton, L., Tornoe, I., Holmskov, U. and Hartshorn, K. L. (2005) Cooperative anti-influenza activities of respiratory innate immune proteins and neuraminidase inhibitor. Am. J. Physiol. Lung Cell Mol. Physiol. 288, L831-L840
18. Hartshorn, K. L., Collamer, M., Auerbach, M., Myers, J. B., Pavlotsky, N. and Tauber, A. I. (1988) Effects of influenza A virus on human neutrophil calcium metabolism. J. Immunol. 141, 1295-1301
19. Tecle, T., White, M. R., Gantz, D., Crouch, E. C. and Hartshorn, K. L. (2007) Human neutrophil defensins increase neutrophil uptake of influenza A virus and bacteria and modify virus-induced respiratory burst responses. J. Immunol. 178, 8046-8052
20. Hartshorn, K., White, M., Voelker, D., Coburn, J., Zaner, K. and Crouch, E. (2000) Mechanism of binding of surfactant surfactant protein D to influenza A viruses: importance of binding to hemagglutinin to antiviral activity. Biochem. J. 351, 449-458
21. Hartshorn, K., White, M., Shepherd, V., Reid, K., Jensenius, J. and Crouch, E. (1997) Mechanisms of anti-influenza activity of pulmonary surfactant proteins A and D: comparison with other collectins. Am. J. Physiol. 273, L1156-L1166
22. Hartshorn, K. L., Collamer, M., White, M. R., Schwartz, J. H. and Tauber, A. I. (1990) Characterization of influenza A virus activation of the human neutrophil. Blood 75, 218-226
23. Tecle, T., White, M. R., Crouch, E. C. and Hartshorn, K. L. (2007) Inhibition of influenza viral neuraminidase activity by collectins. Arch. Virol. 152, 1731-1742
24. Hartshorn, K. L., White, M. R., Tecle, T., Tornoe, I., Sorensen, G. L., Crouch, E. C. and Holmskov, U. (2007) Reduced influenza viral neutralizing activity of natural human trimers of surfactant protein D. Respir. Res. 8, 9
25. White, M. R., Crouch, E., Vesona, J., Tacken, P. J., Batenburg, J. J., Leth-Larsen, R., Holmskov, U. and Hartshorn, K. L. (2005) Respiratory innate immune proteins differentially modulate the neutrophil respiratory burst response to influenza A virus. Am. J. Physiol. Lung Cell Mol. Physiol. 289, L606-L616
26. Brown-Augsburger, P., Hartshorn, K., Chang, D., Rust, K., Fliszar, C., Welgus, H. and Crouch, E. (1996) Site directed mutagenesis of Cys15 and Cys20 of pulmonary surfactant protein D: expression of a trimeric protein with altered anti-viral properties. J. Biol. Chem. 271, 13724-13730
27. Gardai, S., Xiao, Y., Dickinson, M., Nick, J., Voelker, D., Green, K. and Henson, P. (2003) By binding SIRP or calreticulin/CD91. lung collectins act as dual function surveillance molecules to suppress or enhance inflammation Cell 115, 13-23
28. Kingma, P. S., Zhang, L., Ikegami, M., Hartshorn, K., McCormack, F. X. and Whitsett, J. A. (2006) Correction of pulmonary abnormalities in Sftpd-/-mice requires the collagenous domain of surfactant protein D. J. Biol. Chem. 281, 24496-24505
29. Hartshorn, K. L., Liou, L. S., White, M. R., Kazhdan, M. M. and Tauber, J. L. (1995) Neutrophil deactivation by influenza A virus: role of hemagglutinin binding to specific sialic acid-bearing cellular proteins. J. Immunol. 154, 3952-3960
30. Tacken, P. J., Hartshorn, K. L., White, M. R., van Kooten, C., van de Winkel, J. G., Reid, K. B. and Batenburg, J. J. (2004) Effective targeting of pathogens to neutrophils via chimeric surfactant protein D/anti-CD89 protein. J. Immunol. 172, 4934-4940