A unique sugar-binding site mediates the distinct anti-influenza activity of pig surfactant protein D

Journal of Biological Chemistry

Volumn 287, Issue 32, 2012, Pages 26666-26677

  Van Eijk, Martin ^a   Rynkiewicz, Michael J ^b   White, Mitchell R ^b   Hartshorn, Kevan L ^b   Zou, Xueqing ^c   Schulten, Klaus ^c   Luo, Dong ^b   Crouch, Erika C ^d   Cafarella, Tanya R ^b   Head, James F ^b   Haagsman, Henk P ^a   Seaton, Barbara A ^b  

^a UTRECHT UNIVERSITY   (Netherlands)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRYSTALLOGRAPHIC ANALYSIS; GLYCANS; HOST DEFENSE; INFLUENZA A VIRUS; INHIBITORY ACTIVITY; MOLECULAR DYNAMICS SIMULATIONS; PANDEMIC INFLUENZA; STRUCTURAL FEATURE; SUGAR BINDING; SURFACTANT PROTEINS; TRIPEPTIDE;

MOLECULAR DYNAMICS; SUGARS; SURFACE ACTIVE AGENTS; VIRUSES;

MAMMALS;

GLYCAN; MANNOSIDE; RECOMBINANT PROTEIN; SUGAR; SURFACTANT PROTEIN D;

ANTIVIRAL ACTIVITY; ARTICLE; BINDING SITE; CELL STRAIN; CELL STRAIN HEK293; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTALLIZATION; CRYSTALLOGRAPHY; HEMAGGLUTINATION INHIBITION; HUMAN; INFLUENZA A; INFLUENZA VIRUS A; INNATE IMMUNITY; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; SITE DIRECTED MUTAGENESIS; SUGAR BINDING SITE; SWINE; VIRUS INHIBITION; VIRUS STRAIN;

ANIMALS; ANTIVIRAL AGENTS; BASE SEQUENCE; BINDING SITES; CARBOHYDRATE METABOLISM; CELLS, CULTURED; CRYSTALLIZATION; DNA PRIMERS; DOGS; INFLUENZA A VIRUS; MICROBIAL SENSITIVITY TESTS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MUTAGENESIS, SITE-DIRECTED; PULMONARY SURFACTANT-ASSOCIATED PROTEIN D; SWINE;

INFLUENZA A VIRUS; MAMMALIA; SUIDAE; SUS;

EID: 84864570999     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.368571     Document Type: Article

References (65)

1. Novel Swine-Origin Influenza A (H1N1) Virus Investigation Team, Dawood, F. S., Jain, S., Finelli, L., Shaw, M. W., Lindstrom, S., Garten, R. J., Gubareva, L. V., Xu, X., Bridges, C. B., and Uyeki, T. M. (2009) Emergence of a novel swine-origin influenza A (H1N1) virus in humans. N. Engl. J. Med. 360, 2605-2615
2. 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 (Pubitemid 24218106)
3. Hartshorn, K. L., White, M. R., Shepherd, V., Reid, K., Jensenius, J. C., and Crouch, E. C. (1997) Mechanisms of anti-influenza activity of surfactant proteins A and D. Comparison with serum collectins. Am. J. Physiol. 273, L1156-L1166
4. 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 (Pubitemid 39025122)
5. 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 (Pubitemid 33062780)
6. 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 (Pubitemid 41361671)
7. Hartshorn, K. L., Reid, K. B., White, M. R., Jensenius, J. C., Morris, S. M., Tauber, A. I., and Crouch, E. (1996) Neutrophil deactivation by influenza A viruses/ Mechanisms of protection after viral opsonization with collectins and hemagglutination-inhibiting antibodies. Blood 87, 3450-3461 (Pubitemid 26115378)
8. Pastva, A. M., Wright, J. R., and Williams, K. L. (2007) Immunomodulatory roles of surfactant proteins A and D. Implications in lung disease. Proc. Am. Thorac. Soc. 4, 252-257 (Pubitemid 47036444)
9. Crouch, E., Persson, A., Chang, D., and Heuser, J. (1994) Molecular structure of pulmonary surfactant protein D (SP-D). J. Biol. Chem. 269, 17311-17319 (Pubitemid 24204059)
10. van Eijk, M., van de Lest, C. H., Batenburg, J. J., Vaandrager, A. B., Meschi, J., Hartshorn, K. L., van Golde, L. M., and Haagsman, H. P. (2002) Porcine surfactant protein D is N-glycosylated in its carbohydrate recognition domain and is assembled into differently charged oligomers. Am. J. Respir. Cell Mol. Biol. 26, 739-747 (Pubitemid 34557376)
11. Hoppe, H. J., Barlow, P. N., and Reid, K. B. (1994)Aparallel three-stranded α-helical bundle at the nucleation site of collagen triple-helix formation. FEBS Lett. 344, 191-195 (Pubitemid 2085679)
12. Hartshorn, K., Chang, D., Rust, K., White, M., Heuser, J., and Crouch, E. (1996) Interactions of recombinant human pulmonary surfactant protein D and SP-D multimers with influenza A. Am. J. Physiol. 271, L753-L762
13. 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
14. 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 (Pubitemid 41389167)
15. Hartshorn, K. L., White, M. R., Voelker, D. R., Coburn, J., Zaner, K., and Crouch, E. C. (2000) Mechanism of binding of surfactant protein D to influenza A viruses. Importance of binding hemagglutinin to antiviral activity. Biochem. J. 351, 449-458
16. Crouch, E., Nikolaidis, N., McCormack, F. X., McDonald, B., Allen, K., Rynkiewicz, M. J., Cafarella, T. M., White, M., Lewnard, K., Leymarie, N., Zaia, J., Seaton, B. A., and Hartshorn, K. L. (2011) Mutagenesis of surfactant protein D informed by evolution and x-ray crystallography enhances defenses against influenza A virus in vivo. J. Biol. Chem. 286, 40681-40692
17. Hartshorn, K. L., Webby, R., White, M. R., Tecle, T., Pan, C., Boucher, S., Moreland, R. J., Crouch, E. C., and Scheule, R. K. (2008) Role of viral hemagglutinin glycosylation in anti-influenza activities of recombinant surfactant protein D. Respir. Res. 9, 65
18. Reading, P. C., Pickett, D. L., Tate, M. D., Whitney, P. G., Job, E. R., and Brooks, A. G. (2009) Loss of a single N-linked glycan from the hemagglutinin of influenza virus is associated with resistance to collectins and increased virulence in mice. Respir. Res. 10, 117
19. Job, E. R., Deng, Y. M., Tate, M. D., Bottazzi, B., Crouch, E. C., Dean, M. M., Mantovani, A., Brooks, A. G., and Reading, P. C. (2010) Pandemic H1N1 influenza A viruses are resistant to the antiviral activities of innate immune proteins of the collectin and pentraxin superfamilies. J. Immunol. 185, 4284-4291
20. van Eijk, M., Haagsman, H. P., Skinner, T., Archibald, A., Reid, K. B., and Lawson, P. R. (2000) Porcine lung surfactant protein D. Complementary DNAcloning, chromosomal localization, and tissue distribution. J. Immunol. 164, 1442-1450 (Pubitemid 30067259)
21. van Eijk, M., White, M. R., Batenburg, J. J., Vaandrager, A. B., van Golde, L. M., Haagsman, H. P., and Hartshorn, K. L. (2004) Interactions of influenza A virus with sialic acids present on porcine surfactant protein D. Am. J. Respir. Cell Mol. Biol. 30, 871-879 (Pubitemid 38736912)
22. Hillaire, M. L., van Eijk, M., van Trierum, S. E., van Riel, D., Saelens, X., Romijn, R. A., Hemrika, W., Fouchier, R. A., Kuiken, T., Osterhaus, A. D., Haagsman, H. P., and Rimmelzwaan, G. F. (2011) Assessment of the antiviral properties of recombinant porcine SP-D against various influenza A viruses in vitro. PLoS One 6, e25005
23. van Eijk, M., White, M. R., Crouch, E. C., Batenburg, J. J., Vaandrager, A. B., Van Golde, L. M., Haagsman, H. P., and Hartshorn, K. L. (2003) Porcine pulmonary collectins show distinct interactions with influenza A viruses; role of the N-linked oligosaccharides in the carbohydrate recognition domain. J. Immunol. 171, 1431-1440 (Pubitemid 36900077)
24. Webster, R. G. (1997) Influenza virus. Transmission between species and relevance to emergence of the next human pandemic. Arch. Virol. Suppl. 13, 105-113
25. Neumann, G., Noda, T., and Kawaoka, Y. (2009) Emergence and pandemic potential of swine-origin H1N1 influenza virus. Nature 459, 931-939
26. van Eijk, M., Bruinsma, L., Hartshorn, K. L., White, M. R., Rynkiewicz, M. J., Seaton, B. A., Hemrika, W., Romijn, R. A., van Balkom, B. W., and Haagsman, H. P. (2011) Introduction of N-linked glycans in the lectin domain of surfactant protein D. Impact on interactions with influenza A viruses. J. Biol. Chem. 286, 20137-20151
27. Durocher, Y., Perret, S., and Kamen, A. (2002) High level and high throughput recombinant protein production by transient transfection of suspension-growing human 293-EBNA1 cells. Nucleic Acids Res. 30, E9
28. Barash, S., Wang, W., and Shi, Y. (2002) Human secretory signal peptide description by hidden Markov model and generation of a strong artificial signal peptide for secreted protein expression. Biochem. Biophys. Res. Commun. 294, 835-842 (Pubitemid 34687192)
29. Morlot, C., Hemrika, W., Romijn, R. A., Gros, P., Cusack, S., and McCarthy, A. A. (2007) Production of Slit2 LRR domains in mammalian cells for structural studies and the structure of human Slit2 domain 3. Acta Crystallogr. D Biol. Crystallogr. 63, 961-968 (Pubitemid 47346821)
30. Wang, H., Head, J., Kosma, P., Brade, H., Müller-Loennies, S., Sheikh, S., McDonald, B., Smith, K., Cafarella, T., Seaton, B., and Crouch, E. (2008) Recognition of heptoses and the inner core of bacterial lipopolysaccharides by surfactant protein D. Biochemistry 47, 710-720 (Pubitemid 351195442)
31. Hartshorn, K. L., Ligtenberg, A., White, M. R., Van Eijk, M., Hartshorn, M., Pemberton, L., Holmskov, U., and Crouch, E. (2006) Salivary agglutinin and lung scavenger receptor cysteine-rich glycoprotein 340 have broad anti-influenza activities and interactions with surfactant protein D that vary according to donor source and sialylation. Biochem. J. 393, 545-553 (Pubitemid 43099094)
32. Hartshorn, K. L., Sastry, K., White, M. R., Anders, E. M., Super, M., Ezekowitz, R. A., and Tauber, A. I. (1993) Human mannose-binding protein functions as an opsonin for influenza A viruses. J. Clin. Invest. 91, 1414-1420 (Pubitemid 23127341)
33. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX. A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
34. Crouch, E., McDonald, B., Smith, K., Cafarella, T., Seaton, B., and Head, J. (2006) Contributions of phenylalanine 335 to ligand recognition by human surfactant protein D. Ring interactions with SP-D ligands. J. Biol. Chem. 281, 18008-18014 (Pubitemid 44035600)
35. Terwilliger, T. C., Grosse-Kunstleve, R. W., Afonine, P. V., Moriarty, N. W., Zwart, P. H., Hung, L. W., Read, R. J., and Adams, P. D. (2008) Iterative model building, structure refinement, and density modification with the PHENIX AutoBuild wizard. Acta Crystallogr. D Biol. Crystallogr. 64, 61-69 (Pubitemid 350308678)
36. Emsley, P., and Cowtan, K. (2004) Coot. Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (Pubitemid 41742764)
37. Painter, J., and Merritt, E. A. (2006) Optimal description of a protein structure in terms of multiple groups undergoing TLS motion. Acta Crystallogr. D Biol. Crystallogr. 62, 439-450
38. Painter, J., and Merritt, E. A. (2006) TLSMD web server for the generation of multigroup TLS models. J. Appl. Crystallogr. 39, 109-111
39. Guex, N., and Peitsch, M. C. (1997) SWISS-MODEL and the Swiss-Pdb- Viewer. An environment for comparative protein modeling. Electrophoresis 18, 2714-2723 (Pubitemid 28059943)
40. Cason, C., Froehlich, T., Kopp, N., and Parker, R. (2005) Persistence of Vision Raytracer. Pty. Ltd., Version 3.6, Williamstown, Victoria, Australia
41. Calarese, D. A., Scanlan, C. N., Zwick, M. B., Deechongkit, S., Mimura, Y., Kunert, R., Zhu, P., Wormald, M. R., Stanfield, R. L., Roux, K. H., Kelly, J. W., Rudd, P. M., Dwek, R. A., Katinger, H., Burton, D. R., and Wilson, I. A. (2003) Antibody domain exchange is an immunological solution to carbohydrate cluster recognition. Science 300, 2065-2071 (Pubitemid 36760127)
42. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD. Visual molecular dynamics. J. Mol. Graph. 14, 33-38, 27-28
43. Phillips, J. C., Braun, R., Wang, W., Gumbart, J., Tajkhorshid, E., Villa, E., Chipot, C., Skeel, R. D., Kalé, L., and Schulten, K. (2005) Scalable molecular dynamics with NAMD. J. Comput. Chem. 26, 1781-1802 (Pubitemid 43078511)
44. Mackerell, A. D., Jr., Feig, M., and Brooks, C. L., 3rd (2004) Extending the treatment of backbone energetics in protein force fields. Limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations. J. Comput. Chem. 25, 1400-1415
45. Guvench, O., Greene, S. N., Kamath, G., Brady, J. W., Venable, R. M., Pastor, R. W., and Mackerell, A. D., Jr. (2008) Additive empirical force field for hexopyranose monosaccharides. J. Comput. Chem. 29, 2543-2564
46. Guvench, O., Hatcher, E. R., Venable, R. M., Pastor, R. W., and Mackerell, A. D. (2009) CHARMM additive all-atom force field for glycosidic linkages between hexopyranoses. J. Chem. Theory Comput. 5, 2353-2370
47. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., and Klein, M. L. (1983) Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79, 926-935
48. Martyna, G. J., Tobias, D. J., and Klein, M. L. (1994) Constant pressure molecular dynamics algorithms. J. Chem. Phys. 101, 4177-4189
49. Head, J. F., Mealy, T. R., McCormack, F. X., and Seaton, B. A. (2003) Crystal structure of trimeric carbohydrate recognition and neck domains of surfactant protein A. J. Biol. Chem. 278, 43254-43260 (Pubitemid 37345945)
50. Weis, W. I., and Drickamer, K. (1994) Trimeric structure of a C-type mannose-binding protein. Structure 2, 1227-1240 (Pubitemid 124001321)
51. Weis, W. I., Drickamer, K., and Hendrickson, W. A. (1992) Structure of a C-type mannose-binding protein complexed with an oligosaccharide. Nature 360, 127-134
52. 8 oligosaccharide on native ribonuclease B and on the reduced and denatured protein. Arch. Biochem. Biophys. 383, 17-27
53. Crouch, E., Hartshorn, K., Horlacher, T., McDonald, B., Smith, K., Cafarella, T., Seaton, B., Seeberger, P. H., and Head, J. (2009) Recognition of mannosylated ligands and influenza A virus by human surfactant protein D: contributions of an extended site and residue 343. Biochemistry 48, 3335-3345
54. Case, D. A., Cheatham, T. E., 3rd, Darden, T., Gohlke, H., Luo, R., Merz, K. M., Jr., Onufriev, A., Simmerling, C., Wang, B., and Woods, R. J. (2005) The Amber biomolecular simulation programs. J. Comput. Chem. 26, 1668-1688 (Pubitemid 43076180)
55. Vijaykrishna, D., Smith, G. J., Pybus, O. G., Zhu, H., Bhatt, S., Poon, L. L., Riley, S., Bahl, J., Ma, S. K., Cheung, C. L., Perera, R. A., Chen, H., Shortridge, K. F., Webby, R. J., Webster, R. G., Guan, Y., and Peiris, J. S. (2011) Long term evolution and transmission dynamics of swine influenza A virus. Nature 473, 519-522
56. White, M. R., Doss, M., Boland, P., Tecle, T., and Hartshorn, K. L. (2008) Innate immunity to influenza virus: implications for future therapy. Expert Rev. Clin. Immunol. 4, 497-514 (Pubitemid 351903267)
57. White, M., Kingma, P., Tecle, T., Kacak, N., Linders, B., Heuser, J., Crouch, E., and Hartshorn, K. (2008) Multimerization of surfactant protein D, but not its collagen domain, is required for antiviral and opsonic activities related to influenza virus. J. Immunol. 181, 7936-7943
58. Tecle, T., White, M. R., Sorensen, G., Gantz, D., Kacak, N., Holmskov, U., Smith, K., Crouch, E. C., and Hartshorn, K. L. (2008) Critical role for cross-linking of trimeric lectin domains of surfactant protein D in antiviral activity against influenza A virus. Biochem. J. 412, 323-329 (Pubitemid 351758238)
59. Hartshorn, K. L., White, M. R., Smith, K., Sorensen, G., Kuroki, Y., Holmskov, U., Head, J., and Crouch, E. C. (2010) Increasing antiviral activity of surfactant protein D trimers by introducing residues from bovine serum collectins. Dissociation of mannan- binding and antiviral activity. Scand. J. Immunol. 72, 22-30
60. Shrive, A. K., Tharia, H. A., Strong, P., Kishore, U., Burns, I., Rizkallah, P. J., Reid, K. B., and Greenhough, T. J. (2003) High resolution structural insights into ligand binding and immune cell recognition by human lung surfactant protein D. J. Mol. Biol. 331, 509-523 (Pubitemid 36904033)
61. Liu, W., Wei, M. T., Tong, Y., Tang, F., Zhang, L., Fang, L., Yang, H., and Cao, W. C. (2011) Seroprevalence and genetic characteristics of five subtypes of influenza A viruses in the Chinese pig population. A pooled data analysis. Vet. J. 187, 200-206
62. Hinshaw, V. S., Webster, R. G., Easterday, B. C., and Bean, W. J., Jr. (1981) Replication of avian influenza A viruses in mammals. Infect. Immun. 34, 354-361 (Pubitemid 12117530)
63. Kida, H., Ito, T., Yasuda, J., Shimizu, Y., Itakura, C., Shortridge, K. F., Kawaoka, Y., and Webster, R. G. (1994) Potential for transmission of avian influenza viruses to pigs. J. Gen. Virol. 75, 2183-2188 (Pubitemid 24282230)
64. Van Reeth, K. (2007) Avian and swine influenza viruses. Our current understanding of the zoonotic risk. Vet. Res. 38, 243-260
65. Brown, I. H. (2000) The epidemiology and evolution of influenza viruses in pigs. Vet. Microbiol. 74, 29-46