Galectin-1 binds to influenza virus and ameliorates influenza virus pathogenesis

Journal of Virology

Volumn 85, Issue 19, 2011, Pages 10010-10020

  Yang, Mei Lin ^a   Chen, Yu Hung ^a   Wang, Shainn Wei ^a   Huang, Yen Jang ^a   Leu, Chia Hsing ^a   Yeh, Nai Chi ^a   Chu, Chun Yen ^b   Lin, Chia Cheng ^c   Shieh, Gia Shing ^c   Chen, Yuh Ling ^a   Wang, Jen Ren ^a   Wang, Ching Ho ^d   Wu, Chao Liang ^a   Shiau, Ai Li ^a  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b NATIONAL PINGTUNG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Taiwan)

^c Tainan Hospital   (Taiwan)

^d NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

GALECTIN 1; GOLD NANOPARTICLE; RECOMBINANT GALECTIN 1; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIVIRAL ACTIVITY; APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; DISSOCIATION CONSTANT; FEMALE; IN VITRO STUDY; INFECTION SENSITIVITY; INFLUENZA; INFLUENZA VIRUS; INFLUENZA VIRUS A; KNOCKOUT MOUSE; LUNG; MOUSE; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; SURFACE PLASMON RESONANCE; SURVIVAL RATE; TRANSMISSION ELECTRON MICROSCOPY; UPREGULATION; VIRUS HEMAGGLUTINATION; VIRUS INFECTIVITY; VIRUS LOAD; VIRUS PATHOGENESIS; WILD TYPE;

ANIMALS; ANTIVIRAL AGENTS; DISEASE MODELS, ANIMAL; FEMALE; GALECTIN 1; INFLUENZA A VIRUS; KINETICS; LUNG; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON, TRANSMISSION; ORTHOMYXOVIRIDAE INFECTIONS; PROTEIN BINDING; RODENT DISEASES; SURFACE PLASMON RESONANCE; SURVIVAL ANALYSIS; VIRAL LOAD;

INFLUENZA A VIRUS; MUS; ORTHOMYXOVIRIDAE;

EID: 80054002504     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00301-11     Document Type: Article

References (56)

1. Bahnemann, H. G. 1990. Inactivation of viral antigens for vaccine preparation with particular reference to the application of binary ethylenimine. Vaccine 8:299-303.
2. 9-tetrahydrocannabinol in C57BL/6 mice. J. Pharmacol. Exp. Ther. 323: 675-683.
3. Chen, Y.-C., C.-H. Chen, and C.-H. Wang. 2008. H5 antibody detection by blocking enzyme-linked immunosorbent assay using a monoclonal antibody. Avian Dis. 52:124-129.
4. Dhirapong, A., A. Lleo, P. Leung, M. E. Gershwin, and F.-T. Liu. 2009. The immunological potential of galectin-1 and -3. Autoimmun. Rev. 8:360-363.
5. Fields, S., G. Winter, and G. G. Brownlee. 1981. Structure of the neuraminidase gene in human influenza virus A/PR/8/34. Nature 290:213-217.
6. Fowler, M., R. J. Thomas, J. Atherton, I. S. Roberts, and N. J. High. 2006. Galectin-3 binds to Helicobacter pylori O-antigen: it is upregulated and rapidly secreted by gastric epithelial cells in response to H. pylori adhesion. Cell. Microbiol. 8:44-54.
7. Garner, O. B., et al. 2010. Endothelial galectin-1 binds to specific glycans on Nipah virus fusion protein and inhibits maturation, mobility, and function to block syncytium formation. PLoS Pathog. 6:e1000993.
8. Gauthier, S., et al. 2008. Induction of galectin-1 expression by HTLV-1 Tax and its impact on HTLV-1 infectivity. Retrovirology 5:105.
9. Govorkova, E. A., H.-B. Fang, M. Tan, and R. G. Webster. 2004. Neuraminidase inhibitor-rimantadine combinations exert additive and synergistic antiinfluenza virus effects in MDCK Cells. Antimicrob. Agents Chemother. 48:4855-4863.
10. Grabar, K. C., R. G. Freeman, M. B. Hommer, and M. J. Natan. 2002. Preparation and characterization of Au colloid monolayers. Anal. Chem. 67:735-743.
11. Hartshorn, K. L., et al. 1997. Mechanisms of anti-influenza activity of surfactant proteins A and D: comparison with serum collectins. Am. J. Physiol. 273:L1156-1166.
12. Hartshorn, K. L., M. R. White, T. Tecle, U. Holmskov, and E. C. Crouch. 2006. Innate defense against influenza A virus: activity of human neutrophil defensins and interactions of defensins with surfactant protein D. J. Immunol. 176:6962-6972.
13. Hartshorn, K. L., et al. 2000. Mechanism of binding of surfactant protein D to influenza A viruses: importance of binding to haemagglutinin to antiviral activity. Biochem. J. 351(Pt. 2):449-458.
14. Hawgood, S., et al. 2004. Pulmonary collectins modulate strain-specific influenza A virus infection and host responses. J. Virol. 78:8565-8572.
15. Hiti, A. L., and D. P. Nayak. 1982. Complete nucleotide sequence of the neuraminidase gene of human influenza virus A/WSN/33. J. Virol. 41:730- 734.
16. Horváth, A., et al. 2001. Serum amyloid P component inhibits influenza A virus infections: in vitro and in vivo studies. Antivir. Res. 52:43-53.
17. Hsieh, S. H., et al. 2008. Galectin-1, a novel ligand of neuropilin-1, activates VEGFR-2 signaling and modulates the migration of vascular endothelial cells. Oncogene 27:3746-3753.
18. Jia, W., H. Li, and Y. W. He. 2008. Pattern recognition molecule mindin promotes intranasal clearance of influenza viruses. J. Immunol. 180:6255- 6261.
19. Keil, W., et al. 1985. Carbohydrates of influenza virus. Structural elucidation of the individual glycans of the FPV hemagglutinin by two-dimensional 1H NMR and methylation analysis. EMBO J. 4:2711-2720.
20. Krishnamoorthy, L., J. W. Bess, A. B. Preston, K. Nagashima, and L. K. Mahal. 2009. HIV-1 and microvesicles from T cells share a common glycome, arguing for a common origin. Nat. Chem. Biol. 5:244-250.
21. Lee, R. T., and Y. C. Lee. 2000. Affinity enhancement by multivalent lectincarbohydrate interaction. Glycoconj. J. 7:543-551.
22. LeVine, A. M., J. A. Whitsett, K. L. Hartshorn, E. C. Crouch, and T. R. Korfhagen. 2001. Surfactant protein D enhances clearance of influenza A virus from the lung in vivo. J. Immunol. 167:5868-5873.
23. Levroney, E. L., et al. 2005. Novel innate immune functions for galectin-1: galectin-1 inhibits cell fusion by Nipah virus envelope glycoproteins and augments dendritic cell secretion of proinflammatory cytokines. J. Immunol. 175:413-420.
24. Matrosovich, M., and H.-D. Klenk. 2003. Natural and synthetic sialic acidcontaining inhibitors of influenza virus receptor binding. Rev. Med. Virol. 13:85-97.
25. Matsuoka, Y., et al. 2009. Neuraminidase stalk length and additional glycosylation of the hemagglutinin influence the virulence of influenza H5N1 viruses for mice. J. Virol. 83:4704-4708.
26. Mercier, S., et al. 2008. Galectin-1 promotes HIV-1 infectivity in macrophages through stabilization of viral adsorption. Virology 371:121-129.
27. Mitnaul, L. J., et al. 2000. Balanced hemagglutinin and neuraminidase activities are critical for efficient replication of influenza A virus. J. Virol. 74:6015-6020.
28. Nieminen, J., C. St-Pierre, P. Bhaumik, F. Poirier, and S. Sato. 2008. Role of galectin-3 in leukocyte recruitment in a murine model of lung infection by Streptococcus pneumoniae. J. Immunol. 180:2466-2473.
29. Nunoi, H., et al. 2005. Apoptosis under hypercytokinemia is a possible pathogenesis in influenza-associated encephalopathy. Pediatr. Int. 47:175- 179.
30. Ouellet, M., et al. 2005. Galectin-1 acts as a soluble host factor that promotes HIV-1 infectivity through stabilization of virus attachment to host cells. J. Immunol. 174:4120-4126.
31. Poirier, F., and E. J. Robertson. 1993. Normal development of mice carrying a null mutation in the gene encoding the L14 S-type lectin. Development 119:1229-1236.
32. Rabinovich, G. A., F. T. Liu, M. Hirashima, and A. Anderson. 2007. An emerging role for galectins in tuning the immune response: lessons from experimental models of inflammatory disease, autoimmunity and cancer. Scand. J. Immunol. 66:143-158.
33. Rabinovich, G. A., and M. A. Toscano. 2009. Turning "sweet" on immunity: galectin-glycan interactions in immune tolerance and inflammation. Nat. Rev. Immunol. 9:338-352.
34. Rabinovich, G. A., M. A. Toscano, S. S. Jackson, and G. R. Vasta. 2007. Functions of cell surface galectin-glycoprotein lattices. Curr. Opin. Struct. Biol. 17:513-520.
35. Reading, P. C., et al. 2008. Antiviral activity of the long chain pentraxin PTX3 against influenza viruses. J. Immunol. 180:3391-3398.
36. Reading, P. C., L. S. Morey, E. C. Crouch, and E. M. Anders. 1997. Collectinmediated antiviral host defense of the lung: evidence from influenza virus infection of mice. J. Virol. 71:8204-8212.
37. Schulman, J. L., and P. Palese. 1977. Virulence factors of influenza A viruses: WSN virus neuraminidase required for plaque production in MDBK cells. J. Virol. 24:170-176.
38. Skehel, J. J., et al. 1984. A carbohydrate side chain on hemagglutinins of Hong Kong influenza viruses inhibits recognition by a monoclonal antibody. Proc. Natl. Acad. Sci. U. S. A. 81:1779-1783.
39. Skehel, J. J., and D. C. Wiley. 2000. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu. Rev. Biochem. 69:531- 569.
40. Stowell, S. R., et al. 2008. Differential roles of galectin-1 and galectin-3 in regulating leukocyte viability and cytokine secretion. J. Immunol. 180:3091- 3102.
41. Sugiura, A., and M. Ueda. 1980. Neurovirulence of influenza virus in mice. I. Neurovirulence of recombinants between virulent and avirulent virus strains. Virology 101:440-449.
42. Thanh, N. T., and Z. Rosenzweig. 2002. Development of an aggregationbased immunoassay for anti-protein A using gold nanoparticles. Anal. Chem. 74:1624-1628.
43. Tsai, C. Y., et al. 2007. Amelioration of collagen-induced arthritis in rats by nanogold. Arthritis Rheum. 56:544-554.
44. van Kooyk, Y., and G. A. Rabinovich. 2008. Protein-glycan interactions in the control of innate and adaptive immune responses. Nat. Immunol. 9:593-601.
45. Vasta, G. R. 2009. Roles of galectins in infection. Nat. Rev. Microbiol. 7:424-438.
46. Vigerust, D. J., et al. 2007. N-linked glycosylation attenuates H3N2 influenza viruses. J. Virol. 81:8593-8600.
47. Vray, B., et al. 2004. Up-regulation of galectin-3 and its ligands by Trypanosoma cruzi infection with modulation of adhesion and migration of murine dendritic cells. Glycobiology 14:647-657.
48. Wagner, R., T. Wolff, A. Herwig, S. Pleschka, and H.-D. Klenk. 2000. Interdependence of hemagglutinin glycosylation and neuraminidase as regulators of influenza virus growth: a study by reverse genetics. J. Virol. 74:6316-6323.
49. Wang, C.-W., and C.-H. Wang. 2003. Experimental selection of virus derivatives with variations in virulence from a single low-pathogenicity H6N1 avian influenza virus field isolate. Avian Dis. 47:1416-1422.
50. Welliver, T. P., et al. 2007. Severe human lower respiratory tract illness caused by respiratory syncytial virus and influenza virus is characterized by the absence of pulmonary cytotoxic lymphocyte responses. J. Infect. Dis. 195:1126-1136.
51. White, M., et al. 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.
52. White, M. R., E. Crouch, D. Chang, and K. L. Hartshorn. 2001. Increased antiviral and opsonic activity of a highly multimerized collectin chimera. Biochem. Biophys. Res. Commun. 286:206-213.
53. White, M. R., M. Doss, P. Boland, T. Tecle, and K. L. Hartshorn. 2008. Innate immunity to influenza virus: implications for future therapy. Expert Rev. Clin. Immunol. 4:497-514.
54. Wilson, I. A., J. J. Skehel, and D. C. Wiley. 1981. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 Å resolution. Nature 289:366-373.
55. Yingsakmongkon, S., et al. 2008. In vitro inhibition of human influenza A virus infection by fruit-juice concentrate of Japanese plum (Prunus mume SIEB. et ZUCC). Biol. Pharm. Bull. 31:511-515.
56. Zhou, Q., and R. D. Cummings. 1993. L-14 lectin recognition of laminin and its promotion of in vitro cell adhesion. Arch. Biochem. Biophys. 300:6-17.