The human cathelicidin LL-37 inhibits influenza a viruses through a mechanism distinct from that of surfactant protein d or defensins

Journal of General Virology

Volumn 94, Issue PART11, 2013, Pages 40-49

  Tripathi, Shweta ^a   Tecle, Tesfaldet ^a   Verma, Anamika ^a   Crouch, Erika ^b   White, Mitchell ^a   Hartshorn, Kevan L ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 (3 CHLOROANILINO) 6,7 DIMETHOXYQUINAZOLINE; APOLIPOPROTEIN A1; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; DEFENSIN; HIGH DENSITY LIPOPROTEIN; LACTATE DEHYDROGENASE; SURFACTANT PROTEIN D;

ANTIVIRAL ACTIVITY; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENZYME LINKED IMMUNOSORBENT ASSAY; HEMAGGLUTINATION; INFLUENZA VIRUS A H3N2; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIRUS ENVELOPE; VIRUS REPLICATION;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIMICROBIAL CATIONIC PEPTIDES; CHO CELLS; COLLECTINS; CRICETINAE; CRICETULUS; DEFENSINS; DOGS; EPITHELIAL CELLS; HUMANS; INFLUENZA A VIRUS; INFLUENZA A VIRUS, H3N2 SUBTYPE; LIPOPROTEINS, HDL; MADIN DARBY CANINE KIDNEY CELLS; MICE; NEUTROPHILS; ORTHOMYXOVIRIDAE INFECTIONS; PULMONARY SURFACTANT-ASSOCIATED PROTEIN A; PULMONARY SURFACTANT-ASSOCIATED PROTEIN D;

INFLUENZA A VIRUS;

EID: 84871300505     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.045013-0     Document Type: Article

References (33)

1. Barlow, P. G., Svoboda, P., Mackellar, A., Nash, A. A., York, I. A., Pohl, J., Davidson, D. J. & Donis, R. O. (2011). Antiviral activity and increased host defense against influenza infection elicited by the human cathelicidin LL-37. PLoS ONE 6, e25333.
2. Bergman, P., Walter-Jallow, L., Broliden, K., Agerberth, B. & Söderlund, J. (2007). The antimicrobial peptide LL-37 inhibits HIV-1 replication. Curr HIV Res 5, 410-415.
3. Braff, M. H., Jones, A. L., Skerrett, S. J. & Rubens, C. E. (2007). Staphylococcus aureus exploits cathelicidin antimicrobial peptides produced during early pneumonia to promote staphylokinasedependent fibrinolysis. J Infect Dis 195, 1365-1372.
4. Burton, M. F. & Steel, P. G. (2009). The chemistry and biology of LL- 37. Nat Prod Rep 26, 1572-1584.
5. Caverly, J. M., Diamond, G., Gallup, J. M., Brogden, K. A., Dixon, R. A. & Ackermann, M. R. (2003). Coordinated expression of tracheal antimicrobial peptide and inflammatory-response elements in the lungs of neonatal calves with acute bacterial pneumonia. Infect Immun 71, 2950-2955.
6. Chromek, M., Slamová, Z., Bergman, P., Kovács, L., Podracká, L., Ehrén, I., Hökfelt, T., Gudmundsson, G. H., Gallo, R. L. & other authors (2006). The antimicrobial peptide cathelicidin protects the urinary tract against invasive bacterial infection. Nat Med 12, 636-641.
7. Crouch, E., Nikolaidis, N., McCormack, F. X., McDonald, B., Allen, K., Rynkiewicz, M. J., Cafarella, T. M., White, M., Lewnard, K. & other authors (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.
8. Doss, M., White, M. R., Tecle, T., Gantz, D., Crouch, E. C., Jung, G., Ruchala, P., Waring, A. J., Lehrer, R. I. & Hartshorn, K. L. (2009). Interactions of alpha-, beta-, and theta-defensins with influenza A virus and surfactant protein D. J Immunol 182, 7878-7887.
9. Doss, M., White, M. R., Tecle, T. & Hartshorn, K. L. (2010). Human defensins and LL-37 in mucosal immunity. J Leukoc Biol 87, 79-92.
10. Gaudreault, E. & Gosselin, J. (2008). Leukotriene B4 induces release of antimicrobial peptides in lungs of virally infected mice. J Immunol 180, 6211-6221.
11. Gaynor, C. D., McCormack, F. X., Voelker, D. R., McGowan, S. E. & Schlesinger, L. S. (1995). Pulmonary surfactant protein A mediates enhanced phagocytosis of Mycobacterium tuberculosis by a direct interaction with human macrophages. J Immunol 155, 5343-5351.
12. Hansdottir, S., Monick, M. M., Hinde, S. L., Lovan, N., Look, D. C. & Hunninghake, G. W. (2008). Respiratory epithelial cells convert inactive vitamin D to its active form: potential effects on host defense. J Immunol 181, 7090-7099.
13. Hartshorn, K. L. (2010). Role of surfactant protein A and D (SP-A and SP-D) in human antiviral host defense. Front Biosci (Schol Ed) 2, 527-546.
14. Hartshorn, K. L., Collamer, M., Auerbach, M., Myers, J. B., Pavlotsky, N. & Tauber, A. I. (1988). Effects of influenza A virus on human neutrophil calcium metabolism. J Immunol 141, 1295-1301.
15. Hartshorn, K. L., Crouch, E. C., White, M. R., Eggleton, P., Tauber, A. I., Chang, D. & 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.
16. Hartshorn, K., Chang, D., Rust, K., White, M., Heuser, J. & Crouch, E. (1996). Interactions of recombinant human pulmonary surfactant protein D and SP-D multimers with influenza A. Am J Physiol 271, L753-L762.
17. Hartshorn, K. L., Sastry, K. N., Chang, D., White, M. R. & Crouch, E. C. (2000a). Enhanced anti-influenza activity of a surfactant protein D and serum conglutinin fusion protein. Am J Physiol Lung Cell Mol Physiol 278, L90-L98.
18. Hartshorn, K. L., White, M. R., Voelker, D. R., Coburn, J., Zaner, K. & Crouch, E. C. (2000b). Mechanism of binding of surfactant protein D to influenza A viruses: importance of binding to haemagglutinin to antiviral activity. Biochem J 351, 449-458.
19. Hartshorn, K. L., White, M. R., Tecle, T., Holmskov, U. & Crouch, E. C. (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.
20. Hashimoto, Y., Moki, T., Takizawa, T., Shiratsuchi, A. & Nakanishi, Y. (2007). Evidence for phagocytosis of influenza virus-infected, apoptotic cells by neutrophils and macrophages in mice. J Immunol 178, 2448-2457.
21. Lai, Y. & Gallo, R. L. (2009). AMPed up immunity: how antimicrobial peptides have multiple roles in immune defense. Trends Immunol 30, 131-141.
22. Larrick, J. W., Morgan, J. G., Palings, I., Hirata, M. & Yen, M. H. (1991). Complementary DNA sequence of rabbit CAP18 - a unique lipopolysaccharide binding protein. Biochem Biophys Res Commun 179, 170-175.
23. Lau, Y. E., Bowdish, D. M., Cosseau, C., Hancock, R. E. & Davidson, D. J. (2006). Apoptosis of airway epithelial cells: human serum sensitive induction by the cathelicidin LL-37. Am J Respir Cell Mol Biol 34, 399-409.
24. Liu, P. T., Stenger, S., Li, H., Wenzel, L., Tan, B. H., Krutzik, S. R., Ochoa, M. T., Schauber, J., Wu, K. & other authors (2006). Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 311, 1770-1773.
25. Liu, P. T., Stenger, S., Tang, D. H. & Modlin, R. L. (2007). Cutting edge: vitamin D-mediated human antimicrobial activity against Mycobacterium tuberculosis is dependent on the induction of cathelicidin. J Immunol 179, 2060-2063.
26. Oppenheim, J. J. & Yang, D. (2005). Alarmins: chemotactic activators of immune responses. Curr Opin Immunol 17, 359-365.
27. Salvatore, M., Garcia-Sastre, A., Ruchala, P., Lehrer, R. I., Chang, T. & Klotman, M. E. (2007). A-Defensin inhibits influenza virus replication by cell-mediated mechanism(s). J Infect Dis 196, 835-843.
28. Smee, D. F., Bailey, K. W., Wong, M. H., O'Keefe, B. R., Gustafson, K. R., Mishin, V. P. & Gubareva, L. V. (2008). Treatment of influenza A (H1N1) virus infections in mice and ferrets with cyanovirin-N. Antiviral Res 80, 266-271.
29. Sørensen, O. E., Follin, P., Johnsen, A. H., Calafat, J., Tjabringa, G. S., Hiemstra, P. S. & Borregaard, N. (2001). Human cathelicidin, hCAP-18, is processed to the antimicrobial peptide LL-37 by extracellular cleavage with proteinase 3. Blood 97, 3951-3959.
30. Tate, M. D., Deng, Y. M., Jones, J. E., Anderson, G. P., Brooks, A. G. & Reading, P. C. (2009). Neutrophils ameliorate lung injury and the development of severe disease during influenza infection. J Immunol 183, 7441-7450.
31. Tecle, T., White, M. R., Gantz, D., Crouch, E. C. & 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.
32. Tjabringa, G. S., Aarbiou, J., Ninaber, D. K., Drijfhout, J. W., Sørensen, O. E., Borregaard, N., Rabe, K. F. & Hiemstra, P. S. (2003). The antimicrobial peptide LL-37 activates innate immunity at the airway epithelial surface by transactivation of the epidermal growth factor receptor. J Immunol 171, 6690-6696.
33. White, M. R., Doss, M., Boland, P., Tecle, T. & Hartshorn, K. L. (2008). Innate immunity to influenza virus: implications for future therapy. Expert Rev Clin Immunol 4, 497-514.