Defense of zebrafish embryos against Streptococcus pneumoniae infection is dependent on the phagocytic activity of leukocytes

Developmental and Comparative Immunology

Volumn 36, Issue 2, 2012, Pages 342-348

  Rounioja, Samuli ^a,b   Saralahti, Anni ^a   Rantala, Lilli ^a   Parikka, Mataleena ^a   Henriques Normark, Birgitta ^c   Silvennoinen, Olli ^a,b   Rämet, Mika ^a,b  

^a TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^b TAMPERE UNIVERSITY HOSPITAL   (Finland)

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Host pathogens interactions; Innate immunity; Streptococcus pneumoniae; Zebrafish

Indexed keywords

CYTOKINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL VIRULENCE; BONE MARROW CELL; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; EMBRYO; EMBRYO DEATH; IMMUNE RESPONSE; INNATE IMMUNITY; LEUKOCYTE FUNCTION; NONHUMAN; PHAGOCYTE; PHAGOCYTOSIS; PNEUMOCOCCAL INFECTION; PRIORITY JOURNAL; STREPTOCOCCUS PNEUMONIAE; SURVIVAL RATE; WILD TYPE;

BACTERIA (MICROORGANISMS); DANIO RERIO; STREPTOCOCCUS PNEUMONIAE; VERTEBRATA;

EID: 80455174704     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2011.05.008     Document Type: Article

References (43)

1. Aaberge I.S., Eng J., Lermark G., Lovik M. Virulence of Streptococcus pneumoniae in mice. a standardized method for preparation and frozen storage of the experimental bacterial inoculum. Microb. Pathog. 1995, 18:141-152.
2. Albiger B., Sandgren A., Katsuragi H., Meyer-Hoffert U., Beiter K., Wartha F., Hornef M., Normark S., Normark B.H. Myeloid differentiation factor 88-dependent signalling controls bacterial growth during colonization and systemic pneumococcal disease in mice. Cell Microbiol. 2005, 7:1603-1615.
3. Andreansky S., Liu H., Turner S., McCullers J.A., Lang R., Rutschman R., Doherty P.C., Murray P.J., Nienhuis A.W., Strom T.S. WASP- mice exhibit defective immune responses to influenza A virus, Streptococcus pneumoniae, and Mycobacterium bovis BCG. Exp. Hematol. 2005, 33:443-451.
4. Badour K., Zhang J., Siminovitch K.A. The Wiskott-Aldrich syndrome protein: forging the link between actin and cell activation. Immunol. Rev. 2003, 192:98-112.
5. Barocchi M.A., Ries J., Zogaj X., Hemsley C., Albiger B., Kanth A., Dahlberg S., Fernebro J., Moschioni M., Masignani V., Hultenby K., Taddei A.R., Beiter K., Wartha F., von Euler A., Covacci A., Holden D.W., Normark S., Rappuoli R., Henriques-Normark B. A pneumococcal pilus influences virulence and host inflammatory responses. Proc. Natl. Acad. Sci. USA 2006, 103:2857-2862.
6. Berry A.M., Lock R.A., Hansman D., Paton J.C. Contribution of autolysin to virulence of Streptococcus pneumoniae. Infect. Immun. 1989, 57:2324-2330.
7. Berry A.M., Yother J., Briles D.E., Hansman D., Paton J.C. Reduced virulence of a defined pneumolysin-negative mutant of Streptococcus pneumoniae. Infect. Immun. 1989, 57:2037-2042.
8. Brannon M.K., Davis J.M., Mathias J.R., Hall C.J., Emerson J.C., Crosier P.S., Huttenlocher A., Ramakrishnan L., Moskowitz S.M. Pseudomonas aeruginosa Type III secretion system interacts with phagocytes to modulate systemic infection of zebrafish embryos. Cell Microbiol. 2009, 11:755-768.
9. Brown J.S., Hussell T., Gilliland S.M., Holden D.W., Paton J.C., Ehrenstein M.R., Walport M.J., Botto M. The classical pathway is the dominant complement pathway required for innate immunity to Streptococcus pneumoniae infection in mice. Proc. Natl. Acad. Sci. USA 2002, 99:16969-16974.
10. Clatworthy A.E., Lee J.S., Leibman M., Kostun Z., Davidson A.J., Hung D.T. Pseudomonas aeruginosa infection of zebrafish involves both host and pathogen determinants. Infect. Immun. 2009, 77:1293-1303.
11. Clay H., Davis J.M., Beery D., Huttenlocher A., Lyons S.E., Ramakrishnan L. Dichotomous role of the macrophage in early Mycobacterium marinum infection of the zebrafish. Cell Host Microbe 2007, 2:29-39.
12. Gilbert R.J., Jimenez J.L., Chen S., Tickle I.J., Rossjohn J., Parker M., Andrew P.W., Saibil H.R. Two structural transitions in membrane pore formation by pneumolysin, the pore-forming toxin of Streptococcus pneumoniae. Cell 1999, 97:647-655.
13. Hirst R.A., Kadioglu A., O'Callaghan C., Andrew P.W. The role of pneumolysin in pneumococcal pneumonia and meningitis. Clin. Exp. Immunol. 2004, 138:195-201.
14. Hsu K., Traver D., Kutok J.L., Hagen A., Liu T.X., Paw B.H., Rhodes J., Berman J.N., Zon L.I., Kanki J.P., Look A.T. The pu.1 promoter drives myeloid gene expression in zebrafish. Blood 2004, 104:1291-1297.
15. Hyams C., Camberlein E., Cohen J.M., Bax K., Brown J.S. The Streptococcus pneumoniae capsule inhibits complement activity and neutrophil phagocytosis by multiple mechanisms. Infect. Immun. 2010, 78:704-715.
16. Iannelli F., Chiavolini D., Ricci S., Oggioni M.R., Pozzi G. Pneumococcal surface protein C contributes to sepsis caused by Streptococcus pneumoniae in mice. Infect. Immun. 2004, 72:3077-3080.
17. Ishii K.J., Koyama S., Nakagawa A., Coban C., Akira S. Host innate immune receptors and beyond: making sense of microbial infections. Cell Host Microbe 2008, 3:352-363.
18. Jault C., Pichon L., Chluba J. Toll-like receptor gene family and TIR-domain adapters in Danio rerio. Mol. Immunol. 2004, 40:759-771.
19. Jedrzejas, M.J., 2001. Pneumococcal virulence factors: structure and function. Microbiol. Mol. Biol. Rev. 65, 187-207 (first page, table of contents).
20. Levraud J.P., Boudinot P., Colin I., Benmansour A., Peyrieras N., Herbomel P., Lutfalla G. Identification of the zebrafish IFN receptor: implications for the origin of the vertebrate IFN system. J. Immunol. 2007, 178:4385-4394.
21. Lieschke G.J., Oates A.C., Crowhurst M.O., Ward A.C., Layton J.E. Morphologic and functional characterization of granulocytes and macrophages in embryonic and adult zebrafish. Blood 2001, 98:3087-3096.
22. Martner A., Skovbjerg S., Paton J.C., Wold A.E. Streptococcus pneumoniae autolysis prevents phagocytosis and production of phagocyte-activating cytokines. Infect. Immun. 2009, 77:3826-3837.
23. Miller J.D., Neely M.N. Zebrafish as a model host for streptococcal pathogenesis. Acta Trop. 2004, 91:53-68.
24. Miller J.D., Neely M.N. Large-scale screen highlights the importance of capsule for virulence in the zoonotic pathogen Streptococcus iniae. Infect. Immun. 2005, 73:921-934.
25. Morona J.K., Morona R., Paton J.C. Attachment of capsular polysaccharide to the cell wall of Streptococcus pneumoniae type 2 is required for invasive disease. Proc. Natl. Acad. Sci. USA 2006, 103:8505-8510.
26. Nelson A.L., Ries J., Bagnoli F., Dahlberg S., Falker S., Rounioja S., Tschop J., Morfeldt E., Ferlenghi I., Hilleringmann M., Holden D.W., Rappuoli R., Normark S., Barocchi M.A., Henriques-Normark B. RrgA is a pilus-associated adhesin in Streptococcus pneumoniae. Mol. Microbiol. 2007, 66:329-340.
27. Nelson A.L., Roche A.M., Gould J.M., Chim K., Ratner A.J., Weiser J.N. Capsule enhances pneumococcal colonization by limiting mucus-mediated clearance. Infect. Immun. 2007, 75:83-90.
28. Paterson G.K., Mitchell T.J. The role of Streptococcus pneumoniae sortase A in colonisation and pathogenesis. Microbes Infect. 2006, 8:145-153.
29. Prajsnar T.K., Cunliffe V.T., Foster S.J., Renshaw S.A. A novel vertebrate model of Staphylococcus aureus infection reveals phagocyte-dependent resistance of zebrafish to non-host specialized pathogens. Cell Microbiol. 2008, 10:2312-2325.
30. Pressley M.E., Phelan P.E., Witten P.E., Mellon M.T., Kim C.H. Pathogenesis and inflammatory response to Edwardsiella tarda infection in the zebrafish. Dev. Comp. Immunol. 2005, 29:501-513.
31. Roca F.J., Mulero I., Lopez-Munoz A., Sepulcre M.P., Renshaw S.A., Meseguer J., Mulero V. Evolution of the inflammatory response in vertebrates: fish TNF-alpha is a powerful activator of endothelial cells but hardly activates phagocytes. J. Immunol. 2008, 181:5071-5081.
32. Sandgren A., Albiger B., Orihuela C.J., Tuomanen E., Normark S., Henriques-Normark B. Virulence in mice of pneumococcal clonal types with known invasive disease potential in humans. J. Infect. Dis. 2005, 192:791-800.
33. Stockhammer O.W., Zakrzewska A., Hegedus Z., Spaink H.P., Meijer A.H. Transcriptome profiling and functional analyses of the zebrafish embryonic innate immune response to Salmonella infection. J. Immunol. 2009, 182:5641-5653.
34. Sullivan K.E., Mullen C.A., Blaese R.M., Winkelstein J.A. A multiinstitutional survey of the Wiskott-Aldrich syndrome. J. Pediatr. 1994, 125:876-885.
35. Traver D., Herbomel P., Patton E.E., Murphey R.D., Yoder J.A., Litman G.W., Catic A., Amemiya C.T., Zon L.I., Trede N.S. The zebrafish as a model organism to study development of the immune system. Adv. Immunol. 2003, 81:253-330.
36. Tuomanen E.I., Austrian R., Masure H.R. Pathogenesis of pneumococcal infection. N. Engl. J. Med. 1995, 332:1280-1284.
37. van der Poll T., Opal S.M. Pathogenesis, treatment, and prevention of pneumococcal pneumonia. Lancet 2009, 374:1543-1556.
38. van der Sar A.M., Appelmelk B.J., Vandenbroucke-Grauls C.M., Bitter W. A star with stripes: zebrafish as an infection model. Trends Microbiol. 2004, 12:451-457.
39. van der Sar A.M., Stockhammer O.W., van der Laan C., Spaink H.P., Bitter W., Meijer A.H. MyD88 innate immune function in a zebrafish embryo infection model. Infect. Immun. 2006, 74:2436-2441.
40. von Bernuth H., Picard C., Jin Z., Pankla R., Xiao H., Ku C.L., Chrabieh M., Mustapha I.B., Ghandil P., Camcioglu Y., Vasconcelos J., Sirvent N., Guedes M., Vitor A.B., Herrero-Mata M.J., Arostegui J.I., Rodrigo C., Alsina L., Ruiz-Ortiz E., Juan M., Fortuny C., Yague J., Anton J., Pascal M., Chang H.H., Janniere L., Rose Y., Garty B.Z., Chapel H., Issekutz A., Marodi L., Rodriguez-Gallego C., Banchereau J., Abel L., Li X., Chaussabel D., Puel A., Casanova J.L. Pyogenic bacterial infections in humans with MyD88 deficiency. Science 2008, 321:691-696.
41. Wiles T.J., Bower J.M., Redd M.J., Mulvey M.A. Use of zebrafish to probe the divergent virulence potentials and toxin requirements of extraintestinal pathogenic Escherichia coli. PLoS Pathog. 2009, 5:e1000697.
42. Yoder J.A., Nielsen M.E., Amemiya C.T., Litman G.W. Zebrafish as an immunological model system. Microbes Infect. 2002, 4:1469-1478.
43. Yu V.L., Chiou C.C., Feldman C., Ortqvist A., Rello J., Morris A.J., Baddour L.M., Luna C.M., Snydman D.R., Ip M., Ko W.C., Chedid M.B., Andremont A., Klugman K.P. An international prospective study of pneumococcal bacteremia: correlation with in vitro resistance, antibiotics administered, and clinical outcome. Clin. Infect. Dis. 2003, 37:230-237.