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Vol. 4, No. 1, 2012
Issue release date: December 2011
Section title: Short Communication
J Innate Immun 2012;4:111–116
(DOI:10.1159/000329224)

Growing Bacteria Shed Elicitors of Drosophila Humoral Immunity

Karlsson J. · Oldenvi S. · Fahlander C. · Daenthanasanmak A. · Steiner H.
Department of Genetics, Microbiology and Toxicology, Stockholm University, Stockholm, Sweden
email Corresponding Author

Abstract

It has been much debated how the Drosophila immune system can recognize bacterial peptidoglycan that is often hidden. We show that bacteria separated from Drosophila S2 cells by a semipermeable membrane can upregulate the Imd pathway. Supernatants from exponentially growing but not from stationary-phase bacterial cultures induce antimicrobial peptides. It is also made likely that the shed elicitors are of peptidoglycan nature.

© 2011 S. Karger AG, Basel


  

Key Words

  • Innate
  • Insect
  • Peptidoglycan

References

  1. Lemaitre B, Hoffmann J: The host defense of Drosophila melanogaster. Annu Rev Immunol 2007.
  2. Schleifer KH, Kandler O: Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 1972;36:407–477.
  3. Leulier F, Parquet C, Pili-Floury S, Ryu JH, Caroff M, Lee WJ, Mengin-Lecreulx D, Lemaitre B: The drosophila immune system detects bacteria through specific peptidoglycan recognition. Nat Immunol 2003;4:478–484.
  4. Cundell DR, Kanthakumar K, Taylor GW, Goldman WE, Flak T, Cole PJ, Wilson R: Effect of tracheal cytotoxin from Bordetella pertussis on human neutrophil function in vitro. Infect Immun 1994;62:639–643.
  5. Melly MA, McGee ZA, Rosenthal RS: Ability of monomeric peptidoglycan fragments from Neisseria gonorrhoeae to damage human fallopian-tube mucosa. J Infect Dis 1984;149:378–386.
  6. Park JT, Uehara T: How bacteria consume their own exoskeletons (turnover and recycling of cell wall peptidoglycan). Microbiol Mol Biol Rev 2008;72:211–227.
  7. Hultmark D, Borge-Renberg K: Drosophila immunity: is antigen processing the first step? Curr Biol 2007;17:R22–R24.
  8. Bachmann BJ: Pedigrees of some mutant strains of Escherichia coli k-12. Bacteriol Rev 1972;36:525–557.
  9. Boman HG, Nilsson-Faye I, Paul K, Rasmuson T Jr: Insect immunity. I. Characteristics of an inducible cell-free antibacterial reaction in hemolymph of Samia cynthia pupae. Infect Immun 1974;10:136–145.
  10. Gelius E, Persson C, Karlsson J, Steiner H: A mammalian peptidoglycan recognition protein with N-acetylmuramoyl-L-alanine amidase activity. Biochem Biophys Res Commun 2003;306:988–994.
  11. Kaneko T, Goldman WE, Mellroth P, Steiner H, Fukase K, Kusumoto S, Harley W, Fox A, Golenbock D, Silverman N: Monomeric and polymeric Gram-negative peptidoglycan but not purified LPS stimulate the drosophila IMD pathway. Immunity 2004;20:637–649.
  12. Lemaitre B, Reichhart JM, Hoffmann JA: Drosophila host defense: differential induction of antimicrobial peptide genes after infection by various classes of microorganisms. Proc Natl Acad Sci USA 1997;94:14614–14619.
  13. Mellroth P, Karlsson J, Steiner H: A scavenger function for a drosophila peptidoglycan recognition protein. J Biol Chem 2003;278:7059–7064.
  14. Gendrin M, Welchman DP, Poidevin M, Herve M, Lemaitre B: Long-range activation of systemic immunity through peptidoglycan diffusion in drosophila. PLoS Pathog 2009;5:e1000694.
  15. Clarke TB, Davis KM, Lysenko ES, Zhou AY, Yu Y, Weiser JN: Recognition of peptidoglycan from the microbiota by nod1 enhances systemic innate immunity. Nat Med 2010;16:228–231.
  16. Mellroth P, Karlsson J, Håkansson J, Schultz N, Goldman WE, Steiner H: Ligand induced dimerization of Drosophila peptidoglycan recognition proteins in vitro. Proc Natl Acad Sci USA 2005;102:6455–6460.
  17. Takehana A, Katsuyama T, Yano T, Oshima Y, Takada H, Aigaki T, Kurata S: Overexpression of a pattern-recognition receptor, peptidoglycan-recognition protein-le, activates imd/relish-mediated antibacterial defense and the prophenoloxidase cascade in drosophila larvae. Proc Nat Acad Sci USA 2002;99:13705–13710.
  18. Mauck J, Chan L, Glaser L: Turnover of the cell wall of Gram-positive bacteria. J Biol Chem 1971;246:1820–1827.
  19. Lindmark H, Johansson KC, Stöven S, Hultmark D, Engström Y, Söderhall K: Enteric bacteria counteract lipopolysaccharide induction of antimicrobial peptide genes. J Immunol 2001;167:6920–6923.
  20. Haine ER, Moret Y, Siva-Jothy MT, Rolff J: Antimicrobial defense and persistent infection in insects. Science 2008;322:1257–1259.
  21. Kocks C, Cho JH, Nehme N, Ulvila J, Pearson AM, Meister M, Strom C, Conto SL, Hetru C, Stuart LM, Stehle T, Hoffmann JA, Reichhart JM, Ferrandon D, Rämet M, Ezekowitz RA: Eater, a transmembrane protein mediating phagocytosis of bacterial pathogens in drosophila. Cell 2005;123:335–346.
  22. Defaye A, Evans I, Crozatier M, Wood W, Lemaitre B, Leulier F: Genetic ablation of drosophila phagocytes reveals their contribution to both development and resistance to bacterial infection. J Innate Immun 2009;1:322–334.
  23. Charroux B, Royet J: Elimination of plasmatocytes by targeted apoptosis reveals their role in multiple aspects of the drosophila immune response. Proc Natl Acad Sci USA 2009;106:9797–9802.

  

Author Contacts

Dr. Håkan Steiner
Department of Genetics, Microbiology and Toxicology
Stockholm University
SE–106 91 Stockholm (Sweden)
Tel. +46 8 164 161, E-Mail hakan.steiner@gmt.su.se

  

Article Information

Received: December 21, 2010
Accepted after revision: May 10, 2011
Published online: August 9, 2011
Number of Print Pages : 6
Number of Figures : 3, Number of Tables : 0, Number of References : 23

  

Publication Details

Journal of Innate Immunity

Vol. 4, No. 1, Year 2012 (Cover Date: December 2011)

Journal Editor: Herwald H. (Lund), Egesten A. (Lund)
ISSN: 1662-811X (Print), eISSN: 1662-8128 (Online)

For additional information: http://www.karger.com/JIN


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References

  1. Lemaitre B, Hoffmann J: The host defense of Drosophila melanogaster. Annu Rev Immunol 2007.
  2. Schleifer KH, Kandler O: Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 1972;36:407–477.
  3. Leulier F, Parquet C, Pili-Floury S, Ryu JH, Caroff M, Lee WJ, Mengin-Lecreulx D, Lemaitre B: The drosophila immune system detects bacteria through specific peptidoglycan recognition. Nat Immunol 2003;4:478–484.
  4. Cundell DR, Kanthakumar K, Taylor GW, Goldman WE, Flak T, Cole PJ, Wilson R: Effect of tracheal cytotoxin from Bordetella pertussis on human neutrophil function in vitro. Infect Immun 1994;62:639–643.
  5. Melly MA, McGee ZA, Rosenthal RS: Ability of monomeric peptidoglycan fragments from Neisseria gonorrhoeae to damage human fallopian-tube mucosa. J Infect Dis 1984;149:378–386.
  6. Park JT, Uehara T: How bacteria consume their own exoskeletons (turnover and recycling of cell wall peptidoglycan). Microbiol Mol Biol Rev 2008;72:211–227.
  7. Hultmark D, Borge-Renberg K: Drosophila immunity: is antigen processing the first step? Curr Biol 2007;17:R22–R24.
  8. Bachmann BJ: Pedigrees of some mutant strains of Escherichia coli k-12. Bacteriol Rev 1972;36:525–557.
  9. Boman HG, Nilsson-Faye I, Paul K, Rasmuson T Jr: Insect immunity. I. Characteristics of an inducible cell-free antibacterial reaction in hemolymph of Samia cynthia pupae. Infect Immun 1974;10:136–145.
  10. Gelius E, Persson C, Karlsson J, Steiner H: A mammalian peptidoglycan recognition protein with N-acetylmuramoyl-L-alanine amidase activity. Biochem Biophys Res Commun 2003;306:988–994.
  11. Kaneko T, Goldman WE, Mellroth P, Steiner H, Fukase K, Kusumoto S, Harley W, Fox A, Golenbock D, Silverman N: Monomeric and polymeric Gram-negative peptidoglycan but not purified LPS stimulate the drosophila IMD pathway. Immunity 2004;20:637–649.
  12. Lemaitre B, Reichhart JM, Hoffmann JA: Drosophila host defense: differential induction of antimicrobial peptide genes after infection by various classes of microorganisms. Proc Natl Acad Sci USA 1997;94:14614–14619.
  13. Mellroth P, Karlsson J, Steiner H: A scavenger function for a drosophila peptidoglycan recognition protein. J Biol Chem 2003;278:7059–7064.
  14. Gendrin M, Welchman DP, Poidevin M, Herve M, Lemaitre B: Long-range activation of systemic immunity through peptidoglycan diffusion in drosophila. PLoS Pathog 2009;5:e1000694.
  15. Clarke TB, Davis KM, Lysenko ES, Zhou AY, Yu Y, Weiser JN: Recognition of peptidoglycan from the microbiota by nod1 enhances systemic innate immunity. Nat Med 2010;16:228–231.
  16. Mellroth P, Karlsson J, Håkansson J, Schultz N, Goldman WE, Steiner H: Ligand induced dimerization of Drosophila peptidoglycan recognition proteins in vitro. Proc Natl Acad Sci USA 2005;102:6455–6460.
  17. Takehana A, Katsuyama T, Yano T, Oshima Y, Takada H, Aigaki T, Kurata S: Overexpression of a pattern-recognition receptor, peptidoglycan-recognition protein-le, activates imd/relish-mediated antibacterial defense and the prophenoloxidase cascade in drosophila larvae. Proc Nat Acad Sci USA 2002;99:13705–13710.
  18. Mauck J, Chan L, Glaser L: Turnover of the cell wall of Gram-positive bacteria. J Biol Chem 1971;246:1820–1827.
  19. Lindmark H, Johansson KC, Stöven S, Hultmark D, Engström Y, Söderhall K: Enteric bacteria counteract lipopolysaccharide induction of antimicrobial peptide genes. J Immunol 2001;167:6920–6923.
  20. Haine ER, Moret Y, Siva-Jothy MT, Rolff J: Antimicrobial defense and persistent infection in insects. Science 2008;322:1257–1259.
  21. Kocks C, Cho JH, Nehme N, Ulvila J, Pearson AM, Meister M, Strom C, Conto SL, Hetru C, Stuart LM, Stehle T, Hoffmann JA, Reichhart JM, Ferrandon D, Rämet M, Ezekowitz RA: Eater, a transmembrane protein mediating phagocytosis of bacterial pathogens in drosophila. Cell 2005;123:335–346.
  22. Defaye A, Evans I, Crozatier M, Wood W, Lemaitre B, Leulier F: Genetic ablation of drosophila phagocytes reveals their contribution to both development and resistance to bacterial infection. J Innate Immun 2009;1:322–334.
  23. Charroux B, Royet J: Elimination of plasmatocytes by targeted apoptosis reveals their role in multiple aspects of the drosophila immune response. Proc Natl Acad Sci USA 2009;106:9797–9802.