PGRP-SD, an Extracellular Pattern-Recognition Receptor, Enhances Peptidoglycan-Mediated Activation of the Drosophila Imd Pathway

Immunity

Volumn 45, Issue 5, 2016, Pages 1013-1023

  Iatsenko, Igor ^a   Kondo, Shu ^b   Mengin Lecreulx, Dominique ^c   Lemaitre, Bruno ^a  

^a EPFL   (Switzerland)

^b NATIONAL INSTITUTE OF GENETICS   (Japan)

^c INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD14 ANTIGEN; LIPOPOLYSACCHARIDE; MESSENGER RNA; PATTERN RECOGNITION RECEPTOR; PEPTIDOGLYCAN; PEPTIDOGLYCAN RECOGNITION PROTEIN; CARRIER PROTEIN; DROSOPHILA PROTEIN; LMD PROTEIN, DROSOPHILA; MYOGENIC FACTOR;

ARTICLE; BACTERIUM DETECTION; CELL SURFACE; DROSOPHILA; ENTEROCOCCUS FAECALIS; ENZYME ACTIVITY; MICROCOCCUS LUTEUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; DISEASE MODEL; DROSOPHILA MELANOGASTER; GRAM NEGATIVE INFECTION; IMMUNOLOGY; INNATE IMMUNITY; POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

ANIMALS; CARRIER PROTEINS; DISEASE MODELS, ANIMAL; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GRAM-NEGATIVE BACTERIAL INFECTIONS; IMMUNITY, INNATE; MYOGENIC REGULATORY FACTORS; PEPTIDOGLYCAN; POLYMERASE CHAIN REACTION; RECEPTORS, PATTERN RECOGNITION; SIGNAL TRANSDUCTION;

EID: 84999851902     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2016.10.029     Document Type: Article

References (42)

1. Bischoff, V., Vignal, C., Boneca, I.G., Michel, T., Hoffmann, J.A., Royet, J., Function of the drosophila pattern-recognition receptor PGRP-SD in the detection of Gram-positive bacteria. Nat. Immunol. 5 (2004), 1175–1180.
2. Bosco-Drayon, V., Poidevin, M., Boneca, I.G., Narbonne-Reveau, K., Royet, J., Charroux, B., Peptidoglycan sensing by the receptor PGRP-LE in the Drosophila gut induces immune responses to infectious bacteria and tolerance to microbiota. Cell Host Microbe 12 (2012), 153–165.
3. Choe, K.M., Werner, T., Stöven, S., Hultmark, D., Anderson, K.V., Requirement for a peptidoglycan recognition protein (PGRP) in Relish activation and antibacterial immune responses in Drosophila. Science 296 (2002), 359–362.
4. Costechareyre, D., Capo, F., Fabre, A., Chaduli, D., Kellenberger, C., Roussel, A., Charroux, B., Royet, J., Tissue-Specific Regulation of Drosophila NF-kB Pathway Activation by Peptidoglycan Recognition Protein SC. J. Innate Immun. 8 (2016), 67–80.
5. De Gregorio, E., Spellman, P.T., Tzou, P., Rubin, G.M., Lemaitre, B., The Toll and Imd pathways are the major regulators of the immune response in Drosophila. EMBO J. 21 (2002), 2568–2579.
6. Ferrandon, D., Imler, J.-L., Hetru, C., Hoffmann, J.A., The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections. Nat. Rev. Immunol. 7 (2007), 862–874.
7. Gobert, V., Gottar, M., Matskevich, A.A., Rutschmann, S., Royet, J., Belvin, M., Hoffmann, J.A., Ferrandon, D., Dual activation of the Drosophila toll pathway by two pattern recognition receptors. Science 302 (2003), 2126–2130.
8. Gottar, M., Gobert, V., Michel, T., Belvin, M., Duyk, G., Hoffmann, J.A., Ferrandon, D., Royet, J., The Drosophila immune response against Gram-negative bacteria is mediated by a peptidoglycan recognition protein. Nature 416 (2002), 640–644.
9. Gottar, M., Gobert, V., Matskevich, A.A., Reichhart, J.-M., Wang, C., Butt, T.M., Belvin, M., Hoffmann, J.A., Ferrandon, D., Dual detection of fungal infections in Drosophila via recognition of glucans and sensing of virulence factors. Cell 127 (2006), 1425–1437.
10. Hu, B., Jin, J., Guo, A.-Y., Zhang, H., Luo, J., Gao, G., GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31 (2015), 1296–1297.
11. Janeway, C.A. Jr., Medzhitov, R., Innate immune recognition. Annu. Rev. Immunol. 20 (2002), 197–216.
12. Kaneko, T., Goldman, W.E., 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 20 (2004), 637–649.
13. Kaneko, T., Yano, T., Aggarwal, K., Lim, J.-H., Ueda, K., Oshima, Y., Peach, C., Erturk-Hasdemir, D., Goldman, W.E., Oh, B.-H., et al. PGRP-LC and PGRP-LE have essential yet distinct functions in the drosophila immune response to monomeric DAP-type peptidoglycan. Nat. Immunol. 7 (2006), 715–723.
14. Kleino, A., Silverman, N., The Drosophila IMD pathway in the activation of the humoral immune response. Dev. Comp. Immunol. 42 (2014), 25–35.
15. Kondo, S., Ueda, R., Highly improved gene targeting by germline-specific Cas9 expression in Drosophila. Genetics 195 (2013), 715–721.
16. Kurata, S., Peptidoglycan recognition proteins in Drosophila immunity. Dev. Comp. Immunol. 42 (2014), 36–41.
17. Lee, J.D., Kato, K., Tobias, P.S., Kirkland, T.N., Ulevitch, R.J., Transfection of CD14 into 70Z/3 cells dramatically enhances the sensitivity to complexes of lipopolysaccharide (LPS) and LPS binding protein. J. Exp. Med. 175 (1992), 1697–1705.
18. Lemaitre, B., Hoffmann, J., The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 25 (2007), 697–743.
19. Leone, P., Bischoff, V., Kellenberger, C., Hetru, C., Royet, J., Roussel, A., Crystal structure of Drosophila PGRP-SD suggests binding to DAP-type but not lysine-type peptidoglycan. Mol. Immunol. 45 (2008), 2521–2530.
20. Leulier, F., Parquet, C., Pili-Floury, S., Ryu, J.-H., Caroff, M., Lee, W.-J., Mengin-Lecreulx, D., Lemaitre, B., The Drosophila immune system detects bacteria through specific peptidoglycan recognition. Nat. Immunol. 4 (2003), 478–484.
21. Lim, J.-H., Kim, M.-S., Kim, H.-E., Yano, T., Oshima, Y., Aggarwal, K., Goldman, W.E., Silverman, N., Kurata, S., Oh, B.-H., Structural basis for preferential recognition of diaminopimelic acid-type peptidoglycan by a subset of peptidoglycan recognition proteins. J. Biol. Chem. 281 (2006), 8286–8295.
22. Mellroth, P., Steiner, H., PGRP-SB1: an N-acetylmuramoyl L-alanine amidase with antibacterial activity. Biochem. Biophys. Res. Commun. 350 (2006), 994–999.
23. Mellroth, P., Karlsson, J., Steiner, H., A scavenger function for a Drosophila peptidoglycan recognition protein. J. Biol. Chem. 278 (2003), 7059–7064.
24. Neyen, C., Lemaitre, B., Sensing Gram-negative bacteria: a phylogenetic perspective. Curr. Opin. Immunol. 38 (2016), 8–17.
25. Neyen, C., Poidevin, M., Roussel, A., Lemaitre, B., Tissue- and ligand-specific sensing of gram-negative infection in drosophila by PGRP-LC isoforms and PGRP-LE. J. Immunol. 189 (2012), 1886–1897.
26. Neyen, C., Bretscher, A.J., Binggeli, O., Lemaitre, B., Methods to study Drosophila immunity. Methods 68 (2014), 116–128.
27. Neyen, C., Runchel, C., Schüpfer, F., Meier, P., Lemaitre, B., The regulatory isoform rPGRP-LC induces immune resolution via endosomal degradation of receptors. Nat. Immunol. 17 (2016), 1150–1158.
28. Paredes, J.C., Welchman, D.P., Poidevin, M., Lemaitre, B., Negative regulation by amidase PGRPs shapes the Drosophila antibacterial response and protects the fly from innocuous infection. Immunity 35 (2011), 770–779.
29. Park, B.S., Lee, J.-O., Recognition of lipopolysaccharide pattern by TLR4 complexes. Exp. Mol. Med., 45, 2013, e66.
30. Pili-Floury, S., Leulier, F., Takahashi, K., Saigo, K., Samain, E., Ueda, R., Lemaitre, B., In vivo RNA interference analysis reveals an unexpected role for GNBP1 in the defense against Gram-positive bacterial infection in Drosophila adults. J. Biol. Chem. 279 (2004), 12848–12853.
31. Pugin, J., Schürer-Maly, C.C., Leturcq, D., Moriarty, A., Ulevitch, R.J., Tobias, P.S., Lipopolysaccharide activation of human endothelial and epithelial cells is mediated by lipopolysaccharide-binding protein and soluble CD14. Proc. Natl. Acad. Sci. USA 90 (1993), 2744–2748.
32. Royet, J., Gupta, D., Dziarski, R., Peptidoglycan recognition proteins: modulators of the microbiome and inflammation. Nat. Rev. Immunol. 11 (2011), 837–851.
33. Ryder, E., Blows, F., Ashburner, M., Bautista-Llacer, R., Coulson, D., Drummond, J., Webster, J., Gubb, D., Gunton, N., Johnson, G., et al. The DrosDel collection: a set of P-element insertions for generating custom chromosomal aberrations in Drosophila melanogaster. Genetics 167 (2004), 797–813.
34. Schleifer, K.H., Kandler, O., Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol. Rev. 36 (1972), 407–477.
35. Schmidt, R.L., Trejo, T.R., Plummer, T.B., Platt, J.L., Tang, A.H., Infection-induced proteolysis of PGRP-LC controls the IMD activation and melanization cascades in Drosophila. FASEB J. 22 (2008), 918–929.
36. Stenbak, C.R., Ryu, J.-H., Leulier, F., Pili-Floury, S., Parquet, C., Hervé, M., Chaput, C., Boneca, I.G., Lee, W.-J., Lemaitre, B., Mengin-Lecreulx, D., Peptidoglycan molecular requirements allowing detection by the Drosophila immune deficiency pathway. J. Immunol. 173 (2004), 7339–7348.
37. Takehana, A., Yano, T., Mita, S., Kotani, A., Oshima, Y., Kurata, S., Peptidoglycan recognition protein (PGRP)-LE and PGRP-LC act synergistically in Drosophila immunity. EMBO J. 23 (2004), 4690–4700.
38. Valanne, S., Wang, J.-H., Rämet, M., The Drosophila Toll signaling pathway. J. Immunol. 186 (2011), 649–656.
39. Wang, L., Gilbert, R.J.C., Atilano, M.L., Filipe, S.R., Gay, N.J., Ligoxygakis, P., Peptidoglycan recognition protein-SD provides versatility of receptor formation in Drosophila immunity. Proc. Natl. Acad. Sci. USA 105 (2008), 11881–11886.
40. Yoshida, H., Kinoshita, K., Ashida, M., Purification of a peptidoglycan recognition protein from hemolymph of the silkworm, Bombyx mori. J. Biol. Chem. 271 (1996), 13854–13860.
41. Zaidman-Rémy, A., Hervé, M., Poidevin, M., Pili-Floury, S., Kim, M.-S., Blanot, D., Oh, B.-H., Ueda, R., Mengin-Lecreulx, D., Lemaitre, B., The Drosophila amidase PGRP-LB modulates the immune response to bacterial infection. Immunity 24 (2006), 463–473.
42. Zaidman-Rémy, A., Poidevin, M., Hervé, M., Welchman, D.P., Paredes, J.C., Fahlander, C., Steiner, H., Mengin-Lecreulx, D., Lemaitre, B., Drosophila immunity: analysis of PGRP-SB1 expression, enzymatic activity and function. PLoS ONE, 6, 2011, e17231.