Relative roles of the cellular and humoral responses in the Drosophila host defense against three gram-positive bacterial infections

PLoS ONE

Volumn 6, Issue 3, 2011, Pages

  Nehme, Nadine T ^a,c   Quintin, Jessica ^a   Cho, Ju Hyun ^a,b,d   Lee, Janice ^a,b   Lafarge, Marie Céline ^a   Kocks, Christine ^a,b   Ferrandon, Dominique ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c HÔPITAL NECKER ENFANTS MALADES   (France)

^d Gyeongsang National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; GRAM NEGATIVE BINDING PROTEIN 1; OPSONIN; PATTERN RECOGNITION RECEPTOR; PEPTIDOGLYCAN RECOGNITION PROTEIN; UNCLASSIFIED DRUG; ANTIMICROBIAL CATIONIC PEPTIDE; CARRIER PROTEIN; CELL SURFACE RECEPTOR; DROSOPHILA PROTEIN; EATER PROTEIN, DROSOPHILA; GNBP1 PROTEIN, DROSOPHILA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD CELL; CELLULAR IMMUNITY; CONTROLLED STUDY; DROSOPHILA; ENTEROCOCCUS FAECALIS; GRAM POSITIVE INFECTION; HOST PATHOGEN INTERACTION; HOST RESISTANCE; HUMORAL IMMUNITY; IMMUNE DEFICIENCY; MACROPHAGE FUNCTION; MICROCOCCUS LUTEUS; NONHUMAN; PHAGOCYTOSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; STAPHYLOCOCCUS AUREUS; SURVIVAL RATE; WILD TYPE; ANIMAL; CYTOLOGY; DROSOPHILA MELANOGASTER; DRUG EFFECT; GRAM POSITIVE BACTERIUM; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; MICROBIOLOGY; SOLUBILITY;

BACTERIA (MICROORGANISMS); ENTEROCOCCUS FAECALIS; MICROCOCCUS LUTEUS; POSIBACTERIA; STAPHYLOCOCCUS AUREUS;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; CARRIER PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENTEROCOCCUS FAECALIS; GRAM-POSITIVE BACTERIA; GRAM-POSITIVE BACTERIAL INFECTIONS; HOST-PATHOGEN INTERACTIONS; IMMUNITY, CELLULAR; IMMUNITY, HUMORAL; IMMUNITY, INNATE; MICROCOCCUS LUTEUS; OPSONIN PROTEINS; PHAGOCYTOSIS; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; SOLUBILITY; STAPHYLOCOCCUS AUREUS;

EID: 79952285913     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0014743     Document Type: Article

References (58)

1. Lemaitre B, Hoffmann J, (2007) The Host Defense of Drosophila melanogaster. Annu Rev Immunol 25: 697-743.
2. Ferrandon D, Imler JL, Hetru C, Hoffmann JA, (2007) The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections. Nat Rev Immunol 7: 862-874.
3. Royet J, Dziarski R, (2007) Peptidoglycan recognition proteins: pleiotropic sensors and effectors of antimicrobial defences. Nat Rev Microbiol 5: 264-277.
4. Leone P, Bischoff V, Kellenberger C, Hetru C, Royet J, et al. (2008) Crystal structure of Drosophila PGRP-SD suggests binding to DAP-type but not lysine-type peptidoglycan. Mol Immunol 45: 2521-2530.
5. Wang L, Gilbert RJ, Atilano ML, Filipe SR, Gay NJ, et al. (2008) Peptidoglycan recognition protein-SD provides versatility of receptor formation in Drosophila immunity. Proc Natl Acad Sci U S A 105: 11881-11886.
6. Chang CI, Pili-Floury SS, Herve M, Parquet C, Chelliah Y, et al. (2004) A Drosophila pattern recognition receptor contains a peptidoglycan docking groove and unusual l,d-carboxypeptidase activity. PLoS Biol 2: E277.
7. Lemaitre B, Nicolas E, Michaut L, Reichhart JM, Hoffmann JA, (1996) The dorsoventral regulatory gene cassette spätzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86: 973-983.
8. Bulet P, Hetru C, Dimarcq JL, Hoffmann D, (1999) Antimicrobial peptides in insects; structure and function. Dev Comp Immunol 23: 329-344.
9. Tzou P, Reichhart JM, Lemaitre B, (2002) Constitutive expression of a single antimicrobial peptide can restore wild-type resistance to infection in immunodeficient Drosophila mutants. Proc Natl Acad Sci U S A 99: 2152-2157.
10. Imler JL, Bulet P, (2005) Antimicrobial peptides in Drosophila: structures, activities and gene regulation. Chem Immunol Allergy 86: 1-21.
11. Rutschmann S, Jung AC, Hetru C, Reichhart J-M, Hoffmann JA, et al. (2000) The Rel protein DIF mediates the antifungal, but not the antibacterial, response in Drosophila. Immunity 12: 569-580.
12. Tanji T, Hu X, Weber AN, Ip YT, (2007) Toll and IMD pathways synergistically activate an innate immune response in Drosophila melanogaster. Mol Cell Biol 27: 4578-4588.
13. Matova N, Anderson KV, (2006) Rel/NF-kappaB double mutants reveal that cellular immunity is central to Drosophila host defense. Proc Natl Acad Sci U S A 103: 16424-16429.
14. Braun A, Hoffmann JA, Meister M, (1998) Analysis of the Drosophila host defense in domino mutant larvae, which are devoid of hemocytes. Proc Natl Acad Sci U S A 95: 14337-14342.
15. Lanot R, Zachary D, Holder F, Meister M, (2001) Postembryonic hematopoiesis in Drosophila. Dev Biol 230: 243-257.
16. Elrod-Erickson M, Mishra S, Schneider D, (2000) Interactions between the cellular and humoral immune responses in Drosophila. Curr Biol 10: 781-784.
17. Pham LN, Dionne MS, Shirasu-Hiza M, Schneider DS, (2007) A specific primed immune response in Drosophila is dependent on phagocytes. PLoS Pathog 3: e26.
18. Brennan CA, Delaney JR, Schneider DS, Anderson KV, (2007) Psidin is required in Drosophila blood cells for both phagocytic degradation and immune activation of the fat body. Curr Biol 17: 67-72.
19. Avet-Rochex A, Bergeret E, Attree I, Meister M, Fauvarque MO, (2005) Suppression of Drosophila cellular immunity by directed expression of the ExoS toxin GAP domain of Pseudomonas aeruginosa. Cell Microbiol 7: 799-810.
20. Kocks C, Cho JH, Nehme N, Ulvila J, Pearson AM, et al. (2005) Eater, a transmembrane protein mediating phagocytosis of bacterial pathogens in Drosophila. Cell 123: 335-346.
21. Nehme NT, Liegeois S, Kele B, Giammarinaro P, Pradel E, et al. (2007) A Model of Bacterial Intestinal Infections in Drosophila melanogaster. PLoS Pathog 3: e173.
22. Rutschmann S, Kilinc A, Ferrandon D, (2002) The Toll pathway is required for resistance to Gram-positive bacterial infections in Drosophila. J Immunol 168: 1542-1546.
23. Bischoff V, Vignal C, Boneca IG, Michel T, Hoffmann JA, et al. (2004) Function of the drosophila pattern-recognition receptor PGRP-SD in the detection of Gram-positive bacteria. Nat Immunol 5: 1175-1180.
24. Hoffmann D, (1976) [Role of phagocytosis and soluble antibacterial factors in experimental immunization of Locusta migratoria]. C R Acad Sci Hebd Seances Acad Sci D 282: 1021-1024.
25. Garver LS, Wu J, Wu LP, (2006) The peptidoglycan recognition protein PGRP-SC1a is essential for Toll signaling and phagocytosis of Staphylococcus aureus in Drosophila. Proc Natl Acad Sci U S A 103: 660-665.
26. Defaye A, Evans I, Crozatier M, Wood W, Lemaitre B, et al. (2009) Genetic ablation of Drosophila phagocytes reveals their contribution to both development and resistance to bacterial infections. J Innate Immun 1: 322-334.
27. Charroux B, Royet J, (2009) Elimination of plasmatocytes by targeted apoptosis reveals their role in multiple aspects of the Drosophila immune response. Proc Natl Acad Sci U S A 106: 9797-9802.
28. De Gregorio E, Spellman PT, Tzou P, Rubin GM, Lemaitre B, (2002) The Toll and Imd pathways are the major regulators of the immune response in Drosophila. Embo J 21: 2568-2579.
29. Sackton TB, Lazzaro BP, Schlenke TA, Evans JD, Hultmark D, et al. (2007) Dynamic evolution of the innate immune system in Drosophila. Nat Genet 39: 1461-1468.
30. Dimarcq JL, Hoffmann D, Meister M, Bulet P, Lanot R, et al. (1994) Characterization and transcriptional profiles of a Drosophila gene encoding an insect defensin. A study in insect immunity. Eur J Biochem 221: 201-209.
31. Hoffmann JA, Hetru C, (1992) Insect defensins: inducible antibacterial peptides. Immunol Today 13: 411-415.
32. Ferrandon D, Jung AC, Criqui MC, Lemaitre B, Uttenweiler-Joseph S, et al. (1998) A drosomycin-GFP reporter transgene reveals a local immune response in Drosophila that is not dependent on the Toll pathway. EMBO J 17: 1217-1227.
33. Tzou P, Ohresser S, Ferrandon D, Capovilla M, Reichhart JM, et al. (2000) Tissue-specific inducible expression of antimicrobial peptide genes in Drosophila surface epithelia. Immunity 13: 737-748.
34. Michel T, Reichhart J, Hoffmann JA, Royet J, (2001) Drosophila Toll is activated by Gram-positive bacteria through a circulating peptidoglycan recognition protein. Nature 414: 756-759.
35. Avet-Rochex A, Perrin J, Bergeret E, Fauvarque MO, (2007) Rac2 is a major actor of Drosophila resistance to Pseudomonas aeruginosa acting in phagocytic cells. Genes Cells 12: 1193-1204.
36. Bischoff V, Vignal C, Duvic B, Boneca IG, Hoffmann JA, et al. (2006) Downregulation of the Drosophila Immune Response by Peptidoglycan-Recognition Proteins SC1 and SC2. PLoS Pathog 2: e14.
37. Ligoxygakis P, Pelte N, Ji C, Leclerc V, Duvic B, et al. (2002) A serpin mutant links Toll activation to melanization in the host defence of Drosophila. Embo J 21: 6330-6337.
38. Ma C, Kanost MR, (2000) A beta1,3-glucan recognition protein from an insect, Manduca sexta, agglutinates microorganisms and activates the phenoloxidase cascade. J Biol Chem 275: 7505-7514.
39. Matskevich AA, Quintin J, Ferrandon D, (2010) The Drosophila PRR GNBP3 assembles effector complexes involved in antifungal defenses independently of its Toll-pathway activation function. Eur J Immunol 40: 1244-1254.
40. Pluddemann A, Mukhopadhyay S, Gordon S, (2006) The interaction of macrophage receptors with bacterial ligands. Expert Rev Mol Med 8: 1-25.
41. Schleifer KH, Kandler O, (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36: 407-477.
42. Weidenmaier C, Peschel A, (2008) Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions. Nat Rev Microbiol 6: 276-287.
43. Powell DA, Duckworth M, Baddiley J, (1975) A membrane-associated lipomannan in micrococci. Biochem J 151: 387-397.
44. Stuart LM, Deng J, Silver JM, Takahashi K, Tseng AA, et al. (2005) Response to Staphylococcus aureus requires CD36-mediated phagocytosis triggered by the COOH-terminal cytoplasmic domain. J Cell Biol 170: 477-485.
45. Philips JA, Rubin EJ, Perrimon N, (2005) Drosophila RNAi screen reveals CD36 family member required for mycobacterial infection. Science 309: 1251-1253.
46. Kurucz E, Markus R, Zsamboki J, Folkl-Medzihradszky K, Darula Z, et al. (2007) Nimrod, a putative phagocytosis receptor with EGF repeats in Drosophila plasmatocytes. Curr Biol 17: 649-654.
47. Ramet M, Pearson A, Manfruelli P, Li X, Koziel H, et al. (2001) Drosophila scavenger receptor CI is a pattern recognition receptor for bacteria. Immunity 15: 1027-1038.
48. Watson FL, Puttmann-Holgado R, Thomas F, Lamar DL, Hughes M, et al. (2005) Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science 309: 1874-1878.
49. Hashimoto Y, Tabuchi Y, Sakurai K, Kutsuna M, Kurokawa K, et al. (2009) Identification of lipoteichoic acid as a ligand for draper in the phagocytosis of Staphylococcus aureus by Drosophila hemocytes. J Immunol 183: 7451-7460.
50. Stuart LM, Ezekowitz RA, (2008) Phagocytosis and comparative innate immunity: learning on the fly. Nat Rev Immunol 8: 131-141.
51. Aggarwal K, Silverman N, (2008) Positive and negative regulation of the Drosophila immune response. BMB Rep 41: 267-277.
52. Kraaijeveld AR, Godfray HCJ, (1997) Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 389: 278-280.
53. DiAngelo JR, Bland ML, Bambina S, Cherry S, Birnbaum MJ, (2009) The immune response attenuates growth and nutrient storage in Drosophila by reducing insulin signaling. Proc Natl Acad Sci U S A 106: 20853-20858.
54. Rutschmann S, Jung AC, Rui Z, Silverman N, Hoffmann JA, et al. (2000) Role of Drosophila IKKgamma in a Toll-independent antibacterial immune response. Nat Immunology 1: 342-347.
55. Jung A, Criqui M-C, Rutschmann S, Hoffmann J-A, Ferrandon D, (2001) A microfluorometer assay to measure the expression of ß-galactosidase and GFP reporter genes in single Drosophila flies. Biotechniques 30: 594-601.
56. Gobert V, Gottar M, Matskevich A, Rutschmann S, Royet J, et al. (2003) Dual Activation of the Drosophila Toll Pathway by Two Pattern Recognition Receptors. Science 302: 2126-2130.
57. Gottar M, Gobert V, Matskevich AA, Reichhart JM, Wang C, et al. (2006) Dual Detection of Fungal Infections in Drosophila via Recognition of Glucans and Sensing of Virulence Factors. Cell 127: 1425-1437.
58. Ramet M, Manfruelli P, Pearson A, Mathey-Prevot B, Ezekowitz RA, (2002) Functional genomic analysis of phagocytosis and identification of a Drosophila receptor for E. coli. Nature 416: 644-648.