Prophenoloxidase Activation Is Required for Survival to Microbial Infections in Drosophila

PLoS Pathogens

Volumn 10, Issue 5, 2014, Pages

  Binggeli, Olivier ^a   Neyen, Claudine ^a   Poidevin, Mickael ^b   Lemaitre, Bruno ^a  

^a EPFL   (Switzerland)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CATECHOL OXIDASE; DROSOPHILA PROTEIN; ENZYME PRECURSOR; MELANIN; PRO-PHENOLOXIDASE; SERINE PROTEINASE INHIBITOR; SPN27A PROTEIN, DROSOPHILA;

ANIMAL; CYTOLOGY; DROSOPHILA MELANOGASTER; ENZYME ACTIVATION; EPISTASIS; GENE DELETION; GENE SILENCING; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; INFECTION; INNATE IMMUNITY; LARVA; METABOLISM; MICROBIOLOGY; MORTALITY; PHYSIOLOGY; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CATECHOL OXIDASE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENZYME ACTIVATION; ENZYME PRECURSORS; EPISTASIS, GENETIC; GENE DELETION; GENE KNOCKDOWN TECHNIQUES; IMMUNITY, INNATE; INFECTION; LARVA; MELANINS; SERPINS;

EID: 84901675909     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004067     Document Type: Article

References (58)

1. Cerenius L, Lee BL, Soderhall K, (2008) The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immunol 29: 263-271.
2. Tang H (2009) Regulation and function of the melanization reaction in Drosophila. Fly (Austin) 3.
3. Liu H, Jiravanichpaisal P, Cerenius L, Lee BL, Soderhall I, et al. (2007) Phenoloxidase is an important component of the defense against Aeromonas hydrophila Infection in a crustacean, Pacifastacus leniusculus. J Biol Chem 282: 33593-33598.
4. Nappi A, Poirie M, Carton Y, (2009) The role of melanization and cytotoxic by- products in the cellular immune responses of Drosophila against parasitic wasps. Adv Parasitol 70: 99-121.
5. Rizki T, Rizki R, Grell E, (1980) A mutant affecting the crystal cells in Drosophila melanogaster. Roux's Arch Dev Biol 188: 91-99.
6. Lanot R, Zachary D, Holder F, Meister M, (2000) Post-embryonic hematopoiesis in Drosophila. Dev Biol 230: 243-257.
7. Honti V, Csordas G, Kurucz E, Markus R, Ando I, (2014) The cell-mediated immunity of Drosophila melanogaster: Hemocyte lineages, immune compartments, microanatomy and regulation. Dev Comp Immunol 42: 47-56.
8. Bidla G, Dushay MS, Theopold U, (2007) Crystal cell rupture after injury in Drosophila requires the JNK pathway, small GTPases and the TNF homolog Eiger. J Cell Sci 120: 1209-1215.
9. Waltzer L, Ferjoux G, Bataille L, Haenlin M, (2003) Cooperation between the GATA and RUNX factors Serpent and Lozenge during Drosophila hematopoiesis. EMBO J 22: 6516-6525.
10. Irving P, Ubeda JM, Doucet D, Troxler L, Lagueux M, et al. (2005) New insights into Drosophila larval haemocyte functions through genome-wide analysis. Cell Microbiol 7: 335-350.
11. Nam HJ, Jang IH, Asano T, Lee WJ, (2008) Involvement of pro-phenoloxidase 3 in lamellocyte-mediated spontaneous melanization in Drosophila. Mol Cells 26: 606-610.
12. Chen Y, Liu F, Yang B, Lu A, Wang S, et al. (2012) Specific amino acids affecting Drosophila melanogaster prophenoloxidase activity in vitro. Dev Comp Immunol 38: 88-97.
13. Nam HJ, Jang IH, You H, Lee KA, Lee WJ, (2012) Genetic evidence of a redox- dependent systemic wound response via Hayan protease-phenoloxidase system in Drosophila. EMBO J 31: 1253-1265.
14. De Gregorio E, Han SJ, Lee WJ, Baek MJ, Osaki T, et al. (2002) An immune- responsive Serpin regulates the melanization cascade in Drosophila. Dev Cell 3: 581-592.
15. 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.
16. Castillejo-Lopez C, Hacker U, (2005) The serine protease Sp7 is expressed in blood cells and regulates the melanization reaction in Drosophila. Biochem Biophys Res Commun 338: 1075-1082.
17. Leclerc V, Pelte N, El Chamy L, Martinelli C, Ligoxygakis P,et al. (2005) Prophenoloxidase activation is not required for survival to microbial infections in Drosophila. EMBO Rep.
18. Tang H, Kambris Z, Lemaitre B, Hashimoto C (2006) Two proteases defining a melanization cascade in the immune system of drosophila. J Biol Chem.
19. Scherfer C, Tang H, Kambris Z, Lhocine N, Hashimoto C,et al. (2008) Drosophila Serpin-28D regulates hemolymph phenoloxidase activity and adult pigmentation. Dev Biol.
20. Tang H, Kambris Z, Lemaitre B, Hashimoto C, (2008) A serpin that regulates immune melanization in the respiratory system of Drosophila. Dev Cell 15: 617-626.
21. Ahmad ST, Sweeney ST, Lee JA, Sweeney NT, Gao FB, (2009) Genetic screen identifies serpin5 as a regulator of the toll pathway and CHMP2B toxicity associated with frontotemporal dementia. Proc Natl Acad Sci U S A 106: 12168-12173.
22. Yoshida H, Ochiai M, Ashida M, (1986) Beta-1,3-glucan receptor and peptidoglycan receptor are present as separate entities within insect prophenoloxidase activating system. Biochem Biophys Res Commun 141: 1177-1184.
23. Kim CH, Kim SJ, Kan H, Kwon HM, Roh KB, et al. (2008) A three-step proteolytic cascade mediates the activation of the peptidoglycan-induced toll pathway in an insect. J Biol Chem 283: 7599-7607.
24. Bidla G, Hauling T, Dushay MS, Theopold U, (2009) Activation of insect phenoloxidase after injury: endogenous versus foreign elicitors. J Innate Immun 1: 301-308.
25. 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.
26. Ayres JS, Schneider DS, (2008) A signaling protease required for melanization in Drosophila affects resistance and tolerance of infections. PLoS Biol 6: 2764-2773.
27. Rämet M, Lanot R, Zachary D, Manfruelli P, (2001) JNK Signaling Pathway Is Required for Efficient Wound Healing in Drosophila. Dev biol 241: 145-156.
28. Gajewski KM, Sorrentino RP, Lee JH, Zhang Q, Russell M, et al. (2007) Identification of a crystal cell-specific enhancer of the black cells prophenoloxidase gene in Drosophila. Genesis 45: 200-207.
29. Lebestky T, Chang T, Hartenstein V, Banerjee U, (2000) Specification of Drosophila hematopoietic lineage by conserved transcription factors. Science 288: 146-149.
30. Eslin P, Doury G, (2006) The fly Drosophila subobscura: A natural case of innate immunity deficiency. Dev Comp Immunol 30: 977-983.
31. Rizki RM, Rizki TM, (1990) Encapsulation of Parasitoid Eggs in Phenoloxidase- Deficient Mutants of Drosophila-Melanogaster. Journal of Insect Physiology 36: 523-529.
32. Reichhart JM, (2005) Tip of another iceberg: Drosophila serpins. Trends Cell Biol 15: 659-665.
33. Markus R, Laurinyecz B, Kurucz E, Honti V, Bajusz I, et al. (2009) Sessile hemocytes as a hematopoietic compartment in Drosophila melanogaster. Proc Natl Acad Sci U S A 106: 4805-4809.
34. Makhijani K, Alexander B, Tanaka T, Rulifson E, Bruckner K, (2011) The peripheral nervous system supports blood cell homing and survival in the Drosophila larva. Development 138: 5379-5391.
35. Lemaitre B, Hoffmann JA, (2007) The host defense of Drosophila melanogaster. Annu Rev Immunol 25: 697-743.
36. Lemaitre B, Kromer-Metzger E, Michaut L, Nicolas E, Meister M, et al. (1995) A recessive mutation, immune deficiency (imd), defines two distinct control pathways in the Drosophila host defense. Proc Natl Acad Sci USA 92: 9365-9469.
37. 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.
38. Buchon N, Poidevin M, Kwon HM, Guillou A, Sottas V, et al. (2009) A single modular serine protease integrates signals from pattern-recognition receptors upstream of the Drosophila Toll pathway. Proc Natl Acad Sci U S A 106: 12442-12447.
39. Lemaitre B, Reichhart J, Hoffmann J, (1997) Drosophila host defense: differential induction of antimicrobial peptide genes after infection by various classes of microorganisms. Proc Natl Acad Sci USA 94: 14614-14619.
40. Arakane Y, Muthukrishnan S, Beeman RW, Kanost MR, Kramer KJ, (2005) Laccase 2 is the phenoloxidase gene required for beetle cuticle tanning. Proc Natl Acad Sci U S A 102: 11337-11342.
41. Schneider DS, Ayres JS, (2008) Two ways to survive infection: what resistance and tolerance can teach us about treating infectious diseases. Nat Rev Immunol 8: 889-895.
42. Zhao PC, Li JJ, Wang Y, Jiang HB, (2007) Broad-spectrum antimicrobial activity of the reactive compounds generated in vitro by Manduca sexta phenoloxidase. Insect Biochemistry and Molecular Biology 37: 952-959.
43. Kan H, Kim CH, Kwon HM, Park JW, Roh KB, et al. (2008) Molecular control of phenoloxidase-induced melanin synthesis in an insect. J Biol Chem 283: 25316-25323.
44. 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.
45. 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.
46. Garg A, Wu LP (2013) Drosophila Rab14 mediates phagocytosis in the immune response to Staphylococcus aureus. Cell Microbiol.
47. Shiratsuchi A, Mori T, Sakurai K, Nagaosa K, Sekimizu K, et al. (2012) Independent recognition of Staphylococcus aureus by two receptors for phagocytosis in Drosophila. J Biol Chem 287: 21663-21672.
48. Yassine H, Kamareddine L, Osta MA, (2012) The mosquito melanization response is implicated in defense against the entomopathogenic fungus Beauveria bassiana. PLoS Pathog 8: e1003029.
49. Waterhouse RM, Kriventseva EV, Meister S, Xi Z, Alvarez KS, et al. (2007) Evolutionary dynamics of immune-related genes and pathways in disease- vector mosquitoes. Science 316: 1738-1743.
50. De Gregorio E, Spellman PT, Rubin GM, Lemaitre B, (2001) Genome-wide analysis of the Drosophila immune response by using oligonucleotide microarrays. Proc Natl Acad Sci U S A 98: 12590-12595.
51. Kondo S, Ueda R, (2013) Highly improved gene targeting by germline-specific cas9 expression in Drosophila. Genetics 195: 715-721.
52. Baena-Lopez LA, Alexandre C, Mitchell A, Pasakarnis L, Vincent JP (2013) Accelerated homologous recombination and subsequent genome modification in Drosophila. Development.
53. Hedengren M, Asling B, Dushay MS, Ando I, Ekengren S, et al. (1999) Relish, a central factor in the control of humoral but not cellular immunity in Drosophila. Mol Cell 4: 827-837.
54. Gaumer S, Guenal I, Brun S, Theodore L, Mignotte B, (2000) Bcl-2 and Bax mammalian regulators of apoptosis are functional in Drosophila. Cell Death Differ 7: 804-814.
55. Gong WJ, Golic KG, (2004) Genomic deletions of the Drosophila melanogaster Hsp70 genes. Genetics 168: 1467-1476.
56. Paredes JC, Welchman DP, Poidevin M, Lemaitre B, (2011) Negative Regulation by Amidase PGRPs Shapes the Drosophila Antibacterial Response and Protects the Fly from Innocuous Infection. Immunity 35: 770-779.
57. Gaspar F, Teixeira N, Rigottier-Gois L, Marujo P, Nielsen-LeRoux C, et al. (2009) Virulence of Enterococcus faecalis dairy strains in an insect model: the role of fsrB and gelE. Microbiology 155: 3564-3571.
58. Romeo Y, Lemaitre B, (2008) Drosophila immunity: methods for monitoring the activity of toll and imd signaling pathways. Methods Mol Biol 415: 379-394.