A quantitative RNAi Screen for JNK Modifiers Identifies Pvr as a Novel Regulator of DrosophilaImmune Signaling

PLoS Pathogens

Volumn 5, Issue 11, 2009, Pages

  Bond, David ^a   Foley, Edan ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME INHIBITOR; GENE PRODUCT; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN TYROSINE KINASE; PVR; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; PVF2 PROTEIN, DROSOPHILA; PVR PROTEIN, DROSOPHILA; VASCULOTROPIN;

ARTICLE; CYTOLOGY; DROSOPHILA MELANOGASTER; ENZYME ACTIVATION; EUKARYOTIC CELL; GENE NUMBER; IMMUNE RESPONSE; INNATE IMMUNITY; NONHUMAN; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; RNA INTERFERENCE; SCREENING; SIGNAL TRANSDUCTION; ANIMAL; CELL CULTURE; DRUG ANTAGONISM; GENOME; IMMUNOLOGY; METABOLISM; PHYSIOLOGY;

BACTERIA (MICROORGANISMS); DROSOPHILA MELANOGASTER; EUKARYOTA; NEGIBACTERIA;

ANIMALS; CELLS, CULTURED; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENOME, INSECT; IMMUNITY, INNATE; JNK MITOGEN-ACTIVATED PROTEIN KINASES; NF-KAPPA B; RECEPTOR PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTORS;

EID: 73549097550     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000655     Document Type: Article

References (55)

1. Beutler B (2004) Innate immunity: an overview. Mol Immunol 40: 845-859.
2. Lemaitre B, Hoffmann J (2007) The host defense of Drosophila melanogaster. Annu Rev Immunol 25: 697-743.
3. Lemaitre B, Meister M, Govind S, Georgel P, Steward R, et al. (1995) Functional analysis and regulation of nuclear import of dorsal during the immune response in Drosophila. Embo J 14: 536-545.
4. Medzhitov R, Preston-Hurlburt P, Janeway CA, Jr. (1997) A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388: 394-397.
5. 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 U S A 92: 9465-9469.
6. Georgel P, Naitza S, Kappler C, Ferrandon D, Zachary D, et al. (2001) Drosophila immune deficiency (IMD) is a death domain protein that activates antibacterial defense and can promote apoptosis. Dev Cell 1: 503-514.
7. Choe KM, Werner T, Stoven S, Hultmark D, Anderson KV (2002) Requirement for a peptidoglycan recognition protein (PGRP) in Relish activation and antibacterial immune responses in Drosophila. Science 296: 359-362.
8. Gottar M, Gobert V, Michel T, Belvin M, Duyk G, et al. (2002) The Drosophila immune response against Gram-negative bacteria is mediated by a peptidoglycan recognition protein. Nature 416: 640-644.
9. Kaneko T, Goldman WE, Mellroth P, Steiner H, Fukase K, et al. (2004) Monomeric and polymeric gram-negative peptidoglycan but not purified LPS stimulate the Drosophila IMD pathway. Immunity 20: 637-649.
10. Leulier F, Parquet C, Pili-Floury S, Ryu JH, Caroff M, et al. (2003) The Drosophila immune system detects bacteria through specific peptidoglycan recognition. Nat Immunol 4: 478-484.
11. 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.
12. Gesellchen V, Kuttenkeuler D, Steckel M, Pelte N, Boutros M (2005) An RNA interference screen identifies Inhibitor of Apoptosis Protein 2 as a regulator of innate immune signalling in Drosophila. EMBO Rep 6: 979-984.
13. Hu S, Yang X (2000) dFADD, a novel death domain-containing adapter protein for the Drosophila caspase DREDD. J Biol Chem 275: 30761-30764.
14. Kleino A, Valanne S, Ulvila J, Kallio J, Myllymaki H, et al. (2005) Inhibitor of apoptosis 2 and TAK1-binding protein are components of the Drosophila Imd pathway. EMBO J 24: 3423-3434.
15. Leulier F, Rodriguez A, Khush RS, Abrams JM, Lemaitre B (2000) The Drosophila caspase Dredd is required to resist gram-negative bacterial infection. EMBO Rep 1: 353-358.
16. Leulier F, Vidal S, Saigo K, Ueda R, Lemaitre B (2002) Inducible expression of double-stranded RNA reveals a role for dFADD in the regulation of the antibacterial response in Drosophila adults. Curr Biol 12: 996-1000.
17. Naitza S, Rosse C, Kappler C, Georgel P, Belvin M, et al. (2002) The Drosophila immune defense against gram-negative infection requires the death protein dFADD. Immunity 17: 575-581.
18. Silverman N, Zhou R, Erlich RL, Hunter M, Bernstein E, et al. (2003) Immune activation of NF-kappaB and JNK requires Drosophila TAK1. J Biol Chem 278: 48928-48934.
19. Stoven S, Ando I, Kadalayil L, Engstrom Y, Hultmark D (2000) Activation of the Drosophila NF-kappaB factor Relish by rapid endoproteolytic cleavage. EMBO Rep 1: 347-352.
20. Stoven S, Silverman N, Junell A, Hedengren-Olcott M, Erturk D, et al. (2003) Caspase-mediated processing of the Drosophila NF-kappaB factor Relish. Proc Natl Acad Sci U S A 100: 5991-5996.
21. Vidal S, Khush RS, Leulier F, Tzou P, Nakamura M, et al. (2001) Mutations in the Drosophila dTAK1 gene reveal a conserved function for MAPKKKs in the control of rel/NF-kappaB-dependent innate immune responses. Genes Dev 15: 1900-1912.
22. Lu Y, Wu LP, Anderson KV (2001) The antibacterial arm of the drosophila innate immune response requires an IkappaB kinase. Genes Dev 15: 104-110.
23. Rutschmann S, Jung AC, Zhou R, Silverman N, Hoffmann JA, et al. (2000) Role of Drosophila IKK gamma in a toll-independent antibacterial immune response. Nat Immunol 1: 342-347.
24. Silverman N, Zhou R, Stoven S, Pandey N, Hultmark D, et al. (2000) A Drosophila IkappaB kinase complex required for Relish cleavage and antibacterial immunity. Genes Dev 14: 2461-2471.
25. Wu LP, Anderson KV (1998) Regulated nuclear import of Rel proteins in the Drosophila immune response. Nature 392: 93-97.
26. Dushay MS, Asling B, Hultmark D (1996) Origins of immunity: Relish, a compound Rel-like gene in the antibacterial defense of Drosophila. Proc Natl Acad Sci U S A 93: 10343-10347.
27. 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.
28. Erturk-Hasdemir D, Broemer M, Leulier F, Lane WS, Paquette N, et al. (2009) Two roles for the Drosophila IKK complex in the activation of Relish and the induction of antimicrobial peptide genes. Proc Natl Acad Sci U S A.
29. Boutros M, Agaisse H, Perrimon N (2002) Sequential Activation of Signaling Pathways during Innate Immune Responses in Drosophila. Dev Cell 3: 711-722.
30. Park JM, Brady H, Ruocco MG, Sun H, Williams D, et al. (2004) Targeting of TAK1 by the NF-kappa B protein Relish regulates the JNK-mediated immune response in Drosophila. Genes Dev 18: 584-594.
31. Kockel L, Homsy JG, Bohmann D (2001) Drosophila AP-1: lessons from an invertebrate. Oncogene 20: 2347-2364.
32. Martin-Blanco E (1998) Regulatory control of signal transduction during morphogenesis in Drosophila. Int J Dev Biol 42: 363-368.
33. Martin-Blanco E, Gampel A, Ring J, Virdee K, Kirov N, et al. (1998) puckered encodes a phosphatase that mediates a feedback loop regulating JNK activity during dorsal closure in Drosophila. Genes Dev 12: 557-570.
34. Riesgo-Escovar JR, Jenni M, Fritz A, Hafen E (1996) The Drosophila Jun-N-terminal kinase is required for cell morphogenesis but not for DJun-dependent cell fate specification in the eye. Genes Dev 10: 2759-2768.
35. Sluss HK, Han Z, Barrett T, Goberdhan DC, Wilson C, et al. (1996) A JNK signal transduction pathway that mediates morphogenesis and an immune response in Drosophila. Genes Dev 10: 2745-2758.
36. Bianco A, Poukkula M, Cliffe A, Mathieu J, Luque CM, et al. (2007) Two distinct modes of guidance signalling during collective migration of border cells. Nature 448: 362-365.
37. Cho NK, Keyes L, Johnson E, Heller J, Ryner L, et al. (2002) Developmental control of blood cell migration by the Drosophila VEGF pathway. Cell 108: 865-876.
38. Duchek P, Somogyi K, Jekely G, Beccari S, Rorth P (2001) Guidance of cell migration by the Drosophila PDGF/VEGF receptor. Cell 107: 17-26.
39. Ishimaru S, Ueda R, Hinohara Y, Ohtani M, Hanafusa H (2004) PVR plays a critical role via JNK activation in thorax closure during Drosophila metamorphosis. Embo J 23: 3984-3994.
40. Macias A, Romero NM, Martin F, Suarez L, Rosa AL, et al. (2004) PVF1/PVR signaling and apoptosis promotes the rotation and dorsal closure of the Drosophila male terminalia. Int J Dev Biol 48: 1087-1094.
41. McDonald JA, Pinheiro EM, Kadlec L, Schupbach T, Montell DJ (2006) Multiple EGFR ligands participate in guiding migrating border cells. Dev Biol 296: 94-103.
42. McDonald JA, Pinheiro EM, Montell DJ (2003) PVF1, a PDGF/VEGF homolog, is sufficient to guide border cells and interacts genetically with Taiman. Development 130: 3469-3478.
43. Zhou R, Silverman N, Hong M, Liao DS, Chung Y, et al. (2005) The role of ubiquitination in Drosophila innate immunity. J Biol Chem 280: 34048-34055.
44. Friedman A, Perrimon N (2006) A functional RNAi screen for regulators of receptor tyrosine kinase and ERK signalling. Nature 444: 230-234.
45. Dhanasekaran DN, Reddy EP (2008) JNK signaling in apoptosis. Oncogene 27: 6245-6251.
46. Huang C, Jacobson K, Schaller MD (2004) MAP kinases and cell migration. J Cell Sci 117: 4619-4628.
47. Varfolomeev EE, Ashkenazi A (2004) Tumor necrosis factor: an apoptosis JuNKie? Cell 116: 491-497.
48. Bakal C, Linding R, Llense F, Heffern E, Martin-Blanco E, et al. (2008) Phosphorylation networks regulating JNK activity in diverse genetic backgrounds. Science 322: 453-456.
49. Delaney JR, Stoven S, Uvell H, Anderson KV, Engstrom Y, et al. (2006) Cooperative control of Drosophila immune responses by the JNK and NFkappaB signaling pathways. EMBO J 25: 3068-3077.
50. Munier AI, Doucet D, Perrodou E, Zachary D, Meister M, et al. (2002) PVF2, a PDGF/VEGF-like growth factor, induces hemocyte proliferation in Drosophila larvae. EMBO Rep 3: 1195-1200.
51. Bruckner K, Kockel L, Duchek P, Luque CM, Rorth P, et al. (2004) The PDGF/VEGF receptor controls blood cell survival in Drosophila. Dev Cell 7: 73-84.
52. Sims D, Duchek P, Baum B (2009) PDGF/VEGF signaling controls cell size in Drosophila. Genome Biol 10: R20.
53. Foley E, O'Farrell PH (2004) Functional Dissection of an Innate Immune Response by a Genome-Wide RNAi Screen. PLoS Biol 2: e203. doi:10.1371/ journal.pbio.0020203.
54. Bond D, Primrose DA, Foley E (2008) Quantitative evaluation of signaling events in Drosophila s2 cells. Biol Proced Online 10: 20-28.
55. Yu J, Pacifico S, Liu G, Finley RL, Jr. (2008) DroID: the Drosophila Interactions Database, a comprehensive resource for annotated gene and protein interactions. BMC Genomics 9: 461.