Identification of Drosophila Gene Products Required for Phagocytosis of Leishmania donovani

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Peltan, Adam ^a   Briggs, Laura ^a   Matthews, Gareth ^a   Sweeney, Sean T ^a   Smith, Deborah F ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; RAB PROTEIN; THERMOZYMOCIDIN;

AMASTIGOTE; ANIMAL CELL; ARTICLE; CELL COMPARTMENTALIZATION; CELL DIVISION; CELL PHAGOCYTOSIS; CONTROLLED STUDY; DROSOPHILA; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; GENE PRODUCT; GENETIC CONSERVATION; GENOME ANALYSIS; HOST PARASITE INTERACTION; LACE GENE; LEISHMANIA DONOVANI; MACROPHAGE FUNCTION; MAMMAL CELL; NONHUMAN; PHAGOLYSOSOME; RAB5 GENE; RNA INTERFERENCE; SCAR GENE; SPT2 GENE; SRA1 GENE; YKT6 GENE;

ANIMALS; CELL LINE; CYTOCHALASIN D; DROSOPHILA; LEISHMANIA DONOVANI; LIFE CYCLE STAGES; MACROPHAGES; MICE; PHAGOCYTOSIS; RNA INTERFERENCE; TUBULIN MODULATORS;

LEISHMANIA DONOVANI; MAMMALIA; METAZOA; PROTOZOA;

EID: 84871301532     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0051831     Document Type: Article

References (70)

1. Chappuis F, Sundar S, Hailu A, Ghalib H, Rijal S, et al. (2007) Visceral leishmaniasis: what are the needs for diagnosis, treatment and control? Nat Rev Micro.
2. Guerin PJ, Olliaro P, Sundar S, Boelaert M, Croft SL, et al. (2002) Visceral leishmaniasis: current status of control, diagnosis, and treatment, and a proposed research and development agenda. Lancet Infect Dis 2: 494-501.
3. Collin S, Davidson R, Ritmeijer K, Keus K, Melaku Y, et al. (2004) Conflict and kala-azar: determinants of adverse outcomes of kala-azar among patients in southern Sudan. Clin Infect Dis 38: 612-619.
4. Herwaldt BL, (1999) Leishmaniasis. Lancet 354: 1191-1199.
5. Ashford RW, Desjeux P, Deraadt P, (1992) Estimation of population at risk of infection and number of cases of Leishmaniasis. Parasitol Today 8: 104-105.
6. Courret N, Frehel C, Gouhier N, Pouchelet M, Prina E, et al. (2002) Biogenesis of Leishmania-harbouring parasitophorous vacuoles following phagocytosis of the metacyclic promastigote or amastigote stages of the parasites. J Cell Sci 115: 2303-2316.
7. Prina E, Abdi SZ, Lebastard M, Perret E, Winter N, et al. (2004) Dendritic cells as host cells for the promastigote and amastigote stages of Leishmania amazonensis: the role of opsonins in parasite uptake and dendritic cell maturation. J Cell Sci 117: 315-325.
8. Peters NC, Egen JG, Secundino N, Debrabant A, Kimblin N, et al. (2008) In Vivo Imaging Reveals an Essential Role for Neutrophils in Leishmaniasis Transmitted by Sand Flies. Science 321: 970-974.
9. Rittig MG, Bogdan C, (2000) Leishmania-Host-cell Interaction: Complexities and Alternative Views. Parasitology Today 16: 292-297.
10. Love DC, Mentink Kane M, Mosser DM, (1998) Leishmania amazonensis: the phagocytosis of amastigotes by macrophages. Exp Parasitol 88: 161-171.
11. Channon JY, Roberts MB, Blackwell JM, (1984) A study of the differential respiratory burst activity elicited by promastigotes and amastigotes of Leishmania donovani in murine resident peritoneal macrophages. Immunology 53: 345-355.
12. Guy RA, Belosevic M, (1993) Comparison of receptors required for entry of Leishmania major amastigotes into macrophages. Infect Immun 61: 1553-1558.
13. Lodge R, Descoteaux A, (2006) Phagocytosis of Leishmania donovani amastigotes is Rac1 dependent and occurs in the absence of NADPH oxidase activation. Eur J Immunol 36: 2735-2744.
14. Morehead J, Coppens I, Andrews NW, (2002) Opsonization modulates Rac-1 activation during cell entry by Leishmania amazonensis. Infect Immun 70: 4571-4580.
15. Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, et al. (2000) The genome sequence of Drosophila melanogaster. Science 287: 2185-2195.
16. Nagy A, Perrimon N, Sandmeyer S, Plasterk R, (2003) Tailoring the genome: the power of genetic approaches. Nat Genet 33Suppl: 276-284.
17. Foley E, O'Farrell PH, (2004) Functional dissection of an innate immune response by a genome-wide RNAi screen. PLoS Biol 2: E203.
18. Meister M, (2004) Blood cells of Drosophila: cell lineages and role in host defence. Curr Opin Immunol 16: 10-15.
19. Pearson AM, Baksa K, Ramet M, Protas M, McKee M, et al. (2003) Identification of cytoskeletal regulatory proteins required for efficient phagocytosis in Drosophila. Microbes Infect 5: 815-824.
20. Manaka J, Kuraishi T, Shiratsuchi A, Nakai Y, Higashida H, et al. (2004) Draper-mediated and phosphatidylserine-independent phagocytosis of apoptotic cells by Drosophila hemocytes/macrophages. J Biol Chem 279: 48466-48476.
21. Wu HH, Bellmunt E, Scheib JL, Venegas V, Burkert C, et al. (2009) Glial precursors clear sensory neuron corpses during development via Jedi-1, an engulfment receptor. Nat Neurosci 12: 1534-1541.
22. Schneider I, (1972) Cell lines derived from late embryonic stages of Drosophila melanogaster. J Embryol Exp Morphol 27: 353-365.
23. Lavine MD, Strand MR, (2002) Insect hemocytes and their role in immunity. Insect Biochem Mol Biol 32: 1295-1309.
24. Saleh MC, van Rij RP, Hekele A, Gillis A, Foley E, et al. (2006) The endocytic pathway mediates cell entry of dsRNA to induce RNAi silencing. Nat Cell Biol 8: 793-802.
25. Clemens JC, Worby CA, Simonson-Leff N, Muda M, Maehama T, et al. (2000) Use of double-stranded RNA interference in Drosophila cell lines to dissect signal transduction pathways. Proc Natl Acad Sci U S A 97: 6499-6503.
26. Kiger AA, Baum B, Jones S, Jones MR, Coulson A, et al. (2003) A functional genomic analysis of cell morphology using RNA interference. J Biol 2: 27.
27. Bard F, Casano L, Mallabiabarrena A, Wallace E, Saito K, et al. (2006) Functional genomics reveals genes involved in protein secretion and Golgi organization. Nature 439: 604-607.
28. Baeg GH, Zhou R, Perrimon N, (2005) Genome-wide RNAi analysis of JAK/STAT signaling components in Drosophila. Genes Dev 19: 1861-1870.
29. Philips JA, Rubin EJ, Perrimon N, (2005) Drosophila RNAi screen reveals CD36 family member required for mycobacterial infection. Science 309: 1251-1253.
30. Cheng LW, Viala JP, Stuurman N, Wiedemann U, Vale RD, et al. (2005) Use of RNA interference in Drosophila S2 cells to identify host pathways controlling compartmentalization of an intracellular pathogen. Proc Natl Acad Sci U S A 102: 13646-13651.
31. Agaisse H, Burrack LS, Philips JA, Rubin EJ, Perrimon N, et al. (2005) Genome-wide RNAi screen for host factors required for intracellular bacterial infection. Science 309: 1248-1251.
32. Derre I, Pypaert M, Dautry-Varsat A, Agaisse H, (2007) RNAi Screen in Drosophila Cells Reveals the Involvement of the Tom Complex in Chlamydia Infection. PLoS Pathog 3: e155.
33. Elwell C, Engel JN, (2005) Drosophila melanogaster S2 cells: a model system to study Chlamydia interaction with host cells. Cell Microbiol 7: 725-739.
34. Stroschein-Stevenson SL, Foley E, O'Farrell PH, Johnson AD, (2006) Identification of Drosophila gene products required for phagocytosis of Candida albicans. PLoS Biol 4: e4.
35. Hofmann I, Munro S, (2006) An N-terminally acetylated Arf-like GTPase is localised to lysosomes and affects their motility. J Cell Sci 119: 1494-1503.
36. Lang T, Hellio R, Kaye PM, Antoine JC, (1994) Leishmania donovani-infected macrophages: characterization of the parasitophorous vacuole and potential role of this organelle in antigen presentation. J Cell Sci 107 (Pt 8): 2137-2150.
37. Phillips R, Svensson M, Aziz N, Maroof A, Brown N, et al. (2010) Innate Killing of Leishmania donovani by Macrophages of the Splenic Marginal Zone Requires IRF-7. PLoS Pathog 6: e1000813.
38. Vasquez RJ, Howell B, Yvon AM, Wadsworth P, Cassimeris L, (1997) Nanomolar concentrations of nocodazole alter microtubule dynamic instability in vivo and in vitro. Mol Biol Cell 8: 973-985.
39. Randazzo PA, Yang YC, Rulka C, Kahn RA, (1993) Activation of ADP-ribosylation factor by Golgi membranes. Evidence for a brefeldin A- and protease-sensitive activating factor on Golgi membranes. Journal of Biological Chemistry 268: 9555-9563.
40. Donaldson JG, Finazzi D, Klausner RD, (1992) Brefeldin A inhibits Golgi membrane-catalysed exchange of guanine nucleotide onto ARF protein. Nature 360: 350-352.
41. Helms JB, Rothman JE, (1992) Inhibition by brefeldin A of a Golgi membrane enzyme that catalyses exchange of guanine nucleotide bound to ARF. Nature 360: 352-354.
42. Qin Q-M, Pei J, Ancona V, Shaw BD, Ficht TA, et al. (2008) RNAi Screen of Endoplasmic Reticulum Associated Host Factors Reveals a Role for IRE1α in Supporting Brucella Replication. PLoS Pathog 4: e1000110.
43. Chen L-M, Hobbie S, Galan JE, (1996) Requirement of CDC42 for Salmonella-Induced Cytoskeletal and Nuclear Responses. Science 274: 2115-2118.
44. Carpenter AE, Jones TR, Lamprecht MR, Clarke C, Kang IH, et al. (2006) CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol 7: R100.
45. Boutros M, Kiger AA, Armknecht S, Kerr K, Hild M, et al. (2004) Genome-wide RNAi analysis of growth and viability in Drosophila cells. Science 303: 832-835.
46. Kulkarni MM, Booker M, Silver SJ, Friedman A, Hong P, et al. (2006) Evidence of off-target effects associated with long dsRNAs in Drosophila melanogaster cell-based assays. Nat Methods 3: 833-838.
47. Ma Y, Creanga A, Lum L, Beachy PA, (2006) Prevalence of off-target effects in Drosophila RNA interference screens. Nature 443: 359-363.
48. Flockhart I, Booker M, Kiger A, Boutros M, Armknecht S, et al. (2006) FlyRNAi: the Drosophila RNAi screening center database. Nucleic Acids Res 34: D489-494.
49. Echeverri CJ, Beachy PA, Baum B, Boutros M, Buchholz F, et al. (2006) Minimizing the risk of reporting false positives in large-scale RNAi screens. Nat Methods 3: 777-779.
50. Elwell CA, Ceesay A, Kim JH, Kalman D, Engel JN, (2008) RNA Interference Screen Identifies Abl Kinase and PDGFR Signaling in Chlamydia trachomatis Entry. PLoS Pathog 4: e1000021.
51. Hanada K, (2003) Serine palmitoyltransferase, a key enzyme of sphingolipid metabolism. Biochim Biophys Acta 1632: 16-30.
52. Meiringer CT, Auffarth K, Hou H, Ungermann C, (2008) Depalmitoylation of Ykt6 prevents its entry into the multivesicular body pathway. Traffic 9: 1510-1521.
53. Ungermann C, von Mollard GF, Jensen ON, Margolis N, Stevens TH, et al. (1999) Three v-SNAREs and Two t-SNAREs, Present in a Pentameric cis-SNARE Complex on Isolated Vacuoles, Are Essential for Homotypic Fusion. The Journal of Cell Biology 145: 1435-1442.
54. McNew JA, SÃ̧gaard M, Lampen NM, Machida S, Ye RR, et al. (1997) Ykt6p, a Prenylated SNARE Essential for Endoplasmic Reticulum-Golgi Transport. Journal of Biological Chemistry 272: 17776-17783.
55. Isgandarova S, Jones L, Forsberg D, Loncar A, Dawson J, et al. (2007) Stimulation of actin polymerization by vacuoles via Cdc42p-dependent signaling. J Biol Chem 282: 30466-30475.
56. 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.
57. Duclos S, Diez R, Garin J, Papadopoulou B, Descoteaux A, et al. (2000) Rab5 regulates the kiss and run fusion between phagosomes and endosomes and the acquisition of phagosome leishmanicidal properties in RAW 264.7 macrophages. J Cell Sci 113 Pt 19: 3531-3541.
58. Maganto-Garcia E, Punzon C, Terhorst C, Fresno M, (2008) Rab5 Activation by Toll-Like Receptor 2 is Required for Trypanosoma cruzi Internalization and Replication in Macrophages. Traffic 9: 1299-1315.
59. Schenck A, Bardoni B, Langmann C, Harden N, Mandel JL, et al. (2003) CYFIP/Sra-1 controls neuronal connectivity in Drosophila and links the Rac1 GTPase pathway to the fragile X protein. Neuron 38: 887-898.
60. Kobayashi K, Kuroda S, Fukata M, Nakamura T, Nagase T, et al. (1998) p140Sra-1 (specifically Rac1-associated protein) is a novel specific target for Rac1 small GTPase. J Biol Chem 273: 291-295.
61. Niedergang F, Chavrier P, (2005) Regulation of phagocytosis by Rho GTPases. Curr Top Microbiol Immunol 291: 43-60.
62. May RC, Caron E, Hall A, Machesky LM, (2000) Involvement of the Arp2/3 complex in phagocytosis mediated by FcγR or CR3. Nat Cell Biol 2: 246-248.
63. Rogers SL, Wiedemann U, Stuurman N, Vale RD, (2003) Molecular requirements for actin-based lamella formation in Drosophila S2 cells. The Journal of Cell Biology 162: 1079-1088.
64. Kunda P, Craig G, Dominguez V, Baum B, (2003) Abi, Sra1, and Kette Control the Stability and Localization of SCAR/WAVE to Regulate the Formation of Actin-Based Protrusions. 13: 1867.
65. Yeung T, Grinstein S, (2007) Lipid signaling and the modulation of surface charge during phagocytosis. Immunological Reviews 219: 17-36.
66. Kwiatkowska K, Frey J, Sobota A, (2003) Phosphorylation of FcγRIIA is required for the receptor-induced actin rearrangement and capping: the role of membrane rafts. J Cell Sci 116: 537-550.
67. Siqueira-Neto JL, Song O-R, Oh H, Sohn J-H, Yang G, et al. (2010) Antileishmanial High-Throughput Drug Screening Reveals Drug Candidates with New Scaffolds. PLoS Negl Trop Dis 4: e675.
68. St-Denis A, Caouras V, Gervais F, Descoteaux A, (1999) Role of protein kinase Cα in the control of infection by intracellular pathogens in macrophages. J Immunol 163: 5505-5511.
69. Mombaerts P, Clarke AR, Rudnicki MA, Iacomini J, Itohara S, et al. (1992) Mutations in T-cell antigen receptor genes alpha and beta block thymocyte development at different stages. Nature 360: 225-231.
70. He B, Rong M, Lyakhov D, Gartenstein H, Diaz G, et al. (1997) Rapid mutagenesis and purification of phage RNA polymerases. Protein Expr Purif 9: 142-151.