An in vivo RNA interference screen identifies gene networks controlling Drosophila melanogaster blood cell homeostasis

BMC Developmental Biology

Volumn 10, Issue , 2010, Pages

  Avet Rochex, Amélie ^a,b,c   Boyer, Karène ^a,b   Polesello, Cédric ^a,b   Gobert, Vanessa ^a,b   Osman, Dani ^a,b   Roch, Fernando ^a,b   Augé, Benoit ^a,b   Zanet, Jennifer ^a,b,c   Haenlin, Marc ^a,b   Waltzer, Lucas ^a,b  

^a UNIVERSITÉ PAUL SABATIER   (France)

^b CNRS   (France)

^c KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DROSOPHILA MELANOGASTER; METAZOA;

ANIMAL; ARTICLE; BLOOD CELL; CYTOLOGY; DROSOPHILA MELANOGASTER; GENE REGULATORY NETWORK; GENETICS; HEMATOPOIESIS; HOMEOSTASIS; IMMUNOLOGY; METABOLISM; RNA INTERFERENCE; TUMOR SUPPRESSOR GENE;

ANIMALS; DROSOPHILA MELANOGASTER; GENE REGULATORY NETWORKS; GENES, TUMOR SUPPRESSOR; HEMATOPOIESIS; HEMOCYTES; HOMEOSTASIS; RNA INTERFERENCE;

EID: 77953316126     PISSN: None     EISSN: 1471213X     Source Type: Journal    
DOI: 10.1186/1471-213X-10-65     Document Type: Article

References (76)

1. Blood cells and blood cell development in the animal kingdom. V Hartenstein, Annu Rev Cell Dev Biol 2006 22 677 712 10.1146/annurev.cellbio.22. 010605.093317 16824014
2. Biology of hematopoietic stem cells and progenitors: implications for clinical application. M Kondo AJ Wagers MG Manz SS Prohaska DC Scherer GF Beilhack JA Shizuru IL Weissman, Annu Rev Immunol 2003 21 759 806 10.1146/annurev.immunol.21.120601.141007 12615892
3. Drosophila haematopoiesis. M Crozatier M Meister, Cell Microbiol 2007 9 1117 1126 10.1111/j.1462-5822.2007.00930.x 17394559
4. Embryonic origin of hemocytes and their relationship to cell death in Drosophila. U Tepass LI Fessler A Aziz V Hartenstein, Development 1994 120 1829 1837 7924990
5. Postembryonic hematopoiesis in Drosophila. R Lanot D Zachary F Holder M Meister, Dev Biol 2001 230 243 257 10.1006/dbio.2000.0123 11161576
6. The two origins of hemocytes in Drosophila. A Holz B Bossinger T Strasser W Janning R Klapper, Development 2003 130 4955 4962 10.1242/dev.00702 12930778
7. The Drosophila lymph gland as a developmental model of hematopoiesis. SH Jung CJ Evans C Uemura U Banerjee, Development 2005 132 2521 2533 10.1242/dev.01837 15857916
8. Control of blood cell homeostasis in Drosophila larvae by the posterior signalling centre. J Krzemien L Dubois R Makki M Meister A Vincent M Crozatier, Nature 2007 446 325 328 10.1038/nature05650 17361184
9. A Hedgehog-and Antennapedia-dependent niche maintains Drosophila haematopoietic precursors. L Mandal JA Martinez-Agosto CJ Evans V Hartenstein U Banerjee, Nature 2007 446 320 324 10.1038/nature05585 17361183
10. Requirement for croquemort in phagocytosis of apoptotic cells in Drosophila. NC Franc P Heitzler RA Ezekowitz K White, Science 1999 284 1991 1994 10.1126/science.284.5422.1991 10373118
11. Macrophage-mediated corpse engulfment is required for normal Drosophila CNS morphogenesis. HC Sears CJ Kennedy PA Garrity, Development 2003 130 3557 3565 10.1242/dev.00586 12810602
12. Psidin is required in Drosophila blood cells for both phagocytic degradation and immune activation of the fat body. CA Brennan JR Delaney DS Schneider KV Anderson, Curr Biol 2007 17 67 72 10.1016/j.cub.2006.11.026 17208189
13. TM9SF4 is required for Drosophila cellular immunity via cell adhesion and phagocytosis. E Bergeret J Perrin M Williams D Grunwald E Engel D Thevenon E Taillebourg F Bruckert P Cosson MO Fauvarque, Journal of Cell Science 2008 121 3325 3334 10.1242/jcs.030163 18796536
14. Properties of the larval hemocytes of Drosophila melanogaster. TM Rizki RM Rizki, Experientia 1980 36 1223 1226 10.1007/BF01976142 (Pubitemid 11166754)
15. Hemolymph coagulation and phenoloxidase in Drosophila larvae. G Bidla M Lindgren U Theopold MS Dushay, Dev Comp Immunol 2005 29 669 679 10.1016/j.dci.2004.11.007 15854679
16. The prophenoloxidase-activating system in invertebrates. L Cerenius K Soderhall, Immunol Rev 2004 198 116 126 10.1111/j.0105-2896.2004.00116.x 15199959
17. The cellular defense system of Drosophila melanogaster. TM Rizki RM Rizki, Insect ultrastructure New York: Plenum, King RC, Akai H, Plenum 1984 2 579 604 [King RC, Akai H (Series Editor)]
18. Cellular immune response to parasite infection in the Drosophila lymph gland is developmentally regulated. RP Sorrentino Y Carton S Govind, Dev Biol 2002 243 65 80 10.1006/dbio.2001.0542 11846478
19. Ultrastructure and cytochemistry of the cell types in the larval hematopoietic organs and hemolymph of Drosophila melanogaster. R Shrestha E Gateff, Dev Growth Differ 1982 24 65 82 10.1111/j.1440-169X.1982.00065.x
20. Alterations in the haemocyte population of Drosophila melanogaster. TM Rizki, J Morphol 1957 100 437 458 10.1002/jmor.1051000303
21. Experimental analysis of hemocyte morphology in insects. TM Rizki, Am Zool 1962 2 247 256
22. Cellular immune response to parasitization in Drosophila requires the EBF orthologue collier. M Crozatier JM Ubeda A Vincent M Meister, PLoS Biol 2004 2 196 10.1371/journal.pbio.0020196 15314643
23. Genetic analysis of contributions of dorsal group and JAK-Stat92E pathway genes to larval hemocyte concentration and the egg encapsulation response in Drosophila. RP Sorrentino JP Melk S Govind, Genetics 2004 166 1343 1356 10.1534/genetics.166.3.1343 15082553
24. Sessile hemocytes as a hematopoietic compartment in Drosophila melanogaster. R Markus B Laurinyecz E Kurucz V Honti I Bajusz B Sipos K Somogyi J Kronhamn D Hultmark I Ando, Proc Natl Acad Sci USA 2009 106 4805 4809 10.1073/pnas.0801766106 19261847
25. Fruit fly "leukemia". CR Dearolf, Biochim Biophys Acta 1998 1377 13 23 9540809
26. Melanotic mutants in Drosophila: pathways and phenotypes. S Minakhina R Steward, Genetics 2006 174 253 263 10.1534/genetics.106.061978 16816412
27. Lethal(1) aberrant immune response mutations leading to melanotic tumor formation in Drosophila melanogaster. KL Watson TK Johnson RE Denell, Dev Genet 1991 12 173 187 10.1002/dvg.1020120302 1907895
28. kurtz, a novel nonvisual arrestin, is an essential neural gene in Drosophila. G Roman J He RL Davis, Genetics 2000 155 1281 1295 10880488
29. The Drosophila Tumorous-lethal hematopoietic oncogene is a dominant mutation in the hopscotch locus. WP Hanratty CR Dearolf, Mol Gen Genet 1993 238 33 37 8479437
30. An amino acid substitution in the Drosophila hopTum-l Jak kinase causes leukemia-like hematopoietic defects. H Luo WP Hanratty CR Dearolf, Embo J 1995 14 1412 1420 7729418
31. Activation of a Drosophila Janus kinase (JAK) causes hematopoietic neoplasia and developmental defects. DA Harrison R Binari TS Nahreini M Gilman N Perrimon, Embo J 1995 14 2857 2865 7796812
32. cactus, a maternal gene required for proper formation of the dorsoventral morphogen gradient in Drosophila embryos. S Roth Y Hiromi D Godt C Nusslein-Volhard, Development 1991 112 371 388 1794309
33. Zygotic expression and activity of the Drosophila Toll gene, a gene required maternally for embryonic dorsal-ventral pattern formation. S Gerttula YS Jin KV Anderson, Genetics 1988 119 123 133 2456252
34. Functional analysis and regulation of nuclear import of dorsal during the immune response in Drosophila. B Lemaitre M Meister S Govind P Georgel R Steward JM Reichhart JA Hoffmann, Embo J 1995 14 536 545 7859742
35. Resolving embryonic blood cell fate choice in Drosophila: interplay of GCM and RUNX factors. L Bataille B Auge G Ferjoux M Haenlin L Waltzer, Development 2005 132 4635 4644 10.1242/dev.02034 16176949
36. Analysis of Ras-induced overproliferation in Drosophila hemocytes. H Asha I Nagy G Kovacs D Stetson I Ando CR Dearolf, Genetics 2003 163 203 215 12586708
37. Increased expression of Drosophila tetraspanin, Tsp68C, suppresses the abnormal proliferation of ytr-deficient and Ras/Raf-activated hemocytes. SA Sinenko B Mathey-Prevot, Oncogene 2004 23 9120 9128 10.1038/sj.onc.1208156 15480416
38. Elimination of plasmatocytes by targeted apoptosis reveals their role in multiple aspects of the Drosophila immune response. B Charroux J Royet, Proc Natl Acad Sci USA 2009 106 9797 9802 10.1073/pnas.0903971106 19482944
39. Reactive oxygen species prime Drosophila haematopoietic progenitors for differentiation. E Owusu-Ansah U Banerjee, Nature 2009 461 537 541 10.1038/nature08313 19727075
40. A role for the Drosophila Toll/Cactus pathway in larval hematopoiesis. P Qiu PC Pan S Govind, Development 1998 125 1909 1920 9550723
41. The Friend of GATA protein U-shaped functions as a hematopoietic tumor suppressor in Drosophila. RP Sorrentino T Tokusumi RA Schulz, Dev Biol 2007 311 311 323 17936744
42. DREF is required for EGFR signalling during Drosophila wing vein development. H Yoshida E Kwon F Hirose K Otsuki M Yamada M Yamaguchi, Genes Cells 2004 9 935 944 10.1111/j.1365-2443.2004.00775.x 15461664
43. Evidence of off-target effects associated with long dsRNAs in Drosophila melanogaster cell-based assays. MM Kulkarni M Booker SJ Silver A Friedman P Hong N Perrimon B Mathey-Prevot, Nat Methods 2006 3 833 838 16964256
44. Drosophila homolog of the human S6 ribosomal protein is required for tumor suppression in the hematopoietic system. KL Watson KD Konrad DF Woods PJ Bryant, Proc Natl Acad Sci USA 1992 89 11302 11306 10.1073/pnas.89.23.11302 1454811
45. The mitochondrial ribosome-specific MrpL55 protein is essential in Drosophila and dynamically required during development. TV Tselykh C Roos TI Heino, Exp Cell Res 2005 307 354 366 10.1016/j.yexcr.2005.03.037 15894314
46. COP9 signalosome subunit 5 (CSN5/Jab1) regulates the development of the Drosophila immune system: effects on Cactus, Dorsal and hematopoiesis. O Harari-Steinberg R Cantera S Denti E Bianchi E Oron D Segal DA Chamovitz, Genes Cells 2007 12 183 195 10.1111/j.1365-2443.2007.01049.x 17295838
47. Cop9 signalosome subunit 8 (CSN8) is essential for Drosophila development. P Oren-Giladi O Krieger BA Edgar DA Chamovitz D Segal, Genes Cells 2008 13 221 231 10.1111/j.1365-2443.2008.01164.x 18298797
48. Drosophila immunity: analysis of larval hemocytes by P-element-mediated enhancer trap. A Braun B Lemaitre R Lanot D Zachary M Meister, Genetics 1997 147 623 634 9335599
49. Transcriptional regulation of the Drosophila rfc1 gene by the DRE-DREF pathway. A Tsuchiya YH Inoue H Ida Y Kawase K Okudaira K Ohno H Yoshida M Yamaguchi, Febs J 2007 274 1818 1832 10.1111/j.1742-4658.2007.05730.x 17381512 (Pubitemid 46426917)
50. Drosophila damaged DNA-binding protein 1 is an essential factor for development. K Takata H Yoshida M Yamaguchi K Sakaguchi, Genetics 2004 168 855 865 10.1534/genetics.103.025965 15514059
51. Two families of chaperonin: physiology and mechanism. AL Horwich WA Fenton E Chapman GW Farr, Annu Rev Cell Dev Biol 2007 23 115 145 10.1146/annurev.cellbio.23.090506.123555 17489689
52. Lamellocyte differentiation in Drosophila larvae parasitized by Leptopilina. TM Rizki RM Rizki, Dev Comp Immunol 1992 16 103 110 10.1016/0145-305X(92)90011-Z 1499832
53. New insights into Drosophila larval haemocyte functions through genome-wide analysis. P Irving JM Ubeda D Doucet L Troxler M Lagueux D Zachary JA Hoffmann C Hetru M Meister, Cell Microbiol 2005 7 335 350 10.1111/j.1462-5822.2004.00462.x 15679837
54. Fascin is required for blood cell migration during Drosophila embryogenesis. J Zanet B Stramer T Millard P Martin F Payre S Plaza, Development 2009 136 2557 2565 10.1242/dev.036517 19592575
55. A misexpression screen to identify regulators of Drosophila larval hemocyte development. M Stofanko SY Kwon P Badenhorst, Genetics 2008 180 253 267 10.1534/genetics.108.089094 18757933
56. A directed screen for genes involved in Drosophila blood cell activation. CJ Zettervall I Anderl MJ Williams R Palmer E Kurucz I Ando D Hultmark, Proc Natl Acad Sci USA 2004 101 14192 14197 10.1073/pnas.0403789101 15381778
57. The lesswright mutation activates Rel-related proteins, leading to overproduction of larval hemocytes in Drosophila melanogaster. L Huang S Ohsako S Tanda, Dev Biol 2005 280 407 420 10.1016/j.ydbio.2005.02.006 15882582
58. Drosophila Vps35 function is necessary for normal endocytic trafficking and actin cytoskeleton organisation. VI Korolchuk MM Schutz C Gomez-Llorente J Rocha NR Lansu SM Collins YP Wairkar IM Robinson CJ O'Kane, Journal of Cell Science 2007 120 4367 4376 10.1242/jcs.012336 18057029
59. A role for adenosine deaminase in Drosophila larval development. T Dolezal E Dolezelova M Zurovec PJ Bryant, PLoS Biol 2005 3 201 10.1371/journal.pbio.0030201 15907156
60. Yantar, a conserved arginine-rich protein is involved in Drosophila hemocyte development. SA Sinenko EK Kim R Wynn P Manfruelli I Ando KA Wharton N Perrimon B Mathey-Prevot, Dev Biol 2004 273 48 62 10.1016/j.ydbio.2004.05.022 15302597
61. Zfrp8, the Drosophila ortholog of PDCD2, functions in lymph gland development and controls cell proliferation. S Minakhina M Druzhinina R Steward, Development 2007 134 2387 2396 10.1242/dev.003616 17522156
62. Genome-wide RNAi screen identifies genes involved in intestinal pathogenic bacterial infection. SJ Cronin NT Nehme S Limmer S Liegeois JA Pospisilik D Schramek A Leibbrandt M Simoes Rde S Gruber U Puc,, et al. Science 2009 325 340 343 10.1126/science.1173164 19520911
63. Genome-wide analysis of Notch signalling in Drosophila by transgenic RNAi. JL Mummery-Widmer M Yamazaki T Stoeger M Novatchkova S Bhalerao D Chen G Dietzl BJ Dickson JA Knoblich, Nature 2009 458 987 992 10.1038/nature07936 19363474
64. A novel role of the glial fate determinant glial cells missing in hematopoiesis. C Jacques L Soustelle I Nagy C Diebold A Giangrande, Int J Dev Biol 2009 53 1013 1022 10.1387/ijdb.082726cj 19598118
65. A sensitized genetic screen to identify novel regulators and components of the Drosophila janus kinase/signal transducer and activator of transcription pathway. EA Bach S Vincent MP Zeidler N Perrimon, Genetics 2003 165 1149 1166 14668372
66. Basement membrane abnormalities in melanotic tumor formation of Drosophila. RM Rizki TM Rizki, Experientia 1974 30 543 546 10.1007/BF01926343 4208981
67. Toll-dependent antimicrobial responses in Drosophila larval fat body require Spatzle secreted by haemocytes. AK Shia M Glittenberg G Thompson AN Weber JM Reichhart P Ligoxygakis, Journal of Cell Science 2009 122 4505 4515 10.1242/jcs.049155 19934223
68. Drosophila calcineurin promotes induction of innate immune responses. PF Dijkers PH O'Farrell, Curr Biol 2007 17 2087 2093 10.1016/j.cub.2007.11.001 18060786
69. Salmonella pathogenesis reveals that BMP signaling regulates blood cell homeostasis and immune responses in Drosophila. JL Frandsen B Gunn S Muratoglu N Fossett SJ Newfeld, Proc Natl Acad Sci USA 2008 105 14952 14957 10.1073/pnas.0808208105 18815369
70. Two isoforms of Serpent containing either one or two GATA zinc fingers have different roles in Drosophila haematopoiesis. L Waltzer L Bataille S Peyrefitte M Haenlin, Embo J 2002 21 5477 5486 10.1093/emboj/cdf545 12374748
71. The Friend of GATA proteins U-shaped, FOG-1, and FOG-2 function as negative regulators of blood, heart, and eye development in Drosophila. N Fossett SG Tevosian K Gajewski Q Zhang SH Orkin RA Schulz, Proc Natl Acad Sci USA 2001 98 7342 7347 10.1073/pnas.131215798 11404479
72. Upregulation of the Drosophila friend of GATA Gene u-shaped by JAK/STAT signaling maintains lymph gland prohemocyte potency. H Gao X Wu N Fossett, Mol Cell Biol 2009 29 6086 6096 10.1128/MCB.00244-09 19737914
73. Cooperation between the GATA and RUNX factors Serpent and Lozenge during Drosophila hematopoiesis. L Waltzer G Ferjoux L Bataille M Haenlin, Embo J 2003 22 6516 6525 10.1093/emboj/cdg622 14657024
74. A Drosophila model identifies calpains as modulators of the human leukemogenic fusion protein AML1-ETO. D Osman V Gobert F Ponthan O Heidenreich M Haenlin L Waltzer, Proc Natl Acad Sci USA 2009 106 12043 12048 10.1073/pnas.0902449106 19581587
75. Hemese, a hemocyte-specific transmembrane protein, affects the cellular immune response in Drosophila. E Kurucz CJ Zettervall R Sinka P Vilmos A Pivarcsi S Ekengren Z Hegedus I Ando D Hultmark, Proc Natl Acad Sci USA 2003 100 2622 2627 10.1073/pnas.0436940100 12598653
76. A GATA/RUNX cis-regulatory module couples Drosophila blood cell commitment and differentiation into crystal cells. G Ferjoux B Auge K Boyer M Haenlin L Waltzer, Dev Biol 2007 305 726 734 10.1016/j.ydbio.2007.03.010 17418114