1887
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

Advances in Myeloid-Like Cell Origins and Functions in the Model Organism

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
Buy this Microbiology Spectrum Article
Price Non-Member $15.00
  • Authors: Laure El Chamy1, Nicolas Matt2, Jean-Marc Reichhart3
  • Editor: Siamon Gordon4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Laboratoire de Génétique de la drosophile et virulence microbienne, UR. EGFEM, Faculté des Sciences, Université Saint-Joseph de Beyrouth, B.P. 17-5208 Mar Mikhaël Beyrouth 1104 2020, Liban; 2: Université de Strasbourg, UPR 9022 du CNRS, Institut de Biologie Moléculaire et Cellulaire, Strasbourg Cedex 67084, France; 3: Université de Strasbourg, UPR 9022 du CNRS, Institut de Biologie Moléculaire et Cellulaire, Strasbourg Cedex 67084, France; 4: Oxford University, Oxford, United Kingdom
  • Source: microbiolspec January 2017 vol. 5 no. 1 doi:10.1128/microbiolspec.MCHD-0038-2016
  • Received 31 May 2016 Accepted 29 November 2016 Published 20 January 2017
  • Laure El Chamy, Laure.chamy@usj.edu.lb
image of Advances in Myeloid-Like Cell Origins and Functions in the Model Organism <span class="jp-italic">Drosophila melanogaster</span>
    Preview this microbiology spectrum article:
    Zoom in
    Zoomout

    Advances in Myeloid-Like Cell Origins and Functions in the Model Organism , Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/5/1/MCHD-0038-2016-1.gif /docserver/preview/fulltext/microbiolspec/5/1/MCHD-0038-2016-2.gif
  • Abstract:

    has long served as a valuable model for deciphering many biological processes, including immune responses. Indeed, the genetic tractability of this organism is particularly suited for large-scale analyses. Studies performed during the last 3 decades have proven that the signaling pathways that regulate the innate immune response are conserved between and mammals. This review summarizes the recent advances on hematopoiesis and immune cellular responses, with a particular emphasis on phagocytosis.

  • Citation: El Chamy L, Matt N, Reichhart J. 2017. Advances in Myeloid-Like Cell Origins and Functions in the Model Organism . Microbiol Spectrum 5(1):MCHD-0038-2016. doi:10.1128/microbiolspec.MCHD-0038-2016.

Key Concept Ranking

Immune Receptors
0.63729185
Innate Immune System
0.56330013
Immune Systems
0.5541491
Cellular Processes
0.5322873
Immune Response
0.4706958
0.63729185

References

1. Janeway CA, Jr. 1989. Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb Symp Quant Biol 54(Pt 1):1–13. [PubMed]
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. [PubMed]
3. 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. [PubMed]
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. [PubMed]
5. Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, Birdwell D, Alejos E, Silva M, Galanos C, Freudenberg M, Ricciardi-Castagnoli P, Layton B, Beutler B. 1998. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282:2085–2088. [PubMed]
6. Kawai T, Akira S. 2011. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34:637–650. [PubMed]
7. Ferrandon D. 2013. The complementary facets of epithelial host defenses in the genetic model organism Drosophila melanogaster: from resistance to resilience. Curr Opin Immunol 25:59–70. [PubMed]
8. El Chamy L, Matt N, Ntwasa M, Reichhart JM. 2015. The multilayered innate immune defense of the gut. Biomed J 38:276–284. [PubMed]
9. Lemaitre B, Hoffmann J. 2007. The host defense of Drosophila melanogaster. Annu Rev Immunol 25:697–743. [PubMed]
10. Valanne S, Wang JH, Rämet M. 2011. The Drosophila Toll signaling pathway. J Immunol 186:649–656. [PubMed]
11. Myllymäki H, Valanne S, Rämet M. 2014. The Drosophila Imd signaling pathway. J Immunol 192:3455–3462. [PubMed]
12. Royet J, Reichhart JM, Hoffmann JA. 2005. Sensing and signaling during infection in Drosophila. Curr Opin Immunol 17:11–17. [PubMed]
13. Charroux B, Rival T, Narbonne-Reveau K, Royet J. 2009. Bacterial detection by Drosophila peptidoglycan recognition proteins. Microbes Infect 11:631–636. [PubMed]
14. Jang IH, Chosa N, Kim SH, Nam HJ, Lemaitre B, Ochiai M, Kambris Z, Brun S, Hashimoto C, Ashida M, Brey PT, Lee WJ. 2006. A Spätzle-processing enzyme required for Toll signaling activation in Drosophila innate immunity. Dev Cell 10:45–55. [PubMed]
15. El Chamy L, Leclerc V, Caldelari I, Reichhart JM. 2008. Sensing of ‘danger signals’ and pathogen-associated molecular patterns defines binary signaling pathways ‘upstream’ of Toll. Nat Immunol 9:1165–1170. [PubMed]
16. Gottar M, Gobert V, Matskevich AA, Reichhart JM, Wang C, Butt TM, Belvin M, Hoffmann JA, Ferrandon D. 2006. Dual detection of fungal infections in Drosophila via recognition of glucans and sensing of virulence factors. Cell 127:1425–1437. [PubMed]
17. Cerenius L, Kawabata S, Lee BL, Nonaka M, Soderhall K. 2010. Proteolytic cascades and their involvement in invertebrate immunity. Trends Biochem Sci 35:575–583. [PubMed]
18. Tang H. 2009. Regulation and function of the melanization reaction in Drosophila. Fly (Austin) 3:105–111. [PubMed]
19. 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. [PubMed]
20. Boutros M, Agaisse H, Perrimon N. 2002. Sequential activation of signaling pathways during innate immune responses in Drosophila. Dev Cell 3:711–722. [PubMed]
21. Rämet M, Lanot R, Zachary D, Manfruelli P. 2002. JNK signaling pathway is required for efficient wound healing in Drosophila. Dev Biol 241:145–156. [PubMed]
22. Galko MJ, Krasnow MA. 2004. Cellular and genetic analysis of wound healing in Drosophila larvae. PLoS Biol 2:E239. doi:10.1371/journal.pbio.0020239. [PubMed]
23. Lesch C, Jo J, Wu Y, Fish GS, Galko MJ. 2010. A targeted UAS-RNAi screen in Drosophila larvae identifies wound closure genes regulating distinct cellular processes. Genetics 186:943–957. [PubMed]
24. Kwon YC, Baek SH, Lee H, Choe KM. 2010. Nonmuscle myosin II localization is regulated by JNK during Drosophila larval wound healing. Biochem Biophys Res Commun 393:656–661. [PubMed]
25. Ekengren S, Hultmark D. 2001. A family of Turandot-related genes in the humoral stress response of Drosophila. Biochem Biophys Res Commun 284:998–1003. [PubMed]
26. Agaisse H, Petersen UM, Boutros M, Mathey-Prevot B, Perrimon N. 2003. Signaling role of hemocytes in Drosophila JAK/STAT-dependent response to septic injury. Dev Cell 5:441–450. [PubMed]
27. Brun S, Vidal S, Spellman P, Takahashi K, Tricoire H, Lemaitre B. 2006. The MAPKKK Mekk1 regulates the expression of Turandot stress genes in response to septic injury in Drosophila. Genes Cells 11:397–407. [PubMed]
28. Woodcock KJ, Kierdorf K, Pouchelon CA, Vivancos V, Dionne MS, Geissmann F. 2015. Macrophage-derived upd3 cytokine causes impaired glucose homeostasis and reduced lifespan in Drosophila fed a lipid-rich diet. Immunity 42:133–144. [PubMed]
29. Chakrabarti S, Dudzic JP, Li X, Collas EJ, Boquete JP, Lemaitre B. 2016. Remote control of intestinal stem cell activity by haemocytes in Drosophila. PLoS Genet 12:e1006089. doi:10.1371/journal.pgen.1006089. [PubMed]
30. Martins N, Imler JL, Meignin C. 2016. Discovery of novel targets for antivirals: learning from flies. Curr Opin Virol 20:64–70. [PubMed]
31. Xu J, Cherry S. 2014. Viruses and antiviral immunity in Drosophila. Dev Comp Immunol 42:67–84. [PubMed]
32. Dostert C, Jouanguy E, Irving P, Troxler L, Galiana-Arnoux D, Hetru C, Hoffmann JA, Imler JL. 2005. The Jak-STAT signaling pathway is required but not sufficient for the antiviral response of drosophila. Nat Immunol 6:946–953. [PubMed]
33. Carpenter J, Hutter S, Baines JF, Roller J, Saminadin-Peter SS, Parsch J, Jiggins FM. 2009. The transcriptional response of Drosophila melanogaster to infection with the sigma virus (Rhabdoviridae). PLoS One 4:e6838. doi:10.1371/journal.pone.0006838.
34. Castorena KM, Stapleford KA, Miller DJ. 2010. Complementary transcriptomic, lipidomic, and targeted functional genetic analyses in cultured Drosophila cells highlight the role of glycerophospholipid metabolism in Flock House virus RNA replication. BMC Genomics 11:183. doi:10.1186/1471-2164-11-183.
35. Mudiganti U, Hernandez R, Brown DT. 2010. Insect response to alphavirus infection—establishment of alphavirus persistence in insect cells involves inhibition of viral polyprotein cleavage. Virus Res 150:73–84. [PubMed]
36. Xu J, Grant G, Sabin LR, Gordesky-Gold B, Yasunaga A, Tudor M, Cherry S. 2012. Transcriptional pausing controls a rapid antiviral innate immune response in Drosophila. Cell Host Microbe 12:531–543. [PubMed]
37. Kemp C, Mueller S, Goto A, Barbier V, Paro S, Bonnay F, Dostert C, Troxler L, Hetru C, Meignin C, Pfeffer S, Hoffmann JA, Imler JL. 2013. Broad RNA interference-mediated antiviral immunity and virus-specific inducible responses in Drosophila. J Immunol 190:650–658. [PubMed]
38. Cordes EJ, Licking-Murray KD, Carlson KA. 2013. Differential gene expression related to Nora virus infection of Drosophila melanogaster. Virus Res 175:95–100. [PubMed]
39. Huang Z, Kingsolver MB, Avadhanula V, Hardy RW. 2013. An antiviral role for antimicrobial peptides during the arthropod response to alphavirus replication. J Virol 87:4272–4280. [PubMed]
40. Lamiable O, Imler JL. 2014. Induced antiviral innate immunity in Drosophila. Curr Opin Microbiol 20:62–68. [PubMed]
41. Zambon RA, Nandakumar M, Vakharia VN, Wu LP. 2005. The Toll pathway is important for an antiviral response in Drosophila. Proc Natl Acad Sci U S A 102:7257–7262. [PubMed]
42. Avadhanula V, Weasner BP, Hardy GG, Kumar JP, Hardy RW. 2009. A novel system for the launch of alphavirus RNA synthesis reveals a role for the Imd pathway in arthropod antiviral response. PLoS Pathog 5:e1000582. doi:10.1371/journal.ppat.1000582. [PubMed]
43. Costa A, Jan E, Sarnow P, Schneider D. 2009. The Imd pathway is involved in antiviral immune responses in Drosophila. PLoS One 4:e7436. doi:10.1371/journal.pone.0007436. [PubMed]
44. Rancès E, Johnson TK, Popovici J, Iturbe-Ormaetxe I, Zakir T, Warr CG, O’Neill SL. 2013. The Toll and Imd pathways are not required for Wolbachia-mediated dengue virus interference. J Virol 87:11945–11949. [PubMed]
45. Ferreira AG, Naylor H, Esteves SS, Pais IS, Martins NE, Teixeira L. 2014. The Toll-dorsal pathway is required for resistance to viral oral infection in Drosophila. PLoS Pathog 10:e1004507. doi:10.1371/journal.ppat.1004507. [PubMed]
46. Merkling SH, Bronkhorst AW, Kramer JM, Overheul GJ, Schenck A, Van Rij RP. 2015. The epigenetic regulator G9a mediates tolerance to RNA virus infection in Drosophila. PLoS Pathog 11:e1004692. doi:10.1371/journal.ppat.1004692. [PubMed]
47. Shelly S, Lukinova N, Bambina S, Berman A, Cherry S. 2009. Autophagy is an essential component of Drosophila immunity against vesicular stomatitis virus. Immunity 30:588–598. [PubMed]
48. Liu B, Behura SK, Clem RJ, Schneemann A, Becnel J, Severson DW, Zhou L. 2013. P53-mediated rapid induction of apoptosis conveys resistance to viral infection in Drosophila melanogaster. PLoS Pathog 9:e1003137. doi:10.1371/journal.ppat.1003137.
49. Nainu F, Tanaka Y, Shiratsuchi A, Nakanishi Y. 2015. Protection of insects against viral infection by apoptosis-dependent phagocytosis. J Immunol 195:5696–5706. [PubMed]
50. Galiana-Arnoux D, Dostert C, Schneemann A, Hoffmann JA, Imler JL. 2006. Essential function in vivo for Dicer-2 in host defense against RNA viruses in drosophila. Nat Immunol 7:590–597. [PubMed]
51. van Rij RP, Saleh MC, Berry B, Foo C, Houk A, Antoniewski C, Andino R. 2006. The RNA silencing endonuclease Argonaute 2 mediates specific antiviral immunity in Drosophila melanogaster. Genes Dev 20:2985–2995. [PubMed]
52. Wang XH, Aliyari R, Li WX, Li HW, Kim K, Carthew R, Atkinson P, Ding SW. 2006. RNA interference directs innate immunity against viruses in adult Drosophila. Science 312:452–454. [PubMed]
53. Mueller S, Gausson V, Vodovar N, Deddouche S, Troxler L, Perot J, Pfeffer S, Hoffmann JA, Saleh MC, Imler JL. 2010. RNAi-mediated immunity provides strong protection against the negative-strand RNA vesicular stomatitis virus in Drosophila. Proc Natl Acad Sci U S A 107:19390–19395. [PubMed]
54. Bronkhorst AW, van Cleef KW, Vodovar N, Ince IA, Blanc H, Vlak JM, Saleh MC, van Rij RP. 2012. The DNA virus Invertebrate iridescent virus 6 is a target of the Drosophila RNAi machinery. Proc Natl Acad Sci U S A 109:E3604–E3613. doi:10.1073/pnas.1207213109. [PubMed]
55. Bernstein E, Caudy AA, Hammond SM, Hannon GJ. 2001. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409:363–366. [PubMed]
56. Rand TA, Ginalski K, Grishin NV, Wang X. 2004. Biochemical identification of Argonaute 2 as the sole protein required for RNA-induced silencing complex activity. Proc Natl Acad Sci U S A 101:14385–14389. [PubMed]
57. Okamura K, Ishizuka A, Siomi H, Siomi MC. 2004. Distinct roles for Argonaute proteins in small RNA-directed RNA cleavage pathways. Genes Dev 18:1655–1666. [PubMed]
58. Deddouche S, Matt N, Budd A, Mueller S, Kemp C, Galiana-Arnoux D, Dostert C, Antoniewski C, Hoffmann JA, Imler JL. 2008. The DExD/H-box helicase Dicer-2 mediates the induction of antiviral activity in drosophila. Nat Immunol 9:1425–1432. [PubMed]
59. Desmet CJ, Ishii KJ. 2012. Nucleic acid sensing at the interface between innate and adaptive immunity in vaccination. Nat Rev Immunol 12:479–491. [PubMed]
60. Meister M. 2004. Blood cells of Drosophila: cell lineages and role in host defence. Curr Opin Immunol 16:10–15. [PubMed]
61. Crozatier M, Meister M. 2007. Drosophila haematopoiesis. Cell Microbiol 9:1117–1126. [PubMed]
62. Letourneau M, Lapraz F, Sharma A, Vanzo N, Waltzer L, Crozatier M. 2016. Drosophila hematopoiesis under normal conditions and in response to immune stress. FEBS Lett 590:4034–4051. [PubMed]
63. Gold KS, Bruckner K. 2014. Drosophila as a model for the two myeloid blood cell systems in vertebrates. Exp Hematol 42:717–727. [PubMed]
64. Holz A, Bossinger B, Strasser T, Janning W, Klapper R. 2003. The two origins of hemocytes in Drosophila. Development 130:4955–4962. [PubMed]
65. Tepass U, Fessler LI, Aziz A, Hartenstein V. 1994. Embryonic origin of hemocytes and their relationship to cell death in Drosophila. Development 120:1829–1837. [PubMed]
66. Franc NC, Heitzler P, Ezekowitz RA, White K. 1999. Requirement for Croquemort in phagocytosis of apoptotic cells in Drosophila. Science 284:1991–1994. [PubMed]
67. Franc NC. 2002. Phagocytosis of apoptotic cells in mammals, Caenorhabditis elegans and Drosophila melanogaster: molecular mechanisms and physiological consequences. Front Biosci 7:d1298–d1313.
68. Sears HC, Kennedy CJ, Garrity PA. 2003. Macrophage-mediated corpse engulfment is required for normal Drosophila CNS morphogenesis. Development 130:3557–3565. [PubMed]
69. Olofsson B, Page DT. 2005. Condensation of the central nervous system in embryonic Drosophila is inhibited by blocking hemocyte migration or neural activity. Dev Biol 279:233–243. [PubMed]
70. Defaye A, Evans I, Crozatier M, Wood W, Lemaitre B, Leulier F. 2009. Genetic ablation of Drosophila phagocytes reveals their contribution to both development and resistance to bacterial infection. J Innate Immun 1:322–334. [PubMed]
71. Wood W, Jacinto A. 2007. Drosophila melanogaster embryonic haemocytes: masters of multitasking. Nat Rev Mol Cell Biol 8:542–551. [PubMed]
72. Terriente-Felix A, Li J, Collins S, Mulligan A, Reekie I, Bernard F, Krejci A, Bray S. 2013. Notch cooperates with Lozenge/Runx to lock haemocytes into a differentiation programme. Development 140:926–937. [PubMed]
73. Lebestky T, Chang T, Hartenstein V, Banerjee U. 2000. Specification of Drosophila hematopoietic lineage by conserved transcription factors. Science 288:146–149. [PubMed]
74. Bernardoni R, Vivancos V, Giangrande A. 1997. glide/gcm is expressed and required in the scavenger cell lineage. Dev Biol 191:118–130. [PubMed]
75. Lebestky T, Jung SH, Banerjee U. 2003. A Serrate-expressing signaling center controls Drosophila hematopoiesis. Genes Dev 17:348–353. [PubMed]
76. Muratoglu S, Garratt B, Hyman K, Gajewski K, Schulz RA, Fossett N. 2006. Regulation of Drosophila Friend of GATA gene, u-shaped, during hematopoiesis: a direct role for Serpent and Lozenge. Dev Biol 296:561–579. [PubMed]
77. Bataille L, Auge B, Ferjoux G, Haenlin M, Waltzer L. 2005. Resolving embryonic blood cell fate choice in Drosophila: interplay of GCM and RUNX factors. Development 132:4635–4644. [PubMed]
78. Evans CJ, Hartenstein V, Banerjee U. 2003. Thicker than blood: conserved mechanisms in Drosophila and vertebrate hematopoiesis. Dev Cell 5:673–690. [PubMed]
79. Markus R, Laurinyecz B, Kurucz E, Honti V, Bajusz I, Sipos B, Somogyi K, Kronhamn J, Hultmark D, Ando I. 2009. Sessile hemocytes as a hematopoietic compartment in Drosophila melanogaster. Proc Natl Acad Sci U S A 106:4805–4809. [PubMed]
80. Zaidman-Remy A, Regan JC, Brandao AS, Jacinto A. 2012. The Drosophila larva as a tool to study gut-associated macrophages: PI3K regulates a discrete hemocyte population at the proventriculus. Dev Comp Immunol 36:638–647. [PubMed]
81. Stofanko M, Kwon SY, Badenhorst P. 2008. A misexpression screen to identify regulators of Drosophila larval hemocyte development. Genetics 180:253–267. [PubMed]
82. Hashimoto D, Chow A, Noizat C, Teo P, Beasley MB, Leboeuf M, Becker CD, See P, Price J, Lucas D, Greter M, Mortha A, Boyer SW, Forsberg EC, Tanaka M, van Rooijen N, Garcia-Sastre A, Stanley ER, Ginhoux F, Frenette PS, Merad M. 2013. Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity 38:792–804. [PubMed]
83. 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. [PubMed]
84. Makhijani K, Bruckner K. 2012. Of blood cells and the nervous system: hematopoiesis in the Drosophila larva. Fly (Austin) 6:254–260. [PubMed]
85. Honti V, Csordas G, Markus R, Kurucz E, Jankovics F, Ando I. 2010. Cell lineage tracing reveals the plasticity of the hemocyte lineages and of the hematopoietic compartments in Drosophila melanogaster. Mol Immunol 47:1997–2004. [PubMed]
86. Leitão AB, Sucena E. 2015. Drosophila sessile hemocyte clusters are true hematopoietic tissues that regulate larval blood cell differentiation. eLife 4:e06166. doi:10.7554/eLife.06166.
87. Lanot R, Zachary D, Holder F, Meister M. 2001. Postembryonic hematopoiesis in Drosophila. Dev Biol 230:243–257. [PubMed]
88. Pastor-Pareja JC, Wu M, Xu T. 2008. An innate immune response of blood cells to tumors and tissue damage in Drosophila. Dis Model Mech 1:144–154; discussion 153. [PubMed]
89. Zettervall CJ, Anderl I, Williams MJ, Palmer R, Kurucz E, Ando I, Hultmark D. 2004. A directed screen for genes involved in Drosophila blood cell activation. Proc Natl Acad Sci U S A 101:14192–14197. [PubMed]
90. Babcock DT, Brock AR, Fish GS, Wang Y, Perrin L, Krasnow MA, Galko MJ. 2008. Circulating blood cells function as a surveillance system for damaged tissue in Drosophila larvae. Proc Natl Acad Sci U S A 105:10017–10022. [PubMed]
91. Grigorian M, Mandal L, Hartenstein V. 2011. Hematopoiesis at the onset of metamorphosis: terminal differentiation and dissociation of the Drosophila lymph gland. Dev Genes Evol 221:121–131. [PubMed]
92. Rugendorff AE, Younossi-Hartenstein A, Hartenstein V. 1994. Embryonic origin and differentiation of the Drosophila heart. Roux’s Arch Dev Bio 203:266–280.
93. Mandal L, Banerjee U, Hartenstein V. 2004. Evidence for a fruit fly hemangioblast and similarities between lymph-gland hematopoiesis in fruit fly and mammal aorta-gonadal-mesonephros mesoderm. Nat Genet 36:1019–1023. [PubMed]
94. Hartenstein V. 2006. Blood cells and blood cell development in the animal kingdom. Annu Rev Cell Dev Biol 22:677–712. [PubMed]
95. Jung SH, Evans CJ, Uemura C, Banerjee U. 2005. The Drosophila lymph gland as a developmental model of hematopoiesis. Development 132:2521–2533. [PubMed]
96. Krzemień J, Dubois L, Makki R, Meister M, Vincent A, Crozatier M. 2007. Control of blood cell homeostasis in Drosophila larvae by the posterior signalling centre. Nature 446:325–328. [PubMed]
97. Mandal L, Martinez-Agosto JA, Evans CJ, Hartenstein V, Banerjee U. 2007. A Hedgehog- and Antennapedia-dependent niche maintains Drosophila haematopoietic precursors. Nature 446:320–324. [PubMed]
98. Crozatier M, Krzemień J, Vincent A. 2007. The hematopoietic niche: a Drosophila model, at last. Cell Cycle 6:1443–1444. [PubMed]
99. Minakhina S, Steward R. 2010. Hematopoietic stem cells in Drosophila. Development 137:27–31. [PubMed]
100. Mondal BC, Mukherjee T, Mandal L, Evans CJ, Sinenko SA, Martinez-Agosto JA, Banerjee U. 2011. Interaction between differentiating cell- and niche-derived signals in hematopoietic progenitor maintenance. Cell 147:1589–1600. [PubMed]
101. Benmimoun B, Polesello C, Haenlin M, Waltzer L. 2015. The EBF transcription factor Collier directly promotes Drosophila blood cell progenitor maintenance independently of the niche. Proc Natl Acad Sci U S A 112:9052–9057. [PubMed]
102. Morin-Poulard I, Sharma A, Louradour I, Vanzo N, Vincent A, Crozatier M. 2016. Vascular control of the Drosophila haematopoietic microenvironment by Slit/Robo signalling. Nat Commun 7:11634. doi:10.1038/ncomms11634.
103. Sinenko SA, Mandal L, Martinez-Agosto JA, Banerjee U. 2009. Dual role of Wingless signaling in stem-like hematopoietic precursor maintenance in Drosophila. Dev Cell 16:756–763. [PubMed]
104. Shim J, Mukherjee T, Banerjee U. 2012. Direct sensing of systemic and nutritional signals by haematopoietic progenitors in Drosophila. Nat Cell Biol 14:394–400. [PubMed]
105. Owusu-Ansah E, Banerjee U. 2009. Reactive oxygen species prime Drosophila haematopoietic progenitors for differentiation. Nature 461:537–541. [PubMed]
106. Shim J, Mukherjee T, Mondal BC, Liu T, Young GC, Wijewarnasuriya DP, Banerjee U. 2013. Olfactory control of blood progenitor maintenance. Cell 155:1141–1153. [PubMed]
107. Oyallon J, Vanzo N, Krzemień J, Morin-Poulard I, Vincent A, Crozatier M. 2016. Two independent functions of Collier/Early B Cell Factor in the control of Drosophila blood cell homeostasis. PLoS One 11:e0148978. doi:10.1371/journal.pone.0148978.
108. Qiu P, Pan PC, Govind S. 1998. A role for the Drosophila Toll/Cactus pathway in larval hematopoiesis. Development 125:1909–1920. [PubMed]
109. Myrick KV, Dearolf CR. 2000. Hyperactivation of the Drosophila Hop Jak kinase causes the preferential overexpression of eIF1A transcripts in larval blood cells. Gene 244:119–125. [PubMed]
110. Minakhina S, Tan W, Steward R. 2011. JAK/STAT and the GATA factor Pannier control hemocyte maturation and differentiation in Drosophila. Dev Biol 352:308–316. [PubMed]
111. Pennetier D, Oyallon J, Morin-Poulard I, Dejean S, Vincent A, Crozatier M. 2012. Size control of the Drosophila hematopoietic niche by bone morphogenetic protein signaling reveals parallels with mammals. Proc Natl Acad Sci U S A 109:3389–3394. [PubMed]
112. Remillieux-Leschelle N, Santamaria P, Randsholt NB. 2002. Regulation of larval hematopoiesis in Drosophila melanogaster: a role for the multi sex combs gene. Genetics 162:1259–1274. [PubMed]
113. Minakhina S, Druzhinina M, Steward R. 2007. Zfrp8, the Drosophila ortholog of PDCD2, functions in lymph gland development and controls cell proliferation. Development 134:2387–2396. [PubMed]
114. Crozatier M, Ubeda JM, Vincent A, Meister M. 2004. Cellular immune response to parasitization in Drosophila requires the EBF orthologue Collier. PLoS Biol 2:E196. doi:10.1371/journal.pbio.0020196. [PubMed]
115. Rizki TM, Rizki RM. 1992. Lamellocyte differentiation in Drosophila larvae parasitized by Leptopilina. Dev Comp Immunol 16:103–110. [PubMed]
116. Sinenko SA, Shim J, Banerjee U. 2012. Oxidative stress in the haematopoietic niche regulates the cellular immune response in Drosophila. EMBO Rep 13:83–89. [PubMed]
117. Ghosh S, Singh A, Mandal S, Mandal L. 2015. Active hematopoietic hubs in Drosophila adults generate hemocytes and contribute to immune response. Dev Cell 33:478–488. [PubMed]
118. Martinek N, Shahab J, Saathoff M, Ringuette M. 2008. Haemocyte-derived SPARC is required for collagen-IV-dependent stability of basal laminae in Drosophila embryos. J Cell Sci 121:1671–1680. [PubMed]
119. Bunt S, Hooley C, Hu N, Scahill C, Weavers H, Skaer H. 2010. Hemocyte-secreted type IV collagen enhances BMP signaling to guide renal tubule morphogenesis in Drosophila. Dev Cell 19:296–306. [PubMed]
120. Fessler JH, Fessler LI. 1989. Drosophila extracellular matrix. Annu Rev Cell Biol 5:309–339. [PubMed]
121. Gullberg D, Fessler LI, Fessler JH. 1994. Differentiation, extracellular matrix synthesis, and integrin assembly by Drosophila embryo cells cultured on vitronectin and laminin substrates. Dev Dyn 199:116–128. [PubMed]
122. Hortsch M, Olson A, Fishman S, Soneral SN, Marikar Y, Dong R, Jacobs JR. 1998. The expression of MDP-1, a component of Drosophila embryonic basement membranes, is modulated by apoptotic cell death. Int J Dev Biol 42:33–42. [PubMed]
123. Lamiable O, Arnold J, de Faria IJ, Olmo RP, Bergami F, Meignin C, Hoffmann JA, Marques JT, Imler JL. 2016. Analysis of the contribution of hemocytes and autophagy to Drosophila antiviral immunity. J Virol 90:5415–5426. [PubMed]
124. Vlisidou I, Wood W. 2015. Drosophila blood cells and their role in immune responses. FEBS J 282:1368–1382. [PubMed]
125. Elrod-Erickson M, Mishra S, Schneider D. 2000. Interactions between the cellular and humoral immune responses in Drosophila. Curr Biol 10:781–784. [PubMed]
126. Nehme NT, Quintin J, Cho JH, Lee J, Lafarge MC, Kocks C, Ferrandon D. 2011. Relative roles of the cellular and humoral responses in the Drosophila host defense against three Gram-positive bacterial infections. PLoS One 6:e14743. doi:10.1371/journal.pone.0014743.
127. Basset A, Khush RS, Braun A, Gardan L, Boccard F, Hoffmann JA, Lemaitre B. 2000. The phytopathogenic bacteria Erwinia carotovora infects Drosophila and activates an immune response. Proc Natl Acad Sci U S A 97:3376–3381. [PubMed]
128. Shia AK, Glittenberg M, Thompson G, Weber AN, Reichhart JM, Ligoxygakis P. 2009. Toll-dependent antimicrobial responses in Drosophila larval fat body require Spätzle secreted by haemocytes. J Cell Sci 122:4505–4515. [PubMed]
129. Foley E, O’Farrell PH. 2003. Nitric oxide contributes to induction of innate immune responses to gram-negative bacteria in Drosophila. Genes Dev 17:115–125. [PubMed]
130. Wu SC, Liao CW, Pan RL, Juang JL. 2012. Infection-induced intestinal oxidative stress triggers organ-to-organ immunological communication in Drosophila. Cell Host Microbe 11:410–417. [PubMed]
131. Glittenberg MT, Kounatidis I, Christensen D, Kostov M, Kimber S, Roberts I, Ligoxygakis P. 2011. Pathogen and host factors are needed to provoke a systemic host response to gastrointestinal infection of Drosophila larvae by Candida albicans. Dis Model Mech 4:515–525. [PubMed]
132. Parisi F, Stefanatos RK, Strathdee K, Yu Y, Vidal M. 2014. Transformed epithelia trigger non-tissue-autonomous tumor suppressor response by adipocytes via activation of Toll and Eiger/TNF signaling. Cell Rep 6:855–867. [PubMed]
133. 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. [PubMed]
134. Ruhf ML, Braun A, Papoulas O, Tamkun JW, Randsholt N, Meister M. 2001. The domino gene of Drosophila encodes novel members of the SWI2/SNF2 family of DNA-dependent ATPases, which contribute to the silencing of homeotic genes. Development 128:1429–1441. [PubMed]
135. Gateff E. 1994. Tumor suppressor and overgrowth suppressor genes of Drosophila melanogaster: developmental aspects. Int J Dev Biol 38:565–590. [PubMed]
136. 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. [PubMed]
137. Irving P, Ubeda JM, Doucet D, Troxler L, Lagueux M, Zachary D, Hoffmann JA, Hetru C, Meister M. 2005. New insights into Drosophila larval haemocyte functions through genome-wide analysis. Cell Microbiol 7:335–350. [PubMed]
138. 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. [PubMed]
139. 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. [PubMed]
140. Dudzic JP, Kondo S, Ueda R, Bergman CM, Lemaitre B. 2015. Drosophila innate immunity: regional and functional specialization of prophenoloxidases. BMC Biol 13:81. doi:10.1186/s12915-015-0193-6. [PubMed]
141. Leclerc V, Pelte N, El Chamy L, Martinelli C, Ligoxygakis P, Hoffmann JA, Reichhart JM. 2006. Prophenoloxidase activation is not required for survival to microbial infections in Drosophila. EMBO Rep 7:231–235. [PubMed]
142. Tang H, Kambris Z, Lemaitre B, Hashimoto C. 2006. Two proteases defining a melanization cascade in the immune system of Drosophila. J Biol Chem 281:28097–28104. [PubMed]
143. Rizki TM, Rizki RM, Bellotti RA. 1985. Genetics of a Drosophila phenoloxidase. Mol Gen Genet 201:7–13. [PubMed]
144. Ayres JS, Schneider DS. 2008. A signaling protease required for melanization in Drosophila affects resistance and tolerance of infections. PLoS Biol 6:2764–2773. [PubMed]
145. Lemaitre B, Kromer-Metzger E, Michaut L, Nicolas E, Meister M, Georgel P, Reichhart JM, Hoffmann JA. 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. [PubMed]
146. Neyen C, Binggeli O, Roversi P, Bertin L, Sleiman MB, Lemaitre B. 2015. The Black cells phenotype is caused by a point mutation in the Drosophila pro-phenoloxidase 1 gene that triggers melanization and hematopoietic defects. Dev Comp Immunol 50:166–174. [PubMed]
147. Binggeli O, Neyen C, Poidevin M, Lemaitre B. 2014. Prophenoloxidase activation is required for survival to microbial infections in Drosophila. PLoS Pathog 10:e1004067. doi:10.1371/journal.ppat.1004067. [PubMed]
148. 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. [PubMed]
149. Scherfer C, Karlsson C, Loseva O, Bidla G, Goto A, Havemann J, Dushay MS, Theopold U. 2004. Isolation and characterization of hemolymph clotting factors in Drosophila melanogaster by a pullout method. Curr Biol 14:625–629. [PubMed]
150. Goto A, Kadowaki T, Kitagawa Y. 2003. Drosophila hemolectin gene is expressed in embryonic and larval hemocytes and its knock down causes bleeding defects. Dev Biol 264:582–591. [PubMed]
151. Goto A, Kumagai T, Kumagai C, Hirose J, Narita H, Mori H, Kadowaki T, Beck K, Kitagawa Y. 2001. A Drosophila haemocyte-specific protein, hemolectin, similar to human von Willebrand factor. Biochem J 359:99–108. [PubMed]
152. Evans IR, Wood W. 2014. Drosophila blood cell chemotaxis. Curr Opin Cell Biol 30:1–8. [PubMed]
153. Stramer B, Wood W, Galko MJ, Redd MJ, Jacinto A, Parkhurst SM, Martin P. 2005. Live imaging of wound inflammation in Drosophila embryos reveals key roles for small GTPases during in vivo cell migration. J Cell Biol 168:567–573. [PubMed]
154. Wood W, Faria C, Jacinto A. 2006. Distinct mechanisms regulate hemocyte chemotaxis during development and wound healing in Drosophila melanogaster. J Cell Biol 173:405–416. [PubMed]
155. Moreira S, Stramer B, Evans I, Wood W, Martin P. 2010. Prioritization of competing damage and developmental signals by migrating macrophages in the Drosophila embryo. Curr Biol 20:464–470. [PubMed]
156. Razzell W, Evans IR, Martin P, Wood W. 2013. Calcium flashes orchestrate the wound inflammatory response through DUOX activation and hydrogen peroxide release. Curr Biol 23:424–429. [PubMed]
157. Evans IR, Rodrigues FS, Armitage EL, Wood W. 2015. Draper/CED-1 mediates an ancient damage response to control inflammatory blood cell migration in vivo. Curr Biol 25:1606–1612. [PubMed]
158. Stuart LM, Ezekowitz RA. 2008. Phagocytosis and comparative innate immunity: learning on the fly. Nat Rev Immunol 8:131–141. [PubMed]
159. Schneider I. 1972. Cell lines derived from late embryonic stages of Drosophila melanogaster. J Embryol Exp Morphol 27:353–365. [PubMed]
160. Cherry S. 2008. Genomic RNAi screening in Drosophila S2 cells: what have we learned about host-pathogen interactions? Curr Opin Microbiol 11:262–270. [PubMed]
161. Ulvila J, Vanha-Aho LM, Ramet M. 2011. Drosophila phagocytosis—still many unknowns under the surface. APMIS 119:651–662. [PubMed]
162. 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. [PubMed]
163. Stuart LM, Deng J, Silver JM, Takahashi K, Tseng AA, Hennessy EJ, Ezekowitz RA, Moore KJ. 2005. Response to Staphylococcus aureus requires CD36-mediated phagocytosis triggered by the COOH-terminal cytoplasmic domain. J Cell Biol 170:477–485. [PubMed]
164. Stuart LM, Bell SA, Stewart CR, Silver JM, Richard J, Goss JL, Tseng AA, Zhang A, El Khoury JB, Moore KJ. 2007. CD36 signals to the actin cytoskeleton and regulates microglial migration via a p130Cas complex. J Biol Chem 282:27392–27401. [PubMed]
165. Philips JA, Rubin EJ, Perrimon N. 2005. Drosophila RNAi screen reveals CD36 family member required for mycobacterial infection. Science 309:1251–1253. [PubMed]
166. Agaisse H, Burrack LS, Philips JA, Rubin EJ, Perrimon N, Higgins DE. 2005. Genome-wide RNAi screen for host factors required for intracellular bacterial infection. Science 309:1248–1251. [PubMed]
167. Cheng LW, Viala JP, Stuurman N, Wiedemann U, Vale RD, Portnoy DA. 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. [PubMed]
168. 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. doi:10.1371/journal.pbio.0040004. [PubMed]
169. Pearson AM, Baksa K, Ramet M, Protas M, McKee M, Brown D, Ezekowitz RA. 2003. Identification of cytoskeletal regulatory proteins required for efficient phagocytosis in Drosophila. Microbes Infect 5:815–824.
170. Nichols Z, Vogt RG. 2008. The SNMP/CD36 gene family in Diptera, Hymenoptera and Coleoptera: Drosophila melanogaster, D. pseudoobscura, Anopheles gambiae, Aedes aegypti, Apis mellifera, and Tribolium castaneum. Insect Biochem Mol Biol 38:398–415. [PubMed]
171. Franc NC, Dimarcq JL, Lagueux M, Hoffmann J, Ezekowitz RA. 1996. Croquemort, a novel Drosophila hemocyte/macrophage receptor that recognizes apoptotic cells. Immunity 4:431–443.
172. Hoebe K, Georgel P, Rutschmann S, Du X, Mudd S, Crozat K, Sovath S, Shamel L, Hartung T, Zahringer U, Beutler B. 2005. CD36 is a sensor of diacylglycerides. Nature 433:523–527. [PubMed]
173. Talamillo A, Herboso L, Pirone L, Pérez C, González M, Sánchez J, Mayor U, Lopitz-Otsoa F, Rodriguez MS, Sutherland JD, Barrio R. 2013. Scavenger receptors mediate the role of SUMO and Ftz-f1 in Drosophila steroidogenesis. PLoS Genet 9:e1003473. doi:10.1371/journal.pgen.1003473.
174. Benton R, Vannice KS, Vosshall LB. 2007. An essential role for a CD36-related receptor in pheromone detection in Drosophila. Nature 450:289–293. [PubMed]
175. Abrams JM, Lux A, Steller H, Krieger M. 1992. Macrophages in Drosophila embryos and L2 cells exhibit scavenger receptor-mediated endocytosis. Proc Natl Acad Sci U S A 89:10375–10379. [PubMed]
176. Ramet M, Pearson A, Manfruelli P, Li X, Koziel H, Gobel V, Chung E, Krieger M, Ezekowitz RA. 2001. Drosophila scavenger receptor CI is a pattern recognition receptor for bacteria. Immunity 15:1027–1038.
177. Kocks C, Cho JH, Nehme N, Ulvila J, Pearson AM, Meister M, Strom C, Conto SL, Hetru C, Stuart LM, Stehle T, Hoffmann JA, Reichhart JM, Ferrandon D, Rämet M, Ezekowitz RA. 2005. Eater, a transmembrane protein mediating phagocytosis of bacterial pathogens in Drosophila. Cell 123:335–346. [PubMed]
178. Kurucz E, Márkus R, Zsámboki J, Folkl-Medzihradszky K, Darula Z, Vilmos P, Udvardy A, Krausz I, Lukacsovich T, Gateff E, Zettervall CJ, Hultmark D, Andó I. 2007. Nimrod, a putative phagocytosis receptor with EGF repeats in Drosophila plasmatocytes. Curr Biol 17:649–654. [PubMed]
179. Somogyi K, Sipos B, Penzes Z, Ando I. 2010. A conserved gene cluster as a putative functional unit in insect innate immunity. FEBS Lett 584:4375–4378. [PubMed]
180. Chung YS, Kocks C. 2011. Recognition of pathogenic microbes by the Drosophila phagocytic pattern recognition receptor Eater. J Biol Chem 286:26524–26532. [PubMed]
181. Chung YS, Kocks C. 2012. Phagocytosis of bacterial pathogens. Fly (Austin) 6:21–25. [PubMed]
182. Hashimoto Y, Tabuchi Y, Sakurai K, Kutsuna M, Kurokawa K, Awasaki T, Sekimizu K, Nakanishi Y, Shiratsuchi A. 2009. Identification of lipoteichoic acid as a ligand for Draper in the phagocytosis of Staphylococcus aureus by Drosophila hemocytes. J Immunol 183:7451–7460. [PubMed]
183. Shiratsuchi A, Mori T, Sakurai K, Nagaosa K, Sekimizu K, Lee BL, Nakanishi Y. 2012. Independent recognition of Staphylococcus aureus by two receptors for phagocytosis in Drosophila. J Biol Chem 287:21663–21672. [PubMed]
184. Bretscher AJ, Honti V, Binggeli O, Burri O, Poidevin M, Kurucz E, Zsamboki J, Ando I, Lemaitre B. 2015. The Nimrod transmembrane receptor Eater is required for hemocyte attachment to the sessile compartment in Drosophila melanogaster. Biol Open 4:355–363. [PubMed]
185. Gumienny TL, Brugnera E, Tosello-Trampont AC, Kinchen JM, Haney LB, Nishiwaki K, Walk SF, Nemergut ME, Macara IG, Francis R, Schedl T, Qin Y, Van Aelst L, Hengartner MO, Ravichandran KS. 2001. CED-12/ELMO, a novel member of the CrkII/Dock180/Rac pathway, is required for phagocytosis and cell migration. Cell 107:27–41. [PubMed]
186. Gumienny TL, Hengartner MO. 2001. How the worm removes corpses: the nematode C. elegans as a model system to study engulfment. Cell Death Differ 8:564–568. [PubMed]
187. Freeman MR, Delrow J, Kim J, Johnson E, Doe CQ. 2003. Unwrapping glial biology: Gcm target genes regulating glial development, diversification, and function. Neuron 38:567–580.
188. Awasaki T, Tatsumi R, Takahashi K, Arai K, Nakanishi Y, Ueda R, Ito K. 2006. Essential role of the apoptotic cell engulfment genes draper and ced-6 in programmed axon pruning during Drosophila metamorphosis. Neuron 50:855–867. [PubMed]
189. MacDonald JM, Beach MG, Porpiglia E, Sheehan AE, Watts RJ, Freeman MR. 2006. The Drosophila cell corpse engulfment receptor Draper mediates glial clearance of severed axons. Neuron 50:869–881. [PubMed]
190. Hoopfer ED, McLaughlin T, Watts RJ, Schuldiner O, O’Leary DD, Luo L. 2006. Wlds protection distinguishes axon degeneration following injury from naturally occurring developmental pruning. Neuron 50:883–895. [PubMed]
191. Manaka J, Kuraishi T, Shiratsuchi A, Nakai Y, Higashida H, Henson P, Nakanishi Y. 2004. Draper-mediated and phosphatidylserine-independent phagocytosis of apoptotic cells by Drosophila hemocytes/macrophages. J Biol Chem 279:48466–48476. [PubMed]
192. Kurant E, Axelrod S, Leaman D, Gaul U. 2008. Six-microns-under acts upstream of Draper in the glial phagocytosis of apoptotic neurons. Cell 133:498–509. [PubMed]
193. Krivtsov AV, Rozov FN, Zinovyeva MV, Hendrikx PJ, Jiang Y, Visser JW, Belyavsky AV. 2007. Jedi—a novel transmembrane protein expressed in early hematopoietic cells. J Cell Biochem 101:767–784. [PubMed]
194. Hamon Y, Trompier D, Ma Z, Venegas V, Pophillat M, Mignotte V, Zhou Z, Chimini G. 2006. Cooperation between engulfment receptors: the case of ABCA1 and MEGF10. PLoS One 1:e120. doi:10.1371/journal.pone.0000120. [PubMed]
195. Wu HH, Bellmunt E, Scheib JL, Venegas V, Burkert C, Reichardt LF, Zhou Z, Farinas I, Carter BD. 2009. Glial precursors clear sensory neuron corpses during development via Jedi-1, an engulfment receptor. Nat Neurosci 12:1534–1541. [PubMed]
196. Scheib JL, Sullivan CS, Carter BD. 2012. Jedi-1 and MEGF10 signal engulfment of apoptotic neurons through the tyrosine kinase Syk. J Neurosci 32:13022–13031. [PubMed]
197. Ziegenfuss JS, Biswas R, Avery MA, Hong K, Sheehan AE, Yeung YG, Stanley ER, Freeman MR. 2008. Draper-dependent glial phagocytic activity is mediated by Src and Syk family kinase signalling. Nature 453:935–939. [PubMed]
198. Nagaosa K, Okada R, Nonaka S, Takeuchi K, Fujita Y, Miyasaka T, Manaka J, Ando I, Nakanishi Y. 2011. Integrin βν-mediated phagocytosis of apoptotic cells in Drosophila embryos. J Biol Chem 286:25770–25777. [PubMed]
199. Nonaka S, Nagaosa K, Mori T, Shiratsuchi A, Nakanishi Y. 2013. Integrin αPS3/βν-mediated phagocytosis of apoptotic cells and bacteria in Drosophila. J Biol Chem 288:10374–10380. [PubMed]
200. Lettre G, Hengartner MO. 2006. Developmental apoptosis in C. elegans: a complex CEDnario. Nat Rev Mol Cell Biol 7:97–108. [PubMed]
201. Kinchen JM, Ravichandran KS. 2007. Journey to the grave: signaling events regulating removal of apoptotic cells. J Cell Sci 120:2143–2149. [PubMed]
202. Hsu TY, Wu YC. 2010. Engulfment of apoptotic cells in C. elegans is mediated by integrin α/SRC signaling. Curr Biol 20:477–486. [PubMed]
203. Gottar M, Gobert V, Michel T, Belvin M, Duyk G, Hoffmann JA, Ferrandon D, Royet J. 2002. The Drosophila immune response against Gram-negative bacteria is mediated by a peptidoglycan recognition protein. Nature 416:640–644. [PubMed]
204. Choe KM, Werner T, Stöven 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. [PubMed]
205. Lagueux M, Perrodou E, Levashina EA, Capovilla M, Hoffmann JA. 2000. Constitutive expression of a complement-like protein in Toll and JAK gain-of-function mutants of Drosophila. Proc Natl Acad Sci U S A 97:11427–11432. [PubMed]
206. Bou Aoun R, Hetru C, Troxler L, Doucet D, Ferrandon D, Matt N. 2011. Analysis of thioester-containing proteins during the innate immune response of Drosophila melanogaster. J Innate Immun 3:52–64. [PubMed]
207. Levashina EA, Moita LF, Blandin S, Vriend G, Lagueux M, Kafatos FC. 2001. Conserved role of a complement-like protein in phagocytosis revealed by dsRNA knockout in cultured cells of the mosquito, Anopheles gambiae. Cell 104:709–718.
208. Blandin S, Shiao SH, Moita LF, Janse CJ, Waters AP, Kafatos FC, Levashina EA. 2004. Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell 116:661–670. [PubMed]
209. Watson FL, Puttmann-Holgado R, Thomas F, Lamar DL, Hughes M, Kondo M, Rebel VI, Schmucker D. 2005. Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science 309:1874–1878. [PubMed]
210. Schmucker D, Clemens JC, Shu H, Worby CA, Xiao J, Muda M, Dixon JE, Zipursky SL. 2000. Drosophila Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity. Cell 101:671–684.
211. Wojtowicz WM, Flanagan JJ, Millard SS, Zipursky SL, Clemens JC. 2004. Alternative splicing of Drosophila Dscam generates axon guidance receptors that exhibit isoform-specific homophilic binding. Cell 118:619–633. [PubMed]
212. Stuart LM, Boulais J, Charriere GM, Hennessy EJ, Brunet S, Jutras I, Goyette G, Rondeau C, Letarte S, Huang H, Ye P, Morales F, Kocks C, Bader JS, Desjardins M, Ezekowitz RA. 2007. A systems biology analysis of the Drosophila phagosome. Nature 445:95–101. [PubMed]
213. Armitage SA, Sun W, You X, Kurtz J, Schmucker D, Chen W. 2014. Quantitative profiling of Drosophila melanogaster Dscam1 isoforms reveals no changes in splicing after bacterial exposure. PLoS One 9:e108660. doi:10.1371/journal.pone.0108660.
214. 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 3:1446–1458. [PubMed]
215. Koo IC, Ohol YM, Wu P, Morisaki JH, Cox JS, Brown EJ. 2008. Role for lysosomal enzyme β-hexosaminidase in the control of mycobacteria infection. Proc Natl Acad Sci U S A 105:710–715. [PubMed]
216. Ulvila J, Vanha-aho LM, Kleino A, Vähä-Mäkilä M, Vuoksio M, Eskelinen S, Hultmark D, Kocks C, Hallman M, Parikka M, Rämet M. 2011. Cofilin regulator 14-3-3ζ is an evolutionarily conserved protein required for phagocytosis and microbial resistance. J Leukoc Biol 89:649–659. [PubMed]
217. Korolchuk VI, Schütz MM, Gómez-Llorente C, Rocha J, Lansu NR, Collins SM, Wairkar YP, Robinson IM, O’Kane CJ. 2007. Drosophila Vps35 function is necessary for normal endocytic trafficking and actin cytoskeleton organisation. J Cell Sci 120:4367–4376. [PubMed]
218. Charrière GM, Ip WE, Dejardin S, Boyer L, Sokolovska A, Cappillino MP, Cherayil BJ, Podolsky DK, Kobayashi KS, Silverman N, Lacy-Hulbert A, Stuart LM. 2010. Identification of Drosophila Yin and PEPT2 as evolutionarily conserved phagosome-associated muramyl dipeptide transporters. J Biol Chem 285:20147–20154. [PubMed]
219. Akbar MA, Tracy C, Kahr WH, Krämer H. 2011. The full-of-bacteria gene is required for phagosome maturation during immune defense in Drosophila. J Cell Biol 192:383–390. [PubMed]
220. Harrison DA, Binari R, Nahreini TS, Gilman M, Perrimon N. 1995. Activation of a Drosophila Janus kinase (JAK) causes hematopoietic neoplasia and developmental defects. EMBO J 14:2857–2865. [PubMed]
221. Wang L, Kounatidis I, Ligoxygakis P. 2014. Drosophila as a model to study the role of blood cells in inflammation, innate immunity and cancer. Front Cell Infect Microbiol 3:113. doi:10.3389/fcimb.2013.00113. [PubMed]
222. Srivastava A, Pastor-Pareja JC, Igaki T, Pagliarini R, Xu T. 2007. Basement membrane remodeling is essential for Drosophila disc eversion and tumor invasion. Proc Natl Acad Sci U S A 104:2721–2726. [PubMed]
223. Hauling T, Krautz R, Markus R, Volkenhoff A, Kucerova L, Theopold U. 2014. A Drosophila immune response against Ras-induced overgrowth. Biol Open 3:250–260. [PubMed]
224. Fogarty CE, Diwanji N, Lindblad JL, Tare M, Amcheslavsky A, Makhijani K, Bruckner K, Fan Y, Bergmann A. 2016. Extracellular reactive oxygen species drive apoptosis-induced proliferation via Drosophila macrophages. Curr Biol 26:575–584. [PubMed]
225. Ayyaz A, Li H, Jasper H. 2015. Haemocytes control stem cell activity in the Drosophila intestine. Nat Cell Biol 17:736–748. [PubMed]
microbiolspec.MCHD-0038-2016.citations
cm/5/1
content/journal/microbiolspec/10.1128/microbiolspec.MCHD-0038-2016
Loading

Citations loading...

Loading

Article metrics loading...

/content/journal/microbiolspec/10.1128/microbiolspec.MCHD-0038-2016
2017-01-20
2017-09-25

Abstract:

has long served as a valuable model for deciphering many biological processes, including immune responses. Indeed, the genetic tractability of this organism is particularly suited for large-scale analyses. Studies performed during the last 3 decades have proven that the signaling pathways that regulate the innate immune response are conserved between and mammals. This review summarizes the recent advances on hematopoiesis and immune cellular responses, with a particular emphasis on phagocytosis.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of FIGURE 1
FIGURE 1

immune reactions. immune response comprises a local barrier response based on the secretion of AMPs and a fine-tuned oxidative response. Breaching of this barrier triggers a systemic humoral antimicrobial response as well as a cellular response (refer to text for a detailed description).

Source: microbiolspec January 2017 vol. 5 no. 1 doi:10.1128/microbiolspec.MCHD-0038-2016
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2
FIGURE 2

hematopoiesis. Hematopoiesis in starts during embryogenesis and continues till the adult stage. (a) Embryonic hematopoiesis. Schematic presentations of stage 10 and 16 embryos with the head on the left and the ventral axis facing down. The gut is shown in dashed lines (dv, dorsal vessel; e, esophagus; pv, proventriculus; mg, midgut; hg, hindgut). embryonic hemocyte progenitors, the prohemocytes, emanate from the procephalic mesoderm. After their differentiation, plasmatocytes (shown in blue) migrate to populate the whole embryo, whereas crystal cells (shown in yellow) remain around their points of origin and populate the proventriculus. (b) Larval hematopoiesis. Schematic presentation of a third instar larva with the head at left and the ventral axis facing down (top). In the larvae, embryonic hemocytes proliferate within the hematopoietic pockets (HPs), giving rise to sessile hemocytes, which could differentiate into plasmatocytes but also crystal cells and lamellocytes in the case of parasitization. In the larvae, another center of hematopoiesis, the lymph gland (LG), originates from an anlage of the thoracic mesoderm and differentiates into four (to six) bilaterally paired lobes along the anterior part of the dorsal vessel. The cellular organization of the LG is shown (bottom). The primary lobes are indicated in red, the posterior signaling center (PSC) in purple, and the posterior lobes in blue. Within the primary lobes, core progenitor hemocytes are shown in purple, progenitors in dark blue, and plasmatocytes and crystal cells in light blue and yellow, respectively. LG-derived hemocytes are normally released at the beginning of pupariation only under immune challenge. A detailed description of signaling pathways controlling hematopoiesis is reviewed in reference 62 . (c) Adult hematopoiesis. Four hematopoietic hubs (HH) have been identified in the dorsal part of adult fly abdomen. These hubs enclose hematopoietic progenitors, derived from the third and fourth lobes of the LG, together with differentiated hemocytes of embryonic and larval origins.

Source: microbiolspec January 2017 vol. 5 no. 1 doi:10.1128/microbiolspec.MCHD-0038-2016
Permissions and Reprints Request Permissions
Download as Powerpoint

Tables

Generic image for table
TABLE 1

phagocytic receptors and opsonins and their corresponding ligands

Source: microbiolspec January 2017 vol. 5 no. 1 doi:10.1128/microbiolspec.MCHD-0038-2016

Supplemental Material

No supplementary material available for this content.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error