Browse > Article
http://dx.doi.org/10.14348/molcells.2019.0249

The Role of Lozenge in Drosophila Hematopoiesis  

Koranteng, Ferdinand (Department of Life Science, Hanyang University)
Cha, Nuri (Department of Life Science, Hanyang University)
Shin, Mingyu (Department of Life Science, Hanyang University)
Shim, Jiwon (Department of Life Science, Hanyang University)
Publication Information
Molecules and Cells / v.43, no.2, 2020 , pp. 114-120 More about this Journal
Abstract
Drosophila hematopoiesis is comparable to mammalian differentiation of myeloid lineages, and therefore, has been a useful model organism in illustrating the molecular and genetic basis for hematopoiesis. Multiple novel regulators and signals have been uncovered using the tools of Drosophila genetics. A Runt domain protein, lozenge, is one of the first players recognized and closely studied in the hematopoietic lineage specification. Here, we explore the role of lozenge in determination of prohemocytes into a special class of hemocyte, namely the crystal cell, and discuss molecules and signals controlling the lozenge function and its implication in immunity and stress response. Given the highly conserved nature of Runt domain in both invertebrates and vertebrates, studies in Drosophila will enlighten our perspectives on Runx-mediated development and pathologies.
Keywords
crystal cells; Drosophila melanogaster; hematopoiesis; lozenge; lymph gland; melanization; prophenoloxidase; RUNX;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Dormand, E.L. and Brand, A.H. (1998). Runt determines cell fates in the Drosophila embryonic CNS. Development 125, 1659-1667.   DOI
2 Dudzic, J.P., Kondo, S., Ueda, R., Bergman, C.M., and Lemaitre, B. (2015). Drosophila innate immunity: regional and functional specialization of prophenoloxidases. BMC Biol. 13, 81.   DOI
3 Duffy, J.B. and Gergen, J.P. (1991). The Drosophila segmentation gene runt acts as a position-specific numerator element necessary for the uniform expression of the sex-determining gene Sex-lethal. Genes Dev. 5, 2176-2187.   DOI
4 Duffy, J.B., Kania, M.A., and Gergen, J.P. (1991). Expression and function of the Drosophila gene runt in early stages of neural development. Development (Cambridge, England) 113, 1223.   DOI
5 Duvic, B., Hoffmann, J.A., Meister, M., and Royet, J. (2002). Notch signaling controls lineage specification during Drosophila larval hematopoiesis. Curr. Biol. 12, 1923-1927.   DOI
6 Elrod-Erickson, M., Mishra, S., and Schneider, D. (2000). Interactions between the cellular and humoral immune responses in Drosophila. Curr. Biol. 10, 781-784.   DOI
7 Evans, C.J., Hartenstein, V., and Banerjee, U. (2003). Thicker than blood: conserved mechanisms in Drosophila and vertebrate hematopoiesis. Dev. Cell. 5, 673-690.   DOI
8 Ferguson, G.B. and Martinez-Agosto, J.A. (2014a). Kicking it up a notch for the best in show: scalloped leads Yorkie into the haematopoietic arena. Fly (Austin) 8, 206-217.   DOI
9 Ferguson, G.B. and Martinez-Agosto, J.A. (2014b). Yorkie and scalloped signaling regulates notch-dependent lineage specification during Drosophila hematopoiesis. Curr. Biol. 24, 2665-2672.   DOI
10 Moreira, S., Stramer, B., Evans, I., Wood, W., and Martin, P. (2010). Prioritization of competing damage and developmental signals by migrating macrophages in the Drosophila embryo. Curr. Biol. 20, 464-470.   DOI
11 Morin-Poulard, I., Sharma, A., Louradour, I., Vanzo, N., Vincent, A., and Crozatier, M. (2016). Vascular control of the Drosophila haematopoietic microenvironment by Slit/Robo signalling. Nat. Commun. 7, 11634.   DOI
12 Mukherjee, T., Kim, W.S., Mandal, L., and Banerjee, U. (2011). Interaction between Notch and Hif-alpha in development and survival of Drosophila blood cells. Science 332, 1210-1213.   DOI
13 Muratoglu, S., Hough, B., Mon, S.T., and Fossett, N. (2007). The GATA factor Serpent cross-regulates lozenge and u-shaped expression during Drosophila blood cell development. Dev. Biol. 311, 636-649.   DOI
14 Nam, H.J., Jang, I.H., Asano, T., and Lee, W.J. (2008). Involvement of prophenoloxidase 3 in lamellocyte-mediated spontaneous melanization in Drosophila. Mol. Cells 26, 606-610.
15 Owusu-Ansah, E. and Banerjee, U. (2009). Reactive oxygen species prime Drosophila haematopoietic progenitors for differentiation. Nature 461, 537-541.   DOI
16 Okuda, T., van Deursen, J., Hiebert, S.W., Grosveld, G., and Downing, J.R. (1996). AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell 84, 321-330.   DOI
17 Oliver, C.P. (1946). A study of the relationship between facet irregularities and eye color in lozenge alleles of Drosophila melanogaster. Anat. Rec. 94, 416.
18 Olofsson, B. and Page, D.T. (2005). Condensation of the central nervous system in embryonic Drosophila is inhibited by blocking hemocyte migration or neural activity. Dev. Biol. 279, 233-243.   DOI
19 Anderson, R.C. (1945). A study of the factors affecting fertility of lozenge females of Drosophila melanogaster. Genetics 30, 280-296.   DOI
20 Agaisse, H., Petersen, U.M., Boutros, M., Mathey-Prevot, B., and Perrimon, N. (2003). Signaling role of hemocytes in Drosophila JAK/STAT-dependent response to septic injury. Dev. Cell 5, 441-450.   DOI
21 Ashburner, M. and Novitski, E. (1976). Genetics and Biology of Drosophila (London: Academic Press).
22 Bangs, P., Franc, N., and White, K. (2000). Molecular mechanisms of cell death and phagocytosis in Drosophila. Cell Death Differ. 7, 1027-1034.   DOI
23 Gold, K.S. and Bruckner, K. (2015). Macrophages and cellular immunity in Drosophila melanogaster. Semin. Immunol. 27, 357-368.   DOI
24 Flores, G.V., Daga, A., Kalhor, H.R., and Banerjee, U. (1998). Lozenge is expressed in pluripotent precursor cells and patterns multiple cell types in the Drosophila eye through the control of cell-specific transcription factors. Development 125, 3681-3687.   DOI
25 Fossett, N., Hyman, K., Gajewski, K., Orkin, S.H., and Schulz, R.A. (2003). Combinatorial interactions of Serpent, lozenge, and U-shaped regulate crystal cell lineage commitment during Drosophila hematopoiesis. Proc. Natl. Acad. Sci. U. S. A. 100, 11451-11456.   DOI
26 Fossett, N., Tevosian, S.G., Gajewski, K., Zhang, Q., Orkin, S.H., and Schulz, R.A. (2001). The friend of GATA proteins U-shaped, FOG-1, and FOG-2 function as negative regulators of blood, heart, and eye development in Drosophila. Proc. Natl. Acad. Sci. U. S. A. 98, 7342-7347.   DOI
27 Galko, M.J. and Krasnow, M.A. (2004). Cellular and genetic analysis of wound healing in Drosophila larvae. PLoS Biol. 2, E239.   DOI
28 Gergen, J.P. and Wieschaus, E. (1986). Dosage requirements for runt in the segmentation of Drosophila embryos. Cell 45, 289-299.   DOI
29 Grigorian, M., Mandal, L., and Hartenstein, V. (2011). Hematopoiesis at the onset of metamorphosis: terminal differentiation and dissociation of the Drosophila lymph gland. Dev. Genes Evol. 221, 121-131.   DOI
30 Holz, A., Bossinger, B., Strasser, T., Janning, W., and Klapper, R. (2003). The two origins of hemocytes in Drosophila. Development 130, 4955-4962.   DOI
31 Ingham, P. and Gergen, P. (1988). Interactions between the pair-rule genes runt, hairy, even-skipped and fushi tarazu and the establishment of periodic pattern in the Drosophila embryo. Development (Cambridge, England) 104, 51.   DOI
32 Rabbitts, T.H. (1994). Chromosomal translocations in human cancer. Nature 372, 143-149.   DOI
33 Peeples, E.E., Barnett, D.R., and Oliver, C.P. (1968). Phenol oxidases of a lozenge mutant of Drosophila. Science (New York, NY) 159, 548-552.   DOI
34 Peeples, E.E., Geisler, A., Whitcraft, C.J., and Oliver, C.P. (1969a). Activity of phenol oxidases at the puparium formation stage in development of nineteen lozenge mutants of Drosophila melanogaster. Biochem. Genet. 3, 563-569.   DOI
35 Peeples, E.E., Geisler, A., Whitcraft, C.J., and Oliver, C.P. (1969b). Comparative studies of phenol oxidase activity during pupal development of three lozenge mutants (lz8,lz,lzk) of Drosophila melanogaster. Genetics 62, 161-170.   DOI
36 Ramet, M., Lanot, R., Zachary, D., and Manfruelli, P. (2002). JNK signaling pathway is required for efficient wound healing in Drosophila. Dev. Biol. 241, 145-156.   DOI
37 Rizki, M.T.M. (1957). Alterations in the haemocyte population of Drosophila melanogaster. J. Morphol. 100, 437-458.   DOI
38 Razzell, W., Evans, I.R., Martin, P., and Wood, W. (2013). Calcium flashes orchestrate the wound inflammatory response through DUOX activation and hydrogen peroxide release. Curr. Biol. 23, 424-429.   DOI
39 Rennert, J., Coffman, J.A., Mushegian, A.R., and Robertson, A.J. (2003). The evolution of Runx genes I. A comparative study of sequences from phylogenetically diverse model organisms. BMC Evol. Biol. 3, 4.   DOI
40 Rizki, M.T. (1960). Melanotic tumor formation in Drosophila. J. Morphol. 106, 147-157.   DOI
41 Rizki, R.M. and Rizki, T.M. (1974). Basement membrane abnormalities in melanotic tumor formation of Drosophila. Experientia 30, 543-546.   DOI
42 Bidla, G., Dushay, M.S., and Theopold, U. (2007). Crystal cell rupture after injury in Drosophila requires the JNK pathway, small GTPases and the TNF homolog Eiger. J. Cell Sci. 120, 1209-1215.   DOI
43 Bataille, L., Auge, B., Ferjoux, G., Haenlin, M., and Waltzer, L. (2005). Resolving embryonic blood cell fate choice in Drosophila: interplay of GCM and RUNX factors. Development (Cambridge, England) 132, 4635-4644.   DOI
44 Bernardoni, R., Vivancos, V., and Giangrande, A. (1997). glide/gcm is expressed and required in the scavenger cell lineage. Dev. Biol. 191, 118-130.   DOI
45 Berson, A., Goodman, L.D., Sartoris, A.N., Otte, C.G., Aykit, J.A., Lee, V.M., Trojanowski, J.Q., and Bonini, N.M. (2019). Drosophila Ref1/ALYREF regulates transcription and toxicity associated with ALS/FTD disease etiologies. Acta Neuropathol. Commun. 7, 65.   DOI
46 Binggeli, O., Neyen, C., Poidevin, M., and Lemaitre, B. (2014). Prophenoloxidase activation is required for survival to microbial infections in Drosophila. PLoS Pathog. 10, e1004067.   DOI
47 Blanco-Obregon, D.M., Katz, M.J., Durrieu, L., Gandara, L., and Wappner, P. (2019). Context-specific functions of notch in Drosophila blood cell progenitors. bioRxiv 82658.
48 Bras, S., Martin-Lanneree, S., Gobert, V., Auge, B., Breig, O., Sanial, M., Yamaguchi, M., Haenlin, M., Plessis, A., and Waltzer, L. (2012). Myeloid leukemia factor is a conserved regulator of RUNX transcription factor activity involved in hematopoiesis. Proc. Natl. Acad. Sci. U. S. A. 109, 4986-4991.   DOI
49 Canon, J. and Banerjee, U. (2000). Runt and Lozenge function in Drosophila development. Semin. Cell Dev. Biol. 11, 327-336.   DOI
50 Brehelin, M. (1982). Comparative study of structure and function of blood cells from two Drosophila species. Cell Tissue Res. 221, 607-615.   DOI
51 Krzemien, J., Oyallon, J., Crozatier, M., and Vincent, A. (2010). Hematopoietic progenitors and hemocyte lineages in the Drosophila lymph gland. Dev. Biol. 346, 310-319.   DOI
52 Jung, S.H., Evans, C.J., Uemura, C., and Banerjee, U. (2005). The Drosophila lymph gland as a developmental model of hematopoiesis. Development (Cambridge, England) 132, 2521.   DOI
53 Keebaugh, E. and Schlenke, T. (2013). Insights from natural host-parasite interactions: the Drosophila model. Dev. Comp. Immunol. 42, 111-123.   DOI
54 Krzemien, J., Dubois, L., Makki, R., Meister, M., Vincent, A., and Crozatier, M. (2007). Control of blood cell homeostasis in Drosophila larvae by the posterior signalling centre. Nature 446, 325-328.   DOI
55 Kulkarni, V., Khadilkar, R.J., Magadi, S.S., and Inamdar, M.S. (2011). Asrij maintains the stem cell niche and controls differentiation during Drosophila lymph gland hematopoiesis. PLoS One 6, e27667.   DOI
56 Laifook, J. (1966). The repair of wounds in the integument of insects. Phys. Ther. 46, 195-226.   DOI
57 Lanot, R., Zachary, D., Holder, F., and Meister, M. (2001). Postembryonic hematopoiesis in Drosophila. Dev. Biol. 230, 243-257.   DOI
58 Lebestky, T., Chang, T., Hartenstein, V., and Banerjee, U. (2000). Specification of Drosophila hematopoietic lineage by conserved transcription factors. Science 288, 146-149.   DOI
59 Lebestky, T., Jung, S.H., and Banerjee, U. (2003). A serrate-expressing signaling center controls Drosophila hematopoiesis. Genes Dev. 17, 348-353.   DOI
60 Leitao, A.B. and Sucena, E. (2015). Drosophila sessile hemocyte clusters are true hematopoietic tissues that regulate larval blood cell differentiation. eLife 4, e06166.   DOI
61 Rugendorff, A., Younossi-Hartenstein, A., and Hartenstein, V. (1994). Embryonic origin and differentiation of the Drosophila heart. Roux Arch. Dev. Biol. 203, 266-280.   DOI
62 Rizki, R.M. and Rizki, T.M. (1980). Hemocyte responses to implanted tissues in Drosophila melanogaster larvae. Wilehm Roux Arch. Dev. Biol. 189, 207-213.   DOI
63 Rizki, T.M., Rizki, R.M., and Grell, E.H. (1980). A mutant affecting the crystal cells in Drosophila melanogaster. Wilehm Roux Arch. Dev. Biol. 188, 91-99.   DOI
64 Robertson, C.W. (1936). The metamorphosis of Drosophila melanogaster, including an accurately timed account of the principal morphological changes. J. Morphol. 59, 351-399.   DOI
65 Sinenko, S.A., Mandal, L., Martinez-Agosto, J.A., and Banerjee, U. (2009). Dual role of wingless signaling in stem-like hematopoietic precursor maintenance in Drosophila. Dev. Cell 16, 756-763.   DOI
66 Russo, J., Dupas, S., Frey, F., Carton, Y., and Brehelin, M. (1996). Insect immunity: early events in the encapsulation process of parasitoid (Leptopilina boulardi) eggs in resistant and susceptible strains of Drosophila. Parasitology 112, 135-142.   DOI
67 Sanchez, L. and Nothiger, R. (1983). Sex determination and dosage compensation in Drosophila melanogaster: production of male clones in XX females. EMBO J. 2, 485-491.   DOI
68 Shrestha, R. and Gateff, E. (1982). Ultrastructure and cytochemistry of the cell-types in the tumorous hematopoietic organs and the hemolymph of the mutant lethal (1) malignant blood neoplasm (l(1)mbn) of Drosophila melanogaster (Drosophila/mutant blood cells/ultrastructure/cytochemistry). Dev. Growth Differ. 24, 83-98.   DOI
69 Snodgrass, R.E. (1954). Insect Metamorphosis (Washington D.C.: Smithsonian Institution).
70 Cerenius, L., Lee, B.L., and Soderhall, K. (2008). The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immun. 29, 263-271.   DOI
71 Cho, B., Spratford, C.M., Yoon, S., Cha, N., Banerjee, U., and Shim, J. (2018). Systemic control of immune cell development by integrated carbon dioxide and hypoxia chemosensation in Drosophila. Nat. Commun. 9, 2679.   DOI
72 Crew, J.R., Batterham, P., and Pollock, J.A. (1997). Developing compound eye in lozenge mutants of Drosophila: lozenge expression in the R7 equivalence group. Dev. Genes Evol. 206, 481-493.   DOI
73 Crozatier, M., Ubeda, J.M., Vincent, A., and Meister, M. (2004). Cellular immune response to parasitization in Drosophila requires the EBF orthologue collier. PLoS Biol. 2, E196.   DOI
74 Crute, B.E., Lewis, A.F., Wu, Z., Bushweller, J.H., and Speck, N.A. (1996). Biochemical and biophysical properties of the core-binding factor alpha2 (AML1) DNA-binding domain. J. Biol. Chem. 271, 26251-26260.   DOI
75 Daga, A., Karlovich, C.A., Dumstrei, K., and Banerjee, U. (1996). Patterning of cells in the Drosophila eye by Lozenge, which shares homologous domains with AML1. Genes Dev. 10, 1194-1205.   DOI
76 Lo Coco, F., Pisegna, S., and Diverio, D. (1997). The AML1 gene: a transcription factor involved in the pathogenesis of myeloid and lymphoid leukemias. Haematologica 82, 364-370.
77 De Gregorio, E., Han, S.J., Lee, W.J., Baek, M.J., Osaki, T., Kawabata, S., Lee, B.L., Iwanaga, S., Lemaitre, B., and Brey, P.T. (2002). An immune-responsive Serpin regulates the melanization cascade in Drosophila. Dev. Cell 3, 581-592.   DOI
78 Dey, N.S., Ramesh, P., Chugh, M., Mandal, S., and Mandal, L. (2016). Dpp dependent hematopoietic stem cells give rise to Hh dependent blood progenitors in larval lymph gland of Drosophila. eLife 5, e18295.   DOI
79 Carton, Y., Poirie, M., and Nappi, A.J. (2008). Insect immune resistance to parasitoids. Insect Sci. 15, 67-87.   DOI
80 Linford, N.J., Bilgir, C., Ro, J., and Pletcher, S.D. (2013). Measurement of lifespan in Drosophila melanogaster. J. Vis. Exp. 71, 50068.
81 Makhijani, K., Alexander, B., Tanaka, T., Rulifson, E., and Brückner, K. (2011). The peripheral nervous system supports blood cell homing and survival in the Drosophila larva. Development (Cambridge, England) 138, 5379.   DOI
82 Mandal, L., Banerjee, U., and 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.   DOI
83 Mandal, L., Martinez-Agosto, J.A., Evans, C.J., Hartenstein, V., and Banerjee, U. (2007). A hedgehog- and antennapedia-dependent niche maintains Drosophila haematopoietic precursors. Nature 446, 320-324.   DOI
84 Markus, R., Laurinyecz, B., Kurucz, E., Honti, V., Bajusz, I., Sipos, B., Somogyi, K., Kronhamn, J., Hultmark, D., and Ando, I. (2009). Sessile hemocytes as a hematopoietic compartment in Drosophila melanogaster. Proc. Natl. Acad. Sci. U. S. A. 106, 4805-4809.   DOI
85 Tang, H., Kambris, Z., Lemaitre, B., and Hashimoto, C. (2006). Two proteases defining a melanization cascade in the immune system of Drosophila. J. Biol. Chem. 281, 28097-28104.   DOI
86 Sorrentino, R.P., Carton, Y., and Govind, S. (2002). Cellular immune response to parasite infection in the Drosophila lymph gland is developmentally regulated. Dev. Biol. 243, 65-80.   DOI
87 Speck, N.A. and Terryl, S. (1995). A new transcription factor family associated with human leukemias. Crit. Rev. Eukaryot. Gene Expr. 5, 337-364.   DOI
88 Stocker, H. and Gallant, P. (2008). Getting started. In Drosophila: Methods and Protocols, C. Dahmann, ed. (Totowa, USA: Humana Press), pp. 27-44.
89 Milchanowski, A.B., Henkenius, A.L., Narayanan, M., Hartenstein, V., and Banerjee, U. (2004). Identification and characterization of genes involved in embryonic crystal cell formation during Drosophila hematopoiesis. Genetics 168, 325-339.   DOI
90 Miller, M., Chen, A., Gobert, V., Auge, B., Beau, M., Burlet-Schiltz, O., Haenlin, M., and Waltzer, L. (2017). Control of RUNX-induced repression of Notch signaling by MLF and its partner DnaJ-1 during Drosophila hematopoiesis. PLoS Genet. 13, e1006932.   DOI
91 Tepass, U., Fessler, L.I., Aziz, A., and Hartenstein, V. (1994). Embryonic origin of hemocytes and their relationship to cell death in Drosophila. Development (Cambridge, England) 120, 1829-1837.   DOI
92 Terriente-Felix, A., Li, J., Collins, S., Mulligan, A., Reekie, I., Bernard, F., Krejci, A., and Bray, S. (2013). Notch cooperates with Lozenge/Runx to lock haemocytes into a differentiation programme. Development 140, 926-937.   DOI
93 Waltzer, L., Ferjoux, G., Bataille, L., and Haenlin, M. (2003). Cooperation between the GATA and RUNX factors Serpent and Lozenge during Drosophila hematopoiesis. EMBO J 22, 6516-6525.   DOI
94 Wang, Q., Stacy, T., Binder, M., Marin-Padilla, M., Sharpe, A.H., and Speck, N.A. (1996). Disruption of the Cbfa2 gene causes necrosis and hemorrhaging in the central nervous system and blocks definitive hematopoiesis. Proc. Natl. Acad. Sci. U. S. A. 93, 3444.   DOI
95 Wood, W., Faria, C., and Jacinto, A. (2006). Distinct mechanisms regulate hemocyte chemotaxis during development and wound healing in Drosophila melanogaster. J. Cell Biol. 173, 405-416.   DOI