Browse > Article
http://dx.doi.org/10.14348/molcells.2022.2039

Intrinsic and Extrinsic Regulation of Hematopoiesis in Drosophila  

Koranteng, Ferdinand (Department of Life Science, Hanyang University)
Cho, Bumsik (Department of Life Science, Hanyang University)
Shim, Jiwon (Department of Life Science, Hanyang University)
Abstract
Drosophila melanogaster lymph gland, the primary site of hematopoiesis, contains myeloid-like progenitor cells that differentiate into functional hemocytes in the circulation of pupae and adults. Fly hemocytes are dynamic and plastic, and they play diverse roles in the innate immune response and wound healing. Various hematopoietic regulators in the lymph gland ensure the developmental and functional balance between progenitors and mature blood cells. In addition, systemic factors, such as nutrient availability and sensory inputs, integrate environmental variabilities to synchronize the blood development in the lymph gland with larval growth, physiology, and immunity. This review examines the intrinsic and extrinsic factors determining the progenitor states during hemocyte development in the lymph gland and provides new insights for further studies that may extend the frontier of our collective knowledge on hematopoiesis and innate immunity.
Keywords
Drosophila hematopoiesis; hemocyte differentiation; inter-organ regulation; lymph gland; niche regulation; progenitor cell maintenance;
Citations & Related Records
Times Cited By KSCI : 2  (Citation Analysis)
연도 인용수 순위
1 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
2 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
3 Tepass, U., Fessler, L.I., Aziz, A., and Hartenstein, V. (1994). Embryonic origin of hemocytes and their relationship to cell death in Drosophila. Development 120, 1829-1837.   DOI
4 Yamashita, M., Dellorusso, P.V., Olson, O.C., and Passegue, E. (2020). Dysregulated haematopoietic stem cell behaviour in myeloid leukaemogenesis. Nat. Rev. Cancer 20, 365-382.   DOI
5 Kanwal, A., Joshi, P.V., Mandal, S., and Mandal, L. (2021). Ubx-Collier signaling cascade maintains blood progenitors in the posterior lobes of the Drosophila larval lymph gland. PLoS Genet. 17, e1009709.   DOI
6 Kim, H.J., Park, J.W., Kang, J.Y., and Seo, S.B. (2021). Negative regulation of erythroid differentiation via the CBX8-TRIM28 axis. Mol. Cells 44, 444-457.   DOI
7 Krzemien, J., Crozatier, M., and Vincent, A. (2010a). Ontogeny of the Drosophila larval hematopoietic organ, hemocyte homeostasis and the dedicated cellular immune response to parasitism. Int. J. Dev. Biol. 54, 1117-1125.   DOI
8 Krzemien, J., Oyallon, J., Crozatier, M., and Vincent, A. (2010b). Hematopoietic progenitors and hemocyte lineages in the Drosophila lymph gland. Dev. Biol. 346, 310-319.   DOI
9 Lan, W., Liu, S., Zhao, L., and Su, Y. (2020). Regulation of Drosophila hematopoiesis in lymph gland: from a developmental signaling point of view. Int. J. Mol. Sci. 21, 5246.   DOI
10 Kwon, J.Y., Dahanukar, A., Weiss, L.A., and Carlson, J.R. (2007). The molecular basis of CO2 reception in Drosophila. Proc. Natl. Acad. Sci. U. S. A. 104, 3574-3578.   DOI
11 Lanot, R., Zachary, D., Holder, F., and Meister, M. (2001). Postembryonic hematopoiesis in Drosophila. Dev. Biol. 230, 243-257.   DOI
12 Lebestky, T., Jung, S.H., and Banerjee, U. (2003). A Serrate-expressing signaling center controls Drosophila hematopoiesis. Genes Dev. 17, 348-353.   DOI
13 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
14 Lemaitre, B. and Hoffmann, J. (2007). The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 25, 697-743.   DOI
15 Letourneau, M., Lapraz, F., Sharma, A., Vanzo, N., Waltzer, L., and Crozatier, M. (2016). Drosophila hematopoiesis under normal conditions and in response to immune stress. FEBS Lett. 590, 4034-4051.   DOI
16 Lo, P.C., Skeath, J.B., Gajewski, K., Schulz, R.A., and Frasch, M. (2002). Homeotic genes autonomously specify the anteroposterior subdivision of the Drosophila dorsal vessel into aorta and heart. Dev. Biol. 251, 307-319.   DOI
17 Meister, M. and Lagueux, M. (2003). Drosophila blood cells. Cell. Microbiol. 5, 573-580.   DOI
18 Madhwal, S., Shin, M., Kapoor, A., Goyal, M., Joshi, M.K., Ur Rehman, P.M., Gor, K., Shim, J., and Mukherjee, T. (2020). Metabolic control of cellular immune-competency by odors in Drosophila. Elife 9, e60376.   DOI
19 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
20 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
21 Mills, R. and King, R. (1965). The pericardial cells of Drosophila melanogaster. Q. J. Microsc. Sci. 106, 261-268.
22 Minakhina, S. and Steward, R. (2010). Hematopoietic stem cells in Drosophila. Development 137, 27-31.   DOI
23 Sinenko, S.A., Shim, J., and Banerjee, U. (2011). Oxidative stress in the haematopoietic niche regulates the cellular immune response in Drosophila. EMBO Rep. 13, 83-89.   DOI
24 Mondal, B.C., Mukherjee, T., Mandal, L., Evans, C.J., Sinenko, S.A., Martinez-Agosto, J.A., and Banerjee, U. (2011). Interaction between differentiating cell- and niche-derived signals in hematopoietic progenitor maintenance. Cell 147, 1589-1600.   DOI
25 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
26 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
27 Wang, Y., Pu, Y., and Shen, P. (2013). Neuropeptide-gated perception of appetitive olfactory inputs in Drosophila larvae. Cell Rep. 3, 820-830.   DOI
28 Na, J. and Cagan, R. (2013). The Drosophila nephrocyte: back on stage. J. Am. Soc. Nephrol. 24, 161-163.   DOI
29 Crozatier, M. and Meister, M. (2007). Drosophila haematopoiesis. Cell. Microbiol. 9, 1117-1126.   DOI
30 Shim, J., Mukherjee, T., Mondal, B.C., Liu, T., Young, G.C., Wijewarnasuriya, D.P., and Banerjee, U. (2013). Olfactory control of blood progenitor maintenance. Cell 155, 1141-1153.   DOI
31 Snodgrass, R.E. (1954). Insect Metamorphosis (Washington: Smithsonian Institution).
32 Spratford, C.M., Goins, L.M., Chi, F., Girard, J.R., Macias, S.N., Ho, V.W., and Banerjee, U. (2021). Intermediate progenitor cells provide a transition between hematopoietic progenitors and their differentiated descendants. Development 148, dev200216.   DOI
33 Petraki, S., Alexander, B., and Bruckner, K. (2015). Assaying blood cell populations of the Drosophila melanogaster larva. J. Vis. Exp. (105), 52733.
34 Orkin, S.H. and Zon, L.I. (2002). Hematopoiesis and stem cells: plasticity versus developmental heterogeneity. Nat. Immunol. 3, 323-328.   DOI
35 Oyallon, J., Vanzo, N., Krzemien, J., Morin-Poulard, I., Vincent, A., and 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
36 Pennetier, D., Oyallon, J., Morin-Poulard, I., Dejean, S., Vincent, A., and 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.   DOI
37 Rizki, M.T. and Rizki, R.M. (1959). Functional significance of the crystal cells in the larva of Drosophila melanogaster. J. Biophys. Biochem. Cytol. 5, 235-240.   DOI
38 Tokusumi, Y., Tokusumi, T., Shoue, D.A., and Schulz, R.A. (2012). Gene regulatory networks controlling hematopoietic progenitor niche cell production and differentiation in the Drosophila lymph gland. PLoS One 7, e41604.   DOI
39 Sanchez Bosch, P., Makhijani, K., Herboso, L., Gold, K.S., Baginsky, R., Woodcock, K.J., Alexander, B., Kukar, K., Corcoran, S., Jacobs, T., et al. (2019). Adult Drosophila lack hematopoiesis but rely on a blood cell reservoir at the respiratory epithelia to relay infection signals to surrounding tissues. Dev. Cell 51, 787-803.e5.   DOI
40 Sharma, S.K., Ghosh, S., Geetha, A.R., Mandal, S., and Mandal, L. (2019). Cell adhesion-mediated actomyosin assembly regulates the activity of Cubitus interruptus for hematopoietic progenitor maintenance in Drosophila. Genetics 212, 1279-1300.   DOI
41 van Breugel, F., Huda, A., and Dickinson, M.H. (2018). Distinct activity-gated pathways mediate attraction and aversion to CO2 in Drosophila. Nature 564, 420-424.   DOI
42 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
43 Makki, R., Meister, M., Pennetier, D., Ubeda, J.M., Braun, A., Daburon, V., Krzemien, J., Bourbon, H.M., Zhou, R., Vincent, A., et al. (2010). A short receptor downregulates JAK/STAT signalling to control the Drosophila cellular immune response. PLoS Biol. 8, e1000441.   DOI
44 Owusu-Ansah, E. and Banerjee, U. (2009). Reactive oxygen species prime Drosophila haematopoietic progenitors for differentiation. Nature 461, 537-541.   DOI
45 Rizki, M.T.M. (1957). Alterations in the haemocyte population of Drosophila melanogaster. J. Morphol. 100, 437-458.   DOI
46 Swain, A., Inoue, T., Tan, K.S., Nakanishi, Y., and Sugiyama, D. (2014). Intrinsic and extrinsic regulation of mammalian hematopoiesis in the fetal liver. Histol. Histopathol. 29, 1077-1082.
47 Wood, W. and Jacinto, A. (2007). Drosophila melanogaster embryonic haemocytes: masters of multitasking. Nat. Rev. Mol. Cell Biol. 8, 542-551.   DOI
48 Zhang, C.U., Blauwkamp, T.A., Burby, P.E., and Cadigan, K.M. (2014). Wnt-mediated repression via bipartite DNA recognition by TCF in the Drosophila hematopoietic system. PLoS Genet. 10, e1004509.   DOI
49 Zhu, J. and Emerson, S.G. (2002). Hematopoietic cytokines, transcription factors and lineage commitment. Oncogene 21, 3295-3313.   DOI
50 Ramesh, P., Dey, N.S., Kanwal, A., Mandal, S., and Mandal, L. (2021). Relish plays a dynamic role in the niche to modulate Drosophila blood progenitor homeostasis in development and infection. Elife 10, e67158.   DOI
51 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
52 Boulan, L., Milan, M., and Leopold, P. (2015). The systemic control of growth. Cold Spring Harb. Perspect. Biol. 7, a019117.   DOI
53 Banerjee, U., Girard, J.R., Goins, L.M., and Spratford, C.M. (2019). Drosophila as a genetic model for hematopoiesis. Genetics 211, 367-417.   DOI
54 Baron, M.H., Isern, J., and Fraser, S.T. (2012). The embryonic origins of erythropoiesis in mammals. Blood 119, 4828-4837.   DOI
55 Benmimoun, B., Polesello, C., Waltzer, L., and Haenlin, M. (2012). Dual role for Insulin/TOR signaling in the control of hematopoietic progenitor maintenance in Drosophila. Development 139, 1713-1717.   DOI
56 Chavakis, T., Mitroulis, I., and Hajishengallis, G. (2019). Hematopoietic progenitor cells as integrative hubs for adaptation to and fine-tuning of inflammation. Nat. Immunol. 20, 802-811.   DOI
57 Cho, B., Yoon, S.H., Lee, D., Koranteng, F., Tattikota, S.G., Cha, N., Shin, M., Do, H., Hu, Y., Oh, S.Y., et al. (2020). Single-cell transcriptome maps of myeloid blood cell lineages in Drosophila. Nat. Commun. 11, 4483.   DOI
58 Dzierzak, E. and Bigas, A. (2018). Blood development: hematopoietic stem cell dependence and independence. Cell Stem Cell 22, 639-651.   DOI
59 Ferguson, G.B. and Martinez-Agosto, J.A. (2014). Kicking it up a Notch for the best in show: Scalloped leads Yorkie into the haematopoietic arena. Fly (Austin) 8, 206-217.   DOI
60 Goyal, M., Tomar, A., Madhwal, S., and Mukherjee, T. (2022). Blood progenitor redox homeostasis through olfaction-derived systemic GABA in hematopoietic growth control in Drosophila. Development 149, dev199550.   DOI
61 Rugendorff, A., Younossi-Hartenstein, A., and Hartenstein, V. (1994). Embryonic origin and differentiation of the Drosophila heart. Rouxs Arch. Dev. Biol. 203, 266-280.   DOI
62 Arrese, E.L. and Soulages, J.L. (2010). Insect fat body: energy, metabolism, and regulation. Annu. Rev. Entomol. 55, 207-225.   DOI
63 Benmimoun, B., Polesello, C., Haenlin, M., and 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.   DOI
64 Crozatier, M. and Vincent, A. (2011). Drosophila: a model for studying genetic and molecular aspects of haematopoiesis and associated leukaemias. Dis. Model. Mech. 4, 439-445.   DOI
65 Ho, K.Y.L., Khadilkar, R.J., Carr, R.L., and Tanentzapf, G. (2021). A gap-junction-mediated, calcium-signaling network controls blood progenitor fate decisions in hematopoiesis. Curr. Biol. 31, 4697-4712.e6.   DOI
66 Jones, W.D., Cayirlioglu, P., Grunwald Kadow, I., and Vosshall, L.B. (2007). Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature 445, 86-90.   DOI
67 Keebaugh, E. and Schlenke, T. (2014). Insights from natural host-parasite interactions: the Drosophila model. Dev. Comp. Immunol. 42, 111-123.   DOI
68 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
69 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
70 Blanco-Obregon, D., Katz, M.J., Durrieu, L., Gandara, L., and Wappner, P. (2020). Context-specific functions of Notch in Drosophila blood cell progenitors. Dev. Biol. 462, 101-115.   DOI
71 Crossley, A.C. (1972). The ultrastructure and function of pericardial cells and other nephrocytes in an insect: Calliphora erythrocephala. Tissue Cell 4, 529-560.   DOI
72 Girard, J.R., Goins, L.M., Vuu, D.M., Sharpley, M.S., Spratford, C.M., Mantri, S.R., and Banerjee, U. (2021). Paths and pathways that generate cell-type heterogeneity and developmental progression in hematopoiesis. Elife 10, e67516.   DOI
73 Destalminil-Letourneau, M., Morin-Poulard, I., Tian, Y., Vanzo, N., and Crozatier, M. (2021). The vascular niche controls Drosophila hematopoiesis via fibroblast growth factor signaling. Elife 10, e64672.   DOI
74 Makhijani, K. and Bruckner, K. (2012). Of blood cells and the nervous system: hematopoiesis in the Drosophila larva. Fly (Austin) 6, 254-260.   DOI
75 Jung, S.H., Evans, C.J., Uemura, C., and Banerjee, U. (2005). The Drosophila lymph gland as a developmental model of hematopoiesis. Development 132, 2521-2533.   DOI
76 Lebestky, T., Chang, T., Hartenstein, V., and Banerjee, U. (2000). Specification of Drosophila hematopoietic lineage by conserved transcription factors. Science 288, 146-149.   DOI
77 Carton, Y., Poirie, M., and Nappi, A.J. (2008). Insect immune resistance to parasitoids. Insect Sci. 15, 67-87.   DOI
78 Vermehren-Schmaedick, A., Ainsley, J.A., Johnson, W.A., Davies, S.A., and Morton, D.B. (2010). Behavioral responses to hypoxia in Drosophila larvae are mediated by atypical soluble guanylyl cyclases. Genetics 186, 183-196.   DOI
79 Dey, N.S., Ramesh, P., Chugh, M., Mandal, S., and Mandal, L. (2019). Correction: Dpp dependent Hematopoietic stem cells give rise to Hh dependent blood progenitors in larval lymph gland of Drosophila. Elife 8, e51742.   DOI
80 Brogiolo, W., Stocker, H., Ikeya, T., Rintelen, F., Fernandez, R., and Hafen, E. (2001). An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control. Curr. Biol. 11, 213-221.   DOI
81 Hao, Y. and Jin, L.H. (2017). Dual role for Jumu in the control of hematopoietic progenitors in the Drosophila lymph gland. Elife 6, e25094.   DOI
82 Durand, C. and Dzierzak, E. (2005). Embryonic beginnings of adult hematopoietic stem cells. Haematologica 90, 100-108.
83 El Shatoury, H.H. (1955). The structure of the lymph glands ofDrosophila larvae. Wilhelm Roux Arch. Entwickl. Mech. Org. 147, 489-495.   DOI
84 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
85 Ferguson, G.B. and Martinez-Agosto, J.A. (2017). The TEAD family transcription factor Scalloped regulates blood progenitor maintenance and proliferation in Drosophila through PDGF/VEGFR receptor (Pvr) signaling. Dev. Biol. 425, 21-32.   DOI
86 Graham, P. and Pick, L. (2017). Drosophila as a model for diabetes and diseases of insulin resistance. Curr. Top. Dev. Biol. 121, 397-419.   DOI
87 Holz, A., Bossinger, B., Strasser, T., Janning, W., and Klapper, R. (2003). The two origins of hemocytes in Drosophia. Development 130, 4955-4962.   DOI
88 Honti, V., Csordas, G., Kurucz, E., Markus, R., and Ando, I. (2014). The cell-mediated immunity of Drosophila melanogaster: hemocyte lineages, immune compartments, microanatomy and regulation. Dev. Comp. Immunol. 42, 47-56.   DOI
89 Rodrigues, D., Renaud, Y., VijayRaghavan, K., Waltzer, L., and Inamdar, M.S. (2021). Differential activation of JAK-STAT signaling reveals functional compartmentalization in Drosophila blood progenitors. Elife 10, e61409.   DOI
90 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 (Pt 1), 135-142.   DOI
91 Shim, J., Mukherjee, T., and Banerjee, U. (2012). Direct sensing of systemic and nutritional signals by haematopoietic progenitors in Drosophila. Nat. Cell Biol. 14, 394-400.   DOI