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Drosophila melanogaster embryonic haemocytes: masters of multitasking

Key Points

  • Drosophila melanogaster has three types of haemocyte: plasmatocytes, crystal cells and lamellocytes. In the embryo, 95% of all haemocytes are plasmatocytes.

  • D. melanogaster haemocyte development occurs in two waves: the first within the embryonic head mesoderm and the second within a specialized organ in the larva known as the lymph gland.

  • Many parallels exist between blood-cell development in flies and vertebrates, and many of the transcription factors that are required for haematopoiesis in D. melanogaster are homologues of genes that are central to vertebrate haematopoiesis.

  • Embryonic plasmatocytes are professional phagocytes and are responsible for the clearance of all apoptotic-cell debris in the embryo.

  • Plasmatocytes are highly motile cells. During development they migrate from their point of origin and disperse throughout the embryo and will also rapidly migrate towards epithelial wounds in an inflammatory-like response.

  • Embryonic plasmatocytes are a main source of extracellular matrix proteins and are required for the normal development of some tissues, such as the central nervous system and developing gut.

Abstract

Drosophila melanogaster haemocytes constitute the cellular arm of a robust innate immune system in flies. In the adult and larva, these cells operate as the first line of defence against invading microorganisms: they phagocytose pathogens and produce antimicrobial peptides. However, in the sterile environment of the embryo, these important immune functions are largely redundant. Instead, throughout development, embryonic haemocytes are occupied with other tasks: they undergo complex migrations and carry out several non-immune functions that are crucial for successful embryogenesis.

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Figure 1: Haemocyte development in Drosophila melanogaster.
Figure 2: Transcriptional regulation of haematopoiesis.
Figure 3: Developmental migrations.
Figure 4: Haemocyte migration mechanisms.
Figure 5: Multiple haemocyte stimuli.

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Acknowledgements

The authors would like to thank B. Stramer for helpful feedback on the manuscript. W.W. is funded by the Wellcome Trust and A.J. is funded by Fundação para a Ciência e a Tecnologia, Instituto Gulbenkian de Ciência and by the Network of Excellence Cells into Organs, supported by the European Union Framework Programme 6.

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Glossary

Mesoderm

A morphologically distinct cell layer that can be recognized in the early embryos of most bilaterian phyla. It gives rise to tissues that are interposed between ectodermal and endodermal epithelia, including muscle, connective and blood tissue.

Anlage

An initial clustering of embryonic cells that serves as a foundation from which a body part or an organ develops.

Proventriculus

A structure that is located at the caudal end of the oesophagus, formed at the junction of the foregut and the midgut. It serves as a valve that regulates the passage of food into the midgut.

Melanization

A reaction that is used as an immune mechanism in arthropods to encapsulate and kill microbial pathogens. Arthropod melanization is controlled by a cascade of serine proteases that ultimately activates the enzyme prophenoloxidase, which, in turn, catalyses the synthesis of melanin.

Unipotent

A cell that has the capacity to differentiate into only one type of tissue or cell.

Oligopotent

A cell that has the capacity to give rise to several cell types.

Haemangioblast

A multipotent cell that is a common precursor to haematopoietic and endothelial cells. In Drosophila melanogaster, haemangioblasts can give rise to haemocytes or to heart and aorta cells.

Haemocoel

A cavity or series of spaces between the organs of organisms with open circulatory systems.

Gram-positive bacteria

Gram staining is an empirical method of differentiating bacterial species into two groups based on structural differences within their cell walls. Gram-positive bacteria are those that retain the dark-blue dye crystal violet, whereas Gram-negative bacteria do not.

Phagocyte

A cell that ingests and destroys cell debris or foreign matter, such as microorganisms, through a process known as phagocytosis.

Phosphatidylserine receptor

The receptor for phosphatidylserine. It is expressed in phagocytic cells and is used for the detection of apoptotic cells.

Filopodium

A thin rod-like structure that extends from the cell membrane. It contains long actin filaments that are crosslinked into bundles by actin-binding proteins.

Lamellipodium

A two-dimensional actin meshwork that extends from the leading edge of many migrating cells.

Cofilin

An actin-binding protein that causes depolymerization at the minus end of actin filaments.

Haemolymph

A combination of lymph and interstitial fluid that circulates through the haemocoel.

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Wood, W., Jacinto, A. Drosophila melanogaster embryonic haemocytes: masters of multitasking. Nat Rev Mol Cell Biol 8, 542–551 (2007). https://doi.org/10.1038/nrm2202

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