Skip to main content
SpringerLink
Log in

Hematopoiesis and hematopoietic organs in arthropods

  • Review
  • Published:
Development Genes and Evolution Aims and scope Submit manuscript

Abstract

Hemocytes (blood cells) are motile cells that move throughout the extracellular space and that exist in all clades of the animal kingdom. Hemocytes play an important role in shaping the extracellular environment and in the immune response. Developmentally, hemocytes are closely related to the epithelial cells lining the vascular system (endothelia) and the body cavity (mesothelia). In vertebrates and insects, common progenitors, called hemangioblasts, give rise to the endothelia and blood cells. In the adult animal, many differentiated hemocytes seem to retain the ability to proliferate; however, in most cases investigated closely, the bulk of hemocyte proliferation takes place in specialized hematopoietic organs. Hematopoietic organs provide an environment where undifferentiated blood stem cells are able to self-renew, and at the same time generate offspring that differentiate into different blood cell types. Hematopoiesis in vertebrates, taking place in the bone marrow, has been subject to intensive research by immunologists and stem cell biologists. Much less is known about blood cell formation in invertebrate animals. In this review, we will survey structural and functional properties of invertebrate hematopoietic organs, with a main focus on insects and other arthropod taxa. We will then discuss similarities, at the molecular and structural level, that are apparent when comparing the development of blood cells in hematopoietic organs of vertebrates and arthropods. Our comparative review is intended to elucidate aspects of the biology of blood stem cells that are more easily missed when focusing on one or a few model species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Agaisse H, Perrimon N (2004) The roles of JAK/STAT signaling in Drosophila immune responses. Immunol Rev 198:72–82

    Article  PubMed  CAS  Google Scholar 

  • Bauchau A (1981) Crustaceans. In: Ratcliffe NA, Rowley AF (ed) Invertebrate blood cells, vol 2. Academic Press, London, pp. 385–420

  • Böhm GA, Gersch M (1983) The hematopoietic character of the “cephalic gland” in the crayfish Orconectes limosus. Cen Comp Endocrinol 52:102–107

    Article  Google Scholar 

  • Boutros M, Agaisse H, Perrimon N (2002) Sequential activation of signaling pathways during innate immune responses in Drosophila. Dev Cell 3(5):711–722

    Article  PubMed  CAS  Google Scholar 

  • Brehelin M (1982) Comparative study of structure and function of blood cells from two Drosophila species. Cell Tissue Res 221(3):607–615

    PubMed  CAS  Google Scholar 

  • Choi K, Kennedy M, Kazarov A, Papadimitriou JC, Keller G (1998) A common precursor for hematopoietic and endothelial cells. Development 125(4):725–732

    PubMed  CAS  Google Scholar 

  • Cowden R, Curtis S (1981) Cephalopods. In: Ratcliffe NA, Rowley AF (ed) Invertebrate blood cells, vol 1. Academic Press, London, pp 301–321

    Google Scholar 

  • Crozatier M, Ubeda JM, Vincent A, Meister M (2004) Cellular immune response to parasitization in Drosophila requires the EBF orthologue collier. PLoS Biol 2(8):E196

    Article  PubMed  Google Scholar 

  • Cuenot L (1897) Les globules sanguins et les organes lymphides des invertebres. Arch D’Anat Microsc 1:153–192

    Google Scholar 

  • Dales R, Dixon L (1981) Polychaetes. In: Ratcliffe NA, Rowley AF (ed) Invertebrate blood cells, vol 1. Academic Press, London, pp 35–75

    Google Scholar 

  • Datta S, Kankel DR (1992) l(1)trol and l(1)devl, loci affecting the development of the adult central nervous system in Drosophila melanogaster. Genetics 130(3):523–537

    PubMed  CAS  Google Scholar 

  • Eckelbarger K (1976) Origin and development of the amoebocytes of Nicolea zostericola (Polychaeta: Terebellidae) with a discussion of their possible role in oogenesis. Mar Biol 36:169–182

    Article  Google Scholar 

  • Ermak T (1976) The hematogenic tissues of tunicates. In: Wright RK, Cooper EL (eds) Phylogeny of thymus and bone marrow–bursa cells. Elsevier, Amsterdam, pp 45–56

    Google Scholar 

  • Feir D, McClain E (1968) Mitotic activity of the circulating hemocytes of the large milkweed bug, Oncopeltus fasciatus. Ann Entomol Soc Amer 61:413–416

    Google Scholar 

  • Feir D, O’Connor GM Jr (1965) Mitotic activity in the hemocytes of Oncopeltus fasciatus (Dall). Exp Cell Res 39(2):637–642

    Article  PubMed  CAS  Google Scholar 

  • Francois J (1975) Hemocytes et organe hematopoietique de Thermobia domestica (packard) (Thysanura: Lepismatidae). International Journal of Insect Morphology and Embryology 4(6):477–494

    Article  Google Scholar 

  • 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(3):121–131

    Article  PubMed  Google Scholar 

  • Gupta A (1979) Hemocyte types: their structures, synonymies, interrelationships, and taxonomic significance. In: Gupta A (ed) Insect hemocytes. Cambridge University Press, Cambridge

    Chapter  Google Scholar 

  • Haegebarth A, Clevers H (2009) Wnt signaling, lgr5, and stem cells in the intestine and skin. Am J Pathol 174(3):715–721

    Article  PubMed  CAS  Google Scholar 

  • Han SS, Lee MH, Kim WK, Wago H, Yoe SM (1998) Hemocytic differentiation in hemopoietic organ of Bombyx mori larvae. Zoolog Sci 15(3):371–379

    Article  PubMed  CAS  Google Scholar 

  • Hinks C, Arnold J (1977) Haemopoiesis in Lepidoptera. II. The role of the haemopoietic organs. Can J Zool 55:1740–1755

    Article  Google Scholar 

  • Hoffmann JA (1970) [The hemopoietic organs of the two orthopterans Locusta migratoria and Gryllus bimaculatus]. Z Zellforsch Mikrosk Anat 106(3):451–472

    Article  PubMed  CAS  Google Scholar 

  • Hoffmann J, Zachary D, Hoffmann D, Brehelin M, Porte A (1979) Postembryonic development and differentiation: hemopoietic tissues and their functions in some insects. In: Gupta A (ed) Insect hemocytes. Cambridge University Press, Cambridge

    Google Scholar 

  • Huynh MH, Zhu SJ, Kollara A, Brown T, Winklbauer R, Ringuette M (2011) Knockdown of SPARC leads to decreased cell-cell adhesion and lens cataracts during post-gastrula development in Xenopus laevis. Dev Genes Evol 220(11-12):315–327

    Article  PubMed  CAS  Google Scholar 

  • Jeong KH, Lie KJ, Heyneman D (1983) The ultrastructure of the amebocyte-producing organ in Biomphalaria glabrata. Dev Comp Immunol 7(2):217–228

    Article  PubMed  CAS  Google Scholar 

  • Jiang H, Vilcinskas A, Kanost MR (2010) Immunity in lepidopteran insects. Adv Exp Med Biol 708:181–204

    Google Scholar 

  • Jones J (1970) Hemocytopoiesis in insects. In: Gordon A (ed) Regulation of hematopoiesis. Appleton, New York

    Google Scholar 

  • Joo K, Mun J, Lee K, Yu C, Kang S, Seo Y, Han S (2004) Three-dimensional reconstruction of hematopoietic organ of Bombyx mori larva. Entomol Res 34:291–298

    Article  Google Scholar 

  • Jung SH, Evans CJ, Uemura C, Banerjee U (2005) The Drosophila lymph gland as a developmental model of hematopoiesis. Development 132(11):2521–2533

    Article  PubMed  CAS  Google Scholar 

  • Kaaya GP, Ratcliffe NA (1982) Comparative study of hemocytes and associated cells of some medically important dipterans. J Morphol 173(3):351–365

    Article  PubMed  CAS  Google Scholar 

  • Krzemien 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(7133):325–328

    Article  PubMed  CAS  Google Scholar 

  • Krzemien J, Crozatier M, 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(6–7):1117–1125

    Article  PubMed  Google Scholar 

  • Krzemien J, Oyallon J, Crozatier M, Vincent A (2010b) Hematopoietic progenitors and hemocyte lineages in the Drosophila lymph gland. Dev Biol 346(2):310–319

    Article  PubMed  CAS  Google Scholar 

  • Lanot R, Zachary D, Holder F, Meister M (2001) Postembryonic hematopoiesis in Drosophila. Dev Biol 230(2):243–257

    Article  PubMed  CAS  Google Scholar 

  • Lavine MD, Strand MR (2002) Insect hemocytes and their role in immunity. Insect Biochem Mol Biol 32(10):1295–1309

    Article  PubMed  CAS  Google Scholar 

  • Lebestky T, Chang T, Hartenstein V, Banerjee U (2000) Specification of Drosophila hematopoietic lineage by conserved transcription factors. Science 288(5463):146–149

    Article  PubMed  CAS  Google Scholar 

  • Lebestky T, Jung SH, Banerjee U (2003) A Serrate-expressing signaling center controls Drosophila hematopoiesis. Genes Dev 17(3):348–353

    Article  PubMed  CAS  Google Scholar 

  • Lin X, Soderhall I (2011) Crustacean hematopoiesis and the astakine cytokines. Blood 117(24):6417–6424

    Article  PubMed  CAS  Google Scholar 

  • Lin X, Soderhall K, Soderhall I (2008) Transglutaminase activity in the hematopoietic tissue of a crustacean, Pacifastacus leniusculus, importance in hemocyte homeostasis. BMC Immunol 9:58

    Article  PubMed  Google Scholar 

  • Makki R, Meister M, Pennetier D, Ubeda JM, Braun A, Daburon V, Krzemien J, Bourbon HM, Zhou R, Vincent A, Crozatier M (2010) A short receptor downregulates JAK/STAT signalling to control the Drosophila cellular immune response. PLoS Biol 8(8):e1000441

    Article  PubMed  Google Scholar 

  • 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(9):1019–1023

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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(12):4805–4809

    Article  PubMed  CAS  Google Scholar 

  • 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(10):1671–1680

    Article  PubMed  CAS  Google Scholar 

  • Minakhina S, Tan W, Steward R (2011) JAK/STAT and the GATA factor Pannier control hemocyte maturation and differentiation in Drosophila. Dev Biol 352(2):308–316

    Google Scholar 

  • 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(7):1589–1600

    Article  PubMed  CAS  Google Scholar 

  • Nakahara Y, Kanamori Y, Kiuchi M, Kamimura M (2010) Two hemocyte lineages exist in silkworm larval hematopoietic organ. PLoS One 5(7):e11816

    Article  PubMed  Google Scholar 

  • Nappi A, Poirie M, Carton Y (2009) The role of melanization and cytotoxic by-products in the cellular immune responses of Drosophila against parasitic wasps. Adv Parasitol 70:99–121

    Article  PubMed  CAS  Google Scholar 

  • Nardi JB, Pilas B, Ujhelyi E, Garsha K, Kanost MR (2003) Hematopoietic organs of Manduca sexta and hemocyte lineages. Dev Genes Evol 213(10):477–491

    Article  PubMed  Google Scholar 

  • Nittono Y, Tomabechi S, Onodera N (1964) Formation of hemocytes near the imaginal wing disc in the silkworm, Bombyx mori L. (Preliminary note). J Sericult Sci Jpn 33:43–45

  • Noonin C, Lin X, Jiravanichpaisal P, Soderhall K, Soderhall I (2012) Invertebrate hematopoiesis: an anterior proliferation center as a link between the hematopoietic tissue and the brain. Stem Cells Dev 21(17):3173–3186

    Google Scholar 

  • Nutting W (1951) A comparative anatomical study of the heart and accessory structures of the orthopteroid insects. J Morphol 89:501–598

    Article  Google Scholar 

  • Pelc R (1986) The hemocytes and their classification in the larvae and pupae of Mamestra brassicae (L) (Lepidoptera: Noctuidae). Can J Zool 64:2503–2508

    Article  Google Scholar 

  • Ratcliffe NA, Gagen SJ (1977) Studies on the in vivo cellular reactions of insects: an ultrastructural analysis of nodule formation in Galleria mellonella. Tissue Cell 9

  • Ribeiro C, Brehelin M (2006) Insect haemocytes: what type of cell is that? J Insect Physiol 52(5):417–429

    Article  PubMed  CAS  Google Scholar 

  • Rizki T, Rizki R (1984) The cellular defense system of Drosophila melanogaster. In: King R, Akai H (eds) Insect ultrastructure, vol 2. Plenum Press, New York

    Google Scholar 

  • Roehrborn G (1961) Drosophila tumors and the structure of larval lymph glands. Experientia 17:507–509

    Article  PubMed  CAS  Google Scholar 

  • Rowley AF, Ratcliffe NA (1981) Insects. In: Ratcliffe NA, Rowley AF (eds) Invertebrate blood cells, vol 2. Academic Press, London, pp 421–490

    Google Scholar 

  • Rugendorff A, Younossi-Hartenstein A, Hartenstein V (1993) Embryonic development of the Drosophila heart. Roux’s Arch Dev Biol 203:266–280

    Article  Google Scholar 

  • Seitz K (1972) Herzwandung, Bildung und Differenzierung der Haemocyten. Zool Jb Anat 89(351–384)

  • Shim J, Mukherjee T, Banerjee U (2012) Direct sensing of systemic and nutritional signals by haematopoietic progenitors in Drosophila. Nat Cell Biol 14(4):394–400

    Article  PubMed  CAS  Google Scholar 

  • Shrestha R, Gateff E (1982) Ultrastructure and cytochemistry of the cell types in the larval hematopoietic organs and hemolymph of Drosophila melanogaster. Dev Growth Diff 24:65–82

    Article  Google Scholar 

  • 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(5):756–763

    Article  PubMed  CAS  Google Scholar 

  • Stofanko M, Kwon SY, Badenhorst P (2010) Lineage tracing of lamellocytes demonstrates Drosophila macrophage plasticity. PLoS One 5(11):e14051

    Article  PubMed  Google Scholar 

  • Tauber O (1936) Mitosis of circulating cells in the hemolymph of the roach, Blatta orientalis. Iowa State Coll J Sci 10:373–381

    Google Scholar 

  • Teixeira V, Arede N, Gardner R, Rodriguez-Leon J, Tavares AT (2011) Targeting the hemangioblast with a novel cell type-specific enhancer. BMC Dev Biol 11:76

    Article  PubMed  CAS  Google Scholar 

  • Tepass U, Fessler LI, Aziz A, Hartenstein V (1994) Embryonic origin of hemocytes and their relationship to cell death in Drosophila. Development 120(7):1829–1837

    PubMed  CAS  Google Scholar 

  • Van deVyver G (1981) Organisms without special circulatory systems. In: Ratcliffe N, Rowley A (eds) Invertebrate blood cells, vol 1. Academic, New York, pp 19–34

    Google Scholar 

  • Wright R (1981) Urochordates. In: Ratcliffe N, Rowley A (eds) Invertebrate blood cells, vol 2. Academic Press, London, pp 565–628

    Google Scholar 

  • Zachary D, Hoffmann JA (1973) The haemocytes of Calliphora erythrocephala (Meig.) (Diptera). Z Zellforsch Mikrosk Anat 141(1):55–73

    Article  PubMed  CAS  Google Scholar 

  • Zhang ZF, Shao M, Ho Kang K (2006) Classification of haematopoietic cells and haemocytes in Chinese prawn Fenneropenaeus chinensis. Fish Shellfish Immunol 21(2):159–169

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

Part of this work was funded by HFSP Grant RGP0015/2008-C to V.H. and the Ruth L. Kirschstein National Research Service Award GM007185 to M.G.

Author information

Authors and Affiliations

  1. Department of Molecular Cell and Developmental Biology, University of California Los Angeles, Los Angeles, CA, 90095, USA

    Melina Grigorian & Volker Hartenstein

Authors
  1. Melina Grigorian
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Volker Hartenstein
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Volker Hartenstein.

Additional information

Communicated by: S. Roth

Rights and permissions

Reprints and permissions

About this article

Cite this article

Grigorian, M., Hartenstein, V. Hematopoiesis and hematopoietic organs in arthropods. Dev Genes Evol 223, 103–115 (2013). https://doi.org/10.1007/s00427-012-0428-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00427-012-0428-2

Keywords

Search

Navigation