Development Genes and Evolution

, Volume 223, Issue 1–2, pp 103–115 | Cite as

Hematopoiesis and hematopoietic organs in arthropods



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.


Blood Hematopoiesis Stem cell Invertebrate Arthropod 



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.


  1. Agaisse H, Perrimon N (2004) The roles of JAK/STAT signaling in Drosophila immune responses. Immunol Rev 198:72–82PubMedCrossRefGoogle Scholar
  2. Bauchau A (1981) Crustaceans. In: Ratcliffe NA, Rowley AF (ed) Invertebrate blood cells, vol 2. Academic Press, London, pp. 385–420Google Scholar
  3. Böhm GA, Gersch M (1983) The hematopoietic character of the “cephalic gland” in the crayfish Orconectes limosus. Cen Comp Endocrinol 52:102–107CrossRefGoogle Scholar
  4. Boutros M, Agaisse H, Perrimon N (2002) Sequential activation of signaling pathways during innate immune responses in Drosophila. Dev Cell 3(5):711–722PubMedCrossRefGoogle Scholar
  5. Brehelin M (1982) Comparative study of structure and function of blood cells from two Drosophila species. Cell Tissue Res 221(3):607–615PubMedGoogle Scholar
  6. Choi K, Kennedy M, Kazarov A, Papadimitriou JC, Keller G (1998) A common precursor for hematopoietic and endothelial cells. Development 125(4):725–732PubMedGoogle Scholar
  7. Cowden R, Curtis S (1981) Cephalopods. In: Ratcliffe NA, Rowley AF (ed) Invertebrate blood cells, vol 1. Academic Press, London, pp 301–321Google Scholar
  8. 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):E196PubMedCrossRefGoogle Scholar
  9. Cuenot L (1897) Les globules sanguins et les organes lymphides des invertebres. Arch D’Anat Microsc 1:153–192Google Scholar
  10. Dales R, Dixon L (1981) Polychaetes. In: Ratcliffe NA, Rowley AF (ed) Invertebrate blood cells, vol 1. Academic Press, London, pp 35–75Google Scholar
  11. 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):523–537PubMedGoogle Scholar
  12. 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 36:169–182CrossRefGoogle Scholar
  13. 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 45–56Google Scholar
  14. Feir D, McClain E (1968) Mitotic activity of the circulating hemocytes of the large milkweed bug, Oncopeltus fasciatus. Ann Entomol Soc Amer 61:413–416Google Scholar
  15. Feir D, O’Connor GM Jr (1965) Mitotic activity in the hemocytes of Oncopeltus fasciatus (Dall). Exp Cell Res 39(2):637–642PubMedCrossRefGoogle Scholar
  16. Francois J (1975) Hemocytes et organe hematopoietique de Thermobia domestica (packard) (Thysanura: Lepismatidae). International Journal of Insect Morphology and Embryology 4(6):477–494CrossRefGoogle Scholar
  17. 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):121–131PubMedCrossRefGoogle Scholar
  18. Gupta A (1979) Hemocyte types: their structures, synonymies, interrelationships, and taxonomic significance. In: Gupta A (ed) Insect hemocytes. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  19. Haegebarth A, Clevers H (2009) Wnt signaling, lgr5, and stem cells in the intestine and skin. Am J Pathol 174(3):715–721PubMedCrossRefGoogle Scholar
  20. Han SS, Lee MH, Kim WK, Wago H, Yoe SM (1998) Hemocytic differentiation in hemopoietic organ of Bombyx mori larvae. Zoolog Sci 15(3):371–379PubMedCrossRefGoogle Scholar
  21. Hinks C, Arnold J (1977) Haemopoiesis in Lepidoptera. II. The role of the haemopoietic organs. Can J Zool 55:1740–1755CrossRefGoogle Scholar
  22. Hoffmann JA (1970) [The hemopoietic organs of the two orthopterans Locusta migratoria and Gryllus bimaculatus]. Z Zellforsch Mikrosk Anat 106(3):451–472PubMedCrossRefGoogle Scholar
  23. 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, CambridgeGoogle Scholar
  24. 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):315–327PubMedCrossRefGoogle Scholar
  25. Jeong KH, Lie KJ, Heyneman D (1983) The ultrastructure of the amebocyte-producing organ in Biomphalaria glabrata. Dev Comp Immunol 7(2):217–228PubMedCrossRefGoogle Scholar
  26. Jiang H, Vilcinskas A, Kanost MR (2010) Immunity in lepidopteran insects. Adv Exp Med Biol 708:181–204Google Scholar
  27. Jones J (1970) Hemocytopoiesis in insects. In: Gordon A (ed) Regulation of hematopoiesis. Appleton, New YorkGoogle Scholar
  28. 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 34:291–298CrossRefGoogle Scholar
  29. Jung SH, Evans CJ, Uemura C, Banerjee U (2005) The Drosophila lymph gland as a developmental model of hematopoiesis. Development 132(11):2521–2533PubMedCrossRefGoogle Scholar
  30. Kaaya GP, Ratcliffe NA (1982) Comparative study of hemocytes and associated cells of some medically important dipterans. J Morphol 173(3):351–365PubMedCrossRefGoogle Scholar
  31. 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):325–328PubMedCrossRefGoogle Scholar
  32. 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):1117–1125PubMedCrossRefGoogle Scholar
  33. Krzemien J, Oyallon J, Crozatier M, Vincent A (2010b) Hematopoietic progenitors and hemocyte lineages in the Drosophila lymph gland. Dev Biol 346(2):310–319PubMedCrossRefGoogle Scholar
  34. Lanot R, Zachary D, Holder F, Meister M (2001) Postembryonic hematopoiesis in Drosophila. Dev Biol 230(2):243–257PubMedCrossRefGoogle Scholar
  35. Lavine MD, Strand MR (2002) Insect hemocytes and their role in immunity. Insect Biochem Mol Biol 32(10):1295–1309PubMedCrossRefGoogle Scholar
  36. Lebestky T, Chang T, Hartenstein V, Banerjee U (2000) Specification of Drosophila hematopoietic lineage by conserved transcription factors. Science 288(5463):146–149PubMedCrossRefGoogle Scholar
  37. Lebestky T, Jung SH, Banerjee U (2003) A Serrate-expressing signaling center controls Drosophila hematopoiesis. Genes Dev 17(3):348–353PubMedCrossRefGoogle Scholar
  38. Lin X, Soderhall I (2011) Crustacean hematopoiesis and the astakine cytokines. Blood 117(24):6417–6424PubMedCrossRefGoogle Scholar
  39. Lin X, Soderhall K, Soderhall I (2008) Transglutaminase activity in the hematopoietic tissue of a crustacean, Pacifastacus leniusculus, importance in hemocyte homeostasis. BMC Immunol 9:58PubMedCrossRefGoogle Scholar
  40. 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):e1000441PubMedCrossRefGoogle Scholar
  41. 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):1019–1023PubMedCrossRefGoogle Scholar
  42. Mandal L, Martinez-Agosto JA, Evans CJ, Hartenstein V, Banerjee U (2007) A Hedgehog- and Antennapedia-dependent niche maintains Drosophila haematopoietic precursors. Nature 446:320–324PubMedCrossRefGoogle Scholar
  43. 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):4805–4809PubMedCrossRefGoogle Scholar
  44. 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):1671–1680PubMedCrossRefGoogle Scholar
  45. 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):308–316Google Scholar
  46. 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):1589–1600PubMedCrossRefGoogle Scholar
  47. Nakahara Y, Kanamori Y, Kiuchi M, Kamimura M (2010) Two hemocyte lineages exist in silkworm larval hematopoietic organ. PLoS One 5(7):e11816PubMedCrossRefGoogle Scholar
  48. 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 70:99–121PubMedCrossRefGoogle Scholar
  49. Nardi JB, Pilas B, Ujhelyi E, Garsha K, Kanost MR (2003) Hematopoietic organs of Manduca sexta and hemocyte lineages. Dev Genes Evol 213(10):477–491PubMedCrossRefGoogle Scholar
  50. 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 33:43–45Google Scholar
  51. 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):3173–3186Google Scholar
  52. Nutting W (1951) A comparative anatomical study of the heart and accessory structures of the orthopteroid insects. J Morphol 89:501–598CrossRefGoogle Scholar
  53. Pelc R (1986) The hemocytes and their classification in the larvae and pupae of Mamestra brassicae (L) (Lepidoptera: Noctuidae). Can J Zool 64:2503–2508CrossRefGoogle Scholar
  54. 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 9Google Scholar
  55. Ribeiro C, Brehelin M (2006) Insect haemocytes: what type of cell is that? J Insect Physiol 52(5):417–429PubMedCrossRefGoogle Scholar
  56. 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 YorkGoogle Scholar
  57. Roehrborn G (1961) Drosophila tumors and the structure of larval lymph glands. Experientia 17:507–509PubMedCrossRefGoogle Scholar
  58. Rowley AF, Ratcliffe NA (1981) Insects. In: Ratcliffe NA, Rowley AF (eds) Invertebrate blood cells, vol 2. Academic Press, London, pp 421–490Google Scholar
  59. Rugendorff A, Younossi-Hartenstein A, Hartenstein V (1993) Embryonic development of the Drosophila heart. Roux’s Arch Dev Biol 203:266–280CrossRefGoogle Scholar
  60. Seitz K (1972) Herzwandung, Bildung und Differenzierung der Haemocyten. Zool Jb Anat 89(351–384)Google Scholar
  61. Shim J, Mukherjee T, Banerjee U (2012) Direct sensing of systemic and nutritional signals by haematopoietic progenitors in Drosophila. Nat Cell Biol 14(4):394–400PubMedCrossRefGoogle Scholar
  62. 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 24:65–82CrossRefGoogle Scholar
  63. 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):756–763PubMedCrossRefGoogle Scholar
  64. Stofanko M, Kwon SY, Badenhorst P (2010) Lineage tracing of lamellocytes demonstrates Drosophila macrophage plasticity. PLoS One 5(11):e14051PubMedCrossRefGoogle Scholar
  65. Tauber O (1936) Mitosis of circulating cells in the hemolymph of the roach, Blatta orientalis. Iowa State Coll J Sci 10:373–381Google Scholar
  66. 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 11:76PubMedCrossRefGoogle Scholar
  67. Tepass U, Fessler LI, Aziz A, Hartenstein V (1994) Embryonic origin of hemocytes and their relationship to cell death in Drosophila. Development 120(7):1829–1837PubMedGoogle Scholar
  68. Van deVyver G (1981) Organisms without special circulatory systems. In: Ratcliffe N, Rowley A (eds) Invertebrate blood cells, vol 1. Academic, New York, pp 19–34Google Scholar
  69. Wright R (1981) Urochordates. In: Ratcliffe N, Rowley A (eds) Invertebrate blood cells, vol 2. Academic Press, London, pp 565–628Google Scholar
  70. Zachary D, Hoffmann JA (1973) The haemocytes of Calliphora erythrocephala (Meig.) (Diptera). Z Zellforsch Mikrosk Anat 141(1):55–73PubMedCrossRefGoogle Scholar
  71. Zhang ZF, Shao M, Ho Kang K (2006) Classification of haematopoietic cells and haemocytes in Chinese prawn Fenneropenaeus chinensis. Fish Shellfish Immunol 21(2):159–169PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Department of Molecular Cell and Developmental BiologyUniversity of California Los AngelesLos AngelesUSA

Personalised recommendations