Hematopoiesis and hematopoietic organs in arthropods

Abstract

Hemocytes (blood cells) are motile cells moving throughout the extracellular space and 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 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.

Crustacean hematopoiesis

“…Three main classes of hemocytes are recognized in Drosophila: the plasmatocyte (PC), which is phagocytic; the crystal cell (CC), involved in melanization; and the encapsulating lamellocyte (LC). The GC in crayfish is slightly comparable in function to CCs in Drosophila, whereas SGCs and HCs are partially phagocytic but not strictly comparable to plasmatocytes in flies (Grigorian and Hartenstein, 2013;Lin and Söderhäll, 2011a). …”

“…These data were made publically available in the NCBI sequence read archive as BioProject ID: PRJNA259594 at: http://www.ncbi.nlm.nih.gov/bioproject/259594. Because our focus is hematopoiesis in P. leniusculus, we performed a manual BLAST search for transcripts of the genes involved in hematopoietic processes in D. melanogaster (Gold and Brückner, 2014;Grigorian and Hartenstein, 2013;Lebestky et al, 2000;Morin-Poulard et al, 2013). For an evolutionary perspective, a comparative search for these genes in representatives of other insect phyla was conducted where genomes were available, and the following species were selected: D. melanogaster (Diptera), T. castaneum (Coleoptera), A. mellifera (Hymenoptera), Bombyx mori (Lepidoptera), Pediculus humanus corporis (Phthiraptera) and Acyrthosiphon pisum (Hemiptera).…”

“…For an evolutionary perspective, a comparative search for these genes in representatives of other insect phyla was conducted where genomes were available, and the following species were selected: D. melanogaster (Diptera), T. castaneum (Coleoptera), A. mellifera (Hymenoptera), Bombyx mori (Lepidoptera), Pediculus humanus corporis (Phthiraptera) and Acyrthosiphon pisum (Hemiptera). Detailed studies of HPTs from other insects are restricted to Diptera, Lepidoptera and Orthoptera, and among these insects, only Drosophila and Bombyx have been thoroughly studied (Grigorian and Hartenstein, 2013;Hoffmann et al, 1974;Hoffmann and Porte, 1973;Hoffmann, 1970;Nakahara et al, 2010;Nardi et al, 2003). Furthermore, an old structural descriptive study on the hematopoietic organ in the coleopteran Melolontha is available (Brehélin, 1973), whereas no studies of Tribolium, Apis, Acyrthosiphon or Pediculus hematopoiesis have been published.…”

“…Furthermore, an old structural descriptive study on the hematopoietic organ in the coleopteran Melolontha is available (Brehélin, 1973), whereas no studies of Tribolium, Apis, Acyrthosiphon or Pediculus hematopoiesis have been published. Drosophila hematopoiesis has been extensively studied both in terms of morphology and control at the molecular level, and it occurs in two waves: first during embryogenesis in the procephalic mesoderm, and subsequently during the larval stages in the lymph gland (LG), an organ closely associated with the dorsal vessel (Grigorian and Hartenstein, 2013). The different hemocyte types in insects and crustaceans share many properties, but due to a lack of molecular markers for all species, comparisons are primarily performed based on morphological criteria.…”

Reactive Oxygen Species Affect Transglutaminase Activity and Regulate Hematopoiesis in a Crustacean

“…Hematopoiesis, the process by which new blood cells are formed, occurs in different organs in different animal phyla, and several regulatory pathways of this process are evolutionary conserved from invertebrates to vertebrates (1)(2)(3). However, few invertebrate species have been investigated, and therefore knowledge of invertebrate hematopoiesis is lacking.…”