Immunology of Invertebrates: Cellular


Circulating blood cells are the primary mediators of immunity in invertebrates, carrying out the phagocytic, pathogen trapping and other inflammatory responses that protect invertebrates against infection without specific immunoglobulin antibodies and immune memory. Different immune cell types are usually specialised for different functions with, in general, immune cell diversity tending to increase with body complexity and life history. However, common to most species are phagocytic and/or granular‐type cells that synthesise and store bioactive proteins. Cellular immunity is induced by non‐self motifs on the surface of pathogens or parasites recognised by cell‐derived pattern recognition receptors with diverse binding specificities. Cell death appears to be inherent in immune reactivity of many invertebrates and, in some cases, aids pathogen trapping, which prevents their spread around the body. New immune cells are produced, at least in coelomates, by mesodermal haematopoietic tissues.

Key Concepts

  • Immunity in invertebrates is confined to non‐specific inflammatory responses, mediated to a large extent by the circulating blood cells (haemocytes or coelomocytes) or their products.
  • All coelomate invertebrates contain populations of freely circulating cells dedicated to host defence, some well developed for specialist purposes.
  • There are no true vertebrate‐type lymphocytes and no long‐term, highly specific immune memory in invertebrates.
  • The main invertebrate cellular immune responses include phagocytosis, pathogen trapping, cytotoxicity and the synthesis and release of microbicidal agents.
  • These cellular reactions often involve the death of immune cells or their removal from the circulation, requiring new cells to be synthesised in the haemopoietic tissue and released into the blood.
  • Genomic and proteomic studies have enabled many of the proteins responsible for cellular defence in invertebrates to be identified, especially in arthropods.
  • Whilst many of the responses and pathways are ancient and highly conserved, there is great diversity in the effector molecules across the invertebrates as a whole.

Keywords: invertebrate immunity; blood cell; haemocytes/haemocyte; coelomocytes; prohaemocyte; phagocytes; encapsulation reactions; evolution of immunity; comparative immunology; cellular defences

Figure 1. Highly stylised graphic representation of the main blood cell types involved in the immune responses of invertebrates. (a): Prohaemocyte: an immature cell present in the circulation of decapod crustaceans and insects, and probably within the haemopoietic tissue of other invertebrates. Cells with similar appearance, called lymphocyte‐like cells, also occur in ascidians; (b): Amoeboid phagocyte: cells of this type are present in anthozoans, annelids, insects (where they are called plasmatocytes), echinoderms and ascidians; (c): Granular cell: mature cells that synthesise and exocytose many bioactive factors. They are present in decapod crustaceans, insects, bivalves and chelicerates; (d): Hyaline cell: a haemocyte often phagocytic in decapod crustaceans; (e): Semigranular cell: a highly labile haemocyte present in decapod crustaceans; (f): Spherule or morula‐type cell: haemocytes or coelomocytes that synthesise, transport and release various factors in some cnidarians, annelids, insects, echinoderms and ascidians; (g): Cystocyte (sometimes called thrombocytoid): ‘explosive corpuscle’ present in insects that are involved in clotting and melanisation; (h): Oenocytoid: a storage cell that is involved in melanisation in some insects. Modified oenocytoids, called crystal cells, occur in dipterans; (i): Vibratile cell: a motile cell unique to echinoid and some holothurian echinoderms that contributes to clotting; (j): Signet ring cell: a vacuolated coelomocyte present in ascidians; (k): Compartment cell: a multivacuolated coelomocyte present in ascidians. Not to scale. Reproduced with permission from Dr EA Dyrynda (Heriot Watt University, Edinburgh).
Figure 2. Light micrographs of Diff‐Quik (Romanovsky) stained haemocytes from crab, Carcinus maenas; (a): prohaemocyte; (b): intact hyaline cell; (c): late apoptotic hyaline cell showing cell shrinkage, blebbing and chromatin fragmentation; (d): intact semi‐granular cell; (e): intact granular cell. Reproduced with permission from Drs C Robb and EA Dyrynda (Heriot Watt University, Edinburgh).
Figure 3. Generalised and simplified graphic representations of the domain structures of variable recognition receptors in invertebrates. (a): Toll from arthropods; (b): Dscam from decapods; (c): FREP from snail; (d): Sp185/333 from sea urchin, Stronglygocentrotus purpuratus. Abbreviations as follows. cys: cysteine; EGF: epidermal growth factor‐like motif; gly: glycine; his: histidine; ICR: interceding region; IgSF: immunoglobulin superfamily; N: the amino terminus of the protein; RGD: a tripeptide composed of arginine, glycine and asparagine (the motif is associated with cell adhesion and recognition); SCR: small contacting region; SS: Signal sequence (a domain indicating the encoded protein is secreted to the extracellular environment); TLR: Toll‐like receptor; TMD: trans‐membrane domain.
Figure 4. Encapsulation reactions in vivo in the gill filaments of crab, Carcinus maenas (a): Wax section of a gill filament of a control, untreated, crab showing individual unclumped haemocytes; Giemsa stain. (b): Wax section of a gill filament taken from a crab injected 1 h previously with the Gram‐positive bacterium, Bacillus cereus; Giemsa stain. Note the aggregation of bacteria around the bacterial cells; (c): Aradite section of a haemocyte capsule forming in a gill filament 12 h after injection of B. cereus into the haemocoel; Wright's stain. The capsule has layers of flattened haemocytes around a central, necrotising core. Haemocytes cells can be seen still attaching to the outside of the structure. Bacterial cells can be seen enclosed within the cell matrix; (d): Wax section of a gill filament of a control, untreated, crab showing individual unclumped haemocytes; haematoxylin and eosin stain; (e): Wax section of a gill filament taken from a crab injected 1 h previously with lipopolysaccharide (LPS); haematoxylin and eosin stain. The haemocytes are starting to assemble into a mini‐clump, haematoxylin and eosin stain; (f): Wax section of a gill filament taken from a crab injected 24 h previously with LPS depicting a fully formed haemocyte capsule; haematoxylin and eosin stain; (g–i): haemocyte‐derived chromatin participating in encapsulstion reactions in gill filaments as revealed by DAPI (4′,6‐diamidino‐2‐phenylindole) stain; (g): gill from a control, untreated crab; (h): early stage of ETosis by haemocytes in a gill filament 1 h after injection of LPS; (i): late‐stage capsule formed 24 h after injection of LPS. Extracellular chromatin is evident within the capsule matrix. (c) Reproduced from Smith and Ratcliffe () © Elsevier. (d–i) Reproduced from Robb et al. () © Robb et al. (2014). Scale bars: (a) and (b) = 30 μm. ; (c) to (i) = 20 μm.
Figure 5. Highly stylised schematic representation of the cellular immune activities of invertebrates following the entry of infective agents into the body (not to scale). This scheme is based loosely around a typical decapod model. Hollow arrows indicate cell behaviours or changes; dashed arrows represent possible cell death events; dotted arrow and box in bottom right‐hand corner indicate a magnified detail of lysosomal fusion to the phagosome.


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Further Reading

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Smith, Valerie J(Feb 2016) Immunology of Invertebrates: Cellular. In: eLS. John Wiley & Sons Ltd, Chichester. [doi: 10.1002/9780470015902.a0002344.pub3]