Cellular Immunity in Invertebrates

Invertebrate Blood Cells

In the vertebrates, and particularly in the mammals, there are clearly defined relationships between circulating blood cells. In mammals, all circulating blood cells are descended from a common progenitor cell (the pluripotent hematopoietic stem cell). The process of blood cell development and differentiation is referred to haematopoiesis. However, such relationships have not been established amongst blood cells in the invertebrates. Of course, the invertebrates are polyphyletic, meaning that they are not a single homogenous group, such as the vertebrates. Hence, there is no reason to presume that molecular relationships exist between the blood cells of the different invertebrate groups. Furthermore, while the different groups of mammalian blood cells perform distinct functions (e.g. lymphocytes or erythrocytes), the physiological and immunological roles played by the circulating blood cells in the invertebrates are not clear. Apart from the process of phagocytosis, which is performed by amoeboid cells, there is no clear evidence of immunological continuity between the vertebrates and invertebrates. Despite the similarity of the process, there is, yet again, no evidence of evolutionary homology between the phagocytes of different animal groups.


Oyster hemocytes (Image credit 1)

Hemocytes (image credit 2)


Moth (Manduca sexta) hemocytes (image credit 3)


Haematopoiesis

Hematopoiesis in invertebrates is not as well-understood as that in the mammals. In many invertebrates, the density of circulating blood cells varies considerably during the period after an infection. Often, the number of blood cells decreases during the first 24-48 hours after infection. After this period, the density of cells will return to normal levels. This suggests that the blood cells that are 'used up' during an immunological response are 'replenished', probably through a process of cell division (mitosis). There is some evidence to suggest that precursor cells (i.e. stem cells) may be responsible for this and that the replication of those cells may occur in specialised tissues known as haematopoietic tissues. Table 1 summarises the current understanding of haematopoietic tissues in some invertebrates.

PHYLUM ORDER HAEMATOPOIETIC TISSUE
Cnidaria - Endodermis
Annelida - Coelomic epithelium
Arthropoda Decapoda Cephalothorax
Arthropoda Diptera Lymph glands
Arthropoda Lepidoptera Imaginal wing discs
Mollusca Bivalvia (class) Mantle
Mollusca Gastropoda (class) Haemal sinus, kidney connective tissue
Mollusca Cephalopoda (class) White glands, branchial glands
Echinodermata Echinoidea (class) Axial organ, coelomic epithelium
Echinodermata Asteroidea (class) Axial organ, Tiedemann body
Chordata Ascidiacea Branchial sac, gut/gonad epithelium

Table 1: This table summarises the hematopoietic tissues in various invertebrates. Adapted from Smith (2010)

Work on the fruitfly Drosophila melanogaster has provided some information on the molecular aspects of blood cell (hemocyte) formation (Tokusumi et al, 2012). In this organism, hemocyte are derived from precursors cells known as prohemocytes. Indeed, in Drosophila, hemocytes are generated independently during the embryonic and larval stages. In the larvae, an organ known as the lymph gland appears to be the source of new hemocytes. Within the medulla of this organ is a discrete region known as the Posterior Signalling Centre (PSC). When prohemocytes within the lymph gland divide, signals from the PSC are important for determining the fate of the daughter cells. The microenvironment within the PSC determines in the daughter cells remain as prohemocytes or if they differentiate into mature hemocytes. The process of differentiation involves the activation of genetic program - sets of genes that are expressed in a regulated and sequential manner. It appears to being with a process known as chromatin remodelling - this is the physical rearrangement of the nucelosomes within certain parts of a cell's genome. Through this process (specifically, the BRM chromatin remodelling complex), genes which were previously inaccessible to the transcriptional machinery now become available for transcription (of course, chromatin remodelling can also result in the reverse outcome). Chromatin remodelling appears to be the first step in the differentiation pathway and irreversibly commits the cell to undergo the cellular and molecular changes that result in its conversion to a mature hemocyte. A number of intracellular signlaiing pathways also appear to be important for this, including the hedgehog pathway, the insulin-like growth factor signalling pathway, as well as the TOR pathway. A number of transcription factors (e.g. GATA and RUNX) which are responsible for orchestrating the expression of gene networks. In addition, genes involved in cell cycle regulation, transcriptional and translational regulation, tumour suppression are all known to be involved in the differentiation of a prohemocyte into a hemocyte. The process is indeed complex and involves the activation of genes that promote differentiation, whilst repressing those that suppress differentiation. The data suggests that there may be many parallels between hematopoiesis in Drosophila and that seen in the mammals.

Granulocytes: cellular production factories

While phagocytes eliminate infecting pathogen by ingesting them, another group of cells known as granulocytes, respond to infections by producing antimicrobial compounds and other molecules. Granulocytes are not a homogenous population of cells. Cells containing granules are also called spherule cells or morula cells (Smith, 2010). The granules within the cytoplasm of these cells often contain compounds that kill invading microbes. These include lysozyme, lectins (carbohydrate binding proteins), complement proteins, phenoloxidase (anti-microbial enzyme) and antimicrobial peptides. When triggered by the presence of an infecting microbe, granulocytes will release these compounds into the circulating fluids. This type of recognition and killing is referred to as humoral, as the microbes are not killed by the cells directly, but by the molecules they secrete.

Image credits

1.http://www.mdsg.umd.edu/issues/chesapeake/oysters/educatio
2. http://www.staff.ncl.ac.uk/p.dean/Papers/My_Pulications/Spread-Hemocytes.jpg
3. http://www.bios.niu.edu/miller/aggregates.jpg

References

Smith, Valerie J (2010) Immunology of Invertebrates: Cellular. In: Encyclopedia of Life Sciences (ELS). John Wiley & Sons, Ltd: Chichester.

Tokusumi Y, Tokusumi T, Shoue DA, Schulz RA (2012) Gene Regulatory Networks Controlling Hematopoietic Progenitor Niche Cell Production and Differentiation in the Drosophila Lymph Gland. PLoS ONE 7(7): e41604.



sham.nair@mq.edu.au
shamnair@gmail.co

Sham Nair 2014