Adaptive immunity in jawless fish

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Jawless vertebrates, which today consist entirely of lampreys and hagfish, have an adaptive immune system similar to that found in jawed vertebrates. The cells of the agnathan AIS have roles roughly equivalent to those of B-cells and T-cells, with three lymphocyte lineages identified so far:

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VLRA and VLRB were identified in 2009, [1] while VLRC was discovered in 2013. [3] Instead of immunoglobulins, they use variable lymphocyte receptors.

Antigen receptors

Jawless vertebrates do not have immunoglobulins (Igs), the key proteins to B-cells and T-cells. However, they do possess a system of leucine-rich repeat (LRR) proteins that make up variable lymphocyte receptors (VLRs). This system can produce roughly the same number of potential receptors that the Ig-based system found in jawed vertebrates can. [4] Instead of recombination-activating genes (RAGs), genes coding for VLRs can be altered by a family of cytidine deaminases known as APOBEC, possibly through gene conversion. [5] Cytidine deaminase 1 is associated with the assembly of VLRA and VLRC and cytidine deaminase 2 appears to assemble VLRB. [1] [3]

Evolution

The gene expression profiles of lymphocyte-like cells (LLCs) in jawless vertebrates indicate that VLRB+ LLCs and B cells share a common ancestor, and VLRA+ and VLRC+ LLCs and T cells share a common ancestor. [6] Like B cells and T cells, the development of VLRB+ LLCs is spatially separated from the development of VLRA+ and VLRC+ LLCs. VLRB+ LLCs and B cells develop in hematopoietic tissues: VLRB+ LLCs develop in the typhlosole and kidneys and B cells develop in bone marrow. VLRA+ and VLRC+ LLCs develop in a thymus-like organ called the thymoid, similar to T cells developing in the thymus. [7] VLRB molecules and B cells can directly bind to antigens and VLRB-transfected cells secrete VLRB protein products, similar to B cells in jawed vertebrates. VLRA+ LLCs were unable to bind Bacillus anthracis , Escherichia coli , Salmonella typhimurium , or Streptococcus pneumoniae before or after immunization, suggesting that VLRAs require antigen processing like TCRs. [1] However, MHCs or MHC-like molecules that could present processed antigens have not been found in lampreys, [8] and some VLRAs expressed in yeast were able to directly bind to antigens. [9] The antigen binding of VLRCs has not been studied. [10] However, the VLRC gene is close in proximity and sequence to the VLRA gene and the two are often co-expressed in LLCs, suggesting that both are TCR-like receptors. [3]

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Variable lymphocyte receptors (VLRs) belong to the Leucine-rich repeat (LRR) family and mediate adaptive immune responses in the jawless vertebrates, lampreys and hagfish.

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References

  1. 1 2 3 4 5 Guo, Peng; Hirano, Masayuki; Herrin, Brantley R.; Li, Jianxu; Yu, Cuiling; Sadlonova, Andrea; Cooper, Max D. (2009-05-27). "Dual nature of the adaptive immune system in lampreys". Nature. 459 (7248): 796–801. Bibcode:2009Natur.459..796G. doi:10.1038/nature08068. ISSN   0028-0836. PMC   2714547 . PMID   19474790.
  2. ↑ Kishishita, Natsuko; Nagawa, Fumikiyo (March 2014). "Evolution of adaptive immunity: implications of a third lymphocyte lineage in lampreys". BioEssays. 36 (3): 244–250. doi:10.1002/bies.201300145. ISSN   1521-1878. PMID   24853392.
  3. 1 2 3 Hirano, Masayuki; Guo, Peng; McCurley, Nathanael; Schorpp, Michael; Das, Sabyasachi; Boehm, Thomas; Cooper, Max D. (2013-08-11). "Evolutionary implications of a third lymphocyte lineage in lampreys". Nature. 501 (7467): 435–438. Bibcode:2013Natur.501..435H. doi:10.1038/nature12467. ISSN   0028-0836. PMC   3901013 . PMID   23934109.
  4. ↑ Cooper, Max D.; Alder, Matthew N. (2006-02-24). "The evolution of adaptive immune systems". Cell. 124 (4): 815–822. doi: 10.1016/j.cell.2006.02.001 . ISSN   0092-8674. PMID   16497590.
  5. ↑ Hirano, Masayuki (August 2015). "Evolution of vertebrate adaptive immunity: immune cells and tissues, and AID/APOBEC cytidine deaminases". BioEssays. 37 (8): 877–887. doi: 10.1002/bies.201400178 . ISSN   1521-1878. PMID   26212221. S2CID   20163604.
  6. ↑ Kasamatsu, Jun (January 2013). "Evolution of innate and adaptive immune systems in jawless vertebrates". Microbiology and Immunology. 57 (1): 1–12. doi: 10.1111/j.1348-0421.2012.00500.x . ISSN   0385-5600. PMID   22924515.
  7. ↑ Bajoghli, Baubak; Guo, Peng; Aghaallaei, Narges; Hirano, Masayuki; Strohmeier, Christine; McCurley, Nathanael; Bockman, Dale E.; Schorpp, Michael; Cooper, Max D. (2011-02-03). "A thymus candidate in lampreys". Nature. 470 (7332): 90–94. Bibcode:2011Natur.470...90B. doi:10.1038/nature09655. ISSN   0028-0836. PMID   21293377. S2CID   4417477.
  8. ↑ Mayer, Werner E.; Uinuk-ool, Tatiana; Tichy, Herbert; Gartland, Lanier A.; Klein, Jan; Cooper, Max D. (2002-10-29). "Isolation and characterization of lymphocyte-like cells from a lamprey". Proceedings of the National Academy of Sciences. 99 (22): 14350–14355. Bibcode:2002PNAS...9914350M. doi: 10.1073/pnas.212527499 . ISSN   0027-8424. PMC   137887 . PMID   12388781.
  9. ↑ Deng, Lu; Velikovsky, C. Alejandro; Xu, Gang; Iyer, Lakshminarayan M.; Tasumi, Satoshi; Kerzic, Melissa C.; Flajnik, Martin F.; Aravind, L.; Pancer, Zeev (2010-07-27). "A structural basis for antigen recognition by the T cell-like lymphocytes of sea lamprey". Proceedings of the National Academy of Sciences. 107 (30): 13408–13413. Bibcode:2010PNAS..10713408D. doi: 10.1073/pnas.1005475107 . ISSN   0027-8424. PMC   2922149 . PMID   20616002.
  10. ↑ Boehm, Thomas; Hirano, Masayuki; Holland, Stephen J.; Das, Sabyasachi; Schorpp, Michael; Cooper, Max D. (2018-04-26). "Evolution of Alternative Adaptive Immune Systems in Vertebrates". Annual Review of Immunology. 36 (1): 19–42. doi:10.1146/annurev-immunol-042617-053028. hdl: 21.11116/0000-0001-F62D-8 . ISSN   0732-0582. PMID   29144837.

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