Essay: Amphibians

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  • Amphibians
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Amphibians lack the diversity and development of secondary lymphoid organs seen in other vertebrates, such as mammals. The presence of true amphibian lymph nodes is unclear, and no amphibians have been demonstrated to possess Peyer’s patches (PP) or an equivalent1. The amphibian spleen’s role in both differentiation and activation of T and B cells means that it could be considered both a primary and secondary lymphoid organ.2 Thus, most principal sites for interaction of mature lymphocytes with antigens are in the mucosa-associated lymphoid tissue (MALT).
The mucous membranes are a major entry point for pathogens, a problem compounded by the vast surface area of most of these surfaces (e.g. the numerous folds of the small intestine). MALT covers these large areas not as a single lymphoid organ, but as various scattered cells and tissues. These lymphoid tissues serve many immune functions, including being induction sites for antigen sampling, and effector sites for the transport of secretory immunoglobulin. In both mammals and amphibians, MALT has a large population of antibody-producing plasma cells. Classic examples of MALT in mammals include the tonsils and appendix, neither of which has an amphibian analog.
In amphibians, the most significant mucosal surfaces are the skin, lungs, gut, and, in tadpoles, external gills. Of these four, only the gut-associated lymphoid tissues have been studied in depth. Amphibian MALT is markedly less organized than its mammalian counterpart; as stated earlier, amphibians lack the Peyer’s patches and M cells seen in mammals and other vertebrates. However, amphibian MALT does include range of immune cells, which are specialized to their mucosal surfaces.
The amphibian gut consists of four main types of cells: columnar cells, goblet cells, endocrine cells, and leukocytes. These cells rest in this epithelium rest on a continuous basement lamina and are accompanied by the cells of the gut-associated lymphoid tissue (GALT) in the folds of the intestinal wall. One such GALT cell is a large, multinucleated cell granule containing antimicrobial peptides (AMPs), observed in the epithelium of the X.laevis intestine.3 The release of antimicrobial peptides is an especially useful immune response in the epithelial tissues, as it allows the tissues to mount a defense without utilizing a full-blown inflammatory response. These cell granules are similar to mammalian Paneth cells, suggesting a conservation of the antimicrobial peptide host-defense system amongst vertebrates. The amphibian gut-associated lymphoid tissue also contains scattered intraepithelial lymphocytes (IELs), innate cells that destroy both pathogens and infected cells.4 Unlike other T cells, IELs do not need priming, and will instead release cytokines immediately upon encountering antigens. The amphibian intestinal lining is also home to isolated lymphoid follicles (ILFs), cells whose exact roles are unknown, but are believed to function as induction sites in the mucosal immune response.5 These ILFs are theorized to be a prototype to the induced intestinal lymphoid tissue (e.g. lymph nodes or Peyer’s patches) that is seen only in mammals.6 GALT is the site of induction of mucosal immune responses against mucosal pathogens through a variety of antibodies.7 In X.laevis, the antibody IgX has been observed and described as a functional analog of the mammalian IgA.8 Interestingly, thymectomized X.laevis show no difference in IgX levels, suggesting a thymus-independent immune response in the gut of frogs and possibly all amphibians.9,10
The secretion of AMPs is also an important function of MALT in amphibian skin. The peptides act as the first line of defense against bacterial infections, and also regulate the physiological functions of the skin.11

1. Manning, M. J. & Horton, J. D. Histogenesis of lymphoid organs in larvae of the South African clawed toad, Xenopus laevis (Daudin). J. Embryol. Exp. Morphol. 22, 265–77 (1969).
2. Colombo, B. M., Scalvenzi, T., Benlamara, S. & Pollet, N. Microbiota and mucosal immunity in amphibians. Front. Immunol. 6, 1–15 (2015).
3. Reilly, D. S., Tomassini, N., Bevins, C. L. & Zasloff, M. A Paneth cell analogue in Xenopus small intestine expresses antimicrobial peptide genes: conservation of an intestinal host-defense system. J. Histochem. Cytochem. 42, 697–704 (1994).
4. Riera Romo, M., Pérez-Martínez, D. & Castillo Ferrer, C. Innate immunity in vertebrates: an overview. Immunology 148, 125–39 (2016).
5. Lorenz, R. G. & Newberry, R. D. Isolated lymphoid follicles can function as sites for induction of mucosal immune responses. Ann. N. Y. Acad. Sci. 1029, 44–57 (2004).
6. Eberl, G. & Lochner, M. The development of intestinal lymphoid tissues at the interface of self and microbiota. Mucosal Immunol. 2, 478–485 (2009).
7. Du Pasquier, L., Schwager, J. & Flajnik, M. F. The immune system of Xenopus. Annu. Rev. Immunol. 7, 251–275 (1989).
8. Mussmann, R., Du Pasquier, L. & Hsu, E. Is Xenopus IgX an analog of IgA? Eur. J. Immunol. 26, 2823–2830 (1996).
9. Mashoof, S. et al. Ancient T-Independence of Mucosal IgX/A: Gut Microbiota Unaffected by Larval Thymectomy in Xenopus laevis. Mucosal Immunol. 6, 358–368 (2013).
10. Horton, J. et al. T-cell and natural killer cell development in thymectomized Xenopus. Immunol. Rev. 166, 245–258 (1998).
11. Simmaco, M., Mignogna, G. & Barra, D. Antimicrobial peptides from amphibian skin: What do they tell us? Biopolym. – Pept. Sci. Sect. 47, 435–450 (1998).

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