Lamprey lymphocyte-like cells express homologs of genes involved in immunologically relevant activities of mammalian lymphocytes

Uinuk-ool, Tatiana S.; Mayer, Werner E.; Sato, Akie; Dongak, Roman; Cooper, Max D.; Klein, Jan

doi:10.1073/pnas.212527699

Cited by 132 publications

(98 citation statements)

References 40 publications

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“…The earliest forms of secondary lymphoid tissue were diffuse aggregations and infiltrations in the intestinal wall [60].The implication is that many of the functions which we associate with organised lymphoid tissues in mammals (collections of B-cell follicles and associated T-cell zones) originally took place in more diffuse aggregations of leucocytes in mucosal tissues. Consistent with this idea, immunologically-related genes appear to be expressed preferentially in the intestine in the protochordate amphioxus and in the jawless lampreys [50,59]. Since mucosal tissues are permanently exposed to both harmless as well as harmful antigens, mechanisms must exist which activate appropriate, but different responses to different types of antigens.…”

Section: Structure Of the Mucosal Immune Systemmentioning

confidence: 86%

The postnatal development of the mucosal immune system and mucosal tolerance in domestic animals

Bailey

Haverson²

2006

Vet. Res.

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-The mucosal immune system is exposed to a range of antigens associated with pathogens, to which it must mount active immune responses. However, it is also exposed to a large number of harmless antigens associated with food and with commensal microbial flora, to which expression of active, inflammatory immune responses to these antigens is undesirable. The mucosal immune system must contain machinery capable of evaluating the antigens to which it is exposed and mounting appropriate effector or regulatory responses. Since the immune system is likely to have evolved initially in mucosal tissues, the requirement to prevent damaging allergic responses must be at least as old as the adaptive immune system, and studies of the mechanisms should include a range of non-mammalian species. Despite the importance for rational design of vaccines and for control of allergic reactions, the mechanisms involved are still largely unclear. It is not clear that the classical experimental protocol of "oral tolerance" is, in fact, measuring a biologically important phenomenon, nor is it clear whether tolerance is regulated in the evolutionarily recent organised lymphoid tissue (the lymph nodes) or the more ancient, diffuse architecture in the intestine. The capacity of the immune system to discriminate between "dangerous" and "harmless" antigens appears to develop with age and exposure to microbial flora. Thus, the ability of an individual or a group of animals to correctly regulate mucosal immune responses will depend on age, genetics and on their microbial environment and history. Attempts to manipulate the mucosal immune system towards active immune responses by oral vaccines, or towards oral tolerance, are likely to be confounded by environmentally-induced variability between individuals and between groups of animals.

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Section: Structure Of the Mucosal Immune Systemmentioning

confidence: 86%

The postnatal development of the mucosal immune system and mucosal tolerance in domestic animals

Bailey

Haverson²

2006

Vet. Res.

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“…In lampreys, lymphocyte-like cells are located in the larval intestine, both in the connective tissue underlying the mucosa and in the mucosal cell layer itself [39,40]. These locations are analogous to those in which mammalian intestinal T cells are found.…”

Section: Discussionmentioning

confidence: 99%

Intestinal TSH production is localized in crypt enterocytes and in villus ‘hotblocks’ and is coupled to IL-7 production: evidence for involvement of TSH during acute enteric virus infection

et al. 2005

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The immune and neuroendocrine systems have been shown to work conjointly in a number of ways. One aspect of this has to do with a potential role for thyroid stimulating hormone (TSH) in the regulation of the mucosal immune system, although the mechanisms by which this occurs remain vague. To more thoroughly understand how TSH participates in intestinal intraepithelial lymphocyte (IEL) development and immunity, experiments have been conducted to define local sites of intestinal TSH production, and to characterize changes that occur in the synthesis of TSH during acute enteric virus infection. Here, we demonstrate that TSH in the small intestine is specifically localized to regions below villus crypts as seen by immunocytochemical staining, which revealed high-level TSH staining in lower crypts in the absence of IL-7 staining, and TSH and IL-7 costaining in upper crypt regions. Additionally, prominent TSH staining was evident in TSH 'hotblocks' sparsely dispersed throughout the epithelial layer. In rotavirus-infected mice, the TSH staining pattern differed significantly from that of non-infected animals. Notably, at 2 and 3 days post-infection, TSH expression was high in and near apical villi where virus infection was greatest. These findings lend credence to the notion that TSH plays a role both in the development of intestinal T cells, and in the process of local immunity during enteric virus infection.

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“…Accelerated allograft rejection has been documented in lampreys 84 , as have humoral responses to immunization with bacterial and cellular antigens; however, the circulating AGGLUTININS are not related structurally to antibodies 28 . Extensive EXPRESSED SEQUENCE TAG (EST) surveys have failed to identify typical lymphocyte-specific cell-surface determinants in lampreys 85,86 , with the exceptions of a predicted gene product that shows a distant relationship to CD4 (among other molecules) 87 and another monomorphic gene product that has cytosolic ITIMs and can be modelled to TCR V regions but shows only remote primary-structure similarity to jawed-vertebrate TCRs 87 . However, Ikaros and SPI, which are transcription factors that function in higher-vertebrate lymphocyte development and differentiation, have been identified in jawless vertebrates [88][89][90][91] , as have ETS-(M. Anderson, personal communication), GATA-binding protein 2 (GATA2)-and GATA3-type molecules (J.P.C.…”

Section: Anticipatory Immunity In Jawless Vertebratesmentioning

confidence: 99%

Reconstructing immune phylogeny: new perspectives

2005

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Numerous studies of the mammalian immune system have begun to uncover profound interrelationships, as well as fundamental differences, between the adaptive and innate systems of immune recognition. Coincident with these investigations, the increasing experimental accessibility of non-mammalian jawed vertebrates, jawless vertebrates, protochordates and invertebrates has provided intriguing new information regarding the likely patterns of emergence of immune-related molecules during metazoan phylogeny, as well as the evolution of alternative mechanisms for receptor diversification. Such findings blur traditional distinctions between adaptive and innate immunity and emphasize that, throughout evolution, the immune system has used a remarkably extensive variety of solutions to meet fundamentally similar requirements for host protection.The evolutionary development of the METAZOANS was associated with the diversification of a wide range of specialized cell-surface molecules that mediate key metabolic processes, as well as provide crucial contact interfaces and carry out a broad range of other essential functions. It is not unexpected that some of these molecules also came to function as barriers to pathogenic invasion and, in doing so, began to carry out dedicated innate immune protective functions. Whereas the simplest form of protection, barrier formation, is essentially mechanical in nature, relentless pressure from genetic variation in pathogens probably drove the evolution of such innate immune protective molecules towards diversification and, in parallel, towards integration of signalling pathways to regulate cellular responses to external stimulation. However, despite the sophistication that such innate immune mediators achieved over time, their biological complexity, by definition, would be limited by genome space, so with increasing complexity of body plan and/or increasing pathogen sophistication, they could be overwhelmed. NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author ManuscriptMore than 500 million years ago, a TRANSPOSITION event, probably involving a recombinationactivating gene (RAG)-bearing element, might have given rise to the predecessors of the rearranging antigen-binding receptors of the jawed vertebrates, which encompass the vertebrate radiations that extend from the cartilaginous fish through to humans. This is considered the defining point in the emergence of RAG-mediated (conventional) adaptive immunity 1,2 , which has evolved to create a mechanism for deriving almost limitless variation from very few genes. Studies in traditional and non-traditional animal models, such as sharks, bony fish and birds, have brought this event and its ramifications for host defence into sharper focus. We can now predict much about how these rearranging antigenbinding receptors probably arose, what alternative pathways of immune-receptor gene evolution have occurred, what relationships exist between B-and T-cell-mediated immunity and natural killer (NK)-cell function, how complex immune ...

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Lamprey lymphocyte-like cells express homologs of genes involved in immunologically relevant activities of mammalian lymphocytes

Cited by 132 publications

References 40 publications

The postnatal development of the mucosal immune system and mucosal tolerance in domestic animals

The postnatal development of the mucosal immune system and mucosal tolerance in domestic animals

Intestinal TSH production is localized in crypt enterocytes and in villus ‘hotblocks’ and is coupled to IL-7 production: evidence for involvement of TSH during acute enteric virus infection

Reconstructing immune phylogeny: new perspectives

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