Evolutionary Origins of Lymphocytes: Ensembles of T Cell and B Cell Transcriptional Regulators in a Cartilaginous Fish

Anderson, Michael; Pant, Rashmi; Miracle, Ann L.; Sun, Xiao Hong; Luer, Carl A.; Walsh, Catherine J.; Telfer, Janice C.; Litman, Gary W.; Rothenberg, Ellen V.

doi:10.4049/jimmunol.172.10.5851

Cited by 45 publications

(24 citation statements)

References 52 publications

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“…A recent study (49) in the clearnose skate provides further evidence that the mammalian pattern of transcription usage is fundamental to the definition of lymphocytes. Authors show a clear conservation of expression of several lymphoid-specific transcription factors in the skate, including Pax-5.…”

Section: Discussionmentioning

confidence: 94%

B Cell Heterogeneity in the Teleost Kidney: Evidence for a Maturation Gradient from Anterior to Posterior Kidney

Zwollo

Cole

Bromage

et al. 2005

The Journal of Immunology

214

192

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The fish immune system is quite different from the mammalian system because the anterior kidney forms the main site for hematopoiesis in this species. Using transcription factor-specific Abs derived from the murine system, together with anti-trout Ig Abs and Percoll gradient separation, we analyzed B cells from trout kidney sections and compared them to those from spleen and blood. For this study, immune cells were separated by Percoll gradients, and the resulting subpopulations were defined based on expression of B cell-specific transcription factors Pax-5 and B lymphocyte-induced maturation protein-1, as well as proliferative and Ig-secreting properties. Comparison of kidney, blood, and spleen B cell subsets suggest that 1) the anterior kidney contains mostly proliferating B cell precursors and plasma cells; 2) posterior kidney houses significant populations of (partially) activated B cells and plasmablasts; and 3) trout blood contains resting, non-Ig-secreting cells and lacks plasma cells. After LPS induction of resting B cells in vitro, the kidney and spleen have a high capacity for the generation of plasma cells, whereas the blood has virtually none. Our results indicate that trout B cell subsets are profoundly different among blood, anterior kidney, posterior kidney, and spleen. We hypothesize that developing B cells mature in the anterior side of the kidney and then migrate to sites of activation, either the spleen or the posterior kidney. Lastly, our data support the notion that the trout kidney is a complex, multifunctional immune organ with the potential to support both hemopoiesis as well as humoral immune activation.

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Section: Discussionmentioning

confidence: 94%

B Cell Heterogeneity in the Teleost Kidney: Evidence for a Maturation Gradient from Anterior to Posterior Kidney

Zwollo

Cole

Bromage

et al. 2005

The Journal of Immunology

214

192

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“…The origin of lymphocytes is another interesting issue (56). Thus far, no distinct lymphoid tissues have been found in agnathan and protochordate by histologic studies but some lymphocyte-like cells were isolated from the intestine and the associated typhlosole of lamprey (5).…”

Section: Discussionmentioning

confidence: 99%

Genes “Waiting” for Recruitment by the Adaptive Immune System: The Insights from Amphioxus

Yu¹,

Dong²,

Wu³

et al. 2005

The Journal of Immunology

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In seeking evidence of the existence of adaptive immune system (AIS) in ancient chordate, cDNA clones of six libraries from a protochordate, the Chinese amphioxus, were sequenced. Although the key molecules such as TCR, MHC, Ig, and RAG in AIS have not been identified from our database, we demonstrated in this study the extensive molecular evidence for the presence of genes homologous to many genes that are involved in AIS directly or indirectly, including some of which may represent the putative precursors of vertebrate AIS-related genes. The comparative analyses of these genes in different model organisms revealed the different fates of these genes during evolution. Their gene expression pattern suggested that the primitive digestive system is the pivotal place of the origin and evolution of the AIS. Our studies support the general statement that AIS appears after the jawless/jawed vertebrate split. However our study further reveals the fact that AIS is in its twilight in amphioxus and the evolution of the molecules in amphioxus are waiting for recruitment by the emergence of AIS.

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“…T-lineage-specific Helios expression is conserved, like GATA-3 and Runx3 expression, from mammals to cartilaginous fish (80). This suggests that Helios could play an important and specific role in T cell development, but the functional data needed to address this question are lacking.…”

Section: Rothenberg Taghonmentioning

confidence: 98%

“…GATA-3 and Runx3 are probably associated with thymocyte differentiation throughout the jawed vertebrates, as shown by the highlevel coexpression of these factors specifically in the thymus of the cartilaginous fish Raja eglanteria (80). The most abundant Runx factor in the thymus (Runx1) is expressed as a legacy from hematopoietic stem cells, where it plays an indispensable role (81,82).…”

Section: Runx Factorsmentioning

confidence: 99%

Molecular Genetics of T Cell Development

Rothenberg

Taghon

2005

Annu. Rev. Immunol.

Self Cite

233

187

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■ Abstract T cell development is guided by a complex set of transcription factors that act recursively, in different combinations, at each of the developmental choice points from T-lineage specification to peripheral T cell specialization. This review describes the modes of action of the major T-lineage-defining transcription factors and the signal pathways that activate them during intrathymic differentiation from pluripotent precursors. Roles of Notch and its effector RBPSuh (CSL), GATA-3, E2A/HEB and Id proteins, c-Myb, TCF-1, and members of the Runx, Ets, and Ikaros families are critical. Less known transcription factors that are newly recognized as being required for T cell development at particular checkpoints are also described. The transcriptional regulation of T cell development is contrasted with that of B cell development, in terms of their different degrees of overlap with the stem-cell program and the different roles of key transcription factors in gene regulatory networks leading to lineage commitment. OVERVIEW OF T CELL DEVELOPMENT AND ITS REQUIREMENTST cells are the only hematopoietic cells that are not generated in the bone marrow. Instead, virtually all circulating T lymphocytes are generated in the thymus, and many different types exist. T cells are further distinguished among hematopoietic cells by their potentially infinite proliferative life spans and by their capacity for differentiative specialization even after their mature features are in place. Some of this specialization is triggered by environmental signals from antigen recognition and/or other ligand/receptor interactions. Thus T cell development, as a process, incorporates multiple stages at which different choices are available to the cells, extending over many cell cycles and a long period of time. In spite of this complexity, the T cell program as a whole is unified by the identities of the key regulators throughout the process: Many of the same regulatory factors and growth factor receptors are used again and again at different stages. This review focuses on the roles of these factors in establishing T cell identity as they guide uncommitted hematopoietic precursors into, and through, thymic differentiation. ROTHENBERG TAGHON A Map of the Terrain: Stages of T Cell DevelopmentAt least five stages have been defined in which specific regulators are needed for T cell development to proceed. First, there is the specification process, through which multipotent precursors first enter the T cell pathway, usually as they first immigrate to the thymus. Second is the complex process in which proliferative expansion and T cell receptor (TCR) gene rearrangement are combined with commitment to the T lineage within the thymus. These first stages are examined closely at the end of this review. Third is β-selection, which is a cascade of differentiation and proliferation events triggered specifically by "pre-TCR" signaling in precursors of TCRαβ T cells, after successful rearrangement of the TCRβ gene. Fourth is TCR-dependent positive selectio...

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Evolutionary Origins of Lymphocytes: Ensembles of T Cell and B Cell Transcriptional Regulators in a Cartilaginous Fish

Cited by 45 publications

References 52 publications

B Cell Heterogeneity in the Teleost Kidney: Evidence for a Maturation Gradient from Anterior to Posterior Kidney

B Cell Heterogeneity in the Teleost Kidney: Evidence for a Maturation Gradient from Anterior to Posterior Kidney

Genes “Waiting” for Recruitment by the Adaptive Immune System: The Insights from Amphioxus

Molecular Genetics of T Cell Development

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