Evolution of JAK-STAT Pathway Components: Mechanisms and Role in Immune System Development

Liongue, Clifford; O’Sullivan, Lynda A.; Trengove, Monique C.; Ward, Alister C.

doi:10.1371/journal.pone.0032777

Cited by 126 publications

(120 citation statements)

References 82 publications

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“…The JAK/STAT signalling cascade plays an essential role in cell signalling in bilaterians by transducing secreted peptide signals (typically cytokines) into transcriptional activation responses (see [135,136] for recent reviews). Intracellular JAK proteins become activated by complexing with transmembrane receptors in the cytokine receptor class I/II families.…”

Section: Pathways Restricted To Cnidaria þ Bilateria (A) Hedgehog Sigmentioning

confidence: 99%

Phylogenetic evidence for the modular evolution of metazoan signalling pathways

Babonis¹,

Martindale²

2017

Phil. Trans. R. Soc. B

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One contribution of 17 to a theme issue 'Evo-devo in the genomics era, and the origins of morphological diversity'. Communication among cells was paramount to the evolutionary increase in cell type diversity and, ultimately, the origin of large body size. Across the diversity of Metazoa, there are only few conserved cell signalling pathways known to orchestrate the complex cell and tissue interactions regulating development; thus, modification to these few pathways has been responsible for generating diversity during the evolution of animals. Here, we summarize evidence for the origin and putative function of the intracellular, membrane-bound and secreted components of seven metazoan cell signalling pathways with a special focus on early branching metazoans (ctenophores, poriferans, placozoans and cnidarians) and basal unikonts (amoebozoans, fungi, filastereans and choanoflagellates). We highlight the modular incorporation of intra-and extracellular components in each signalling pathway and suggest that increases in the complexity of the extracellular matrix may have further promoted the modulation of cell signalling during metazoan evolution. Most importantly, this updated view of metazoan signalling pathways highlights the need for explicit study of canonical signalling pathway components in taxa that do not operate a complete signalling pathway. Studies like these are critical for developing a deeper understanding of the evolution of cell signalling.This article is part of the themed issue 'Evo-devo in the genomics era, and the origins of morphological diversity'.

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Section: Pathways Restricted To Cnidaria þ Bilateria (A) Hedgehog Sigmentioning

confidence: 99%

Phylogenetic evidence for the modular evolution of metazoan signalling pathways

Babonis¹,

Martindale²

2017

Phil. Trans. R. Soc. B

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“…Proteins containing SOCS box domains were identified in extant choanoflagellates (12), but only porifera possess proteins in which a SOCS box is associated with an SH2 domain and small N-terminal sequence to form an archetypal SOCS protein (12). Interestingly, this pathway component was subsequently replicated to yield three distinct lineages in bilateria (37), which are differentially used in the CytoR signaling paradigm (38,39). Assembling the components.…”

Section: Emergence Of the Pathwaymentioning

confidence: 99%

“…As a result, the majority of the CytoR-JAK-STAT signaling components were already in place at the time of divergence of bony fish (including mammals) and cartilaginous fish (including sharks) around 420 million years ago, representing the "core" CytoR signaling network. Local duplications of individual components appear to have contributed to this process, but the two rounds of whole-genome duplication (WGD) that occurred during early vertebrate evolution (49) represent the major mediator of the expansion (20,34,37). Cyto/CytoRs.…”

Section: Expansion Of the Pathwaymentioning

confidence: 99%

Evolution of Cytokine Receptor Signaling

Liongue

Sertori

Ward

2016

The Journal of Immunology

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104

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Cytokines represent essential mediators of cell–cell communication with particularly important roles within the immune system. These secreted factors are produced in response to developmental and/or environmental cues and act via cognate cytokine receptors on target cells, stimulating specific intracellular signaling pathways to facilitate appropriate cellular responses. This review describes the evolution of cytokine receptor signaling, focusing on the class I and class II receptor families and the downstream JAK–STAT pathway along with its key negative regulators. Individual components generated over a long evolutionary time frame coalesced to form an archetypal signaling pathway in bilateria that was expanded extensively during early vertebrate evolution to establish a substantial “core” signaling network, which has subsequently undergone limited diversification within discrete lineages. The evolution of cytokine receptor signaling parallels that of the immune system, particularly the emergence of adaptive immunity, which has likely been a major evolutionary driver.

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“…However, owing to the high degree of sequence homology to their mammalian counterparts, and conserved syntenic relationships, the cish.a and cish.b designations are consistent with the Zebrafish Nomenclature Committee guidelines and should take precedence. Indeed, the identification of two zebrafish CISH paralogs is especially significant, given that both the JAK2 and STAT5 genes are also duplicated in zebrafish (37,38,40). Whether this reflects functional redundancy or specification into distinct pathways is an important question for further study.…”

Section: Discussionmentioning

confidence: 99%

“…Definitive hematopoietic stem cells expressing c-myb emerge in the dorsal aorta (34), and following a transient phase within the caudal hematopoietic tissue (35), they populate the developing kidney, the major adult hematopoietic site, and the thymus, where early lymphoid precursors expressing ikaros (27) give rise to mature T cells, expressing markers such as rag1 and tcra (36). Zebrafish has also been shown to possess homologs for JAK2 and STAT5, as well as the relevant upstream cytokine receptors (37)(38)(39)(40). Therefore, to gain insight into the role played by CISH in vivo we have employed bioinformatics and biochemical approaches together with expression analysis and morpholino-mediated knockdown in zebrafish.…”

mentioning

confidence: 99%

Regulation of Embryonic Hematopoiesis by a Cytokine-Inducible SH2 Domain Homolog in Zebrafish

Lewis

Noor

Fraser

et al. 2014

The Journal of Immunology

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Cytokine-inducible SH2 domain–containing protein (CISH), a member of the suppressor of cytokine signaling family of negative feedback regulators, is induced by cytokines that activate STAT5 and can inhibit STAT5 signaling in vitro. However, demonstration of a definitive in vivo role for CISH during development has remained elusive. This study employed expression analysis and morpholino-mediated knockdown in zebrafish in concert with bioinformatics and biochemical approaches to investigate CISH function. Two zebrafish CISH paralogs were identified, cish.a and cish.b, with high overall conservation (43–46% identity) with their mammalian counterparts. The cish.a gene was maternally derived, with transcripts present throughout embryogenesis, and increasing at 4–5 d after fertilization, whereas cish.b expression commenced at 8 h after fertilization. Expression of cish.a was regulated by the JAK2/STAT5 pathway via conserved tetrameric STAT5 binding sites (TTCN3GAA) in its promoter. Injection of morpholinos targeting cish.a, but not cish.b or control morpholinos, resulted in enhanced embryonic erythropoiesis, myelopoiesis, and lymphopoiesis, including a 2- 3-fold increase in erythrocytic markers. This occurred concomitantly with increased activation of STAT5. This study indicates that CISH functions as a conserved in vivo target and regulator of STAT5 in the control of embryonic hematopoiesis.

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Evolution of JAK-STAT Pathway Components: Mechanisms and Role in Immune System Development

Cited by 126 publications

References 82 publications

Phylogenetic evidence for the modular evolution of metazoan signalling pathways

Phylogenetic evidence for the modular evolution of metazoan signalling pathways

Evolution of Cytokine Receptor Signaling

Regulation of Embryonic Hematopoiesis by a Cytokine-Inducible SH2 Domain Homolog in Zebrafish

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