Multiple and highly divergent IL-11 genes in teleost fish

Huising, Mark O.; Kruiswijk, Corine P.; Schijndel, Jessica E. van; Savelkoul, H.F.J.; Flik, G.; Kemenade, B.M.L. Verburg-van

doi:10.1007/s00251-005-0012-2

Cited by 64 publications

(31 citation statements)

References 55 publications

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“…A similar phenomenon has been observed for interleukin-11 genes in teleosts. Fish IL-11a and IL-11b both possess a single cysteine residue near the C-terminus, whereas mammalian IL-11 does not (Huising et al 2005). Medaka leptin-b lacks an additional cysteine, indicating that this is not a universal feature among teleostean Figure 9 General phylogenetic tree of vertebrate evolution.…”

Section: Discussionmentioning

confidence: 99%

“…A major genome duplication (Taylor et al 2003, Volff 2005) is thought to have yielded several duplicate class-I helical cytokines, viz. duplicate interleukin-11 (Huising et al 2005), IL-12p35 (Huising et al 2006b), CXCL12 (Huising et al 2004), and cytokine receptor (IL12p40; Huising et al 2006c) genes. We could not retrieve a leptin-b orthologue from the available pufferfish genomes (tiger pufferfish; Takifugu rubripes, and the green spotted pufferfish; Tetraodon nigroviridis).…”

Section: Discussionmentioning

confidence: 99%

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Two divergent leptin paralogues in zebrafish (Danio rerio) that originate early in teleostean evolution

Gorissen¹,

Bernier²,

Nabuurs³

et al. 2009

Journal of Endocrinology

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We describe duplicate leptin genes in zebrafish (Danio rerio) that share merely 24% amino acid identity with each other and only 18% with human leptin. We were also able to retrieve a second leptin gene in medaka (Oryzias latipes). The presence of duplicate leptin genes in these two distantly related teleosts suggests that duplicate leptin genes are a common feature of teleostean fishes. Despite low primary sequence conservation, we are confident in assigning orthology between mammalian and zebrafish leptins for several reasons. First, both zebrafish leptins share their characteristic gene structure and display key features of conserved synteny with mammalian leptin genes. Secondly, the cysteine residues that make up leptin's single disulphide bridge are equally spaced in mammalian and zebrafish leptins and are unique among all members of the class-I helical cytokine family. Thirdly, the zebrafish leptins cluster with other fish leptins and mammalian leptins in phylogenetic analysis, supported by high bootstrap values. Within the leptin cluster, leptin-b forms a separate clade with the leptin-b orthologue from medaka. Finally, our prediction of the tertiary structures shows that both leptins conform to the typical four a-helix bundle structure of the class-I a-helical cytokines. The zebrafish leptins are differentially expressed; the liver shows high leptin-a expression (in concordance with what we observed for carp leptins), while leptin-b is expressed at much lower levels, which are downregulated further upon fasting. The finding of duplicate leptin genes in teleosts adds to our understanding of the evolution of leptin physiology in the early vertebrate lineage.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Two divergent leptin paralogues in zebrafish (Danio rerio) that originate early in teleostean evolution

Gorissen¹,

Bernier²,

Nabuurs³

et al. 2009

Journal of Endocrinology

Self Cite

194

160

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“…This may reflect protective effects of IL-11 at mucosal surfaces throughout the vertebrates. IL-11 expression in carp head kidney primary macrophages or a trout RTS-11 monocyte/ macrophage cell line is reproducibly upregulated in response to various pro-inflammatory stimuli such as LPS, concanavalin A, polyI:C and recombinant IL-1 (Huising et al 2005, Wang et al 2005, establishing the involvement of IL-11 in the immune response from fish to mammals.…”

Section: Il-11mentioning

confidence: 99%

“…IL-11 orthologs have been characterised recently in carp (Huising et al 2005) and rainbow trout (Wang et al 2005) that share only limited primary sequence identity (maximally 31%) with mammalian IL-11. In fish, IL-11 is ubiquitously, albeit not very abundantly, expressed in most organs and tissues examined (Huising et al 2005, Wang et al 2005. Differences in the IL-11 expression between organs are less pronounced in carp than in trout, where gills and intestine express more IL-11 than any other organ.…”

Section: Il-11mentioning

confidence: 99%

Phylogeny and evolution of class-I helical cytokines

Huising¹,

Kruiswijk

Flik³

2006

Journal of Endocrinology

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136

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The class-I helical cytokines constitute a large group of signalling molecules that play key roles in a plethora of physiological processes including host defence, immune regulation, somatic growth, reproduction, food intake and energy metabolism, regulation of neural growth and many more. Despite little primary amino acid sequence similarity, the view that all contemporary class-I helical cytokines have expanded from a single ancestor is widely accepted, as all class-I helical cytokines share a similar three-dimensional fold, signal via related class-I helical cytokine receptors and activate similar intracellular signalling cascades. Virtually all of our knowledge on class-I helical cytokine signalling derives from research on primate and rodent species. Information on the presence, structure and function of class-I helical cytokines in non-mammalian vertebrates and non-vertebrates is fragmentary. Consequently, our ideas about the evolution of this versatile multigene family are often based on a limited comparison of human and murine orthologs. In the last 5 years, whole genome sequencing projects have yielded draft genomes of the early vertebrates, pufferfish (Takifugu rubripes), spotted green pufferfish (Tetraodon nigroviridis) and zebrafish (Danio rerio). Fuelled by this development, fish orthologs of a number of mammalian class-I helical cytokines have recently been discovered. In this review, we have characterised the mammalian class-I helical cytokine family and compared it with the emerging class-I helical cytokine repertoire of teleost fish. This approach offers important insights into cytokine evolution as it identifies the helical cytokines shared by fish and mammals that, consequently, existed before the divergence of teleosts and tetrapods. A 'fish-mammalian' comparison will identify the class-I helical cytokines that still await discovery in fish or, alternatively, may have been evolutionarily recent additions to the mammalian cytokine repertoire.

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“…Human prolactin (hPRL), 2 growth hormone (hGH), and placental lactogen (hPL) are hormones belonging to the class 1 cytokine family (1). These three proteins share significant sequence homologies; the more closely related hPL and hPRL display 85% sequence identity, and hPRL shares a 23% identity with hGH.…”

mentioning

confidence: 99%

Obligate Ordered Binding of Human Lactogenic Cytokines

Voorhees

Brooks

2010

Journal of Biological Chemistry

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Class 1 cytokines bind two receptors to create an active heterotrimeric complex. It has been argued that ligand binding to their receptors is an ordered process, but a structural mechanism describing this process has not been determined. We have previously described an obligate ordered binding mechanism for the human prolactin/prolactin receptor heterotrimeric complex. In this work we expand this conceptual understanding of ordered binding to include three human lactogenic hormones: prolactin, growth hormone, and placental lactogen. We independently blocked either of the two receptor binding sites of each hormone and used surface plasmon resonance to measure human prolactin receptor binding kinetics and stoichiometries to the remaining binding surface. When site 1 of any of the three hormones was blocked, site 2 could not bind the receptor. But blocking site 2 did not affect receptor binding at site 1, indicating a requirement for receptor binding to site 1 before site 2 binding. In addition we noted variable responses to the presence of zinc in hormone-receptor interaction. Finally, we performed Förster resonance energy transfer (FRET) analyses where receptor binding at subsaturating stoichiometries induced changes in FRET signaling, indicative of binding-induced changes in hormone conformation, whereas at receptor: hormone ratios in excess of 2:1 no additional changes in FRET signaling were observed. These results strongly support a conformationally mediated obligate-ordered receptor binding for each of the three lactogenic hormones.Human prolactin (hPRL), 2 growth hormone (hGH), and placental lactogen (hPL) are hormones belonging to the class 1 cytokine family (1). These three proteins share significant sequence homologies; the more closely related hPL and hPRL display 85% sequence identity, and hPRL shares a 23% identity with hGH. Each of these four-helix bundle proteins is recognized as a lactogenic hormone based on their ability to bind and activate primate prolactin receptors (2). The binding reaction that takes place between lactogenic hormones and the prolactin receptor results in the formation of a heterotrimeric complex with a 2:1 ratio of receptor to hormone (3) (Fig. 1). The formation of this ternary complex is believed to proceed in an ordered process in which the N-terminal S1 subdomain of the prolactin receptor first binds at a hormone surface comprised of elements of helices 1 and 4 as well as the sequence connecting helices 1 and 2 (site 1) before subsequently binding a second prolactin receptor by its S1 subdomain at a hormone surface composed of elements of helices 1 and 3 (site 2). During secondary receptor binding, an additional receptor-receptor binding surface is formed between the C-terminal S2 subdomains of the membrane-bound receptors and is distal to the bound hormone. Thus, for site 2 the ⌬G is divided between the hormone/ receptor interfaces and the two interacting S2 receptor surfaces. The formation of this extracellular trimolecular complex orients the intracellular domains of the...

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Multiple and highly divergent IL-11 genes in teleost fish

Cited by 64 publications

References 55 publications

Two divergent leptin paralogues in zebrafish (Danio rerio) that originate early in teleostean evolution

Two divergent leptin paralogues in zebrafish (Danio rerio) that originate early in teleostean evolution

Phylogeny and evolution of class-I helical cytokines

Obligate Ordered Binding of Human Lactogenic Cytokines

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