IGF‐I and the IGF‐I receptor in development of nonmammalian vertebrates

Pablo, Flora de; Pérez-Villamil, Beatriz; Serna, J; González-Guerrero, P. R.; López-Carranza, A; Rosa, Enrique J. de la; Alemany, Jorge; Caldés, Trinidad

doi:10.1002/mrd.1080350418

Cited by 43 publications

(18 citation statements)

References 30 publications

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“…IGFs are known to be critical for proper cell growth and differentiation during vertebrate development (De Pablo et al, 1993;Dupont and Holzenberger, 2003;Eivers et al, 2004; …”

Section: Discussionmentioning

confidence: 99%

“…The IGF family includes IGF-I and IGF-II proteins, and both of these proteins have been shown to regulate various aspects of development in invertebrate and vertebrate embryos (Dupont and Holzenberger, 2003). Increased IGF signaling is almost always associated with increased cell growth, proliferation and differentiation in a variety of vertebrates including humans, birds and fish (De Pablo et al, 1993;Eivers et al, 2004;Furstenberger and Senn, 2002;Kajimura et al, 2005;Kamei et al, 2011;Oldham and Hafen, 2003;Salvatori, 2004). In mice, IGF-II null mutants grew to only 60% of normal birth weight and IGF-II −/−…”

Section: Introductionmentioning

confidence: 99%

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Insulin-like growth factor signaling regulates developmental trajectory associated with diapause in embryos of the annual killifish Austrofundulus limnaeus

Woll

Podrabsky

2017

Journal of Experimental Biology

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Annual killifishes exhibit a number of unique life history characters including the occurrence of embryonic diapause, unique cell movements associated with dispersion and subsequent reaggregation of the embryonic blastomeres, and a short postembryonic life span. Insulin-like growth factor (IGF) signaling is known to play a role in the regulation of metabolic dormancy in a number of animals but has not been explored in annual killifishes. The abundance of IGF proteins during development and the developmental effects of blocking IGF signaling by pharmacological inhibition of the insulin-like growth factor I receptor (IGF1R) were explored in embryos of the annual killifish Austrofundulus limnaeus. Blocking of IGF signaling in embryos that would normally escape entrance into diapause resulted in a phenotype that was remarkably similar to that of embryos entering diapause. IGF-I protein abundance spikes during early development in embryos that will not enter diapause. In contrast, IGF-I levels remain low during early development in embryos that will enter diapause II. IGF-II protein is packaged at higher levels in escape-bound embryos compared with diapause-bound embryos. However, IGF-II levels quickly decrease and remain low during early development and only increase substantially during late development in both developmental trajectories. Developmental patterns of IGF-I and IGF-II protein abundance under conditions that would either induce or bypass entrance into diapause are consistent with a role for IGF signaling in the regulation of developmental trajectory and entrance into diapause in this species. We propose that IGF signaling may be a unifying regulatory pathway that explains the larger suite of characters that are associated with the complex life history of annual killifishes.

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“…IGFs are known to be critical for proper cell growth and differentiation during vertebrate development (De Pablo et al, 1993;Dupont and Holzenberger, 2003;Eivers et al, 2004; …”

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Insulin-like growth factor signaling regulates developmental trajectory associated with diapause in embryos of the annual killifish Austrofundulus limnaeus

Woll

Podrabsky

2017

Journal of Experimental Biology

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“…Accordingly, other classes of membrane and nuclear receptors are expressed in the developing retina of the chicken embryo, including glucocorticoid hormone receptors (Ben-Or and Dovrat, 1980;Koehler and Moscona, 1975), insulin-like growth factor receptors (de Pablo et al, 1993), fibroblast growth factor receptors (Tcheng et al, 1994a), integrins (Bradshaw et al, 1995;Bronner-Fraser et al, 1992;de Curtis and Reichardt, 1993), and thyroid hormone receptors (TRs) (Sjøberg et al, 1992). Of these, only the thyroid hormone receptor TR␤2 variant appears to have a protracted expression pattern within the apical retinal epithelium that might be consistent with photoreceptor-specific expression (Sjøberg et al, 1992).…”

Section: Expression Of Other Receptors In the Developing Retina Of Thmentioning

confidence: 97%

Retinoid X receptor ? gene transcripts are expressed by a subset of early generated retinal cells and eventually restricted to photoreceptors

Hoover

Seleiro²,

Kielland

et al. 1998

J. Comp. Neurol.

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We have examined the distribution of the retinoid X receptor gamma (RXRgamma) in the developing chicken retina by using in situ hybridization and RNase protection assays. We detected RXRgamma transcripts as early as 4 days of embryonic development (d4) in central regions of the retina, spreading to more peripheral regions by d8. The first few RXRgamma-positive cells were scattered within the depth of the retinal neuroepithelium, but as they increased in number they became localized predominantly to the apical (outer, ventricular) layer. The identity of the RXRgamma-positive cells at these stages is unknown, due to the lack of cell type-specific markers. By d10, when photoreceptors and ganglion cells have been generated and begun to establish their definitive layers, RXRgamma-positive cells were virtually restricted to the photoreceptor layer, and maintained this distribution to posthatch stages. RNase protection assays were performed on whole retinae to verify the temporal pattern of in situ hybridization results and showed that between d5 and d16 there was a significant increase in the mRNA levels of the RXRgamma2 isoform. Between d16 and early posthatch stages the level of RXRgamma2 mRNA did not change significantly. Consistent with previous studies, mRNA levels of the RXRgamma1 isoform were substantially lower than mRNA levels of the RXRgamma2 isoform at all time points examined. These results demonstrate that RXRgamma mRNA is expressed in photoreceptors in the developing chicken retina and implicate RXRgamma as the earliest marker of photoreceptor differentiation documented to date.

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“…see Duret et al 1998, Reinecke & Collet 1998, Kelley et al 2000. The involvement of these proteins in cellular anabolic processes is widespread throughout the animal world, where both ligand and receptor homologs are seen to regulate metabolite uptake, mitogenesis, synthetic and growth functions, and developmental processes (reviewed by Bern et al 1991, de Pablo et al 1993, Reinecke & Collet 1998, Upton et al 1998, Kelley et al 2000.…”

Section: Igf Peptidesmentioning

confidence: 99%

“…Thus, substantial molecular divergence between the insulin and IGF receptors is at least observable at the level of teleost fishes. DNA encoding receptors for insulin and IGF-I have also been cloned in an amphibian (Xenopus laevis; Scavo et al 1991, Groigno et al 1996, Zhu et al 1998, the chicken (see de Pablo et al 1993, Holzenberger et al 1996, McMurtry et al 1997, and Japanese quail (Coturnix coturnix japonica; Fu et al 2001), but not in any reptilian vertebrate.…”

Section: Igf Receptorsmentioning

confidence: 99%

Comparative endocrinology of the insulin-like growth factor-binding protein

Kelley¹,

Schmidt²,

Berg³

et al. 2002

Journal of Endocrinology

105

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Emerging early in chordate evolution, the IGF-regulatory axis diverged from an insulin-like predecessor into a vertebrate regulatory system specializing in cell growth activation and allied anabolic functions. Essential to the divergence of the IGF and insulin systems was an early presence of soluble IGF-binding proteins (IGFBPs), which bind IGF peptides at much higher affinity than that of the insulin receptor but at comparable affinities to that of the IGF receptor. IGFBPs have no homology with IGF receptors. Instead, IGFBPs are a derived group of proteins within a superfamily of cysteine-rich growth factors, whose members are found throughout the animal taxa. While blocking IGF actions through the insulin receptor is a fundamental role, IGFBPs evolved within the vertebrate line into centralized, 'integrators' of the endocrine growth-regulatory apparatus. IGFBPs have substantial influences on the distribution and bioavailability of IGF peptides in the cellular and physiological environments, but they have a variety of other properties. The six principal mammalian IGFBPs exhibit an array of specialized properties that appear to be derived from a complex evolutionary history (including cell membrane association, interaction with proteins that post-translationally modify them, direct IGF-independent effects on cells, and others) and they are regulated by a diversity of 'outside' factors (e.g. other hormones, metabolic status, stress). Thus, IGFBPs are multifunctional integrators having diverse physiological 'agendas'. Much less is known about IGFBPs and their properties in the other vertebrate taxa. Increasingly, however, it is being recognized that they play equally important endocrine roles, in both conserved and non-conserved ways, when compared with those currently defined in mammals. This review highlights selected 'comparative aspects' in current IGFBP research, in an attempt to view this essential group of endocrine regulators from a wider, biological perspective.

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IGF‐I and the IGF‐I receptor in development of nonmammalian vertebrates

Cited by 43 publications

References 30 publications

Insulin-like growth factor signaling regulates developmental trajectory associated with diapause in embryos of the annual killifish Austrofundulus limnaeus

Insulin-like growth factor signaling regulates developmental trajectory associated with diapause in embryos of the annual killifish Austrofundulus limnaeus

Retinoid X receptor ? gene transcripts are expressed by a subset of early generated retinal cells and eventually restricted to photoreceptors

Comparative endocrinology of the insulin-like growth factor-binding protein

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