Monotreme <i>IGF2</i> expression and ancestral origin of genomic imprinting

Killian, J. Keith; Nolan, Catherine M.; Stewart, Niall; Munday, B. L.; Andersen, Niels A.; Nicol, Stewart C.; Jirtle, Randy L.

doi:10.1002/jez.1070

Cited by 119 publications

(88 citation statements)

References 38 publications

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“…This observation underscores the importance of broad taxonomic sampling for understanding the function and evolution of pathways important to human health-for which rodent models may not always be the most appropriate. Together, our molecular evolution and expression data suggest that the IGF2 protein may have a more stable role in IIS/TOR signaling across reptiles, in contrast to the more variable and specialized roles of IGF2 across mammals (64).…”

Section: Members Of Iis/tor Network Are Outliers In Evolutionary Ratementioning

confidence: 79%

Rapid molecular evolution across amniotes of the IIS/TOR network

McGaugh

Bronikowski

Kuo

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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The insulin/insulin-like signaling and target of rapamycin (IIS/TOR) network regulates lifespan and reproduction, as well as metabolic diseases, cancer, and aging. Despite its vital role in health, comparative analyses of IIS/TOR have been limited to invertebrates and mammals. We conducted an extensive evolutionary analysis of the IIS/TOR network across 66 amniotes with 18 newly generated transcriptomes from nonavian reptiles and additional available genomes/transcriptomes. We uncovered rapid and extensive molecular evolution between reptiles (including birds) and mammals: (i) the IIS/TOR network, including the critical nodes insulin receptor substrate (IRS) and phosphatidylinositol 3-kinase (PI3K), exhibit divergent evolutionary rates between reptiles and mammals; (ii) compared with a proxy for the rest of the genome, genes of the IIS/TOR extracellular network exhibit exceptionally fast evolutionary rates; and (iii) signatures of positive selection and coevolution of the extracellular network suggest reptile-and mammal-specific interactions between members of the network. In reptiles, positively selected sites cluster on the binding surfaces of insulin-like growth factor 1 (IGF1), IGF1 receptor (IGF1R), and insulin receptor (INSR); whereas in mammals, positively selected sites clustered on the IGF2 binding surface, suggesting that these hormone-receptor binding affinities are targets of positive selection. Further, contrary to reports that IGF2R binds IGF2 only in marsupial and placental mammals, we found positively selected sites clustered on the hormone binding surface of reptile IGF2R that suggest that IGF2R binds to IGF hormones in diverse taxa and may have evolved in reptiles. These data suggest that key IIS/TOR paralogs have sub-or neofunctionalized between mammals and reptiles and that this network may underlie fundamental life history and physiological differences between these amniote sister clades.insulin signaling | insulin growth factor | molecular evolution | rapamycin T he last 20 y has provided overwhelming support that the insulin-and insulin-like signaling/target of rapamycin (IIS/TOR) molecular network responds to stress and nutrients and underlies a wide range of physiological functions (1); cancer, metabolic syndrome, and diabetes (2); and the timing of life events (e.g., growth, maturation, reproduction, and aging) (3). The vertebrate IIS/TOR network consists of peptide hormones, binding proteins that regulate hormone bioavailability, and cell membrane receptors (hereafter, extracellular proteins of the IIS/TOR network) that induce an intracellular signaling cascade (hereafter, intracellular proteins of the IIS/TOR network) to stimulate cell proliferation, survival, and metabolism (Fig. S1). The core intracellular signal transduction genes in this network are largely conserved across deep phylogenetic time (4, 5). In contrast, genes encoding the IIS/TOR extracellular network have diverged in the vertebrate lineage (6-8) and may have variable roles among taxa (9, 10). Despite its central rol...

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Section: Members Of Iis/tor Network Are Outliers In Evolutionary Ratementioning

confidence: 79%

Rapid molecular evolution across amniotes of the IIS/TOR network

McGaugh

Bronikowski

Kuo

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…The net function of this activity is to attenuate IGF-II-driven proliferation and growth. During gestation, IGFR-2 serves a crucial global function because it prevents fetal overgrowth and birth-related injury due to fetal-pelvic disproportion (Lau et al 1994, Wang et al 1994, D'Ercole 1999, Killian et al 2000, 2001a, Young et al 2001. However, release from IGFR-2 growth attenuation in the perinatal period is a developmental event that is not well studied and could be sensitive to glucocorticoids.…”

Section: Introductionmentioning

confidence: 99%

The cellular repressor of E1A-stimulated genes mediates glucocorticoid-induced loss of the type-2 IGF receptor in ileal epithelial cells

Gordon

Paxton²,

Fox³

2005

Journal of Endocrinology

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Glucocorticoids induce hypertrophy of the neonatal ileal mucosa but the molecular mechanisms behind this growth induction remain poorly understood. Ileal epithelial cells (IECs) are dependent upon IGF-II for proliferation both in vivo and in culture. The type-2 IGF receptor (IGFR-2) is a lysosomal transport protein that attenuates IGF-IIdriven growth and is highly abundant in the ileum. The cellular repressor of E1A-stimulated genes (CREG) is a secreted phosphoglycoprotein that affects cell fate via ligand binding with IGFR-2, although the mechanism by which it does so is unknown. We hypothesized that glucocorticoids might facilitate IGF-mediated hypertrophy through CREG-mediated degradation of IGFR-2. To test this hypothesis, confluent rat IECs (IEC-18) were cultured for 72 h with or without dexamethasone (DEX) and harvested for Western blot, immunocytochemistry, gene array and CREG immunoneutralization experiments.IGFR-2 and CREG immunohistochemistry were also performed in archived ileal specimens from control and DEX-exposed newborn mice and extremely premature infants to investigate in vivo and clinical relevance. DEX exposure was found to diminish IGFR-2 immunolocalization in cultured rat IECs, newborn mouse ileal mucosa and human neonatal ileal mucosa. Gene array data indicated that IGFR-2 expression was unchanged with DEX treatment, suggesting a mechanism of protein degradation. CREG immunolocalization and abundance was found to be increased by DEX and immunoneutralization of CREG resulted in the abolition of IGFR-2 degradation. We have concluded that CREG is a secreted mediator by which DEX induces degradation of IGFR-2 and speculate that this is a fundamental mechanism of mucosal growth induction.

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“…This scenario is consistent with the far greater homology of the X and Y in monotremes, where there is no opportunity for prenatal conflicts for resources (although some might be expected postnatally), and no evidence of parental imprinting has been found. (20) If correct, this scenario suggests that Y degeneration followed (rather than preceded) the evolution of imprinting. The two scenarios that I have outlined are not mutually exclusive.…”

Section: Introductionmentioning

confidence: 99%

The evolution of the peculiarities of mammalian sex chromosomes: an epigenetic view

Jablonka

2004

BioEssays

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SummaryIn most discussions of the evolution of sex chromosomes, it is presumed that the morphological differences between the X and Y were initiated by genetic changes. An alternative possibility is that, in the early stages, a key role was played by epigenetic modifications of chromatin structure that did not depend directly on genetic changes. Such modifications could have resulted from spontaneous epimutations at a sex-determining locus or, in mammals, from selection in females for the epigenetic silencing of imprinted regions of the paternally derived sex chromosome. Other features of mammalian sex chromosomes that are easier to explain if the epigenetic dimension of chromosome evolution is considered include the relatively large number of X-linked genes associated with human brain development, and the overrepresentation of spermatogenesis genes on the X. Both may be evolutionary consequences of dosage compensation through X-inactivation.

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Monotreme IGF2 expression and ancestral origin of genomic imprinting

Cited by 119 publications

References 38 publications

Rapid molecular evolution across amniotes of the IIS/TOR network

Rapid molecular evolution across amniotes of the IIS/TOR network

The cellular repressor of E1A-stimulated genes mediates glucocorticoid-induced loss of the type-2 IGF receptor in ileal epithelial cells

The evolution of the peculiarities of mammalian sex chromosomes: an epigenetic view

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