Publications by authors named "Benjamin Mayne"

10 Publications

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Nonlethal age estimation of three threatened fish species using DNA methylation: Australian lungfish, Murray cod and Mary River cod.

Mol Ecol Resour 2021 Oct 23;21(7):2324-2332. Epub 2021 Jun 23.

School of Biological Sciences, The University of Western Australia, Crawley, WA, Australia.

Age-based demography is fundamental to management of wild fish populations. Age estimates for individuals can determine rates of change in key life-history parameters such as length, maturity, mortality and fecundity. These age-based characteristics are critical for population viability analysis in endangered species and for developing sustainable harvest strategies. For teleost fish, age has traditionally been determined by counting increments formed in calcified structures such as otoliths. However, the collection of otoliths is lethal and therefore undesirable for threatened species. At a molecular level, age can be predicted by measuring DNA methylation. Here, we use previously identified age-associated sites of DNA methylation in zebrafish (Danio rerio) to develop two epigenetic clocks for three threatened freshwater fish species. One epigenetic clock was developed for the Australian lungfish (Neoceratodus forsteri) and the second for the Murray cod (Maccullochella peelii) and Mary River cod (Maccullochella mariensis). Age estimation models were calibrated using either known-age individuals, ages derived from otoliths or bomb radiocarbon dating of scales. We demonstrate a high Pearson's correlation between the chronological and predicted age in both the Lungfish clock (cor = .98) and Maccullochella clock (cor = .92). The median absolute error rate for both epigenetic clocks was also low (Lungfish = 0.86 years; Maccullochella = 0.34 years). This study demonstrates the transferability of DNA methylation sites for age prediction between highly phylogenetically divergent fish species. Given the method is nonlethal and suited to automation, age prediction by DNA methylation has the potential to improve fisheries and other wildlife management settings.
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http://dx.doi.org/10.1111/1755-0998.13440DOI Listing
October 2021

Optimal sample size for calibrating DNA methylation age estimators.

Mol Ecol Resour 2021 Oct 18;21(7):2316-2323. Epub 2021 Jun 18.

School of Biological Sciences, The University of Western Australia, Perth, WA, Australia.

Age is a fundamental parameter in wildlife management as it is used to determine the risk of extinction, manage invasive species, and regulate sustainable harvest. In a broad variety of vertebrates species, age can be determined by measuring DNA methylation. Animals with known ages are initially required during development, calibration, and validation of these epigenetic clocks. However, wild animals with known ages are frequently difficult to obtain. Here, we perform Monte-Carlo simulations to determine the optimal sample size required to create an accurate calibration model for age estimation by elastic net regression modelling of cytosine-phosphate-guanine methylation data. Our results suggest a minimum calibration population size of 70, but ideally 134 individuals or more for accurate and precise models. We also provide estimates to the extent a model can be extrapolated beyond a distribution of ages that was used during calibration. The findings can assist researchers to better design age estimation models and decide if their model is adequate for determining key population attributes.
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http://dx.doi.org/10.1111/1755-0998.13437DOI Listing
October 2021

A DNA methylation age predictor for zebrafish.

Aging (Albany NY) 2020 12 23;12(24):24817-24835. Epub 2020 Dec 23.

School of Biological Sciences, The University of Western Australia, Perth, Western Australia, Australia.

Changes in DNA methylation at specific CpG sites have been used to build predictive models to estimate animal age, predominantly in mammals. Little testing for this effect has been conducted in other vertebrate groups, such as bony fish, the largest vertebrate class. The development of most age-predictive models has relied on a genome-wide sequencing method to obtain a DNA methylation level, which makes it costly to deploy as an assay to estimate age in many samples. Here, we have generated a reduced representation bisulfite sequencing data set of caudal fin tissue from a model fish species, zebrafish (), aged from 11.9-60.1 weeks. We identified changes in methylation at specific CpG sites that correlated strongly with increasing age. Using an optimised unique set of 26 CpG sites we developed a multiplex PCR assay that predicts age with an average median absolute error rate of 3.2 weeks in zebrafish between 10.9-78.1 weeks of age. We also demonstrate the use of multiplex PCR as an efficient quantitative approach to measure DNA methylation for the use of age estimation. This study highlights the potential further use of DNA methylation as an age estimation method in non-mammalian vertebrate species.
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http://dx.doi.org/10.18632/aging.202400DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7803548PMC
December 2020

Lifespan estimation in marine turtles using genomic promoter CpG density.

PLoS One 2020 31;15(7):e0236888. Epub 2020 Jul 31.

School of Biological Sciences, University of Western Australia, Perth, Western Australia, Australia.

Maximum lifespan for most animal species is difficult to define. This is challenging for wildlife management as it is critical for estimating important aspects of population biology such as mortality rate, population viability, and period of reproductive potential. Recently, it has been shown cytosine-phosphate-guanine (CpG) density is predictive of maximum lifespan in vertebrates. This has made it possible to predict lifespan in long-lived species, which are generally the most intractable. In this study, we use gene promoter CpG density to predict the lifespan of five marine turtle species. Marine turtles are a particularly difficult group for lifespan estimation because of their migratory behaviour, longevity and high juvenile mortality rates, which all restrict individual tracking over their lifespan. Sanger sequencing was used to determine the CpG density in selected promoters. We predicted the lifespans for marine turtle species ranged from 50.4 years (flatback turtle, Natator depressus) to 90.4 years (leatherback turtle, Dermochelys coriacea). These lifespan predictions have broad applications in marine turtle research such as better understanding life cycles and determining population viability.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0236888PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7394378PMC
September 2020

A genomic predictor of lifespan in vertebrates.

Sci Rep 2019 12 12;9(1):17866. Epub 2019 Dec 12.

Environomics Future Science Platform, Indian Oceans Marine Research Centre, Commonwealth Scientific and Industrial Research Organisation, Crawley, Western Australia, Australia.

Biological ageing and its mechanistic underpinnings are of immense biomedical and ecological significance. Ageing involves the decline of diverse biological functions and places a limit on a species' maximum lifespan. Ageing is associated with epigenetic changes involving DNA methylation. Furthermore, an analysis of mammals showed that the density of CpG sites in gene promoters, which are targets for DNA methylation, is correlated with lifespan. Using 252 whole genomes and databases of animal age and promotor sequences, we show a pattern across vertebrates. We also derive a predictive lifespan clock based on CpG density in a selected set of promoters. The lifespan clock accurately predicts maximum lifespan in vertebrates (R = 0.76) from the density of CpG sites within only 42 selected promoters. Our lifespan clock provides a wholly new method for accurately estimating lifespan using genome sequences alone and enables estimation of this challenging parameter for both poorly understood and extinct species.
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http://dx.doi.org/10.1038/s41598-019-54447-wDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6908713PMC
December 2019

msgbsR: An R package for analysing methylation-sensitive restriction enzyme sequencing data.

Sci Rep 2018 02 1;8(1):2190. Epub 2018 Feb 1.

Robinson Research Institute, University of Adelaide, Adelaide, SA, 5005, Australia.

Genotyping-by-sequencing (GBS) or restriction-site associated DNA marker sequencing (RAD-seq) is a practical and cost-effective method for analysing large genomes from high diversity species. This method of sequencing, coupled with methylation-sensitive enzymes (often referred to as methylation-sensitive restriction enzyme sequencing or MRE-seq), is an effective tool to study DNA methylation in parts of the genome that are inaccessible in other sequencing techniques or are not annotated in microarray technologies. Current software tools do not fulfil all methylation-sensitive restriction sequencing assays for determining differences in DNA methylation between samples. To fill this computational need, we present msgbsR, an R package that contains tools for the analysis of methylation-sensitive restriction enzyme sequencing experiments. msgbsR can be used to identify and quantify read counts at methylated sites directly from alignment files (BAM files) and enables verification of restriction enzyme cut sites with the correct recognition sequence of the individual enzyme. In addition, msgbsR assesses DNA methylation based on read coverage, similar to RNA sequencing experiments, rather than methylation proportion and is a useful tool in analysing differential methylation on large populations. The package is fully documented and available freely online as a Bioconductor package ( https://bioconductor.org/packages/release/bioc/html/msgbsR.html ).
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http://dx.doi.org/10.1038/s41598-018-19655-wDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5794748PMC
February 2018

Accelerated placental aging in early onset preeclampsia pregnancies identified by DNA methylation.

Epigenomics 2017 03 29;9(3):279-289. Epub 2016 Nov 29.

Robinson Research Institute, University of Adelaide, SA, 5005, Australia.

Aim: To determine whether dynamic DNA methylation changes in the human placenta can be used to predict gestational age.

Materials & Methods: Publicly available placental DNA methylation data from 12 studies, together with our own dataset, using Illumina Infinium Human Methylation BeadChip arrays.

Results & Conclusion: We developed an accurate tool for predicting gestational age of placentas using 62 CpG sites. There was a higher predicted gestational age for placentas from early onset preeclampsia cases, but not term preeclampsia, compared with their chronological age. Therefore, early onset preeclampsia is associated with placental aging. Gestational age acceleration prediction from DNA methylation array data may provide insight into the molecular mechanisms of pregnancy disorders.
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http://dx.doi.org/10.2217/epi-2016-0103DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6040051PMC
March 2017

Large Scale Gene Expression Meta-Analysis Reveals Tissue-Specific, Sex-Biased Gene Expression in Humans.

Front Genet 2016 13;7:183. Epub 2016 Oct 13.

Robinson Research Institute, University of AdelaideAdelaide, SA, Australia; Adelaide Medical School, University of AdelaideAdelaide, SA, Australia.

The severity and prevalence of many diseases are known to differ between the sexes. Organ specific sex-biased gene expression may underpin these and other sexually dimorphic traits. To further our understanding of sex differences in transcriptional regulation, we performed meta-analyses of sex biased gene expression in multiple human tissues. We analyzed 22 publicly available human gene expression microarray data sets including over 2500 samples from 15 different tissues and 9 different organs. Briefly, by using an inverse-variance method we determined the effect size difference of gene expression between males and females. We found the greatest sex differences in gene expression in the brain, specifically in the anterior cingulate cortex, (1818 genes), followed by the heart (375 genes), kidney (224 genes), colon (218 genes), and thyroid (163 genes). More interestingly, we found different parts of the brain with varying numbers and identity of sex-biased genes, indicating that specific cortical regions may influence sexually dimorphic traits. The majority of sex-biased genes in other tissues such as the bladder, liver, lungs, and pancreas were on the sex chromosomes or involved in sex hormone production. On average in each tissue, 32% of autosomal genes that were expressed in a sex-biased fashion contained androgen or estrogen hormone response elements. Interestingly, across all tissues, we found approximately two-thirds of autosomal genes that were sex-biased were not under direct influence of sex hormones. To our knowledge this is the largest analysis of sex-biased gene expression in human tissues to date. We identified many sex-biased genes that were not under the direct influence of sex chromosome genes or sex hormones. These may provide targets for future development of sex-specific treatments for diseases.
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http://dx.doi.org/10.3389/fgene.2016.00183DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5062749PMC
October 2016

First trimester trophoblasts forming endothelial-like tubes in vitro emulate a 'blood vessel development' gene expression profile.

Gene Expr Patterns 2016 07 21;21(2):103-10. Epub 2016 May 21.

School of Medicine, Robinson Research Institute, University of Adelaide, Adelaide, South Australia, Australia.

Extravillous cytotrophoblasts isolated from first trimester placenta, and immortalised cell lines derived from them, have the intrinsic ability to form endothelial-like tubes when cultured on Matrigel™ extracellular matrix. This in vitro tube formation may model placental angiogenesis and/or endovascular differentiation by trophoblasts. To interpret the relevance of this phenomenon to placental development, we used a gene expression microarray approach to identify which genes and pathways are associated with the tube-forming phenotype of HTR8/SVneo first trimester trophoblasts (HTR8-M), compared with HTR8/SVneo not forming tubes on plastic culture surface (HTR8-P). Furthermore, we used weighted gene co-expression network analysis (WGCNA) of microarray data to identify modules of co-expressed genes underlying the biological processes. There were 481 genes differentially expressed between HTR8-M and HTR8-P and these were significantly enriched for blood vessel development and related gene ontologies. WGCNA clustered the genes into 9 co-expression modules. One module was significantly associated with HTR8-M (p = 1.15E-05) and contained genes involved in actin cytoskeleton organization, cell migration and blood vessel development, consistent with tube formation on Matrigel. Another module was significantly associated with HTR8-P (p = 1.94E-05) and was enriched for genes involved in mitosis, consistent with proliferation by cells on plastic which do not differentiate. Up-regulation of angiogenesis and vascular development pathways in endovascular trophoblasts in vivo could underpin spiral artery remodelling processes, which are defective in preeclamptic pregnancies.
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http://dx.doi.org/10.1016/j.gep.2016.05.001DOI Listing
July 2016

Recent progress towards understanding the role of DNA methylation in human placental development.

Reproduction 2016 07 29;152(1):R23-30. Epub 2016 Mar 29.

Robinson Research InstituteUniversity of Adelaide, Adelaide, South Australia, Australia School of MedicineUniversity of Adelaide, Adelaide, South Australia, Australia.

Epigenetic modifications, and particularly DNA methylation, have been studied in many tissues, both healthy and diseased, and across numerous developmental stages. The placenta is the only organ that has a transient life of 9 months and undergoes rapid growth and dynamic structural and functional changes across gestation. Additionally, the placenta is unique because although developing within the mother, its genome is identical to that of the foetus. Given these distinctive characteristics, it is not surprising that the epigenetic landscape affecting placental gene expression may be different to that in other healthy tissues. However, the role of epigenetic modifications, and particularly DNA methylation, in placental development remains largely unknown. Of particular interest is the fact that the placenta is the most hypomethylated human tissue and is characterized by the presence of large partially methylated domains (PMDs) containing silenced genes. Moreover, how and why the placenta is hypomethylated and what role DNA methylation plays in regulating placental gene expression across gestation are poorly understood. We review genome-wide DNA methylation studies in the human placenta and highlight that the different cell types that make up the placenta have very different DNA methylation profiles. Summarizing studies on DNA methylation in the placenta and its relationship with pregnancy complications are difficult due to the limited number of studies available for comparison. To understand the key steps in placental development and hence what may be perturbed in pregnancy complications requires large-scale genome-wide DNA methylation studies coupled with transcriptome analyses.
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http://dx.doi.org/10.1530/REP-16-0014DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5064761PMC
July 2016
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