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Multi-omics analysis reveals changes in tryptophan and cholesterol metabolism before and after sexual maturation in captive macaques

Rhesus macaques (Macaca mulatta, RMs) are widely used in sexual maturation studies due to their high genetic and physiological similarity to humans. However, judging sexual maturity in captive RMs based on blood physiological indicators, female menstruation, and male ejaculation behavior can be inac...

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Autores principales: Liu, Xu, Liu, Xuyuan, Wang, Xinqi, Shang, Ke, Li, Jiawei, Lan, Yue, Wang, Jiao, Li, Jing, Yue, Bisong, He, Miao, Fan, Zhenxin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10249198/
https://www.ncbi.nlm.nih.gov/pubmed/37286946
http://dx.doi.org/10.1186/s12864-023-09404-3
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author Liu, Xu
Liu, Xuyuan
Wang, Xinqi
Shang, Ke
Li, Jiawei
Lan, Yue
Wang, Jiao
Li, Jing
Yue, Bisong
He, Miao
Fan, Zhenxin
author_facet Liu, Xu
Liu, Xuyuan
Wang, Xinqi
Shang, Ke
Li, Jiawei
Lan, Yue
Wang, Jiao
Li, Jing
Yue, Bisong
He, Miao
Fan, Zhenxin
author_sort Liu, Xu
collection PubMed
description Rhesus macaques (Macaca mulatta, RMs) are widely used in sexual maturation studies due to their high genetic and physiological similarity to humans. However, judging sexual maturity in captive RMs based on blood physiological indicators, female menstruation, and male ejaculation behavior can be inaccurate. Here, we explored changes in RMs before and after sexual maturation based on multi-omics analysis and identified markers for determining sexual maturity. We found that differentially expressed microbiota, metabolites, and genes before and after sexual maturation showed many potential correlations. Specifically, genes involved in spermatogenesis (TSSK2, HSP90AA1, SOX5, SPAG16, and SPATC1) were up-regulated in male macaques, and significant changes in gene (CD36), metabolites (cholesterol, 7-ketolithocholic acid, and 12-ketolithocholic acid), and microbiota (Lactobacillus) related to cholesterol metabolism were also found, suggesting the sexually mature males have stronger sperm fertility and cholesterol metabolism compared to sexually immature males. In female macaques, most differences before and after sexual maturity were related to tryptophan metabolism, including changes in IDO1, IDO2, IFNGR2, IL1Β, IL10, L-tryptophan, kynurenic acid (KA), indole-3-acetic acid (IAA), indoleacetaldehyde, and Bifidobacteria, indicating that sexually mature females exhibit stronger neuromodulation and intestinal immunity than sexually immature females. Cholesterol metabolism-related changes (CD36, 7-ketolithocholic acid, 12-ketolithocholic acid) were also observed in female and male macaques. Exploring differences before and after sexual maturation through multi-omics, we identified potential biomarkers of sexual maturity in RMs, including Lactobacillus (for males) and Bifidobacterium (for females) valuable for RM breeding and sexual maturation research. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-023-09404-3.
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spelling pubmed-102491982023-06-09 Multi-omics analysis reveals changes in tryptophan and cholesterol metabolism before and after sexual maturation in captive macaques Liu, Xu Liu, Xuyuan Wang, Xinqi Shang, Ke Li, Jiawei Lan, Yue Wang, Jiao Li, Jing Yue, Bisong He, Miao Fan, Zhenxin BMC Genomics Research Rhesus macaques (Macaca mulatta, RMs) are widely used in sexual maturation studies due to their high genetic and physiological similarity to humans. However, judging sexual maturity in captive RMs based on blood physiological indicators, female menstruation, and male ejaculation behavior can be inaccurate. Here, we explored changes in RMs before and after sexual maturation based on multi-omics analysis and identified markers for determining sexual maturity. We found that differentially expressed microbiota, metabolites, and genes before and after sexual maturation showed many potential correlations. Specifically, genes involved in spermatogenesis (TSSK2, HSP90AA1, SOX5, SPAG16, and SPATC1) were up-regulated in male macaques, and significant changes in gene (CD36), metabolites (cholesterol, 7-ketolithocholic acid, and 12-ketolithocholic acid), and microbiota (Lactobacillus) related to cholesterol metabolism were also found, suggesting the sexually mature males have stronger sperm fertility and cholesterol metabolism compared to sexually immature males. In female macaques, most differences before and after sexual maturity were related to tryptophan metabolism, including changes in IDO1, IDO2, IFNGR2, IL1Β, IL10, L-tryptophan, kynurenic acid (KA), indole-3-acetic acid (IAA), indoleacetaldehyde, and Bifidobacteria, indicating that sexually mature females exhibit stronger neuromodulation and intestinal immunity than sexually immature females. Cholesterol metabolism-related changes (CD36, 7-ketolithocholic acid, 12-ketolithocholic acid) were also observed in female and male macaques. Exploring differences before and after sexual maturation through multi-omics, we identified potential biomarkers of sexual maturity in RMs, including Lactobacillus (for males) and Bifidobacterium (for females) valuable for RM breeding and sexual maturation research. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-023-09404-3. BioMed Central 2023-06-07 /pmc/articles/PMC10249198/ /pubmed/37286946 http://dx.doi.org/10.1186/s12864-023-09404-3 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Liu, Xu
Liu, Xuyuan
Wang, Xinqi
Shang, Ke
Li, Jiawei
Lan, Yue
Wang, Jiao
Li, Jing
Yue, Bisong
He, Miao
Fan, Zhenxin
Multi-omics analysis reveals changes in tryptophan and cholesterol metabolism before and after sexual maturation in captive macaques
title Multi-omics analysis reveals changes in tryptophan and cholesterol metabolism before and after sexual maturation in captive macaques
title_full Multi-omics analysis reveals changes in tryptophan and cholesterol metabolism before and after sexual maturation in captive macaques
title_fullStr Multi-omics analysis reveals changes in tryptophan and cholesterol metabolism before and after sexual maturation in captive macaques
title_full_unstemmed Multi-omics analysis reveals changes in tryptophan and cholesterol metabolism before and after sexual maturation in captive macaques
title_short Multi-omics analysis reveals changes in tryptophan and cholesterol metabolism before and after sexual maturation in captive macaques
title_sort multi-omics analysis reveals changes in tryptophan and cholesterol metabolism before and after sexual maturation in captive macaques
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10249198/
https://www.ncbi.nlm.nih.gov/pubmed/37286946
http://dx.doi.org/10.1186/s12864-023-09404-3
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