Cargando…

Ovarian activation delays in peripubertal ewe lambs infected with Haemonchus contortus can be avoided by supplementing protein in their diets

BACKGROUND: The ewe lamb nutritional and physiological state interfere with the ovarian environment and fertility. The lack or excess of circulating nutrients reaching the ovary can change its gene expression. A protein deficiency in the blood caused by an Haemonchus contortus abomasal infection is...

Descripción completa

Detalles Bibliográficos
Autores principales: Suarez-Henriques, Paula, de Miranda e Silva Chaves, Camila, Cardoso-Leite, Ricardo, Gomes-Caldas, Danielle G., Morita-Katiki, Luciana, Tsai, Siu Mui, Louvandini, Helder
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8565066/
https://www.ncbi.nlm.nih.gov/pubmed/34732186
http://dx.doi.org/10.1186/s12917-021-03020-7
_version_ 1784593742450130944
author Suarez-Henriques, Paula
de Miranda e Silva Chaves, Camila
Cardoso-Leite, Ricardo
Gomes-Caldas, Danielle G.
Morita-Katiki, Luciana
Tsai, Siu Mui
Louvandini, Helder
author_facet Suarez-Henriques, Paula
de Miranda e Silva Chaves, Camila
Cardoso-Leite, Ricardo
Gomes-Caldas, Danielle G.
Morita-Katiki, Luciana
Tsai, Siu Mui
Louvandini, Helder
author_sort Suarez-Henriques, Paula
collection PubMed
description BACKGROUND: The ewe lamb nutritional and physiological state interfere with the ovarian environment and fertility. The lack or excess of circulating nutrients reaching the ovary can change its gene expression. A protein deficiency in the blood caused by an Haemonchus contortus abomasal infection is detrimental to the organism’s development during puberty. The peripubertal period is a time of intensive growth that requires a high level of nutrients. An essential feature controlling pubertal arousal and female reproductive potential is ovarian follicle growth activation. Protein supplementation improves the sheep’s immune response to helminthic infections. We aimed to determine if supplementing protein in infected ewe lambs’ diet would impact the ovarian environment leading to earlier ovarian follicle activation than in infected not supplemented animals. METHODS: We fed 18 Santa Ines ewe lambs (Ovis aries) - bred by the same ram - with either 12% protein (Control groups) or 19% protein (Supplemented groups) in their diets. After 35 days of the diet, they were each artificially infected or not with 10,000 Haemonchus contortus L3 larvae. Following 77 days of the diet and 42 days of infection, we surgically collected their left ovaries and examined their genes expression through RNA sequencing. RESULTS: We found that protein supplementation in infected animals led to an up-regulation of genes (FDR p-values < 0.05) and biological processes (p-value cut-off = 0.01) linked to meiotic activation in pre-ovulatory follicles and primordial follicle activation, among others. The supplemented not infected animals also up-regulated genes and processes linked to meiosis and others, such as circadian behaviour. The not supplemented animals had these same processes down-regulated while up-regulated processes related to tissue morphogenesis, inflammation and immune response. CONCLUSION: Diet’s protein supplementation of peripubertal infected animals allowed them to express genes related to a more mature ovarian follicle stage than their half-sisters that were not supplemented. These results could be modelling potential effects of the interaction between environmental factors, nutrition and infection on reproductive health. When ovarian activation is achieved in a timely fashion, the ewe may generate more lambs during its reproductive life, increasing sheep breeders’ productivity. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12917-021-03020-7.
format Online
Article
Text
id pubmed-8565066
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-85650662021-11-04 Ovarian activation delays in peripubertal ewe lambs infected with Haemonchus contortus can be avoided by supplementing protein in their diets Suarez-Henriques, Paula de Miranda e Silva Chaves, Camila Cardoso-Leite, Ricardo Gomes-Caldas, Danielle G. Morita-Katiki, Luciana Tsai, Siu Mui Louvandini, Helder BMC Vet Res Research BACKGROUND: The ewe lamb nutritional and physiological state interfere with the ovarian environment and fertility. The lack or excess of circulating nutrients reaching the ovary can change its gene expression. A protein deficiency in the blood caused by an Haemonchus contortus abomasal infection is detrimental to the organism’s development during puberty. The peripubertal period is a time of intensive growth that requires a high level of nutrients. An essential feature controlling pubertal arousal and female reproductive potential is ovarian follicle growth activation. Protein supplementation improves the sheep’s immune response to helminthic infections. We aimed to determine if supplementing protein in infected ewe lambs’ diet would impact the ovarian environment leading to earlier ovarian follicle activation than in infected not supplemented animals. METHODS: We fed 18 Santa Ines ewe lambs (Ovis aries) - bred by the same ram - with either 12% protein (Control groups) or 19% protein (Supplemented groups) in their diets. After 35 days of the diet, they were each artificially infected or not with 10,000 Haemonchus contortus L3 larvae. Following 77 days of the diet and 42 days of infection, we surgically collected their left ovaries and examined their genes expression through RNA sequencing. RESULTS: We found that protein supplementation in infected animals led to an up-regulation of genes (FDR p-values < 0.05) and biological processes (p-value cut-off = 0.01) linked to meiotic activation in pre-ovulatory follicles and primordial follicle activation, among others. The supplemented not infected animals also up-regulated genes and processes linked to meiosis and others, such as circadian behaviour. The not supplemented animals had these same processes down-regulated while up-regulated processes related to tissue morphogenesis, inflammation and immune response. CONCLUSION: Diet’s protein supplementation of peripubertal infected animals allowed them to express genes related to a more mature ovarian follicle stage than their half-sisters that were not supplemented. These results could be modelling potential effects of the interaction between environmental factors, nutrition and infection on reproductive health. When ovarian activation is achieved in a timely fashion, the ewe may generate more lambs during its reproductive life, increasing sheep breeders’ productivity. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12917-021-03020-7. BioMed Central 2021-11-03 /pmc/articles/PMC8565066/ /pubmed/34732186 http://dx.doi.org/10.1186/s12917-021-03020-7 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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
Suarez-Henriques, Paula
de Miranda e Silva Chaves, Camila
Cardoso-Leite, Ricardo
Gomes-Caldas, Danielle G.
Morita-Katiki, Luciana
Tsai, Siu Mui
Louvandini, Helder
Ovarian activation delays in peripubertal ewe lambs infected with Haemonchus contortus can be avoided by supplementing protein in their diets
title Ovarian activation delays in peripubertal ewe lambs infected with Haemonchus contortus can be avoided by supplementing protein in their diets
title_full Ovarian activation delays in peripubertal ewe lambs infected with Haemonchus contortus can be avoided by supplementing protein in their diets
title_fullStr Ovarian activation delays in peripubertal ewe lambs infected with Haemonchus contortus can be avoided by supplementing protein in their diets
title_full_unstemmed Ovarian activation delays in peripubertal ewe lambs infected with Haemonchus contortus can be avoided by supplementing protein in their diets
title_short Ovarian activation delays in peripubertal ewe lambs infected with Haemonchus contortus can be avoided by supplementing protein in their diets
title_sort ovarian activation delays in peripubertal ewe lambs infected with haemonchus contortus can be avoided by supplementing protein in their diets
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8565066/
https://www.ncbi.nlm.nih.gov/pubmed/34732186
http://dx.doi.org/10.1186/s12917-021-03020-7
work_keys_str_mv AT suarezhenriquespaula ovarianactivationdelaysinperipubertalewelambsinfectedwithhaemonchuscontortuscanbeavoidedbysupplementingproteinintheirdiets
AT demirandaesilvachavescamila ovarianactivationdelaysinperipubertalewelambsinfectedwithhaemonchuscontortuscanbeavoidedbysupplementingproteinintheirdiets
AT cardosoleitericardo ovarianactivationdelaysinperipubertalewelambsinfectedwithhaemonchuscontortuscanbeavoidedbysupplementingproteinintheirdiets
AT gomescaldasdanielleg ovarianactivationdelaysinperipubertalewelambsinfectedwithhaemonchuscontortuscanbeavoidedbysupplementingproteinintheirdiets
AT moritakatikiluciana ovarianactivationdelaysinperipubertalewelambsinfectedwithhaemonchuscontortuscanbeavoidedbysupplementingproteinintheirdiets
AT tsaisiumui ovarianactivationdelaysinperipubertalewelambsinfectedwithhaemonchuscontortuscanbeavoidedbysupplementingproteinintheirdiets
AT louvandinihelder ovarianactivationdelaysinperipubertalewelambsinfectedwithhaemonchuscontortuscanbeavoidedbysupplementingproteinintheirdiets