Heat-induced hyperthermia impacts the follicular fluid proteome of the periovulatory follicle in lactating dairy cows.

We hypothesized that heat-induced perturbations in cumulus cells surrounding the maturing oocyte may extend to the mural granulosa of the periovulatory follicle in the heat-stressed cow to subsequently the follicular fluid proteome. Lactating Holsteins were pharmacologically stimulated to have a dom...

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Main Authors: Louisa A Rispoli, J Lannett Edwards, Ky G Pohler, Stephen Russell, Richard I Somiari, Rebecca R Payton, F Neal Schrick
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2019-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0227095
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spelling doaj-b717b77cacda48619b5703e89f31cd692021-03-03T21:20:48ZengPublic Library of Science (PLoS)PLoS ONE1932-62032019-01-011412e022709510.1371/journal.pone.0227095Heat-induced hyperthermia impacts the follicular fluid proteome of the periovulatory follicle in lactating dairy cows.Louisa A RispoliJ Lannett EdwardsKy G PohlerStephen RussellRichard I SomiariRebecca R PaytonF Neal SchrickWe hypothesized that heat-induced perturbations in cumulus cells surrounding the maturing oocyte may extend to the mural granulosa of the periovulatory follicle in the heat-stressed cow to subsequently the follicular fluid proteome. Lactating Holsteins were pharmacologically stimulated to have a dominant follicle that was capable of responding to a gonadotropin releasing hormone-induced luteinizing hormone surge. Following gonadotropin releasing hormone administration, cows were maintained at ~67 temperature humidity index (THI; thermoneutral conditions) or exposed to conditions simulating an acute heat stress event (71 to 86 THI; heat stress for ~12 h). Dominant follicle collection was conducted in the periovulatory period ~16 h after gonadotropin releasing hormone. Follicular fluid proteome from thermoneutral (n = 5) and hyperthermic (n = 5) cows was evaluated by quantitative tandem mass spectrometry (nano LC-MS/MS). We identified 35 differentially-abundant proteins. Functional annotation revealed numerous immune-related proteins. Subsequent efforts revealed an increase in levels of the proinflammatory mediator bradykinin in follicular fluid (P = 0.0456) but not in serum (P = 0.9319) of hyperthermic cows. Intrafollicular increases in transferrin (negative acute phase protein) in hyperthermic cows (P = 0.0181) coincided with a tendency for levels to be increased in the circulation (P = 0.0683). Nine out of 15 cytokines evaluated were detected in follicular fluid. Heat stress increased intrafollicular interleukin 6 levels (P = 0.0160). Whether hyperthermia-induced changes in the heat-stressed cow's follicular fluid milieu reflect changes in mural granulosa, cumulus, other cell types secretions, and/or transudative changes from circulation remains unclear. Regardless of origin, heat stress/hyperthermia related changes in the follicular fluid milieu may have an impact on components important for ovulation and competence of the cumulus-oocyte complex contained within the periovulatory follicle.https://doi.org/10.1371/journal.pone.0227095
collection DOAJ
language English
format Article
sources DOAJ
author Louisa A Rispoli
J Lannett Edwards
Ky G Pohler
Stephen Russell
Richard I Somiari
Rebecca R Payton
F Neal Schrick
spellingShingle Louisa A Rispoli
J Lannett Edwards
Ky G Pohler
Stephen Russell
Richard I Somiari
Rebecca R Payton
F Neal Schrick
Heat-induced hyperthermia impacts the follicular fluid proteome of the periovulatory follicle in lactating dairy cows.
PLoS ONE
author_facet Louisa A Rispoli
J Lannett Edwards
Ky G Pohler
Stephen Russell
Richard I Somiari
Rebecca R Payton
F Neal Schrick
author_sort Louisa A Rispoli
title Heat-induced hyperthermia impacts the follicular fluid proteome of the periovulatory follicle in lactating dairy cows.
title_short Heat-induced hyperthermia impacts the follicular fluid proteome of the periovulatory follicle in lactating dairy cows.
title_full Heat-induced hyperthermia impacts the follicular fluid proteome of the periovulatory follicle in lactating dairy cows.
title_fullStr Heat-induced hyperthermia impacts the follicular fluid proteome of the periovulatory follicle in lactating dairy cows.
title_full_unstemmed Heat-induced hyperthermia impacts the follicular fluid proteome of the periovulatory follicle in lactating dairy cows.
title_sort heat-induced hyperthermia impacts the follicular fluid proteome of the periovulatory follicle in lactating dairy cows.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2019-01-01
description We hypothesized that heat-induced perturbations in cumulus cells surrounding the maturing oocyte may extend to the mural granulosa of the periovulatory follicle in the heat-stressed cow to subsequently the follicular fluid proteome. Lactating Holsteins were pharmacologically stimulated to have a dominant follicle that was capable of responding to a gonadotropin releasing hormone-induced luteinizing hormone surge. Following gonadotropin releasing hormone administration, cows were maintained at ~67 temperature humidity index (THI; thermoneutral conditions) or exposed to conditions simulating an acute heat stress event (71 to 86 THI; heat stress for ~12 h). Dominant follicle collection was conducted in the periovulatory period ~16 h after gonadotropin releasing hormone. Follicular fluid proteome from thermoneutral (n = 5) and hyperthermic (n = 5) cows was evaluated by quantitative tandem mass spectrometry (nano LC-MS/MS). We identified 35 differentially-abundant proteins. Functional annotation revealed numerous immune-related proteins. Subsequent efforts revealed an increase in levels of the proinflammatory mediator bradykinin in follicular fluid (P = 0.0456) but not in serum (P = 0.9319) of hyperthermic cows. Intrafollicular increases in transferrin (negative acute phase protein) in hyperthermic cows (P = 0.0181) coincided with a tendency for levels to be increased in the circulation (P = 0.0683). Nine out of 15 cytokines evaluated were detected in follicular fluid. Heat stress increased intrafollicular interleukin 6 levels (P = 0.0160). Whether hyperthermia-induced changes in the heat-stressed cow's follicular fluid milieu reflect changes in mural granulosa, cumulus, other cell types secretions, and/or transudative changes from circulation remains unclear. Regardless of origin, heat stress/hyperthermia related changes in the follicular fluid milieu may have an impact on components important for ovulation and competence of the cumulus-oocyte complex contained within the periovulatory follicle.
url https://doi.org/10.1371/journal.pone.0227095
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