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...
Main Authors: | , , , , , , |
---|---|
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 |
id |
doaj-b717b77cacda48619b5703e89f31cd69 |
---|---|
record_format |
Article |
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 |
work_keys_str_mv |
AT louisaarispoli heatinducedhyperthermiaimpactsthefollicularfluidproteomeoftheperiovulatoryfollicleinlactatingdairycows AT jlannettedwards heatinducedhyperthermiaimpactsthefollicularfluidproteomeoftheperiovulatoryfollicleinlactatingdairycows AT kygpohler heatinducedhyperthermiaimpactsthefollicularfluidproteomeoftheperiovulatoryfollicleinlactatingdairycows AT stephenrussell heatinducedhyperthermiaimpactsthefollicularfluidproteomeoftheperiovulatoryfollicleinlactatingdairycows AT richardisomiari heatinducedhyperthermiaimpactsthefollicularfluidproteomeoftheperiovulatoryfollicleinlactatingdairycows AT rebeccarpayton heatinducedhyperthermiaimpactsthefollicularfluidproteomeoftheperiovulatoryfollicleinlactatingdairycows AT fnealschrick heatinducedhyperthermiaimpactsthefollicularfluidproteomeoftheperiovulatoryfollicleinlactatingdairycows |
_version_ |
1714817381158617088 |