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: | , , , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2019-01-01
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| Series: | PLoS ONE |
| Online Access: | https://doi.org/10.1371/journal.pone.0227095 |
| _version_ | 1818919251139887104 |
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| author | Louisa A Rispoli J Lannett Edwards Ky G Pohler Stephen Russell Richard I Somiari Rebecca R Payton F Neal Schrick |
| 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 |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-20T01:02:53Z |
| format | Article |
| id | doaj.art-b717b77cacda48619b5703e89f31cd69 |
| institution | Directory Open Access Journal |
| issn | 1932-6203 |
| language | English |
| last_indexed | 2024-12-20T01:02:53Z |
| publishDate | 2019-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS ONE |
| spelling | doaj.art-b717b77cacda48619b5703e89f31cd692022-12-21T19:58:56ZengPublic 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 |
| 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 |
| title | 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_short | 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 |
| url | https://doi.org/10.1371/journal.pone.0227095 |
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