The Estrous Cycle of the Ewe Is Resistant to Disruption by Repeated, Acute Psychosocial Stress1
Open accessAbstract
Five experiments were conducted to test the hypothesis that psychosocial stress interferes with the estrous cycle of sheep. In experiment 1, ewes were repeatedly isolated during the follicular phase. Timing, amplitude, and duration of the preovulatory luteinizing hormone (LH) surge were not affected. In experiment 2, follicular-phase ewes were subjected twice to a "layered stress" paradigm consisting of sequential, hourly application of isolation, restraint, blindfold, and predator cues. This reduced the LH pulse amplitude but did not affect the LH surge. In experiment 3, different acute stressors were given sequentially within the follicular phase: food denial plus unfamiliar noises and forced exercise, layered stress, exercise around midnight, and transportation. This, too, did not affect the LH surge. In experiment 4, variable acute psychosocial stress was given every 1-2 days for two entire estrous cycles; this did not disrupt any parameter of the cycle monitored. Lastly, experiment 5 examined whether the psychosocial stress paradigms of experiment 4 would disrupt the cycle and estrous behavior if sheep were metabolically stressed by chronic food restriction. Thirty percent of the food-restricted ewes exhibited deterioration of estrous cycle parameters followed by cessation of cycles and failure to express estrous behavior. However, disruption was not more evident in ewes that also encountered psychosocial stress. Collectively, these findings indicate the estrous cycle of sheep is remarkably resistant to disruption by acute bouts of psychosocial stress applied intermittently during either a single follicular phase or repeatedly over two estrous cycles.
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If stress exposure occurs too close to the proestrus stage, resilience molecular mechanisms ensure the GnRH/LH surge continues as normal and triggers ovulation.
“While our model suggests that the GnRH/LH surge should be delayed under frequent exposure to stressors, if the exposure occurs too close to the proestrus stage then these resilience molecular mechanisms ensure the surge continues as normal and triggers ovulation (Wagenmaker et al., 2010; Wagenmaker and Moenter, 2017).”
From Dynamic Hormone Control of Stress and Fertility (2020) · cites this paper as Wagenmaker et al., 2010
The Discussion (page not provided) reports that repeated acute psychosocial stress did not alter the preovulatory LH surge in ewes. It does not establish that this resistance depends on stress occurring close to proestrus or identify molecular resilience mechanisms; it also says ovulation was not monitored. (LLM, conf=0.88)
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Cites
Cluster analysis: a simple, versatile, and robust algorithm for endocrine pulse detection
Veldhuis, J. D., & Johnson, M. L. (1986) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1986.250.4.e486 · Cited by 855 · see citing works
Rivier, C., & Rivest, S. (1991) · Biology of Reproduction · doi:10.1095/biolreprod45.4.523 · Cited by 799 · see citing works
Radioimmunoassay for Bovine and Ovine Luteinizing Hormone1
NISWENDER, G. D., REICHERT, L. E., MIDGLEY, A. R., & Nalbandov, A. V. (1969) · Endocrinology · doi:10.1210/endo-84-5-1166 · Cited by 757 · see citing works
What is stress, and how does it affect reproduction?
Dobson, H., & Smith, R. F. (2000) · Animal Reproduction Science · doi:10.1016/s0378-4320(00)00080-4 · Cited by 549 · see citing works
Tilbrook, A. (2000) · Reviews of Reproduction · doi:10.1530/ror.0.0050105 · Cited by 467 · see citing works
Self-citationPitman, D. L., Ottenweller, J. E., & Natelson, B. H. (1988) · Physiology & Behavior · doi:10.1016/0031-9384(88)90097-2 · Cited by 295 · see citing works
Hauger, R. L., Karsch, F. J., & Foster, D. L. (1977) · Endocrinology · doi:10.1210/endo-101-3-807 · Cited by 263 · see citing works
Self-citationPsychological correlates of functional hypothalamic amenorrhea
Marcus, M. D., Loucks, T. L., & Berga, S. L. (2001) · Fertility and Sterility · doi:10.1016/s0015-0282(01)01921-5 · Cited by 208 · see citing works
Chronic stress differentially regulates glucocorticoid negative feedback response in rats
Mizoguchi, K., Yuzurihara, M., Ishige, A., Sasaki, H., Chui, D., & Tabira, T. (2001) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(01)00004-x · Cited by 173 · see citing works
Williams, N. I., Berga, S. L., & Cameron, J. L. (2007) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00108.2007 · Cited by 169 · see citing works
Kenagy, G. J., & Place, N. J. (2000) · General and Comparative Endocrinology · doi:10.1006/gcen.1999.7397 · Cited by 162 · see citing works
Endocrine Alterations That Underlie Endotoxin-Induced Disruption of the Follicular Phase in Ewes1
Battaglia, D. F., Krasa, H. B., Padmanabhan, V., Viguié, C., & Karsch, F. J. (2000) · Biology of Reproduction · doi:10.1095/biolreprod62.1.45 · Cited by 157 · see citing works
Self-citationBattaglia, D. F., Bowen, J. M., Krasa, H. B., Thrun, L. A., Viguié, C., & Karsch, F. J. (1997) · Endocrinology · doi:10.1210/endo.138.10.5449 · Cited by 149 · see citing works
Self-citationNew insights regarding glucocorticoids, stress and gonadotropin suppression
BREEN, K., & KARSCH, F. (2006) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2006.03.335 · Cited by 131 · see citing works
Self-citationEndocrine Basis for Disruptive Effects of Cortisol on Preovulatory Events
Breen, K. M., Billings, H. J., Wagenmaker, E. R., Wessinger, E. W., & Karsch, F. J. (2005) · Endocrinology · doi:10.1210/en.2004-1457 · Cited by 126 · see citing works
Self-citationPsychogenic or “Hypothalamic” Amenorrhea
Reifenstein, E. C. (1946) · Medical Clinics of North America · doi:10.1016/s0025-7125(16)35908-9 · Cited by 106 · see citing works
Evidence for Short or Ultrashort Loop Negative Feedback of Gonadotropin-Releasing Hormone Secretion
Padmanabhan, V., Evans, N. P., Dahl, G. E., McFadden, K. L., Mauger, D. T., & Karsch, F. J. (2008) · Neuroendocrinology · doi:10.1159/000127011 · Cited by 93 · see citing works
Self-citationMacfarlane, M., Breen, K. M., Sakurai, H., Adams, B. M., & Adams, T. E. (2000) · Animal Reproduction Science · doi:10.1016/s0378-4320(00)00179-2 · Cited by 90 · see citing works
Self-citationSusceptibility of reproduction in female pigs to impairment by stress or elevation of cortisol
Turner, A. I., Hemsworth, P. H., & Tilbrook, A. J. (2005) · Domestic Animal Endocrinology · doi:10.1016/j.domaniend.2005.02.031 · Cited by 85 · see citing works
Self-citationWagenmaker, E. R., Breen, K. M., Oakley, A. E., Tilbrook, A. J., & Karsch, F. J. (2008) · Endocrinology · doi:10.1210/en.2008-0757 · Cited by 83 · see citing works
Self-citationDebus, N., Breen, K. M., Barrell, G. K., Billings, H. J., Brown, M. E., Young, E. A., & Karsch, F. J. (2002) · Endocrinology · doi:10.1210/en.2002-220291 · Cited by 80 · see citing works
Self-citationThe Psychoneuroendocrinology of Functional Hypothalamic Amenorrhea
Berga, S. L., & GIRTON, L. (1989) · Psychiatric Clinics of North America · doi:10.1016/s0193-953x(18)30454-4 · Cited by 80 · see citing works
Xiao, E., Xia‐Zhang, L., Barth, A., Zhu, J., & Ferin, M. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.83.7.4926 · Cited by 79 · see citing works
Neurobiology of Stress-Induced Reproductive Dysfunction in Female Macaques
Bethea, C. L., Centeno, M. L., & Cameron, J. L. (2008) · Molecular Neurobiology · doi:10.1007/s12035-008-8042-z · Cited by 78 · see citing works
Cleeff, J. V., Karsch, F. J., & Padmanabhan, V. (1998) · Domestic Animal Endocrinology · doi:10.1016/s0739-7240(97)00059-3 · Cited by 70 · see citing works
Self-citationXiao, E. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.83.7.2454 · Cited by 67 · see citing works
McCandless, E. L., & Dye, J. A. (1950) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1950.162.2.434 · Cited by 66 · see citing works
Xiao, E., Xia‐Zhang, L., & Ferin, M. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.87.5.8500 · Cited by 65 · see citing works
Breen, K. M., Oakley, A. E., Pytiak, A. V., Tilbrook, A. J., Wagenmaker, E. R., & Karsch, F. J. (2007) · Endocrinology · doi:10.1210/en.2006-0973 · Cited by 62 · see citing works
Self-citationNappi, R. E., & Rivest, S. (1997) · Endocrinology · doi:10.1210/endo.138.4.5044 · Cited by 62 · see citing works
Xiao, E., Xia‐Zhang, L., & Ferin, M. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.2.5448 · Cited by 57 · see citing works
Psychosocial stress suppresses attractivity, proceptivity and pulsatile LH secretion in the ewe
Pierce, B., Hemsworth, P. H., Rivalland, E. T. A., Wagenmaker, E. R., Morrissey, A. D., Papargiris, M., Clarke, I. J., Karsch, F. J., Turner, A. I., & Tilbrook, A. J. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.04.005 · Cited by 52 · see citing works
Self-citationEffect of transport on pulsatile and surge secretion of LH in ewes in the breeding season
Dobson, H., Tebble, J., Phogat, J. B., & Smith, R. F. (1999) · Reproduction · doi:10.1530/jrf.0.1160001 · Cited by 52 · see citing works
Short Days Increase Hypothalamic-Pituitary-Adrenal Axis Responsiveness
Pyter, L. M., Steinmetz, J. D., & Nelson, R. J. (2007) · Endocrinology · doi:10.1210/en.2006-1432 · Cited by 48 · see citing works
Henry, B. A., Goding, J. W., Tilbrook, A. J., et al. (2004) · Journal of Neuroendocrinology · doi:10.1111/j.0953-8194.2004.01157.x · Cited by 44 · see citing works
Self-citationLuteinizing hormone in nutrient-restricted ovariectomized ewes2
Tatman, W. R., Judkins, M. B., Dunn, T. G., et al. (1990) · Journal of Animal Science · doi:10.2527/1990.6841097x · Cited by 38 · see citing works
Cortisol Interferes with the Estradiol-Induced Surge of Luteinizing Hormone in the Ewe1
Wagenmaker, E. R., Breen, K. M., Oakley, A. E., Pierce, B., Tilbrook, A. J., Turner, A. I., & Karsch, F. J. (2008) · Biology of Reproduction · doi:10.1095/biolreprod.108.074252 · Cited by 36 · see citing works
Self-citationStackpole, C. A. (2003) · Biology of Reproduction · doi:10.1095/biolreprod.103.016428 · Cited by 36 · see citing works
Dobson, H., Tebble, J., Ozturk, M., et al. (1999) · Reproduction · doi:10.1530/jrf.0.1170213 · Cited by 34 · see citing works
Ferin, M. (1993) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1993.tb49927.x · Cited by 28 · see citing works
Hileman, S. M., Schillo, K. K., Boling, J. A., et al. (1990) · Experimental Biology and Medicine · doi:10.3181/00379727-194-43048 · Cited by 21 · see citing works
Cortisol disrupts the ability of estradiol-17β to induce the LH surge in ovariectomized ewes
Pierce, B., Clarke, I. J., Turner, A. I., Rivalland, E. T. A., & Tilbrook, A. J. (2008) · Domestic Animal Endocrinology · doi:10.1016/j.domaniend.2008.11.003 · Cited by 20 · see citing works
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Research works printed but not linked: 2
- Reifenstein EC., JrPsychogenic or “hypothalamic” amenorrhea. Med Clin North Am 1946; 30: 1103–1114. [DOI] [PubMed] [Google Scholar]
- Niswender GD, Midgley AR, Jr, Reichert LE., JrRadioimmunologic studies with murine, ovine and porcine luteinizing hormone. Rosenborg E.Gonadotropins Los Altos, CA:Geron-X;1968: 299–306. [Google Scholar]
Cited by
Sorted by citations
Wagenmaker, E. R., & Moenter, S. M. (2017) · Endocrinology · doi:10.1210/en.2017-00341 · Cited by 61 · see citing works
Self-citationDynamic Hormone Control of Stress and Fertility
Zavala, E., Voliotis, M., Zerenner, T., Tabak, J., Walker, J. J., Li, X. F., Terry, J. R., Lightman, S. L., O'Byrne, K., & Tsaneva-Atanasova, K. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.598845 · Cited by 34 · see citing works
“While our model suggests that the 224 GnRH/LH surge should be delayed under frequent exposure to stressors, if the exposure occurs too close to 225 the proestrus stage then these resilience molecular mechanisms ensure the surge continues as normal and 226 triggers ovulation [35, 36].”
BackgroundMethod
- Authors
- Wagenmaker, E. R., Breen, K. M., Oakley, A. E., Tilbrook, A. J., & Karsch, F. J.
- Affiliations
- University of Michigan (US)
- Monash University (AU)
- Corresponding author
- Karsch, Fred J.
- Venue
- Biology of Reproduction
- Publisher
- Oxford University Press (OUP)
- Published
- 2010-06-01
- Volume
- 82
- Issue
- 6
- Pages
- 1206-1215
- ISSN
- 0006-3363 (ISSN-L)
- 1529-7268
- PMC
- PMC2874503
- OpenAlex
- W2120990509
- Cited by
- 15
- References
- 42
- Citations by year
- 2024: 1 · 2022: 1 · 2020: 1 · 2018: 2 · 2017: 3 · 2016: 3 · 2014: 1 · 2013: 3
- FWCI
- 2.04
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Biology of Reproduction (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- BioOne Complete (BioOne) (submittedVersion)
- Funders
- National Institutes of Health
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD030773, F32HD051360, HD051360, K99HD060947, HD-30773)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Agronomy and Crop Science › Reproductive Physiology in Livestock
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
- Keywords
- estrous cycle, ewes, psychosocial stress, acute stress, luteinizing hormone surge, follicular phase, dietary restriction, metabolic stress, estrous behavior, isolation stress, predator cues, sheep reproduction
- MeSH terms
- Animals, Blindness, Female, Follicular Phase, Luteinizing Hormone, Progesterone, Restraint, Physical, Sheep, Social Isolation, Stress, Psychological, Estrous Cycle
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