Effect of elevated temperatures on bovine corpus luteum function: expression of heat-shock protein 70, cell viability and production of progesterone and prostaglandins by cultured luteal cells
Makoto Iwazawa A and Tomas J. Acosta A B
+ Author Affiliations
- Author Affiliations
A Laboratory of Reproductive Physiology, Graduate School of Environmental and Life Science, Okayama University, Okayama 700-8530, Japan.
B Corresponding author. Email: acosta@cc.okayama-u.ac.jp
Animal Production Science 54(3) 285-291 https://doi.org/10.1071/AN13027
Submitted: 29 January 2013 Accepted: 27 March 2013 Published: 9 May 2013
Abstract
Summer heat stress lowers fertility in cattle in hot environments by influencing oocyte quality, follicular activity and progesterone (P4) level in blood plasma. However, the mechanisms by which elevated temperature influences corpus luteum function remain unclear. Elevated temperature has generally been known to upregulate the gene expression of heat-shock protein (HSP) 70 in a variety of cell types. To clarify the direct effects of elevated temperature on bovine corpus luteum function, we examined the expressions of HSP70, cell viability and the production of P4 and prostaglandins (PGs) in luteal cells cultured at 37.5°C (normal temperature in our culture system), 39.0°C (moderately elevated temperature) or 41.0°C (severely elevated temperature) for 12 or 24 h. HSP70 mRNA expression was increased by incubation at 39.0°C for 12 h and at 41.0°C for 12 and 24 h, whereas HSP70 protein expression was not significantly affected. The viability of luteal cells cultured for 24 h, measured by flow cytometry with propidium iodide staining, was not significantly affected by temperature. Interestingly, the production of P4 by cultured luteal cells was higher at 39.0°C than at 37.5°C after 12 and 24 h of incubation. The production of PGF2α was higher at 39.0°C and 41.0°C than at 37.5°C after 12 and 24 h of incubation. The production of PGE2 was higher at 41.0°C than at 37.5°C after 24 h of incubation. The overall results suggested that elevated temperature does not negatively affect luteal function, and that the low fertility observed during summer is not due to a direct effect of elevated temperature on luteal cells.
Additional keywords: cell viability, heat stress.
References
Anderson RL, Parker R (1982) Analysis of membrane lipid composition of mammalian cells during the development of thermotolerance. International Journal of Radiation Biology 42, 57–69.| Analysis of membrane lipid composition of mammalian cells during the development of thermotolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38Xlt1GisL0%3D&md5=41f2fd7256d798e239a03b49559e87c6CAS |
Badinga L, Collier RJ, Thatcher WW, Wilcox CJ (1985) Effects of climatic and management factors on conception rate of dairy cattle in subtropical environment. Journal of Dairy Science 68, 78–85.
| Effects of climatic and management factors on conception rate of dairy cattle in subtropical environment.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2M7lvVCkuw%3D%3D&md5=b640a2b4cb340cd6ed0bcd85e8170421CAS | 3980812PubMed |
Badinga L, Thatcher WW, Diaz T, Drost M, Wolfenson D (1993) Effect of environmental heat stress on follicular development and steroidogenesis in lactating Holstein cows. Theriogenology 39, 797–810.
| Effect of environmental heat stress on follicular development and steroidogenesis in lactating Holstein cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXkvVKnu78%3D&md5=4e5d65a7f3e02b0a5a06e30c5c0fd59dCAS | 16727254PubMed |
Berman A, Folman Y, Kaim M, Mamen M, Herz Z, Wolfenson D, Arieli A, Graber Y (1985) Upper critical temperatures and forced ventilation effects for high-yielding dairy cows in a subtropical climate. Journal of Dairy Science 68, 1488–1495.
| Upper critical temperatures and forced ventilation effects for high-yielding dairy cows in a subtropical climate.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2M3mt1Wqug%3D%3D&md5=0ac3deea2b252d8bfad86565943a8921CAS | 4019887PubMed |
Bowler K, Duncan CJ, Gladwell RT, Davison TF (1973) Cellular heat injury. Comparative Biochemistry and Physiology. Part A, Physiology 45, 441–450.
| Cellular heat injury.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3sXktFKisLo%3D&md5=a73f893f46367b7e3c41d37c461c68b0CAS |
Bowolaksono A, Nishimura R, Hojo T, Sakumoto R, Acosta TJ, Okuda K (2008) Anti-apoptotic roles of prostaglandin E2 and F2α in bovine luteal steroidogenic cells. Biology of Reproduction 79, 310–317.
| Anti-apoptotic roles of prostaglandin E2 and F2α in bovine luteal steroidogenic cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXovFWmsLs%3D&md5=2bba337b12f74403ac8b3b89cd9527caCAS | 18463360PubMed |
Bridges PJ, Brusie MA, Fortune JE (2005) Elevated temperature (heat stress) in vitro reduces androstenedione and estradiol and increases progesterone secretion by follicular cells from bovine dominant follicles. Domestic Animal Endocrinology 29, 508–522.
| Elevated temperature (heat stress) in vitro reduces androstenedione and estradiol and increases progesterone secretion by follicular cells from bovine dominant follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpvV2msLY%3D&md5=872fa45e014c7c87391af59e8e71c7fdCAS | 16153500PubMed |
Calderwood SK, Stevenson MA, Hahn GM (1987) Heat stress stimulates inositol trisphosphate release and phosphorylation of phosphoinositides in CHO and Balb C 3T3 cells. Journal of Cellular Physiology 130, 369–376.
| Heat stress stimulates inositol trisphosphate release and phosphorylation of phosphoinositides in CHO and Balb C 3T3 cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXhvFemtL4%3D&md5=29aa967bfc00888779555c9e13a7b841CAS | 3031088PubMed |
Cavestany D, el-Wishy AB, Foote RH (1985) Effect of season and high environmental temperature on fertility of Holstein cattle. Journal of Dairy Science 68, 1471–1478.
| Effect of season and high environmental temperature on fertility of Holstein cattle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2M3mt1WqtA%3D%3D&md5=850746b49c9ad9540f1b358fc5f675cdCAS | 4019885PubMed |
Clark BJ, Wells J, King SR, Stocco DM (1994) The purification, cloning, and expression of a novel luteinizing hormone-induced mitochondrial protein in MA-10 mouse Leydig tumor cells. characterization of the steroidogenic acute regulatory protein (StAR). The Journal of Biological Chemistry 269, 28 314–28 322.
de Oliveira AT, Lopes RF, Rodrigues JL (2005) Gene expression and developmental competence of bovine embryos produced in vitro under varying embryo density conditions. Theriogenology 64, 1559–1572.
| Gene expression and developmental competence of bovine embryos produced in vitro under varying embryo density conditions.Crossref | GoogleScholarGoogle Scholar | 15878193PubMed |
De Rensis F, Marconi P, Capelli T, Gattim F, Facciolongo F, Franzini S, Scaramuzzi RJ (2002) Fertility in postpartum dairy cows in winter or summer following estrus synchronization and fixed time AI after the induction of an LH surge with GnRH or hCG. Theriogenology 58, 1675–1687.
| Fertility in postpartum dairy cows in winter or summer following estrus synchronization and fixed time AI after the induction of an LH surge with GnRH or hCG.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XoslGgsrk%3D&md5=52b6e823a6a996a9b17a8b966c52780fCAS | 12472138PubMed |
Du J, Di HS, Guo L, Li ZH, Wang GL (2008) Hyperthermia causes bovine mammary epithelial cell death by a mitochondrial-induced pathway. Journal of Thermal Biology 33, 37–47.
| Hyperthermia causes bovine mammary epithelial cell death by a mitochondrial-induced pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVOru7rP&md5=b21e4e02ec47c04d2b321e203ad716ddCAS |
Flint AP, Leat WM, Sheldrick EL, Stewart HJ (1986) Stimulation of phosphoinositide hydrolysis by oxytocin and the mechanism by which oxytocin controls prostaglandin synthesis in the ovine endometrium. Biochemistry Journal 237, 797–805.
Grinsted J, Blendstrup K, Andreasen MP, Byskov AG (1980) Temperature measurements of rabbit antral follicles. Journal of Reproduction and Fertility 60, 149–155.
| Temperature measurements of rabbit antral follicles.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3M%2FkvFamsA%3D%3D&md5=4136b483fedc3bf6bc3f11b28fc17ab8CAS | 7431316PubMed |
Grinsted J, Kjer JJ, Blendstrup K, Pedersen JF (1985) Is low temperature of the follicular fluid prior to ovulation necessary for normal oocyte development? Fertility and Sterility 43, 34–39.
Grøndahl C, Greve T, Schmidt M, Hunter R (1996) Bovine pre-ovulatory follicles are cooler than ovarian stroma and deep rectal temperature. Theriogenology 45, 289
| Bovine pre-ovulatory follicles are cooler than ovarian stroma and deep rectal temperature.Crossref | GoogleScholarGoogle Scholar |
Guzeloglu A, Ambrose JD, Kassa T, Diaz T, Thatcher MJ, Thatcher WW (2001) Long-term follicular dynamics and biochemical characteristics of dominant follicles in dairy cows subjected to acute heat stress. Animal Reproduction Science 66, 15–34.
| Long-term follicular dynamics and biochemical characteristics of dominant follicles in dairy cows subjected to acute heat stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtlCjurc%3D&md5=1b57245b07f53ef79528fcd5cd56e3baCAS | 11343839PubMed |
Hendrick JP, Hartl FU (1993) Molecular chaperone functions of heat-shock proteins. Annual Review of Biochemistry 62, 349–384.
| Molecular chaperone functions of heat-shock proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlsFCjurw%3D&md5=94d7fb2c353fe5ea22725507e973bafaCAS | 8102520PubMed |
Hunter RH, Bogh IB, Einer-Jensen N, Muller S, Greve T (2000) Pre-ovulatory graafian follicles are cooler than neighbouring stroma in pig ovaries. Human Reproduction 15, 273–283.
| Pre-ovulatory graafian follicles are cooler than neighbouring stroma in pig ovaries.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7it1eksQ%3D%3D&md5=2a8df478f1db74ffd031c85d5ea9b4b8CAS | 10655296PubMed |
James P, Pfund C, Craig EA (1997) Functional specificity among Hsp70 molecular chaperones. Science 275, 387–389.
| Functional specificity among Hsp70 molecular chaperones.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmtlOjtQ%3D%3D&md5=a715b8597c5df0406d3895b6de04bfa1CAS | 8994035PubMed |
Jolly C, Morimoto RI (2000) Role of the heat shock response and molecular chaperones in oncogenesis and cell death. Journal of the National Cancer Institute 92, 1564–1572.
| Role of the heat shock response and molecular chaperones in oncogenesis and cell death.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnsVKitr4%3D&md5=924b8fe37e2781239085743ef5ea4c72CAS | 11018092PubMed |
Kuroiwa T, Ishibashi A, Fukuda M, Kim S, Tanaka T, Kamomae H (2005) Estrus synchronization and conception rate after a progesterone releasing intravaginal device (PRID) treatment from the early luteal phase in heifers. The Journal of Reproduction and Development 51, 669–673.
| Estrus synchronization and conception rate after a progesterone releasing intravaginal device (PRID) treatment from the early luteal phase in heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XktVGjsQ%3D%3D&md5=a37ee8648229a4256015204e2c5a50daCAS | 16046838PubMed |
Lim CU, Zhang Y, Fox MH (2006) Cell cycle dependent apoptosis and cell cycle blocks induced by hyperthermia in HL-60 cells. International Journal of Hyperthermia 22, 77–91.
| Cell cycle dependent apoptosis and cell cycle blocks induced by hyperthermia in HL-60 cells.Crossref | GoogleScholarGoogle Scholar | 16423754PubMed |
Liu X, Kim CN, Yang J, Jemmerson R, Wang X (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86, 147–157.
| Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XktlGnsbY%3D&md5=d57d827502ea9a1eb1285438c2e6cdf1CAS | 8689682PubMed |
Malayer JR, Hansen PJ, Buhi WC (1988) Effect of day of the oestrous cycle, side of the reproductive tract and heat shock on in-vitro protein secretion by bovine endometrium. Journal of Reproduction and Fertility 84, 567–578.
| Effect of day of the oestrous cycle, side of the reproductive tract and heat shock on in-vitro protein secretion by bovine endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXltler&md5=167e2135ce668cb2b0e90d83e3a4f7e3CAS | 3199376PubMed |
McCracken JA, Custer EE, Lamsa JC (1999) Luteolysis: a neuroendocrine-mediated event. Physiological Reviews 79, 263–323.
Miyamoto Y, Skarzynski DJ, Uenoyama Y, Okuda K (1998) Secretion of prostaglandin E2 and F2α by the bovine endometrium in response to oxytocin during the estrous cycle. The Journal of Reproduction and Development 44, 289–295.
| Secretion of prostaglandin E2 and F2α by the bovine endometrium in response to oxytocin during the estrous cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnsVSmt70%3D&md5=7bdf8a79c45e31b75ff6c3e3b31fe451CAS |
Miyamoto Y, Skarzynski DJ, Okuda K (2000) Is tumor necrosis factor α a trigger for the initiation of endometrial prostaglandin F2α release at luteolysis in cattle? Biology of Reproduction 62, 1109–1115.
| Is tumor necrosis factor α a trigger for the initiation of endometrial prostaglandin F2α release at luteolysis in cattle?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisl2htr8%3D&md5=6a39ee70cacf25c4535db226746fbe7dCAS | 10775155PubMed |
Nishimura R, Shibaya M, Skarzynski DJ, Okuda K (2004) Progesterone stimulation by LH involves the phospholipase-C pathway in bovine luteal cells. The Journal of Reproduction and Development 50, 257–261.
| Progesterone stimulation by LH involves the phospholipase-C pathway in bovine luteal cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltlKhtbs%3D&md5=eba74ecfa7f7ee71989b67f7c398f6c0CAS | 15118253PubMed |
Okuda K, Miyamoto A, Sauerwein H, Schweigert FJ, Schams D (1992) Evidence for oxytocin receptors in cultured bovine luteal cells. Biology of Reproduction 46, 1001–1006.
| Evidence for oxytocin receptors in cultured bovine luteal cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XktVWgtL8%3D&md5=50569febc955dcef7e018a5d99382e46CAS | 1327197PubMed |
Okuda K, Uenoyama Y, Fujita Y, Iga K, Sakamoto K, Kimura T (1997) Functional oxytocin receptors in bovine granulosa cells. Biology of Reproduction 56, 625–631.
| Functional oxytocin receptors in bovine granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXht1Gjs74%3D&md5=d72f3129965f3e98f6650f3e4c909a9eCAS | 9047006PubMed |
Osnes T, Sandstad O, Skar V, Osnes M, Kierulf P (1993) Total protein in common duct bile measured by acetonitrile precipitation and a micro bicinchoninic acid (BCA) method. Scandinavian Journal of Clinical and Laboratory Investigation 53, 757–763.
| Total protein in common duct bile measured by acetonitrile precipitation and a micro bicinchoninic acid (BCA) method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXitFWqsbw%3D&md5=a3cc691edadb6b10475e452bb81b9333CAS | 8272764PubMed |
Pirkkala L, Nykanen P, Sistonen L (2001) Roles of the heat shock transcription factors in regulation of the heat shock response and beyond. Federation of American Societies for Experimental Biology Journal 15, 1118–1131.
| Roles of the heat shock transcription factors in regulation of the heat shock response and beyond.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlvVOms78%3D&md5=eb7dcc9208ad8da175516f04d60b0ba1CAS |
Pratt BR, Butcher RL, Inskeep EK (1977) Antiluteolytic effect of the conceptus and of PGE2 in ewes. Journal of Animal Science 45, 784–791.
Putney DJ, Malayer JR, Gross TS, Thatcher WW, Hansen PJ, Drost M (1988) Heat stress-induced alterations in the synthesis and secretion of proteins and prostaglandins by cultured bovine conceptuses and uterine endometrium. Biology of Reproduction 39, 717–728.
| Heat stress-induced alterations in the synthesis and secretion of proteins and prostaglandins by cultured bovine conceptuses and uterine endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXmt1ehtbk%3D&md5=587ff8eb6f409ee100d146cc679cdc55CAS | 3196802PubMed |
Rosenberg M, Folman Y, Herz Z, Flamenbaum I, Berman A, Kaim M (1982) Effect of climatic conditions on peripheral concentrations of LH, progesterone and oestradiol-17β in high milk-yielding cows. Journal of Reproduction and Fertility 66, 139–146.
| Effect of climatic conditions on peripheral concentrations of LH, progesterone and oestradiol-17β in high milk-yielding cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XlslGgurs%3D&md5=0c110ebf490eea2d64d85ef0ee42a975CAS | 7120177PubMed |
Sakumoto R, Berisha B, Kawate N, Schams D, Okuda K (2000) Tumor necrosis factor-α and its receptor in bovine corpus luteum throughout the estrous cycle. Biology of Reproduction 62, 192–199.
| Tumor necrosis factor-α and its receptor in bovine corpus luteum throughout the estrous cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhslKkuw%3D%3D&md5=36467f1552036bd40340d0b7c2aa379dCAS | 10611085PubMed |
Skarzynski DJ, Ferreira-Dias G, Okuda K (2008) Regulation of luteal function and corpus luteum regression in cows: hormonal control, immune mechanisms and intercellular communication. Reproduction in Domestic Animals 43, 57–65.
| Regulation of luteal function and corpus luteum regression in cows: hormonal control, immune mechanisms and intercellular communication.Crossref | GoogleScholarGoogle Scholar | 18638105PubMed |
Thatcher WW, Bazer FW, Sharp DC, Roberts RM (1986) Interrelationships between uterus and conceptus to maintain corpus luteum function in early pregnancy: sheep, cattle, pigs and horses. Journal of Animal Science 62, 25–46.
Uenoyama Y, Hattori S, Miyake M, Okuda K (1997) Up-regulation of oxytocin receptors in porcine endometrium by adenosine 3′,5′-monophosphate. Biology of Reproduction 57, 723–728.
| Up-regulation of oxytocin receptors in porcine endometrium by adenosine 3′,5′-monophosphate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmtFCqsrk%3D&md5=34789e609f1125a5e980cb7159e443b0CAS | 9314572PubMed |
Wilson SJ, Kirby CJ, Koenigsfeld AT, Keisler DH, Lucy MC (1998a) Effects of controlled heat stress on ovarian function of dairy cattle. 2. Heifers. Journal of Dairy Science 81, 2132–2138.
| Effects of controlled heat stress on ovarian function of dairy cattle. 2. Heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlvVCmtrY%3D&md5=085b5abaf19ff75050cc42deeb36817bCAS | 9749377PubMed |
Wilson SJ, Marion RS, Spain JN, Spiers DE, Keisler DH, Lucy MC (1998b) Effects of controlled heat stress on ovarian function of dairy cattle. 1. Lactating cows. Journal of Dairy Science 81, 2124–2131.
| Effects of controlled heat stress on ovarian function of dairy cattle. 1. Lactating cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlvVCmtrk%3D&md5=ba9641ccd9f27911b762aa7980db9467CAS | 9749376PubMed |
Wolfenson D, Flamenbaum I, Berman A (1988) Hyperthermia and body energy store effects on estrous behavior, conception rate, and corpus luteum function in dairy cows. Journal of Dairy Science 71, 3497–3504.
| Hyperthermia and body energy store effects on estrous behavior, conception rate, and corpus luteum function in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1M7nsFKktQ%3D%3D&md5=98f5c59701a043debf810f2ff2e1c3dbCAS | 3235739PubMed |
Wolfenson D, Lew BJ, Thatcher WW, Graber Y, Meidan R (1997) Seasonal and acute heat stress effects on steroid production by dominant follicles in cows. Animal Reproduction Science 47, 9–19.
| Seasonal and acute heat stress effects on steroid production by dominant follicles in cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXksVSku7o%3D&md5=ef81ad2a97dcf3bb5c8407909c3efb91CAS | 9233502PubMed |
Yousef MK (1985). Thermoneutral zone. In ‘Stress physiology in livestock, Vol. 1’. (Ed. MK Yousef) pp. 67–74. (CRC Press: Boca Raton, FL)
