Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Temporal regulation of extracellular signal-regulated kinase 1/2 phosphorylation, heat shock protein 70 and activating transcription factor 3 during prostaglandin F-induced luteal regression in pseudopregnant rats following heat stress

Wu-jiao Bai A , Peng-jing Jin A , Mei-qian Kuang A , Quan-wei Wei A , Fang-xiong Shi A , John S. Davis B and Da-gan Mao A C
+ Author Affiliations
- Author Affiliations

A College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, Jiangsu, 210095, China.

B VA Nebraska–Western Iowa Health Care System and Department of Obstetrics and Gynecology, University of Nebraska Medical Center, Omaha, NE 68198, USA.

C Corresponding author. Email: maodagan@njau.edu.cn

Reproduction, Fertility and Development 29(6) 1184-1193 https://doi.org/10.1071/RD15415
Submitted: 15 October 2015  Accepted: 17 March 2016   Published: 12 May 2016

Abstract

The aim of the present study was to investigate the effects of heat stress on heat shock protein (HSP) 70 expression and mitogen-activated protein kinase (MAPK) and protein kinase (PK) B signalling during prostaglandin F (PGF)-induced luteal regression. During pseudopregnancy, rats were exposed to heat stress (HS, 40°C, 2 h) for 7 days and treated with PGF or physiological saline on Day 7; serum and ovaries were collected 0, 1, 2, 8 or 24 h after PGF treatment. The early inhibitory effect of PGF on progesterone was reduced in HS rats. HSP70 expression in response to PGF was significantly enhanced in HS rats. PGF-induced phosphorylation of extracellular signal-regulated kinase (ERK) 1/2 was significantly greater in the HS group; however, HS rats exhibited elevated basal levels of phosphorylation of p38 MAPK, but not ERK1/2. PGF treatment increased expression of activating transcription factor (ATF) 3 at 2 h, which was inhibited by heat stress. Evaluating PKB signalling revealed that phosphorylation of p-Akt (Thr308 and Ser473) was reduced at 8 and 24 h after PGF treatment in both non-heat stress (NHS) and HS groups, but there were no significant differences between the HS and NHS groups at any of the time points. In conclusion, the present study provides further evidence that heat stress may enhance HSP70 and affect ERK1/2 and ATF3 expression, but not Akt activation, during PGF-induced luteal regression in pseudopregnant rats.

Additional keywords: Akt, corpus luteum, elevated temperature, luteolysis, mitogen-activated protein kinase, p38 MAPK, progesterone.


References

Arvisais, E., Hou, X., Wyatt, T. A., Shirasuna, K., Bollwein, H., Miyamoto, A., Hansen, T. R., Rueda, B. R., and Davis, J. S. (2010). Prostaglandin F2alpha represses IGF-I-stimulated IRS1/phosphatidy-linositol-3-kinase/AKT signaling in the corpus luteum: role of ERK and P70 ribosomal S6 kinase. Mol. Endocrinol. 24, 632–643.
Prostaglandin F2alpha represses IGF-I-stimulated IRS1/phosphatidy-linositol-3-kinase/AKT signaling in the corpus luteum: role of ERK and P70 ribosomal S6 kinase.CrossRef | 1:CAS:528:DC%2BC3cXjt1ehs74%3D&md5=5a4a3374a9cffa9c042bc2d4645263c8CAS | 20160123PubMed |

Atli, M. O., Bender, R. W., Mehta, V., Bastos, M. R., Luo, W., Vezina, C. M., and Wiltbank, M. C. (2012). Patterns of gene expression in the bovine corpus luteum following repeated intrauterine infusions of low doses of prostaglandin F2alpha. Biol. Reprod. 86, 130.
Patterns of gene expression in the bovine corpus luteum following repeated intrauterine infusions of low doses of prostaglandin F2alpha.CrossRef | 22262696PubMed |

Balogh, G., Peter, M., Glatz, A., Gombos, I., Torok, Z., Horvath, I., Harwood, J. L., and Vigh, L. (2013). Key role of lipids in heat stress management. FEBS Lett. 587, 1970–1980.
Key role of lipids in heat stress management.CrossRef | 1:CAS:528:DC%2BC3sXot1Krt70%3D&md5=b7f3cc37d6d010ce1ef0bcba6e49aaf7CAS | 23684645PubMed |

Banerjee Mustafi, S., Chakraborty, P. K., Dey, R. S., and Raha, S. (2009). Heat stress upregulates chaperone heat shock protein 70 and antioxidant manganese superoxide dismutase through reactive oxygen species (ROS), p38MAPK, and Akt. Cell Stress Chaperones 14, 579–589.
Heat stress upregulates chaperone heat shock protein 70 and antioxidant manganese superoxide dismutase through reactive oxygen species (ROS), p38MAPK, and Akt.CrossRef | 1:CAS:528:DC%2BD1MXhtlyhu7zP&md5=6b632409bf205d25bdf8c5efdd37f5c3CAS | 19291423PubMed |

Banerjee Mustafi, M. S., Chakraborty, P. K., and Raha, S. (2010). Modulation of Akt and ERK1/2 pathways by resveratrol in chronic myelogenous leukemia (CML) cells results in the downregulation of Hsp70. PLoS One 5, e8719.
Modulation of Akt and ERK1/2 pathways by resveratrol in chronic myelogenous leukemia (CML) cells results in the downregulation of Hsp70.CrossRef |

Beckham, J. T., Mackanos, M. A., Crooke, C., Takahashi, T., O’Connell-Rodwell, C., Contag, C. H., and Jansen, E. D. (2004). Assessment of cellular response to thermal laser injury through bioluminescence imaging of heat shock protein 70. Photochem. Photobiol. 79, 76–85.
Assessment of cellular response to thermal laser injury through bioluminescence imaging of heat shock protein 70.CrossRef | 1:CAS:528:DC%2BD2cXnslyjsA%3D%3D&md5=14ffb16725c19d90362ab83a5d64235dCAS | 14974719PubMed |

Cecconi, S., Rossi, G., Santilli, A., Stefano, L. D., Hoshino, Y., Sato, E., Palmerini, M. G., and Macchiarelli, G. (2010). Akt expression in mouse oocytes matured in vivo and in vitro. Reprod. Biomed. Online 20, 35–41.
Akt expression in mouse oocytes matured in vivo and in vitro.CrossRef | 1:CAS:528:DC%2BC3cXhtFegsLjE&md5=9ca442dfb86418c9388f4f3cb60b0053CAS | 20158985PubMed |

Chang, A., Zhang, Z., Jia, L., Zhang, L., Gao, Y., and Zhang, L. (2013). Alteration of heat shock protein 70 expression levels in term and preterm delivery. J. Matern. Fetal Neonatal Med. 26, 1581–1585.
Alteration of heat shock protein 70 expression levels in term and preterm delivery.CrossRef | 1:CAS:528:DC%2BC3sXhvVGhtb7N&md5=6502359bf0940b6f057834e298993532CAS | 23581516PubMed |

Chen, D. B., Westfall, S. D., Fong, H. W., Roberson, M. S., and Davis, J. S. (1998). Prostaglandin F2alpha stimulates the Raf/MEK1/mitogen-activated protein kinase signaling cascade in bovine luteal cells. Endocrinology 139, 3876–3885.
Prostaglandin F2alpha stimulates the Raf/MEK1/mitogen-activated protein kinase signaling cascade in bovine luteal cells.CrossRef | 1:CAS:528:DyaK1cXlsFOiuro%3D&md5=cdadc9d8e33bf5d4420676e50f3f64eaCAS | 9724043PubMed |

Chen, D., Fong, H. W., and Davis, J. S. (2001). Induction of c-fos and c-jun messenger ribonucleic acid expression by prostaglandin F2alpha is mediated by a protein kinase C-dependent extracellular signal-regulated kinase mitogen-activated protein kinase pathway in bovine luteal cells. Endocrinology 142, 887–895.
Induction of c-fos and c-jun messenger ribonucleic acid expression by prostaglandin F2alpha is mediated by a protein kinase C-dependent extracellular signal-regulated kinase mitogen-activated protein kinase pathway in bovine luteal cells.CrossRef | 1:CAS:528:DC%2BD3MXhtFSrur4%3D&md5=aeaeff6a8c0ee366745684d91de84818CAS | 11159862PubMed |

Currie, W. D., Li, W., Baimbridge, K. G., Yuen, B. H., and Leung, P. C. (1992). Cytosolic free calcium increased by prostaglandin F2 alpha (PGF2 alpha), gonadotropin-releasing hormone, and angiotensin II in rat granulosa cells and PGF2 alpha in human granulosa cells. Endocrinology 130, 1837–1843.
Cytosolic free calcium increased by prostaglandin F2 alpha (PGF2 alpha), gonadotropin-releasing hormone, and angiotensin II in rat granulosa cells and PGF2 alpha in human granulosa cells.CrossRef | 1:CAS:528:DyaK38XitVyntbs%3D&md5=05071312c1e0cec12c5ebf71c313f815CAS | 1547713PubMed |

Davis, J. S., Weakland, L. L., Weiland, D. A., Farese, R. V., and West, L. A. (1987). Prostaglandin F stimulates phosphatidylinositol 4,5-biphosphate hydrolysis and mobilizes intracellular Ca2+ in bovine luteal cells. Proc. Natl Acad. Sci. USA 84, 3728–3732.
Prostaglandin F stimulates phosphatidylinositol 4,5-biphosphate hydrolysis and mobilizes intracellular Ca2+ in bovine luteal cells.CrossRef | 1:CAS:528:DyaL2sXktleqsr4%3D&md5=011867caab4af238ce2ebe0eb5c73da0CAS | 3035550PubMed |

Dokladny, K., Zuhl, M. N., Mandell, M., Bhattacharya, D., Schneider, S., Deretic, V., and Moseley, P. L. (2013). Regulatory coordination between two major intracellular homeostatic systems: heat shock response and autophagy. J. Biol. Chem. 288, 14 959–14 972.
Regulatory coordination between two major intracellular homeostatic systems: heat shock response and autophagy.CrossRef | 1:CAS:528:DC%2BC3sXot1WhsL4%3D&md5=1ef1546f1474cecec443e294b9b7d0d7CAS |

Dorion, S., and Landry, J. (2002). Activation of the mitogen-activated protein kinase pathways by heat shock. Cell Stress Chaperones 7, 200–206.
Activation of the mitogen-activated protein kinase pathways by heat shock.CrossRef | 1:CAS:528:DC%2BD38XptV2gsLk%3D&md5=f851fbf1eecee98f064eba6d5baa05caCAS | 12380688PubMed |

Gabai, V. L., and Sherman, M. Y. (2002). Invited review: interplay between molecular chaperones and signaling pathways in survival of heat shock. J. Appl. Physiol. 92, 1743–1748.
Invited review: interplay between molecular chaperones and signaling pathways in survival of heat shock.CrossRef | 1:CAS:528:DC%2BD38XjtVKjtLk%3D&md5=f838dca9f92fd88e7398f154203203f2CAS | 11896044PubMed |

Gilad, E., Meidan, R., Berman, A., Graber, Y., and Wolfenson, D. (1993). Effect of heat stress on tonic and GnRH-induced gonadotrophin secretion in relation to concentration of oestradiol in plasma of cyclic cows. J. Reprod. Fertil. 99, 315–321.
Effect of heat stress on tonic and GnRH-induced gonadotrophin secretion in relation to concentration of oestradiol in plasma of cyclic cows.CrossRef | 1:CAS:528:DyaK2cXhvVegtbc%3D&md5=ddaf362945a16646acb8d51017d89753CAS | 8107012PubMed |

Gonzalez, E., and McGraw, T. E. (2009). The Akt kinases: isoform specificity in metabolism and cancer. Cell Cycle 8, 2502–2508.
The Akt kinases: isoform specificity in metabolism and cancer.CrossRef | 1:CAS:528:DC%2BC3cXjsl2mu7o%3D&md5=e1994368cb0da9e2de048c5c3060d300CAS | 19597332PubMed |

Guo, N., Meng, C., Bai, W., Wei, Q., Shi, F., Davis, J. S., and Mao, D. (2015). Prostaglandin F2alpha induces expression of activating transcription factor 3 (ATF3) and activates MAPK signaling in the rat corpus luteum. Acta Histochem. 117, 211–218.
Prostaglandin F2alpha induces expression of activating transcription factor 3 (ATF3) and activates MAPK signaling in the rat corpus luteum.CrossRef | 1:CAS:528:DC%2BC2MXovVeisA%3D%3D&md5=da4321095ed234a43cc78f0d02fedd6bCAS | 25614048PubMed |

Guzeloglu, A., Ambrose, J. D., Kassa, T., Diaz, T., Thatcher, M. J., and Thatcher, W. W. (2001). Long term follicular dynamics and biochemical characteristics of dominant follicles in dairy cows subjected to acute heat stress. Anim. Reprod. Sci. 66, 15–34.
Long term follicular dynamics and biochemical characteristics of dominant follicles in dairy cows subjected to acute heat stress.CrossRef | 1:CAS:528:DC%2BD3MXjtlCjurc%3D&md5=310b082d17dff889dddec4f2b87f5904CAS | 11343839PubMed |

Gwag, T., Park, K., Kim, E., Son, C., Park, J., Nikawa, T., and Choi, I. (2013). Inhibition of C2C12 myotube atrophy by a novel HSP70 inducer, celastrol, via activation of Akt1 and ERK1/2 pathways. Arch. Biochem. Biophys. 537, 21–30.
Inhibition of C2C12 myotube atrophy by a novel HSP70 inducer, celastrol, via activation of Akt1 and ERK1/2 pathways.CrossRef | 1:CAS:528:DC%2BC3sXht12gtLnP&md5=01792183213220ed81f56769ec72262dCAS | 23810294PubMed |

Hai, T., Wolfgang, C. D., Marsee, D. K., Allen, A. E., and Sivaprasad, U. (1999). ATF3 and stress responses. Gene Expr. 7, 321–335.
| 1:CAS:528:DyaK1MXltVKmtLo%3D&md5=b2d848d037bfc6db9b9670afd9c916ccCAS | 10440233PubMed |

Han, Y. L., Yang, W. X., Long, L. L., Sheng, Z., Zhou, Y., Zhao, Y. Q., Wang, Y. F., and Zhu, J. Q. (2016). Molecular cloning, expression pattern, and chemical analysis of heat shock protein 70 (HSP70) in the mudskipper Boleophthalmus pectinirostris: evidence for its role in regulating spermatogenesis. Gene 575, 331–338.
Molecular cloning, expression pattern, and chemical analysis of heat shock protein 70 (HSP70) in the mudskipper Boleophthalmus pectinirostris: evidence for its role in regulating spermatogenesis.CrossRef | 1:CAS:528:DC%2BC2MXhsVygtLjL&md5=55f16fe33b8f30e97496cf2e826452f2CAS | 26361844PubMed |

Hansen, P. J. (2004). Physiological and cellular adaptations of zebu cattle to thermal stress. Anim. Reprod. Sci. 82–83, 349–360.
Physiological and cellular adaptations of zebu cattle to thermal stress.CrossRef | 15271465PubMed |

Hansen, P. J. (2009). Effects of heat stress on mammalian reproduction. Philosop. Trans. R. Soc. Lond. B. Biol. Sci. 364, 3341–3350.
Effects of heat stress on mammalian reproduction.CrossRef |

Hou, X., Arvisais, E. W., Jiang, C., Chen, D. B., Roy, S. K., Pate, J. L., Hansen, T. R., Rueda, B. R., and Davis, J. S. (2008). Prostaglandin F2alpha stimulates the expression and secretion of transforming growth factor B1 via induction of the early growth response 1 gene (EGR1) in the bovine corpus luteum. Mol. Endocrinol. 22, 403–414.
Prostaglandin F2alpha stimulates the expression and secretion of transforming growth factor B1 via induction of the early growth response 1 gene (EGR1) in the bovine corpus luteum.CrossRef | 1:CAS:528:DC%2BD1cXhtlWiu70%3D&md5=dbfee38fa139b35d21241b0a22946253CAS | 17916653PubMed |

Hu, C. L., Cowan, R. G., Harman, R. M., and Quirk, S. M. (2004). Cell cycle progression and activation of Akt kinase are required for insulin-like growth factor I-mediated suppression of apoptosis in granulosa cells. Mol. Endocrinol. 18, 326–338.
Cell cycle progression and activation of Akt kinase are required for insulin-like growth factor I-mediated suppression of apoptosis in granulosa cells.CrossRef | 1:CAS:528:DC%2BD2cXhtVChsro%3D&md5=fbc2675f4abb41c26fdba0bfdf570b05CAS | 14593075PubMed |

Hunt, D., Raivich, G., and Anderson, P. N. (2012). Activating transcription factor 3 and the nervous system. Front. Mol. Neurosci. 5, Article 7.
Activating transcription factor 3 and the nervous system.CrossRef |

Inoue, K., Zama, T., Kamimoto, T., Aoki, R., Ikeda, Y., Kimura, H., and Hagiwara, M. (2004). TNFalpha-induced ATF3 expression is bidirectionally regulated by the JNK and ERK pathways in vascular endothelial cells. Genes Cells 9, 59–70.
TNFalpha-induced ATF3 expression is bidirectionally regulated by the JNK and ERK pathways in vascular endothelial cells.CrossRef | 1:CAS:528:DC%2BD2cXhtFKrtrk%3D&md5=42b6057afab7ae28c97721e014db0907CAS | 14723708PubMed |

Johnson, A. L., Bridgham, J. T., and Swenson, J. A. (2001). Activation of the Akt/protein kinase B signaling pathway is associated with granulosa cell survival. Biol. Reprod. 64, 1566–1574.
Activation of the Akt/protein kinase B signaling pathway is associated with granulosa cell survival.CrossRef | 1:CAS:528:DC%2BD3MXjtFKqsLg%3D&md5=e39b13ad0e6d06d13981ca056591b5f7CAS | 11319165PubMed |

Jonsson, N. N., McGowan, M. R., McGuigan, K., Davison, T. M., Hussain, A. M., Kafi, M., and Matschoss, A. (1997). Relationships among calving season, heat load, energy balance and postpartum ovulation of dairy cows in a subtropical environment. Anim. Reprod. Sci. 47, 315–326.
Relationships among calving season, heat load, energy balance and postpartum ovulation of dairy cows in a subtropical environment.CrossRef | 1:CAS:528:DyaK2sXmtVWhs7k%3D&md5=98658186c9d06d99c119d330e10665f1CAS | 9360770PubMed |

Khanna, A., Aten, R. F., and Behrman, H. R. (1995a). Heat shock protein-70 induction mediates luteal regression in the rat. Mol. Endocrinol. 9, 1431–1440.
Heat shock protein-70 induction mediates luteal regression in the rat.CrossRef | 1:CAS:528:DyaK2MXptV2hurw%3D&md5=43a9eb59b5fa1fe4659b514d75d9ccebCAS | 8584020PubMed |

Khanna, A., Aten, R. F., and Behrman, H. R. (1995b). Physiological and pharmacological inhibitors of luteinizing hormone-dependent steroidogenesis induce heat shock protein-70 in rat luteal cells. Endocrinology 136, 1775–1781.
Physiological and pharmacological inhibitors of luteinizing hormone-dependent steroidogenesis induce heat shock protein-70 in rat luteal cells.CrossRef | 1:CAS:528:DyaK2MXks1Citr8%3D&md5=10389a2a68923bb33e31efd0c8fb63dcCAS | 7895690PubMed |

Kobayashi, Y., Wakamiya, K., Kohka, M., Yamamoto, Y., and Okuda, K. (2013). Summer heat stress affects prostaglandin synthesis in the bovine oviduct. Reproduction 146, 103–110.
Summer heat stress affects prostaglandin synthesis in the bovine oviduct.CrossRef | 1:CAS:528:DC%2BC3sXhtlSnsb7P&md5=95f4683848a5904ba401deb3bd06dd97CAS | 23704311PubMed |

Koivisto, E., Jurado, A. A., Moilanen, A. M., Tokola, H., Aro, J., Pennanen, H., Sakkinen, H., Kaikkonen, L., Ruskoaho, H., and Rysa, J. (2014). Characterization of the regulatory mechanisms of activating transcription factor 3 by hypertrophic stimuli in rat cardiomyocytes. PLoS One 9, e105168.
Characterization of the regulatory mechanisms of activating transcription factor 3 by hypertrophic stimuli in rat cardiomyocytes.CrossRef | 25136830PubMed |

Lee, J. S., Lee, J. J., and Seo, J. S. (2005). HSP70 deficiency results in activation of c-Jun N-terminal kinase, extracellular signal-regulated kinase, and caspase-3 in hyperosmolarity-induced apoptosis. J. Biol. Chem. 280, 6634–6641.
HSP70 deficiency results in activation of c-Jun N-terminal kinase, extracellular signal-regulated kinase, and caspase-3 in hyperosmolarity-induced apoptosis.CrossRef | 1:CAS:528:DC%2BD2MXhsV2qsbo%3D&md5=5097f76691ba9261efa63b88581927c6CAS | 15590690PubMed |

Lennikov, A., Kitaichi, N., Kase, S., Noda, K., Horie, Y., Nakai, A., Ohno, S., and Ishida, S. (2013). Induction of heat shock protein 70 ameliorates ultraviolet-induced photokeratitis in mice. Int. J. Mol. Sci. 14, 2175–2189.
Induction of heat shock protein 70 ameliorates ultraviolet-induced photokeratitis in mice.CrossRef | 1:CAS:528:DC%2BC3sXhvF2hsLg%3D&md5=6ffca64c33249d3029ece23b86935a6dCAS | 23340653PubMed |

Liu, X., Shi, Y., Hou, X., Wan, C., He, S., Chong, X., Liu, M., Liu, H., and Liu, F. (2014). Microarray analysis of intestinal immune-related gene expression in heat-stressed rats. Int. J. Hyperthermia 30, 324–327.
Microarray analysis of intestinal immune-related gene expression in heat-stressed rats.CrossRef | 25144822PubMed |

Mao, D., Hou, X., Talbott, H., Cushman, R., Cupp, A., and Davis, J. S. (2013). ATF3 expression in the corpus luteum: possible role in luteal regression. Mol. Endocrinol. 27, 2066–2079.
ATF3 expression in the corpus luteum: possible role in luteal regression.CrossRef | 1:CAS:528:DC%2BC3sXhvFWqt7rL&md5=2c3a29241a3a9e754f44198ca441bbf9CAS | 24196350PubMed |

McPherson, L. A., Van Kirk, E. A., and Murdoch, W. J. (1993). Localization of stress protein-70 in ovine corpora lutea during prostaglandin-induced luteolysis. Prostaglandins 46, 433–440.
Localization of stress protein-70 in ovine corpora lutea during prostaglandin-induced luteolysis.CrossRef | 1:CAS:528:DyaK2cXisVaiuw%3D%3D&md5=59ce0c1f191856b1ea428189b0523ae8CAS | 8278620PubMed |

Miyabara, E. H., Nascimento, T. L, Rodrigues, D. C., Moriscot, A. S., Davila, W. F., AitMou, Y., deTombe, P. P., and Mestril, R. (2012). Overexpression of inducible 70-kDa heat shock protein in mouse improves structural and functional recovery of skeletal muscles from atrophy. Pflugers Arch. 463, 733–741.
Overexpression of inducible 70-kDa heat shock protein in mouse improves structural and functional recovery of skeletal muscles from atrophy.CrossRef | 1:CAS:528:DC%2BC38Xlt1ynt7c%3D&md5=b154d2708eb415ffe1fe2f831fd4af3cCAS | 22391802PubMed |

Narayansingh, R. M., Senchyna, M., Vijayan, M. M., and Carlson, J. C. (2004). Expression of prostaglandin G/H synthase (PGHS) and heat shock protein-70 (HSP-70) in the corpus luteum (CL) of prostaglandin F2 alpha-treated immature superovulated rats. Can. J. Physiol. Pharmacol. 82, 363–371.
Expression of prostaglandin G/H synthase (PGHS) and heat shock protein-70 (HSP-70) in the corpus luteum (CL) of prostaglandin F2 alpha-treated immature superovulated rats.CrossRef | 1:CAS:528:DC%2BD2cXntlCnur8%3D&md5=6d3b46d2f765651c5d1941c0c2a1cb4fCAS | 15381959PubMed |

Ozawa, M., Tabayashi, D., Latief, T. A., Shimizu, T., Oshima, I., and Kanai, Y. (2005). Alterations in follicular dynamics and steroidogenic abilities induced by heat stress during follicular recruitment in goats. Reproduction 129, 621–630.
Alterations in follicular dynamics and steroidogenic abilities induced by heat stress during follicular recruitment in goats.CrossRef | 1:CAS:528:DC%2BD2MXksFGku7Y%3D&md5=3cf032f054d97f6bdeb3f532587c8450CAS | 15855625PubMed |

Pan, H., Cui, H., Liu, S., Qian, Y., Wu, H., Li, L., Guan, Y., Guan, X., Zhang, L., Fan, H. Y., Ma, Y., Li, R., Liu, M., and Li, D. (2014). LGR4 gene regulates corpus luteum maturation through modulation of the WNT-mediated EGFR–ERK signaling pathway. Endocrinology 155, 3624–3637.
LGR4 gene regulates corpus luteum maturation through modulation of the WNT-mediated EGFR–ERK signaling pathway.CrossRef | 24877628PubMed |

Putney, D. J., Malayer, J. R., Gross, T. S., Thatcher, W. W., Hansen, P. J., and Drost, M. (1988). Heat stress-induced alterations in the synthesis and secretion of proteins and prostaglandins by cultured bovine conceptuses and uterine endometrium. Biol. Reprod. 39, 717–728.
Heat stress-induced alterations in the synthesis and secretion of proteins and prostaglandins by cultured bovine conceptuses and uterine endometrium.CrossRef | 1:CAS:528:DyaL1cXmt1ehtbk%3D&md5=d0033ac7dfa554bc20dbc63b939e3a97CAS | 3196802PubMed |

Reddy, P., Shen, L., Ren, C., Boman, K., Lundin, E., Ottander, U., Lindgren, P., Liu, Y. X., Sun, Q. Y., and Liu, K. (2005). Activation of Akt (PKB) and suppression of FKHRL1 in mouse and rat oocytes by stem cell factor during follicular activation and development. Dev. Biol. 281, 160–170.
Activation of Akt (PKB) and suppression of FKHRL1 in mouse and rat oocytes by stem cell factor during follicular activation and development.CrossRef | 1:CAS:528:DC%2BD2MXkt1Gjtr4%3D&md5=67d1199f46e643b11312d950ab8f65c1CAS | 15893970PubMed |

Reddy, P., Adhikari, D., Zheng, W., Liang, S., Hamalainen, T., Tohonen, V., Ogawa, W., Noda, T., Volarevic, S., Huhtaniemi, I., and Liu, K. (2009). PDK1 signaling in oocytes controls reproductive aging and lifespan by manipulating the survival of primordial follicles. Hum. Mol. Genet. 18, 2813–2824.
PDK1 signaling in oocytes controls reproductive aging and lifespan by manipulating the survival of primordial follicles.CrossRef | 1:CAS:528:DC%2BD1MXosVansLc%3D&md5=8dbd1d8a3cb0649c2e160d2250fee36fCAS | 19423553PubMed |

Risso, G., Blaustein, M., Pozzi, B., Mammi, P., and Srebrow, A. (2015). Akt/PKB: one kinase, many modifications. Biochem. J. 468, 203–214.
Akt/PKB: one kinase, many modifications.CrossRef | 1:CAS:528:DC%2BC2MXovVSgsrY%3D&md5=1fdda8cdf80cbaef2af3c00d7936abb0CAS | 25997832PubMed |

Rodway, M. R., Steele, G. L., Baimbridge, K. G., and Leung, P. C. (1992). Prostaglandin F2 alpha and gonadotropin-releasing hormone increase intracellular free calcium in rat granulosa cells. Mol. Cell. Endocrinol. 84, 137–143.
Prostaglandin F2 alpha and gonadotropin-releasing hormone increase intracellular free calcium in rat granulosa cells.CrossRef | 1:CAS:528:DyaK38XhvVymtrc%3D&md5=56cea583520bfbbcd69882e8a49d9ac8CAS | 1639216PubMed |

Roth, Z., Meidan, R., Braw-Tal, R., and Wolfenson, D. (2000). Immediate and delayed effects of heat stress on follicular development and its association with plasma FSH and inhibin concentration in cows. J. Reprod. Fertil. 120, 83–90.
| 1:CAS:528:DC%2BD3cXntlCiurs%3D&md5=78c083f728088663e780760b56c7da70CAS | 11006149PubMed |

Seo, M. S., Oh, S. Y., Park, M. J., Kim, S. M., Kim, M. Y., Han, S. I., Park, H. G., and Kang, H. S. (2005). Implication of reactive oxygen species, ERK1/2, and p38MAPK in sodium salicylate-induced heat shock protein 72 expression in C6 glioma cells. Int. J. Mol. Med. 16, 841–849.
| 1:CAS:528:DC%2BD2MXhtFygsr7E&md5=46ef0975aa50c35d1310de616fcb527bCAS | 16211253PubMed |

Sisti, G., Kanninen, T. T., Ramer, I., and Witkin, S. S. (2015). Interaction between the inducible 70-kDa heat shock protein and autophagy: effects on fertility and pregnancy. Cell Stress Chaperones 20, 753–758.
Interaction between the inducible 70-kDa heat shock protein and autophagy: effects on fertility and pregnancy.CrossRef | 1:CAS:528:DC%2BC2MXhtVOhsLrJ&md5=6c8164cdd1130eb96fdcdac36c65f1adCAS | 26081752PubMed |

Stocco, C. O., Lau, L. F., and Gibori, G. (2002). A calcium/calmodulin-dependent activation of ERK1/2 mediates JunD phosphorylation and induction of nur77 and 20alpha-hsd genes by prostaglandin F2alpha in ovarian cells. J. Biol. Chem. 277, 3293–3302.
A calcium/calmodulin-dependent activation of ERK1/2 mediates JunD phosphorylation and induction of nur77 and 20alpha-hsd genes by prostaglandin F2alpha in ovarian cells.CrossRef | 1:CAS:528:DC%2BD38XhtVaksLc%3D&md5=941e9b59ce65353befc7f37d62c095a9CAS | 11719525PubMed |

Stocco, C., Telleria, C., and Gibori, G. (2007). The molecular control of corpus luteum formation, function, and regression. Endocr. Rev. 28, 117–149.
The molecular control of corpus luteum formation, function, and regression.CrossRef | 1:CAS:528:DC%2BD2sXjtFCgsrc%3D&md5=8cff66998bb05182271c94ffd58f5d41CAS | 17077191PubMed |

Takahashi, M. (2012). Heat stress on reproductive function and fertility in mammals. Reprod. Med. Biol. 11, 37–47.
Heat stress on reproductive function and fertility in mammals.CrossRef |

Trout, J. P., McDowell, L. R., and Hansen, P. J. (1998). Characteristics of the estrous cycle and antioxidant status of lactating Holstein cows exposed to heat stress. J. Dairy Sci. 81, 1244–1250.
Characteristics of the estrous cycle and antioxidant status of lactating Holstein cows exposed to heat stress.CrossRef | 1:CAS:528:DyaK1cXjsVOqurg%3D&md5=736c7982bf6f046d76a7fd0b525eb5a0CAS | 9621225PubMed |

Velazquez, M. M., Alfaro, N. S., Dupuy, C. R., Salvetti, N. R., Rey, F., and Ortega, H. H. (2010). Heat shock protein patterns in the bovine ovary and relation with cystic ovarian disease. Anim. Reprod. Sci. 118, 201–209.
Heat shock protein patterns in the bovine ovary and relation with cystic ovarian disease.CrossRef | 1:CAS:528:DC%2BC3cXhtVGlur4%3D&md5=e89729f44966afcc666512cf34531780CAS | 19744807PubMed |

Weems, C. W., Pexton, J. E., Butcher, R. L., and Inskeep, E. K. (1975). Prostaglandins F in uterine tissue and venous plasma of pseudopregnant rats: effect of deciduomata. Biol. Reprod. 13, 282–288.
Prostaglandins F in uterine tissue and venous plasma of pseudopregnant rats: effect of deciduomata.CrossRef | 1:CAS:528:DyaE28XoslCjuw%3D%3D&md5=6b100f8e391a6929b6e6361d9c095236CAS | 1218193PubMed |

Wei, H., and Vander, H. R. (2010). Ischemic preconditioning and heat shock activate Akt via a focal adhesion kinase-mediated pathway in Langendorff-perfused adult rat hearts. Am. J. Physiol. Heart Circ. Physiol. 298, H152–H157.
Ischemic preconditioning and heat shock activate Akt via a focal adhesion kinase-mediated pathway in Langendorff-perfused adult rat hearts.CrossRef | 1:CAS:528:DC%2BC3cXhsFKls7Y%3D&md5=10a707cdefc2a4f1d3cf3c51bba7b522CAS | 19880666PubMed |

Westfall, S. D., Hendry, I. R., Obholz, K. L., Rueda, B. R., and Davis, J. S. (2000). Putative role of the phosphatidylinositol 3-kinase-Akt signaling pathway in the survival of granulosa cells. Endocrine 12, 315–321.
Putative role of the phosphatidylinositol 3-kinase-Akt signaling pathway in the survival of granulosa cells.CrossRef | 1:CAS:528:DC%2BD3cXktlWhtr8%3D&md5=65d1c3442a968aac35c0497ffd6d07ceCAS | 10963053PubMed |

Wilson, S. J., Marion, R. S., Spain, J. N., Spiers, D. E., Keisler, D. H., and Lucy, M. C. (1998). Effect of controlled heat stress on ovarian function in dairy cattle: I. Lactating cows. J. Dairy Sci. 81, 2124–2131.
Effect of controlled heat stress on ovarian function in dairy cattle: I. Lactating cows.CrossRef | 1:CAS:528:DyaK1cXlvVCmtrk%3D&md5=0c1f8e2389c3b9c732cbbdf781ba977cCAS | 9749376PubMed |

Wise, M. E., Armstrong, D. V., Huber, J. T., Hunter, R., and Wiersma, F. (1988). Hormonal alterations in the lactating dairy cow in response to thermal stress. J. Dairy Sci. 71, 2480–2485.
Hormonal alterations in the lactating dairy cow in response to thermal stress.CrossRef | 1:CAS:528:DyaL1cXls1ertLY%3D&md5=5aeea951e9d523e4cf1b3bca5f4afc26CAS | 3183143PubMed |

Woessmann, W., Meng, Y. H., and Mivechi, N. F. (1999). An essential role for mitogen-activated protein kinases, ERKs, in preventing heat-induced cell death. J. Cell. Biochem. 74, 648–662.
An essential role for mitogen-activated protein kinases, ERKs, in preventing heat-induced cell death.CrossRef | 1:CAS:528:DyaK1MXltFeqtbo%3D&md5=f6d26c9f7d8ab70d38ee50ab60064b20CAS | 10440934PubMed |

Wright, E. C., Boehmer, B. H., Cooper-Prado, M. J., Bailey, C. L., and Wettemann, R. P. (2014). Effect of elevated ambient temperature at parturition on duration of gestation, ruminal temperature, and endocrine function of fall-calving beef cows. J. Anim. Sci. 92, 4449–4456.
Effect of elevated ambient temperature at parturition on duration of gestation, ruminal temperature, and endocrine function of fall-calving beef cows.CrossRef | 1:CAS:528:DC%2BC2cXhvFOhsLfN&md5=42454d16141595bd026d4d246a78d48fCAS | 25085395PubMed |

Yadav, V. K., and Medhamurthy, R. (2006). Dynamic changes in mitogen-activated protein kinase (MAPK) activities in the corpus luteum of the bonnet monkey (Macaca radiata) during development, induced luteolysis, and simulated early pregnancy: a role for p38 MAPK in the regulation of luteal function. Endocrinology 147, 2018–2027.
Dynamic changes in mitogen-activated protein kinase (MAPK) activities in the corpus luteum of the bonnet monkey (Macaca radiata) during development, induced luteolysis, and simulated early pregnancy: a role for p38 MAPK in the regulation of luteal function.CrossRef | 1:CAS:528:DC%2BD28Xjt1OhtbY%3D&md5=5b188f5843a977deb168003f319a0d35CAS | 16410301PubMed |

Yadav, V. K., Sudhagar, R. R., and Medhamurthy, R. (2002). Apoptosis during spontaneous and prostaglandin F(2alpha)-induced luteal regression in the buffalo cow (Bubalus bubalis): involvement of mitogen-activated protein kinases. Biol. Reprod. 67, 752–759.
Apoptosis during spontaneous and prostaglandin F(2alpha)-induced luteal regression in the buffalo cow (Bubalus bubalis): involvement of mitogen-activated protein kinases.CrossRef | 1:CAS:528:DC%2BD38XmsV2js7g%3D&md5=12e8d2ef66ccf2b8ab80cb79350ecc86CAS | 12193381PubMed |

Yoshihara, T., Naito, H., Kakigi, R., Ichinoseki-Sekine, N., Ogura, Y., Sugiura, T., and Katamoto, S. (2013). Heat stress activates the Akt/mTOR signalling pathway in rat skeletal muscle. Acta Physiol. (Oxf.) 207, 416–426.
Heat stress activates the Akt/mTOR signalling pathway in rat skeletal muscle.CrossRef | 1:CAS:528:DC%2BC3sXkvVOksg%3D%3D&md5=7f3483306e12f855d09f74f9d35ee310CAS | 23167446PubMed |

Yu, J., Liu, F., Yin, P., Zhu, X., Cheng, G., Wang, N., Lu, A., Luan, W., Zhang, N., Li, J., Guo, K., Yin, Y., Wang, H., and Xu, J. (2011). Integrating miRNA and mRNA expression profiles in response to heat stress-induced injury in rat small intestine. Funct. Integr. Genomics 11, 203–213.
Integrating miRNA and mRNA expression profiles in response to heat stress-induced injury in rat small intestine.CrossRef | 1:CAS:528:DC%2BC3MXmtlGlsrc%3D&md5=18e62528e70a24f1b2a47933a5799c7bCAS | 21057845PubMed |

Yu, J., Liu, F., Yin, P., Zhao, H., Luan, W., Hou, X., Zhong, Y., Jia, D., Zan, J., Ma, W., Shu, B., and Xu, J. (2013). Involvement of oxidative stress and mitogen-activated protein kinase signaling pathways in heat stress-induced injury in the rat small intestine. Stress 16, 99–113.
Involvement of oxidative stress and mitogen-activated protein kinase signaling pathways in heat stress-induced injury in the rat small intestine.CrossRef | 1:CAS:528:DC%2BC38XhvVajtr3N&md5=8b74e3afac45769fc99cb64744aef93fCAS | 22452662PubMed |

Zhou, J., Schmid, T., Frank, R., and Brune, B. (2004). PI3K/Akt is required for heat shock proteins to protect hypoxia-inducible factor 1alpha from pVHL-independent degradation. J. Biol. Chem. 279, 13506–13513.
PI3K/Akt is required for heat shock proteins to protect hypoxia-inducible factor 1alpha from pVHL-independent degradation.CrossRef | 1:CAS:528:DC%2BD2cXis1emu74%3D&md5=a1c272ae233c298ee9ca06e1537f3df9CAS | 14726529PubMed |



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