リケラボ論文検索は、全国の大学リポジトリにある学位論文・教授論文を一括検索できる論文検索サービスです。

リケラボ 全国の大学リポジトリにある学位論文・教授論文を一括検索するならリケラボ論文検索大学・研究所にある論文を検索できる

リケラボ 全国の大学リポジトリにある学位論文・教授論文を一括検索するならリケラボ論文検索大学・研究所にある論文を検索できる

大学・研究所にある論文を検索できる 「Study on the effect of Asparagus officinalis stem extract on the induction of molecular chaperone and cellular function of bovine granulosa cells」の論文概要。リケラボ論文検索は、全国の大学リポジトリにある学位論文・教授論文を一括検索できる論文検索サービスです。

コピーが完了しました

URLをコピーしました

論文の公開元へ論文の公開元へ
書き出し

Study on the effect of Asparagus officinalis stem extract on the induction of molecular chaperone and cellular function of bovine granulosa cells

HO, Khoi Thieu 北海道大学

2022.03.24

概要

The defence response to stress from outside enviroment is important for maintaining the functions of cells, tissues, organs and whole animal bodies, and therefore lives have various defence mechanisms. Heat stress (HS) negatively affects various cell functions, including intracellular protein activity, gene expressions, and viability. In contrast, cells also have a defensive response mechanism to protect themselves. Heat shock protein (HSP) 70 is a well-known HS-induced protein and acts as an intracellular molecular chaperone to protect cells against stress conditions. Although HSP70 is induced by HS to confer stress resistance to cells, simultaneously HS causes cell toxicity by increasing reactive oxygen species (ROS). Recently, a standardized extract of Asparagus officinalis stem (EAS), produced from the by-product of asparagus, has been shown to induce HS independent induction of HSP70 in several somatic cells such as Hela cell, liver cell and pheochromocytoma cells in relation with regulating intracellular redox balance. However, the effects of EAS on reproductive cell function remain unknown.

In this chapter 2, I investigated the effect of EAS on HSP70 induction and oxidative redox balance in cultured bovine granulosa cells (GC). EAS treatment significantly increased HSP70 expression level, whereas no significant effect was observed on HSP27 and HSP90 expression level under non-HS condition. EAS treatment decreased ROS generation and DNA damage with increase in glutathione (GSH) synthesis under both non-HS and HS conditions. Moreover, EAS synergistically increased HSP70 and heat shock factor (HSF)1 and progesterone (P4) levels by HS treatment in GC. In order to know the effect of EAS under HS condition, the bovine GC were exposed to HS at 41 °C along with control groups (38.5 °C). Besides, treatment with an HSP70 inhibitor significantly increased ROS level, decreased GSH level, and decreased HSF1, nuclear factor erythroid 2-related factor 2 (NFE2L2, also known as NRF2), and Kelch-like ECHassociated protein 1 (KEAP1) in the presence of EAS. Furthermore, EAS treatment significantly increased P4 synthesis in CG. Thus, EAS improves HSP70- mediated redox balance and cell function in bovine CG.

P4 is a well-known steroid hormone and has role in ovarian function including oocyte growth and maintenance of pregnancy in mammals. HS by high ambient temperature in summer season is known to decrease P4 synthesis in the ovarian corpus luteum (CL) with collapsing a balance of intracellular redox status. P4 biosynthesis occurs in mitochondria. For utilizing, cholesterol from lipid droplet is transported into the mitochondrial inner membrane by steroidogenic acute regulatory protein (STAR). The enzyme Cytochrome P450, family 11, subfamily A, polypeptide 1 (CYP11A1) conversed cholesterol to pregnenolone which is catalysed into P4 by 3β-hydroxysteroid dehydrogenase (3β-HSD).

In chapter 3, to clarify the steroidgenesis pathway including mitochondrial could be affected by HS and possibly be controled by HSP70, I investigated the effect of EAS on P4 level, expression of steroidogenesis genes, mitochondrial activity and lipid metabolism of GC under non-HS and HS conditions. P4 level was increased by EAS treatment in association with the increase in STAR, 3β-HSD, mitochondrial membrane activity and lipid droplet both under non-HS and HS conditions. Notably, synergistic effect of EAS with HS co-treatment was observed to show a greater increase in P4 synthesis when comparison with EAS treatment under nonHS condition. Furthermore, inhibition of HSP70 significantly reduced EASinduced P4 synthesis, mitochondrial activity and synthesis of lipid droplets. Overall results show that EAS-induced P4 synthesis is mediated by activation STAR and 3β-HSD pathway together with improvement mitochondrial and lipid metabolism through HSP70-mediated redox balance and chaperone function in bovine GC.

The main purpose of cell freezing is to maintain sufficient cell number to provide a stable cell supply and fewer passage number. Freezing of bovine GC is commonly applied as coculture cells with supporting the embryo growth for embryo transfer and donor cells for nuclear transfer. However, little is known about the effect of EAS pre-freezing treatment on post-freezing viability and redox status.

In chapter 4, I investigated the effect of EAS on the post-freezing viability of HS treated bovine GC in relation to the redox balance. HS pre-treatment significantly decreased the post-freezing viability, whereas EAS pre-treatment significantly increased the post-freezing viability of HS treated cells. ROS levels were increased by HS and decreased after EAS pre-treatment. GSH levels were increased by EAS pre-treatment. These results suggest that EAS affects the postfreezing viability of HS bovine GC by improving intracellular molecular chaperones and the redox status.

In conclusion, EAS improved reproductive function and cellular protection in bovine GC. Moreover, synergistic effect of EAS and HS co-treatment on HSP70 production can contribute to improvement of P4 synthesis and cellular survival.

この論文で使われている画像

参考文献

Abedel-Majed, M. A., S. M. Romereim, J. S. Davis, and A. S. Cupp. 2019. Perturbations in Lineage Specification of Granulosa and Theca Cells May Alter Corpus Luteum Formation and Function. Frontiers in Endocrinology. 10. doi:10.3389/fendo.2019.00832.

Amin, A., A. Gad, D. Salilew-Wondim, S. Prastowo, E. Held, M. Hoelker, F. Rings, E. Tholen, C. Neuhoff, C. Looft, K. Schellander, and D. Tesfaye. 2014. Bovine embryo survival under oxidative-stress conditions is associated with activity of the NRF2-mediated oxidative-stress-response pathway. Mol Reprod Dev. 81:497–513. doi:10.1002/mrd.22316.

Andersson B.E., J. H. 1993. Temperature regulation and environmental physiology. R. W. O. Swenson M.J., editor. Dukes’ Physiology of Domestic Animals ( 11th ed. ). 886–895.

Bachhawat, A. K., and S. Yadav. 2018. The glutathione cycle: Glutathione metabolism beyond the gamma-glutamyl cycle. Iubmb Life. 70:585–592. doi:10.1002/iub.1756.

Bae, S. H., S. H. Sung, S. Y. Oh, J. M. Lim, S. K. Lee, Y. N. Park, H. E. Lee, D. Kang, and S. G. Rhee. 2013. Sestrins Activate Nrf2 by Promoting p62- Dependent Autophagic Degradation of Keap1 and Prevent Oxidative Liver Damage. Cell Metabolism. 17:73–84. doi:10.1016/j.cmet.2012.12.002.

Balaburski, G. M., J. I.-J. Leu, N. Beeharry, S. Hayik, M. D. Andrake, G. Zhang, M. Herlyn, J. Villanueva, R. L. Dunbrack, T. Yen, D. L. George, and M. E. Murphy. 2013. A modified HSP70 inhibitor shows broad activity as an anticancer agent. Mol Cancer Res. 11:219–229. doi:10.1158/1541- 7786.MCR-12-0547-T.

Bassi, G., S. K. Sidhu, and S. Mishra. 2021. The Expanding Role of Mitochondria, Autophagy and Lipophagy in Steroidogenesis. Cells. 10:1851. doi:10.3390/cells10081851.

Bates, K. A., A. R. Harvey, M. Carruthers, and R. N. Martins. 2005. Androgens, andropause and neurodegeneration: exploring the link between steroidogenesis, androgens and Alzheimer’s disease. Cell Mol Life Sci. 62:281–292. doi:10.1007/s00018-004-4383-1.

Bazer, F. W., T. E. Spencer, G. A. Johnson, and R. C. Burghardt. 2011. Uterine receptivity to implantation of blastocysts in mammals. Front Biosci (Schol Ed). 3:745–767. doi:10.2741/s184.

Broussard, J. R., J. K. Thibodeaux, M. W. Myers, J. D. Roussel, S. G. Prough, J. Blackwell, and R. A. Godke. 1994. Frozen-thawed cumulus-granulosa cells support bovine embryo development during coculture. Fertility and Sterility. 62:176–180.

Bryan, H. K., A. Olayanju, C. E. Goldring, and B. K. Park. 2013. The Nrf2 cell defence pathway: Keap1-dependent and -independent mechanisms of regulation. Biochemical Pharmacology. 85:705–717. doi:10.1016/j.bcp.2012.11.016.

Bukau, B., E. Deuerling, C. Pfund, and E. A. Craig. 2000. Getting newly synthesized proteins into shape. Cell. 101:119–122. doi:10.1016/S0092- 8674(00)80806-5.

Burke, J. M., D. E. Spiers, F. N. Kojima, G. A. Perry, B. E. Salfen, S. L. Wood, D. J. Patterson, M. F. Smith, M. C. Lucy, W. G. Jackson, and E. L. Piper. 2001. Interaction of endophyte-infected fescue and heat stress on ovarian function in the beef heifer. Biol Reprod. 65:260–268. doi:10.1095/biolreprod65.1.260.

Calderwood, S. K., M. A. Stevenson, and A. Murshid. 2012. Heat Shock Proteins, Autoimmunity, and Cancer Treatment. Autoimmune Dis. 2012:486069. doi:10.1155/2012/486069.

Carroll, R., and D. Yellon. 1999. Heat Stress Proteins and Their Relationship to Myocardial Protection. doi:10.1007/978-3-642-58259-2_12.

Chapman, J. C., J. R. Polanco, S. Min, and S. D. Michael. 2005. Mitochondrial 3 beta-hydroxysteroid dehydrogenase (HSD) is essential for the synthesis of progesterone by corpora lutea: An hypothesis. Reproductive Biology and Endocrinology. 3:11. doi:10.1186/1477-7827-3-11.

Collier, R. J., G. E. Dahl, and M. J. VanBaale. 2006. Major advances associated with environmental effects on dairy cattle. Journal of Dairy Science. 89:1244–1253. doi:10.3168/jds.S0022-0302(06)72193-2.

Conley, A. J., and I. M. Bird. 1997. The role of cytochrome P450 17 alphahydroxylase and 3 beta-hydroxysteroid dehydrogenase in the integration of gonadal and adrenal steroidogenesis via the delta 5 and delta 4 pathways of steroidogenesis in mammals. Biol Reprod. 56:789–799. doi:10.1095/biolreprod56.4.789.

Cotgreave, I. A. 2003. Analytical developments in the assay of intra- and extracellular GSH homeostasis: Specific protein S-glutathionylation, cellular GSH and mixed disulphide compartmentalisation and interstitial GSH redox balance (Reprinted from Thiol Metabolism and Redox Regulation of Cellular Functions). Biofactors. 17:269–277. doi:10.1002/biof.5520170126.

Dalcin, L., R. C. Silva, F. Paulini, B. D. M. Silva, J. P. Neves, and C. M. Lucci. 2013. Cytoskeleton structure, pattern of mitochondrial activity and ultrastructure of frozen or vitrified sheep embryos. Cryobiology. 67:137– 145. doi:10.1016/j.cryobiol.2013.05.012.

Dasgupta, J., S. Kar, R. Liu, J. Joseph, B. Kalyanaraman, S. J. Remington, C. Chen, and J. A. Melendezi. 2010. Reactive Oxygen Species Control SenescenceAssociated Matrix Metalloproteinase-1 Through c-Jun-N-Terminal Kinase. Journal of Cellular Physiology. 225:52–62. doi:10.1002/jcp.22193.

deMatos, D. G., C. C. Furnus, and D. F. Moses. 1997. Glutathione synthesis during in vitro maturation of bovine oocytes: Role of cumulus cells. Biology of Reproduction. 57:1420–1425. doi:10.1095/biolreprod57.6.1420.

Edwards, J. L., A. D. Ealy, V. H. Monterroso, and P. J. Hansen. 1997. Ontogeny of temperature-regulated heat shock protein 70 synthesis in preimplantation bovine embryos. Molecular Reproduction and Development. 48:25–33. doi:10.1002/(sici)1098-2795(199709)48:13.0.co;2-r.

Elis, S., A. Desmarchais, V. Maillard, S. Uzbekova, P. Monget, and J. Dupont. 2015. Cell proliferation and progesterone synthesis depend on lipid metabolism in bovine granulosa cells. Theriogenology. 83:840–853. doi:10.1016/j.theriogenology.2014.11.019.

Elliott, R. M. A., R. E. Lloyd, A. Fazeli, E. Sostaric, A. S. Georgiou, N. Satake, P. F. Watson, and W. V. Holt. 2009. Effects of HSPA8, an evolutionarily conserved oviductal protein, on boar and bull spermatozoa. Reproduction. 137:191–203. doi:10.1530/rep-08-0298.

Endo, T., R. F. Aten, L. Leykin, and H. R. Behrman. 1993. Hydrogen peroxide evokes antisteroidogenic and antigonadotropic actions in human granulosa luteal cells. The Journal of Clinical Endocrinology & Metabolism. 76:337– 342. doi:10.1210/jcem.76.2.7679398.

Espinosa-Diez, C., V. Miguel, D. Mennerich, T. Kietzmann, P. Sanchez-Perez, S. Cadenas, and S. Lamas. 2015. Antioxidant responses and cellular adjustments to oxidative stress. Redox Biology. 6:183–197. doi:10.1016/j.redox.2015.07.008.

Faden, A. I., V. A. Movsesyan, S. M. Knoblach, F. Ahmed, and I. Cernak. 2005. Neuroprotective effects of novel small peptides in vitro and after brain injury. Neuropharmacology. 49:410–424. doi:10.1016/j.neuropharm.2005.04.001.

Fair, T., and P. Lonergan. 2012. The role of progesterone in oocyte acquisition of developmental competence. Reprod Domest Anim. 47 Suppl 4:142–147. doi:10.1111/j.1439-0531.2012.02068.x.

Fang, C.-T., H.-H. Kuo, S.-C. Hsu, and L.-H. Yih. 2019. HSP70 is required for the proper assembly of pericentriolar material and function of mitotic centrosomes. Cell Division. 14:4. doi:10.1186/s13008-019-0047-7.

Fatehi, R., A. ,. Roelen, B. ,. Colenbrander, B. ,. Schoevers, E. ,. Gadella, B. ,. Bevers, M. ,. &. Van den Hurk. 2005. Presence of cumulus cells during in vitro fertilization protects the bovine oocyte against oxidative stress and improves first cleavage but does not affect further development. Zygote. 13:177–185. doi:doi:10.1017/S0967199405003126.

Gavet, O., and J. Pines. 2010. Activation of cyclin B1-Cdk1 synchronizes events in the nucleus and the cytoplasm at mitosis. Journal of Cell Biology. 189:247–259. doi:10.1083/jcb.200909144.

George, L. E., M. F. Lokhandwala, and M. Asghar. 2012. Novel role of NF-kappa B-p65 in antioxidant homeostasis in human kidney-2 cells. American Journal of Physiology-Renal Physiology. 302:F1440–F1446. doi:10.1152/ajprenal.00006.2012.

Glory, A., and D. A. Averill-Bates. 2016. The antioxidant transcription factor Nrf2 contributes to the protective effect of mild thermotolerance (40 degrees C) against heat shock-induced apoptosis. Free Radical Biology and Medicine. 99:485–497. doi:10.1016/j.freeradbiomed.2016.08.032.

Guerin, P., S. El Mouatassim, and Y. Menezo. 2001. Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Human Reproduction Update. 7:175–189. doi:10.1093/humupd/7.2.175.

Guo, S. H., W. Wharton, P. Moseley, and H. L. Shi. 2007. Heat shock protein 70 regulates cellular redox status by modulating glutathione-related enzyme activities. Cell Stress & Chaperones. 12:245–254. doi:10.1379/csc-265.1.

Halliwell, B. 2000. The antioxidant paradox. Lancet. 355:1179–1180. doi:10.1016/s0140-6736(00)02075-4.

Hargitai, J., H. Lewis, I. Boros, T. Rácz, A. Fiser, I. Kurucz, I. Benjamin, L. Vígh, Z. Pénzes, P. Csermely, and D. S. Latchman. 2003. Bimoclomol, a heat shock protein co-inducer, acts by the prolonged activation of heat shock factor-1. Biochem Biophys Res Commun. 307:689–695. doi:10.1016/s0006-291x(03)01254-3.

Hartl, F. U., A. Bracher, and M. Hayer-Hartl. 2011. Molecular chaperones in protein folding and proteostasis. Nature. 475:324–332. doi:10.1038/nature10317.

Hartl, F. U., and M. Hayer-Hartl. 2002. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science. 295:1852–1858. doi:10.1126/science.1068408.

Hayden, M. S., and S. Ghosh. 2008. Shared principles in NF-kappa B signaling. Cell. 132:344–362. doi:10.1016/j.cell.2008.01.020.

Hayes, J. D., and A. T. Dinkova-Kostova. 2014. The Nrf2 regulatory network provides an interface between redox and intermediary metabolism. Trends in Biochemical Sciences. 39:199–218. doi:10.1016/j.tibs.2014.02.002.

Hendrick, J. P., and F. U. Hartl. 1993. Molecular chaperone functions of heatshock proteins. Annu Rev Biochem. 62:349–384. doi:10.1146/annurev.bi.62.070193.002025.

Hensen, S. M. M., L. Heldens, C. M. W. van Enckevort, S. T. van Genesen, G. J. M. Pruijn, and N. H. Lubsen. 2013. Activation of the antioxidant response in methionine deprived human cells results in an HSF1-independent increase in HSPA1A mRNA levels. Biochimie. 95:1245–1251. doi:10.1016/j.biochi.2013.01.017.

Hesselink JM, K. 2016. Bimoclomol and arimoclomol: hsp-co-inducers for the treatment of protein misfolding disorders, neuropathy and neuropathic pain. J Pain Relief. 06. doi:10.4172/2167-0846.1000279.

Hirakawa, T., K. Rokutan, T. Nikawa, and K. Kishi. 1996. Geranylgeranylacetone induces heat shock proteins in cultured guinea pig gastric mucosal cells and rat gastric mucosa. Gastroenterology. 111:345–357. doi:10.1053/gast.1996.v111.pm8690199.

Hiroi, M., T. Ogihara, K. Hirano, M. Hasegawa, T. Morinobu, H. Tamai, and E. Niki. 2005. Regulation of apoptosis by glutathione redox state in PC12 cells exposed simultaneously to iron and ascorbic acid. Free Radical Biology and Medicine. 38:1057–1072. doi:10.1016/j.freeradbiomed.2005.01.001.

Hoque, S. A. M., T. Umehara, T. Kawai, and M. Shimada. 2021. Adverse effect of superoxide-induced mitochondrial damage in granulosa cells on follicular development in mouse ovaries. Free Radic Biol Med. 163:344– 355. doi:10.1016/j.freeradbiomed.2020.12.434.

Howell, J. L., J. W. Fuquay, and A. E. Smith. 1994. Corpus luteum growth and function in lactating holstein cows during spring and summer. Journal of Dairy Science. 77:735–739. doi:10.3168/jds.S0022-0302(94)77007-7.

Hwang, I.-S., H.-K. Bae, and H.-T. Cheong. 2013. Mitochondrial and DNA damage in bovine somatic cell nuclear transfer embryos. J Vet Sci. 14:235– 240. doi:10.4142/jvs.2013.14.3.235.

Ichimura, Y., S. Waguri, Y. Sou, S. Kageyama, J. Hasegawa, R. Ishimura, T. Saito, Y. J. Yang, T. Kouno, T. Fukutomi, T. Hoshii, A. Hirao, K. Takagi, T. Mizushima, H. Motohashi, M. S. Lee, T. Yoshimori, K. Tanaka, M. Yamamoto, and M. Komatsu. 2013. Phosphorylation of p62 Activates the Keap1-Nrf2 Pathway during Selective Autophagy. Molecular Cell. 51:618– 631. doi:10.1016/j.molcel.2013.08.003.

Imamoto, N. 2018. Heat stress-induced nuclear transport mediated by Hikeshi confers nuclear function of Hsp70s. Current Opinion in Cell Biology. 52:82–87. doi:10.1016/j.ceb.2018.02.010.

Inoue, S., J. Takanari, K. Abe, A. Nagayama, Y. Ikeya, and N. Kohda. 2020. Isolation and structure determination of a heat shock protein inducer, asparagus-derived proline-containing 3-alkyldiketopiperazines (asparaprolines), from a standardized extract of asparagus officinalis stem. Natural Product Communications. 15. doi:10.1177/1934578x20914681.

Ito, Tomohiro, K. Goto, J. Takanari, T. Miura, K. Wakame, H. Nishioka, A. Tanaka, and J. Nishihira. 2014. Effects of enzyme-treated asparagus extract on heat shock protein 70, stress indices, and sleep in healthy adult men. J Nutr Sci Vitaminol (Tokyo). 60:283–290. doi:10.3177/jnsv.60.283.

Ito, T., T. Maeda, K. Goto, T. Miura, K. Wakame, H. Nishioka, and A. Sato. 2014. Enzyme-Treated Asparagus Extract Promotes Expression of Heat Shock Protein and Exerts Antistress Effects. Journal of Food Science. 79:H413– H419. doi:10.1111/1750-3841.12371.

Ito, T., A. Sato, T. Ono, K. Goto, T. Maeda, J. Takanari, H. Nishioka, K. Komatsu, and H. Matsuura. 2013. Isolation, Structural Elucidation, and Biological Evaluation of a 5-Hydroxymethyl-2-furfural Derivative, Asfural, from Enzyme-Treated Asparagus Extract. Journal of Agricultural and Food Chemistry. 61:9155–9159. doi:10.1021/jf402010c.

Jarc, E., and T. Petan. 2019. Lipid Droplets and the Management of Cellular Stress. Yale J Biol Med. 92:435–452.

Jashni, H. K., H. K. Jahromi, A. G. Ranjbary, Z. K. Jahromi, and Z. K. Kherameh. 2016. Effects of aqueous extract from Asparagus officinalis L. roots on hypothalamic-pituitary-gonadal axis hormone levels and the number of ovarian follicles in adult rats. International Journal of Reproductive Biomedicine. 14:75–80.

Jeng, W., S. Lee, N. Sung, J. Lee, and F. T. F. Tsai. 2015. Molecular chaperones: guardians of the proteome in normal and disease states. F1000Res. 4:F1000 Faculty Rev-1448. doi:10.12688/f1000research.7214.1.

Jiang, H., J. He, S. Pu, C. Tang, and G. Xu. 2007. Heat shock protein 70 is translocated to lipid droplets in rat adipocytes upon heat stimulation. Biochim Biophys Acta. 1771:66–74. doi:10.1016/j.bbalip.2006.10.004.

Khan, A., J. H. Dou, Y. C. Wang, X. L. Jiang, M. Z. Khan, H. P. Luo, T. Usman, and H. B. Zhu. 2020. Evaluation of heat stress effects on cellular and transcriptional adaptation of bovine granulosa cells. Journal of Animal Science and Biotechnology. 11. doi:10.1186/s40104-019-0408-8.

Kim, B. Y., Z. G. Cui, S. R. Lee, S. J. Kim, H. K. Kang, Y. K. Lee, and D. B. Park. 2009. Effects of Asparagus officinalis extracts on liver cell toxicity and ethanol metabolism. Journal of Food Science. 74:H204–H208. doi:10.1111/j.1750-3841.2009.01263.x.

Kim, J. Y., Y. Han, J. E. Lee, and M. A. Yenari. 2018. The 70-kDa heat shock protein (Hsp70) as a therapeutic target for stroke. Expert Opinion on Therapeutic Targets. 22:191–199. doi:10.1080/14728222.2018.1439477.

Kotoglou, P., A. Kalaitzakis, P. Vezyraki, T. Tzavaras, L. K. Michalis, F. Dantzer, J. U. Jung, and C. Angelidis. 2009. Hsp70 translocates to the nuclei and nucleoli, binds to XRCC1 and PARP-1, and protects HeLa cells from singlestrand DNA breaks. Cell Stress & Chaperones. 14:391–406. doi:10.1007/s12192-008-0093-6.

Krajka-Kuzniak, V., J. Paluszczak, and W. Baer-Dubowska. 2017. The Nrf2-ARE signaling pathway: An update on its regulation and possible role in cancer prevention and treatment. Pharmacological Reports. 69:393–402. doi:10.1016/j.pharep.2016.12.011.

Kregel, K. C. 2002. Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. Journal of Applied Physiology. 92:2177–2186. doi:10.1152/japplphysiol.01267.2001.

Kuo, L. J., and L. X. Yang. 2008. gamma-H2AX - A novel biomarker for DNA double-strand breaks. In Vivo. 22:305–309.

Lee, S.-J., J. Zhang, A. M. K. Choi, and H. P. Kim. 2013. Mitochondrial dysfunction induces formation of lipid droplets as a generalized response to stress. Oxid Med Cell Longev. 2013:327167. doi:10.1155/2013/327167.

Lees, A. M., V. Sejian, J. C. Lees, M. L. Sullivan, A. T. Lisle, and J. B. Gaughan. 2019. Evaluating rumen temperature as an estimate of core body temperature in Angus feedlot cattle during summer. International Journal of Biometeorology. 63:939–947. doi:10.1007/s00484-019-01706-0.

Leibfriedrutledge, M. L., E. S. Critser, J. J. Parrish, and N. L. First. 1989. Invitro maturation and fertilization of bovine oocytes. Theriogenology. 31:61–74. doi:10.1016/0093-691x(89)90564-5.

Leu, J. I.-J., J. Pimkina, A. Frank, M. E. Murphy, and D. L. George. 2009. A small molecule inhibitor of inducible heat shock protein 70. Mol Cell. 36:15–27. doi:10.1016/j.molcel.2009.09.023.

Li, J., Y. A. Liu, P. K. Duan, R. G. Yu, Z. T. Gu, L. Li, Z. F. Liu, and L. Su. 2018. NF-kappa B regulates HSF1 and c-Jun activation in heat stress-induced intestinal epithelial cell apoptosis. Molecular Medicine Reports. 17:3388– 3396. doi:10.3892/mmr.2017.8199.

Li, J. Y., H. Gao, Z. Tian, Y. Wu, Y. Z. Wang, Y. Fang, L. Lin, Y. Han, S. S. Wu, I. Haq, and S. M. Zeng. 2016. Effects of chronic heat stress on granulosa cell apoptosis and follicular atresia in mouse ovary. Journal of Animal Science and Biotechnology. 7. doi:10.1186/s40104-016-0116-6.

Li, L., J. Wu, M. Luo, Y. Sun, and G. L. Wang. 2016. The effect of heat stress on gene expression, synthesis of steroids, and apoptosis in bovine granulosa cells. Cell Stress & Chaperones. 21:467–475. doi:10.1007/s12192-016- 0673-9.

Lindquist, S. 1986. The heat-shock response. Annual Review of Biochemistry. 55:1151–1191. doi:10.1146/annurev.bi.55.070186.005443.

Linfor, J. J., and S. A. Meyers. 2002. Detection of DNA damage in response to cooling injury in equine spermatozoa using single-cell gel electrophoresis. Journal of Andrology. 23:107–113. doi:10.1002/j.1939- 4640.2002.tb02603.x.

Loi, P., K. Matsukawa, G. Ptak, M. Clinton, J. F. Jr, Y. Nathan, and A. Arav. 2008. Freeze-dried somatic cells direct embryonic development after nuclear transfer. PLOS ONE. 3:e2978. doi:10.1371/journal.pone.0002978.

Lonergan, P., N. Forde, T. Spencer, P. Lonergan, N. Forde, and T. Spencer. 2016. Role of progesterone in embryo development in cattle. Reprod. Fertil. Dev. 28:66–74. doi:10.1071/RD15326.

Lu, X. Y., L. Xiao, L. Wang, and D. M. Ruden. 2012. Hsp90 inhibitors and drug resistance in cancer: The potential benefits of combination therapies of Hsp90 inhibitors and other anti-cancer drugs. Biochemical Pharmacology. 83:995–1004. doi:10.1016/j.bcp.2011.11.011.

Lucy, M. C. 2001. ADSA Foundation Scholar Award - Reproductive loss in highproducing dairy cattle: Where will it end? Journal of Dairy Science. 84:1277–1293. doi:10.3168/jds.S0022-0302(01)70158-0.

Luvoni, G. C., L. Keskintepe, and B. G. Brackett. 1996. Improvement in bovine embryo production in vitro by glutathione-containing culture media. Molecular Reproduction and Development. 43:437–443. doi:10.1002/(sici)1098-2795(199604)43:43.0.co;2-q.

Makris, D. P., and J. T. Rossiter. 2001. Domestic processing of onion bulbs (Allium cepa) and asparagus spears (Asparagus officinalis): Effect on flavonol content and antioxidant status. Journal of Agricultural and Food Chemistry. 49:3216–3222. doi:10.1021/jf001497z.

Manousakidi, S., A. Guillaume, C. Pirou, S. Bouleau, B. Mignotte, F. Renaud, and N. Le Floch. 2018. FGF1 induces resistance to chemotherapy in ovarian granulosa tumor cells through regulation of p53 mitochondrial localization. Oncogenesis. 7:1–13. doi:10.1038/s41389-018-0033-y.

Massa, S. M., R. A. Swanson, and F. R. Sharp. 1996. The stress gene response in brain. Cerebrovasc Brain Metab Rev. 8:95–158.

Maya-Soriano, M. J., E. Taberner, and M. López-Béjar. 2013. Retinol improves in vitro oocyte nuclear maturation under heat stress in heifers. Zygote. 21:377– 384. doi:10.1017/S0967199412000135.

Mayer, M. P., and B. Bukau. 2005. Hsp70 chaperones: Cellular functions and molecular mechanism. Cell Mol Life Sci. 62:670–684. doi:10.1007/s00018- 004-4464-6.

Mazur, P., S. P. Leibo, and E. H. Y. Chu. 1972. 2-factor hypothesis of freezing injury - evidence from chinese-hamster tissue-culture cells. Experimental Cell Research. 71:345-. doi:10.1016/0014-4827(72)90303-5.

McAllister, J. M., J. I. Mason, W. Byrd, J. M. Trant, M. R. Waterman, and E. R. Simpson. 1990. Proliferating human granulosa-lutein cells in long-term monolayer-culture - expression of aromatase, cholesterol side-chain cleavage, and 3-beta-hydroxysteroid dehydrogenase. Journal of Clinical Endocrinology & Metabolism. 71:26–33. doi:10.1210/jcem-71-1-26.

McClellan, A. J., Y. Xia, A. M. Deutschbauer, R. W. Davis, M. Gerstein, and J. Frydman. 2007. Diverse cellular functions of the Hsp90 molecular chaperone uncovered using systems approaches. Cell. 131:121–135. doi:10.1016/j.cell.2007.07.036.

McGann, L. E., H. Y. Yang, and M. Walterson. 1988. Manifestations of celldamage after freezing and thawing. Cryobiology. 25:178–185. doi:10.1016/0011-2240(88)90024-7.

Meister, A. 1982. Metabolism and function of glutathione - an overview. Biochemical Society Transactions. 10:78–79. doi:10.1042/bst0100078.

Michels, A. A., B. Kanon, A. W. Konings, K. Ohtsuka, O. Bensaude, and H. H. Kampinga. 1997. Hsp70 and Hsp40 chaperone activities in the cytoplasm and the nucleus of mammalian cells. J Biol Chem. 272:33283–33289. doi:10.1074/jbc.272.52.33283.

Mizutani, T., S. Ishikane, S. Kawabe, A. Umezawa, and K. Miyamoto. 2015. Transcriptional regulation of genes related to progesterone production [Review]. Endocrine Journal. 62:757–763. doi:10.1507/endocrj.EJ15-0260.

Montaño, E., M. Olivera, and Z. T. Ruiz-Cortés. 2009. Association between leptin, LH and its receptor and luteinization and progesterone accumulation (P4) in bovine granulosa cell in vitro. Reprod Domest Anim. 44:699–704. doi:10.1111/j.1439-0531.2007.01053.x.

Mori, M., T. Hayashi, Y. Isozaki, N. Takenouchi, and M. Sakatani. 2015. Heat shock decreases the embryonic quality of frozen-thawed bovine blastocysts produced in vitro. Journal of Reproduction and Development. 61:423–429. doi:10.1262/jrd.2015-003.

Mosser, D. D., and R. I. Morimoto. 2004. Molecular chaperones and the stress of oncogenesis. Oncogene. 23:2907–2918. doi:10.1038/sj.onc.1207529.

Murdoch, W. J. 1998. Inhibition by oestradiol of oxidative stress-induced apoptosis in pig ovarian tissues. Journal of Reproduction and Fertility. 114:127–130.

Nabenishi, H., H. Ohta, T. Nishimoto, T. Morita, K. Ashizawa, and Y. Tsuzuki. 2011. Effect of the temperature-humidity index on body temperature and conception rate of lactating dairy cows in southwestern Japan. Journal of Reproduction and Development. 57:450–456. doi:10.1262/jrd.10-135T.

Nabenishi, H., S. Takagi, H. Kamata, T. Nishimoto, T. Morita, K. Ashizawa, and Y. Tsuzuki. 2012. The role of mitochondrial transition pores on bovine oocyte competence after heat stress, as determined by effects of cyclosporin A. Mol Reprod Dev. 79:31–40. doi:10.1002/mrd.21401.

Naidu, S. D., R. V. Kostov, and A. T. Dinkova-Kostova. 2015. Transcription factors Hsf1 and Nrf2 engage in crosstalk for cytoprotection. Trends in Pharmacological Sciences. 36:6–14. doi:10.1016/j.tips.2014.10.011.

Nandi, S., M. S. Chauhan, and P. Palta. 1998. Influence of cumulus cells and sperm concentration on cleavage rate and subsequent embryonic development of buffalo (Bubalus bubalis) oocytes matured and fertilized in vitro. Theriogenology. 50:1251–1262. doi:10.1016/s0093-691x(98)00224-6.

Nishizawa, M., M. Kano, T. Okuyama, T. Okumura, and Y. Ikeya. 2016. Antiinflammatory effects of enzyme-treated asparagus extract and its constituents in hepatocytes. Functional Foods in Health and Disease. 6:91– 109.

Ogasawara, J., T. Ito, K. Wakame, K. Kitadate, T. Sakurai, S. Sato, Y. Ishibashi, T. Izawa, K. Takahashi, H. Ishida, I. Takabatake, T. Kizaki, and H. Ohno. 2014. ETAS, an enzyme-treated asparagus extract, attenuates amyloid betainduced cellular disorder in PC12 cells. Natural Product Communications. 9:561–564.

Ohtsuka, K., D. Kawashima, Y. Gu, and K. Saito. 2005. Inducers and co-inducers of molecular chaperones. Int J Hyperthermia. 21:703–711. doi:10.1080/02656730500384248.

Olzmann, J. A., and P. Carvalho. 2019. Dynamics and functions of lipid droplets. Nat Rev Mol Cell Biol. 20:137–155. doi:10.1038/s41580-018-0085-z.

Orrenius, S., A. Gogvadze, and B. Zhivotovsky. 2007. Mitochondrial oxidative stress: Implications for cell death. Annual Review of Pharmacology and Toxicology. 47:143–183. doi:10.1146/annurev.pharmtox.47.120505.105122.

Östling, P., J. K. Björk, P. Roos-Mattjus, V. Mezger, and L. Sistonen. 2007. Heat Shock Factor 2 (HSF2) contributes to inducible expression of hsp genes through Interplay with HSF1. Journal of Biological Chemistry. 282:7077– 7086. doi:10.1074/jbc.M607556200.

Parida, S., S. R. Mishra, C. Mishra, N. Dalai, S. Mohapatra, A. P. K. Mahapatra, and A. K. Kundu. 2020. Impact of heat stress on expression kinetics of HSP27 in cardiac cells of goats. Biological Rhythm Research. 51:925–933. doi:10.1080/09291016.2018.1564578.

Park, S. J., H. R. Choi, K. M. Nam, J. I. Na, C. H. Huh, and K. C. Park. 2013. Immediate induction of heat shock proteins is not protective against cryopreservation in normal human fibroblasts. Cryoletters. 34:239–247.

Payton, R. R., R. Romar, P. Coy, A. M. Saxton, J. L. Lawrence, and J. L. Edwards. 2004. Susceptibility of bovine germinal vesicle-stage oocytes from antral follicles to direct effects of heat stress in vitro. Biology of Reproduction. 71:1303–1308. doi:10.1095/biolreprod.104.029892.

Pirkkala, L., P. Nykänen, and L. Sistonen. 2001. Roles of the heat shock transcription factors in regulation of the heat shock response and beyond. FASEB J. 15:1118–1131. doi:10.1096/fj00-0294rev.

Pizarro, B. M., A. Cordeiro, M. W. Reginatto, S. P. C. Campos, A. C. A. Mancebo, P. C. F. Areas, R. A. Antunes, M. do C. B. Souza, K. J. Oliveira, F. F. Bloise, E. Bloise, R. S. Fortunato, and T. M. Ortiga-Carvalho. 2020. Estradiol and progesterone levels are related to redox status in the follicular fluid during in vitro fertilization. Journal of the Endocrine Society. 4. doi:10.1210/jendso/bvaa064.

Plachot, M., J. M. Antoine, S. Alvarez, C. Firmin, A. Pfister, J. Mandelbaum, A. M. Junca, and J. Salatbaroux. 1993. Granulosa-cells improve human embryo development in-vitro. Human Reproduction. 8:2133–2140. doi:10.1093/oxfordjournals.humrep.a137995.

Reddy, V. S., B. Yadav, C. L. Yadav, M. Anand, D. K. Swain, D. Kumar, D. Kritani, A. K. Madan, J. Kumar, and S. Yadav. 2018. Effect of sericin supplementation on heat shock protein 70 (HSP70) expression, redox status and post thaw semen quality in goat. Cryobiology. 84:33–39. doi:10.1016/j.cryobiol.2018.08.005.

Rekawiecki, R., M. K. Kowalik, D. Slonina, and J. Kotwica. Regulation of progesterone synthesis and action in bovine corpus luteum. 15.

Rensis, F. D., and R. J. Scaramuzzi. 2003. Heat stress and seasonal effects on reproduction in the dairy cow—a review. Theriogenology. 60:1139–1151. doi:10.1016/S0093-691X(03)00126-2.

Rispoli, L. A., R. R. Payton, C. Gondro, A. M. Saxton, K. A. Nagle, B. W. Jenkins, F. N. Schrick, and J. L. Edwards. 2013. Heat stress effects on the cumulus cells surrounding the bovine oocyte during maturation: altered matrix metallopeptidase 9 and progesterone production. Reproduction. 146:193– 207. doi:10.1530/REP-12-0487.

Rodgers, R. J., and H. F. Irving-Rodgers. 2010. Formation of the ovarian follicular antrum and follicular fluid. Biol Reprod. 82:1021–1029. doi:10.1095/biolreprod.109.082941.

Rojas-Downing, M. M., A. P. Nejadhashemi, T. Harrigan, and S. A. Woznicki. 2017. Climate change and livestock: Impacts, adaptation, and mitigation. Climate Risk Management. 16:145–163. doi:10.1016/j.crm.2017.02.001.

Rone, M. B., J. Fan, and V. Papadopoulos. 2009. Cholesterol transport in steroid biosynthesis: role of protein-protein interactions and implications in disease states. Biochim Biophys Acta. 1791:646–658. doi:10.1016/j.bbalip.2009.03.001.

Roth, Z. 2015. Physiology and endocrinology symposium: Cellular and molecular mechanisms of heat stress related to bovine ovarian function. Journal of Animal Science. 93:2034–2044. doi:10.2527/jas.2014-8625.

Roth, Z., A. Arav, A. Bor, Y. Zeron, R. Braw-Tal, and D. Wolfenson. 2001a. Improvement of quality of oocytes collected in the autumn by enhanced removal of impaired follicles from previously heat-stressed cows. Reproduction. 122:737–744. doi:10.1530/rep.0.1220737.

Roth, Z., and P. J. Hansen. 2005. Disruption of nuclear maturation and rearrangement of cytoskeletal elements in bovine oocytes exposed to heat shock during maturation. Reproduction. 129:235–244. doi:10.1530/rep.1.00394.

Roth, Z., R. Meidan, A. Shaham-Albalancy, R. Braw-Tal, and D. Wolfenson. 2001b. Delayed effect of heat stress on steroid production in medium-sized and preovulatory bovine follicles. Reproduction. 121:745–751.

Russell, D. L., R. B. Gilchrist, H. M. Brown, and J. G. Thompson. 2016. Bidirectional communication between cumulus cells and the oocyte: Old hands and new players? Theriogenology. 86:62–68. doi:10.1016/j.theriogenology.2016.04.019.

de S Torres-Júnior, J. R., M. de F A Pires, W. F. de Sá, A. de M Ferreira, J. H. M. Viana, L. S. A. Camargo, A. A. Ramos, I. M. Folhadella, J. Polisseni, C. de Freitas, C. a. A. Clemente, M. F. de Sá Filho, F. F. Paula-Lopes, and P. S. Baruselli. 2008. Effect of maternal heat-stress on follicular growth and oocyte competence in Bos indicus cattle. Theriogenology. 69:155–166. doi:10.1016/j.theriogenology.2007.06.023.

Saibil, H. 2013. Chaperone machines for protein folding, unfolding and disaggregation. Nature Reviews Molecular Cell Biology. 14:630–642. doi:10.1038/nrm3658.

Sakurai, T., T. Ito, K. Wakame, K. Kitadate, T. Arai, J. Ogasawara, T. Kizaki, S. Sato, Y. Ishibashi, T. Fujiwara, K. Akagawa, H. Ishida, and H. Ohno. 2014. Enzyme-treated Asparagus officinalis extract shows neuroprotective effects and attenuates cognitive impairment in senescence-accelerated mice. Natural Product Communications. 9:101–106.

Salminen, A., T. Paimela, T. Suuronen, and K. Kaarniranta. 2008. Innate immunity meets with cellular stress at the IKK complex: regulation of the IKK complex by HSP70 and HSP90. Immunol Lett. 117:9–15. doi:10.1016/j.imlet.2007.12.017.

Santoro, M. G. 2000. Heat shock factors and the control of the stress response. Biochemical Pharmacology. 59:55–63. doi:10.1016/s0006-2952(99)00299- 3.

de los Santos, M. J., V. García-Láez, D. Beltrán-Torregrosa, J. A. Horcajadas, J. A. Martínez-Conejero, F. J. Esteban, A. Pellicer, and E. Labarta. 2012. Hormonal and molecular characterization of follicular fluid, cumulus cells and oocytes from pre-ovulatory follicles in stimulated and unstimulated cycles. Hum Reprod. 27:1596–1605. doi:10.1093/humrep/des082.

Sartori, R., G. J. M. Rosa, and M. C. Wiltbank. 2002. Ovarian structures and circulating steroids in heifers and lactating cows in summer and lactating and dry cows in winter. Journal of Dairy Science. 85:2813–2822. doi:10.3168/jds.S0022-0302(02)74368-3.

Shahat, A. M., G. Rizzoto, and J. P. Kastelic. 2020. Amelioration of heat stressinduced damage to testes and sperm quality. Theriogenology. 158:84–96. doi:10.1016/j.theriogenology.2020.08.034.

Shaik, S., D. Hayes, J. Gimble, and R. Devireddy. 2017. Inducing heat shock proteins enhances the stemness of frozen-thawed adipose tissue-derived stem cells. Stem Cells and Development. 26:608–616. doi:10.1089/scd.2016.0289.

Shi, B., D. Feng, M. Sagnelli, J. Jiao, X. Sun, X. Wang, and D. Li. 2020. Fructose levels are elevated in women with polycystic ovary syndrome with obesity and hyperinsulinemia. Hum Reprod. 35:187–194. doi:10.1093/humrep/dez239.

Shirato, K., J. Takanari, J. Ogasawara, T. Sakurai, K. Imaizumi, H. Ohno, and T. Kizaki. 2016. Enzyme-treated Asparagus extract attenuates hydrogen peroxide-induced matrix metalloproteinase-9 expression in murine skin fibroblast L929 cells. Natural Product Communications. 11:677–680.

Sirotkin, A. V. 2010. Effect of two types of stress (heat shock/high temperature and malnutrition/serum deprivation) on porcine ovarian cell functions and their response to hormones. Journal of Experimental Biology. 213:2125– 2130. doi:10.1242/jeb.040626.

Sottile, M. L., and S. B. Nadin. 2018. Heat shock proteins and DNA repair mechanisms: an updated overview. Cell Stress & Chaperones. 23:303–315. doi:10.1007/s12192-017-0843-4.

Steele, M. L., S. Fuller, M. Patel, C. Kersaitis, L. Ooi, and G. Munch. 2013. Effect of Nrf2 activators on release of glutathione, cysteinylglycine and homocysteine by human U373 astroglial cells. Redox Biology. 1:441–445. doi:10.1016/j.redox.2013.08.006.

Su, Y. Q., K. Sugiura, and J. J. Eppig. 2009. Mouse oocyte control of granulosa cell development and function: paracrine regulation of cumulus cell metabolism. Seminars in Reproductive Medicine. 27:32–42. doi:10.1055/s0028-1108008.

Su, Y.-Q., X. Wu, M. J. O’Brien, F. L. Pendola, J. N. Denegre, M. M. Matzuk, and J. J. Eppig. 2004. Synergistic roles of BMP15 and GDF9 in the development and function of the oocyte-cumulus cell complex in mice: genetic evidence for an oocyte-granulosa cell regulatory loop. Dev Biol. 276:64–73. doi:10.1016/j.ydbio.2004.08.020.

Suzuki, H., B. S. Jeong, and X. Z. Yang. 2000. Dynamic changes of cumulusoocyte cell communication during in vitro maturation of porcine oocytes. Biology of Reproduction. 63:723–729. doi:10.1095/biolreprod63.3.723.

Takahashi, M., T. Sakurai, and T. Hisajima. 2016. Effect of Enzyme-Treated Asparagus Extract on brain function. The FASEB Journal. 30:1176.10- 1176.10. doi:10.1096/fasebj.30.1_supplement.1176.10.

Tatemoto, H., N. Sakurai, and N. Muto. 2000. Protection of porcine oocytes against apoptotic cell death caused by oxidative stress during in vitro maturation: Role of cumulus cells. Biology of Reproduction. 63:805–810. doi:10.1095/biolreprod63.3.805.

Tatone, C., F. Amicarelli, M. C. Carbone, P. Monteleone, D. Caserta, R. Marci, P. G. Artini, P. Piomboni, and R. Focarelli. 2008. Cellular and molecular aspects of ovarian follicle ageing. Human Reproduction Update. 14:131– 142. doi:10.1093/humupd/dmm048.

Tchouague, M., M. Grondin, A. Glory, and D. Averill-Bates. 2019. Heat shock induces the cellular antioxidant defenses peroxiredoxin, glutathione and glucose 6-phosphate dehydrogenase through Nrf2. Chemico-Biological Interactions. 310. doi:10.1016/j.cbi.2019.06.030.

Thomas, J. L., and H. S. Bose. 2015. Regulation of human 3-beta-hydroxysteroid dehydrogenase type-2 (3βHSD2) by molecular chaperones and the mitochondrial environment affects steroidogenesis. J Steroid Biochem Mol Biol. 151:74–84. doi:10.1016/j.jsbmb.2014.11.018.

Thomson, L. K., S. D. Fleming, R. J. Aitken, G. N. De Iuliis, J. A. Zieschang, and A. M. Clark. 2009. Cryopreservation-induced human sperm DNA damage is predominantly mediated by oxidative stress rather than apoptosis. Human Reproduction. 24:2061–2070. doi:10.1093/humrep/dep214.

Tsai, S.-C., C.-C. Lu, C.-S. Lin, and P. S. Wang. 2003. Antisteroidogenic actions of hydrogen peroxide on rat Leydig cells. J Cell Biochem. 90:1276–1286. doi:10.1002/jcb.10738.

Tubbs, A., and A. Nussenzweig. 2017. Endogenous DNA Damage as a Source of Genomic Instability in Cancer. Cell. 168. doi:10.1016/j.cell.2017.01.002. Available from: ://WOS:000396277600015

Vanselow, J., A. Vernunft, D. Koczan, M. Spitschak, and B. Kuhla. 2016. Exposure of Lactating Dairy Cows to Acute Pre-Ovulatory Heat Stress Affects Granulosa Cell-Specific Gene Expression Profiles in Dominant Follicles. PLOS ONE. 11:e0160600. doi:10.1371/journal.pone.0160600.

Vigh, L., P. N. Literati, I. Horvath, Z. Torok, G. Balogh, A. Glatz, E. Kovacs, I. Boros, P. Ferdinandy, B. Farkas, L. Jaszlits, A. Jednakovits, L. Koranyi, and B. Maresca. 1997. Bimoclomol: A nontoxic, hydroxylamine derivative with stress protein-inducing activity and cytoprotective effects. Nature Medicine. 3:1150–1154. doi:10.1038/nm1097-1150.

Voronina, E., L. A. Lovasco, A. Gyuris, R. A. Baumgartner, A. F. Parlow, and R. N. Freiman. 2007. Ovarian granulosa cell survival and proliferation requires the gonad-selective TFIID subunit TAF4b. Dev Biol. 303:715–726. doi:10.1016/j.ydbio.2006.12.011.

Wakayo, B. U., P. S. Brar, and S. Prabhakar. 2015. Review on mechanisms of dairy summer infertility and implications for hormonal intervention. Open Vet J. 5:6–10.

Wang, M., Y. Li, A. Molenaar, Q. Li, Y. Cao, Y. Shen, P. Chen, J. Yan, Y. Gao, and J. Li. 2021. Vitamin E and selenium supplementation synergistically alleviate the injury induced by hydrogen peroxide in bovine granulosa cells. Theriogenology. 170:91–106. doi:10.1016/j.theriogenology.2021.04.015.

Wang, P. T., Z. Q. Shu, L. Q. He, X. D. Cui, Y. Z. Wang, and D. Y. Gao. 2005. The pertinence of expression of heat shock proteins (HSPs) to the efficacy of cryopreservation in HELAS. Cryoletters. 26:7–16.

Wei, Y. H., and H. C. Lee. 2002. Oxidative stress, mitochondrial DNA mutation, and impairment of antioxidant enzymes in aging. Experimental Biology and Medicine. 227:671–682.

Westerheide, S. D., J. D. Bosman, B. N. A. Mbadugha, T. L. A. Kawahara, G. Matsumoto, S. J. Kim, W. X. Gu, J. P. Devlin, R. B. Silverman, and R. I. Morimoto. 2004. Celastrols as inducers of the heat shock response and cytoprotection. Journal of Biological Chemistry. 279:56053–56060. doi:10.1074/jbc.M409267200.

Wilson, S. J., R. S. Marion, J. N. Spain, D. E. Spiers, D. H. Keisler, and M. C. Lucy. 1998. Effects of controlled heat stress on ovarian function of dairy cattle. 1. Lactating cows. Journal of Dairy Science. 81:2124–2131. doi:10.3168/jds.S0022-0302(98)75788-1.

Wolfenson, D., H. Sonego, A. Bloch, A. Shaham-Albalancy, M. Kaim, Y. Folman, and R. Meidan. 2002. Seasonal differences in progesterone production by luteinized bovine thecal and granulosa cells. Domest Anim Endocrinol. 22:81–90. doi:10.1016/s0739-7240(01)00127-8.

Wu, X., Y. H. Zhang, Y. L. Yin, Z. Ruan, H. M. Yu, Z. L. Wu, and G. Y. Wu. 2013. Roles of heat-shock protein 70 in protecting against intestinal mucosal damage. Frontiers in Bioscience-Landmark. 18:356–365. doi:10.2741/4106.

Yan, D., K. Saito, Y. Ohmi, N. Fujie, and K. Ohtsuka. 2004. Paeoniflorin, a novel heat shock protein-inducing compound. Cell Stress & Chaperones. 9:378– 389. doi:10.1379/csc-51r.1.

Zhang, J., N. Fan, and Y. Peng. 2018. Heat shock protein 70 promotes lipogenesis in HepG2 cells. Lipids in Health and Disease. 17:73. doi:10.1186/s12944- 018-0722-8.

Zorzi, E., and P. Bonvini. 2011. Inducible Hsp70 in the Regulation of Cancer Cell Survival: Analysis of Chaperone Induction, Expression and Activity. Cancers (Basel). 3:3921–3956. doi:10.3390/cancers3043921.

Zweytick, D., K. Athenstaedt, and G. Daum. 2000. Intracellular lipid particles of eukaryotic cells. Biochim Biophys Acta. 1469:101–120. doi:10.1016/s0005-2736(00)00294-7.

参考文献をもっと見る

全国の大学の
卒論・修論・学位論文

一発検索!

この論文の関連論文を見る