β-hydroxybutyrate induces endoplasmic reticulum stress in bovine cumulus cells during oocyte maturation in vitro
Daniele Missio; Julia Koch; Zigomar da Silva; Francielli Weber Santos Cibin; Marcos Henrique Barreta; Vitor Braga Rissi; André Lucio Fontana Goetten; Fernando Silveira Mesquita; Valério Marques Portela; Paulo Bayard Dias Gonçalves; Rogério Ferreira
Abstract
Keywords
References
Aardema H, Lolicato F, van de Lest CH, Brouwers JF, Vaandrager AB, van Tol HT, Roelen BA, Vos PL, Helms JB, Gadella BM. Bovine cumulus cells protect maturing oocytes from increased fatty acid levels by massive intracellular lipid storage. Biol Reprod. 2013;88(6):164.
Aardema H, van Tol HTA, Vos PLAM. An overview on how cumulus cells interact with the oocyte in a condition with elevated NEFA levels in dairy cows. Anim Reprod Sci. 2019;207:131-7.
Bae HR, Kim DH, Park MH, Lee B, Kim MJ, Lee EK, Chung KW, Kim SM, Im DS, Chung HY. β-Hydroxybutyrate suppresses inflammasome formation by ameliorating endoplasmic reticulum stress via AMPK activation. Oncotarget. 2016;7(41):66444-54.
Benzie IF, Strain JJ. The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem. 1996;239(1):70-6.
Campen KA, Mcnatty KP, Pitman JL. A protective role of cumulus cells after short-term exposure of rat cumulus cell-oocyte complexes to lifestyle or environmental contaminants. Reprod Toxicol. 2017;69:19-33.
Cetica PD, Pintos LN, Dalvit GC, Beconi MT. Antioxidant enzyme activity and oxidative stress in bovine oocyte
Chen Z, Lei L, Wen D, Yang L. Melatonin attenuates palmitic acid-induced mouse granulosa cells apoptosis via endoplasmic reticulum stress. J Ovarian Res. 2019;12(1):43.
Combelles CM, Gupta S, Agarwal A. Could oxidative stress influence the in-vitro maturation of oocytes? Reprod Biomed Online. 2009;18(6):864-80.
Duffield TF, Lissemore KD, McBride BW, Leslie KE. Impact of hyperketonemia in early lactation dairy cows on health and production. J Dairy Sci. 2009;92(2):571-80.
Dumesic DA, Meldrum DR, Katz-Jaffe MG, Krisher RL, Schoolcraft WB. Oocyte environment: follicular fluid and cumulus cells are critical for oocyte health. Fertil Steril. 2015;103(2):303-16.
Dunning KR, Lane M, Brown HM, Yeo C, Robker RL, Russell DL. Altered composition of the cumulus-oocyte complex matrix during
Fernández A, Ordóñez R, Reiter RJ, González-Gallego J, Mauriz JL. Melatonin and endoplasmic reticulum stress: relation to autophagy and apoptosis. J Pineal Res. 2015;59(3):292-307.
Ferst JG, Glanzner WG, Gutierrez K, Macedo MP, Ferreira R, Gasperin BG, Duggavathi R, Gonçalves PB, Bordignon V. Supplementation of oleic acid, stearic acid, palmitic acid and β-hydroxybutyrate increase H3K9me3 in endometrial epithelial cells of cattle cultured
Foster LA. Clinical Ketosis. Vet Clin North Am Food Anim Pract. 1988;4(2):253-67.
Hawkins RA, Biebuyck JF. Ketone bodies are selectively used by individual brain regions. Science. 1979;205(4403):325-7.
Hill SL, Olson KC, Jaeger JR, Stevenson JS. Serum and plasma metabolites associated with postpartum ovulation and pregnancy risks in suckled beef cows subjected to artificial insemination. J Anim Sci. 2018;96(1):258-72.
Holczer M, Márton M, Kurucz A, Bánhegyi G, Kapuy O. A comprehensive systems biological study of autophagy-apoptosis crosstalk during endoplasmic reticulum stress. BioMed Res Int. 2015;2015:319589.
Holm P, Booth PJ, Schmidt MH, Greve T, Callesen H. High bovine blastocyst development in a static
Hotamisligil GS. Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell. 2010;140(6):900-17.
Islam MA, Adachi S, Shiiba Y, Takeda KI, Haga S, Yonekura S. Effects of starvation-induced negative energy balance on ER stress in the liver of cows. Anim Biosci. 2021;35(1):22-8.
Itle AJ, Huzzey JM, Weary DM, von Keyserlingk MA. Clinical ketosis and standing behavior in transition cows. J Dairy Sci. 2015;98(1):128-34.
Kadowaki H, Nishitoh H. Signaling pathways from the endoplasmic reticulum and their roles in disease. Genes. 2013;4(3):306-33.
Kaneko T, Saito H, Toya M, Satio T, Nakahara K, Hiroi M. Hyaluronic acid inhibits apoptosis in granulosa cells via CD44. J Assist Reprod Genet. 2000;17(3):162-7.
Kashiwaya Y, Takeshima T, Mori N, Nakashima K, Clarke K, Veech RL. d-β-Hydroxybutyrate protects neurons in models of Alzheimer’s and Parkinson’s disease. Proc Natl Acad Sci USA. 2000;97(10):5440-4.
Kidder GM, Vanderhyden BC. Bidirectional communication between oocytes and follicle cells: ensuring oocyte developmental competence. Can J Physiol Pharmacol. 2010;88(4):399-413.
Kong G, Huang Z, Ji W, Wang X, Liu J, Wu X, Huang Z, Li R, Zhu Q. The ketone metabolite β-hydroxybutyrate attenuates oxidative stress in spinal cord injury by suppression of class I histone deacetylases. J Neurotrauma. 2017;34(18):2645-55.
Leibfried L, First NL. Characterization of bovine follicular oocytes and their ability to mature
Leroy JL, Vanholder T, Delanghe JR, Opsomer G, van Soom A, Bols PE, Dewulf J, de Kruif A. Metabolic changes in follicular fluid of the dominant follicle in high-yielding dairy cows early post partum. Theriogenology. 2004;62(6):1131-43.
Leroy JL, Vanholder T, Mateusen B, Christophe A, Opsomer G, de Kruif A, Genicot G, van Soom A. Non-esterified fatty acids in follicular fluid of dairy cows and their effect on developmental capacity of bovine oocytes
Leroy JL, Vanholder T, Opsomer G, van Soom A, de Kruif A. The
Leroy JL, van Soom A, Opsomer G, Bols PE. The consequences of metabolic changes in high-yielding dairy cows on oocyte and embryo quality. Animal. 2008;2(8):1120-7.
Leroy JL, Valckx SD, Jordaens L, De Bie J, Desmet KL, van Hoeck V, Britt JH, Marei WF, Bols PE. Nutrition and maternal metabolic health in relation to oocyte and embryo quality: critical views on what we learned from the dairy cow model. Reprod Fertil Dev. 2015;27(4):693-703.
Li Y, Ding HY, Wang XC, Feng SB, Li XB, Wang Z, Liu GW, Li XW. An association between the level of oxidative stress and the concentrations of NEFA and BHBA in the plasma of ketotic dairy cows. J Anim Physiol Anim Nutr. 2016;100(5):844-51.
Li P, Li L, Zhang C, Cheng X, Zhang Y, Guo Y, Long M, Yang S, He J. Palmitic acid and β-hydroxybutyrate induce inflammatory responses in bovine endometrial cells by activating oxidative stress-mediated NF-κB signaling. Molecules. 2019;24(13):2421.
Lin P, Yang Y, Li X, Chen F, Cui C, Hu L, Li Q, Liu W, Jin Y. Endoplasmic reticulum stress is involved in granulosa cell apoptosis during follicular atresia in goat ovaries. Mol Reprod Dev. 2012;79(6):423-32.
Loetchutinat C, Kothan S, Dechsupa S, Meesungnoen J, Jay-Gerin JP, Mankhetkorn S. Spectrofluorometric determination of intracellular levels of reactive oxygen species in drug-sensitive and drug-resistant cancer cells using the 2′,7′-dichlorofluorescein diacetate assay. Radiat Phys Chem. 2005;72(2-3):323-31.
Missio D, Fritzen A, Vieira CC, Ferst JG, Fiorenza MF, Andrade LG, Menezes BM, Rovani MT, Gasperin BG, Gonçalves PBD, Ferreira R. Increased β-hydroxybutyrate (BHBA) concentration affect follicular growth in cattle. Anim Reprod Sci. 2022;243:107033.
Nagao M, Toh R, Irino Y, Mori T, Nakajima H, Hara T, Honjo T, Satomi-Kobayashi S, Shinke T, Tanaka H, Ishida T, Hirata K. β-Hydroxybutyrate elevation as a compensatory response against oxidative stress in cardiomyocytes. Biochem Biophys Res Commun. 2006;475(4):322-8.
Navarro-Yepes J, Burns M, Anandhan A, Khalimonchuk O, del Razo LM, Quintanilla-Vega B, Pappa A, Panayiotidis MI, Franco R. Oxidative stress, redox signaling, and autophagy: cell death versus survival. Antioxid Redox Signal. 2014;21(1):66-85.
Newman JC, Verdin E. Ketone bodies as signaling metabolites. Trends Endocrinol Metab. 2014;25(1):42-52.
Parrish JJ, Susko-Parrish JL, Leibfried-Rutledge ML, Critser ES, Eyestone WH, First NL. Bovine
Peng H, Zhou JL, Liu SQ, Hu QJ, Ming JH, Qiu B. Hyaluronic acid inhibits nitric oxide-induced apoptosis and dedifferentiation of articular chondrocytes
Perry GA, Smith MF, Lucy MC, Green JA, Parks TE, MacNeil MD, Roberts AJ, Geary TW. Relationship between follicle size at insemination and pregnancy success. Proc Natl Acad Sci USA. 2005;102(14):5268-73.
Pfaffl MW. A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res. 2001;29(9):e45.
Raboisson D, Mounié M, Maigné E. Diseases, reproductive performance, and changes in milk production associated with subclinical ketosis in dairy cows: a meta-analysis and review. J Dairy Sci. 2014;97(12):7547-63.
Read CC, Edwards L, Schrick N, Rhinehart JD, Payton RR, Campagna SR, Castro HF, Klabnik JL, Horn EJ, Moorey SE. Correlation between pre-ovulatory follicle diameter and follicular fluid metabolome profiles in lactating beef cows. Metabolites. 2021;11(9):623.
Roche JR, Burke CR, Crookenden MA, Heiser A, Loor JL, Meier S, Mitchell MD, Phyn CVC, Turner SA. Fertility and the transition dairy cow. Reprod Fertil Dev. 2017;30(1):85-100.
Sangalli JR, Nociti RP, Del Collado M, Sampaio RV, da Silveira JC, Perecin F, Smith LC, Ross PJ, Meirelles FV. Characterization of histone lysine β‐hydroxybutyrylation in bovine tissues, cells, and cumulus–oocyte complexes. Mol Reprod Dev. 2022;89(9):375-98.
Sangalli JR, Sampaio RV, Del Collado M, da Silveira JC, De Bem THC, Perecin F, Smith LC, Meirelles FV. Metabolic gene expression and epigenetic effects of the ketone body β -hydroxybutyrate on H3K9ac in bovine cells, oocytes and embryos. Sci Rep. 2018;8(1):13766.
Shi X, Li X, Li D, Li Y, Song Y, Deng Q, Wang J, Zhang Y, Ding H, Yin L, Zhang Y, Wang Z, Li X, Liu G. B-Hydroxybutyrate activates the NF-κB signaling pathway to promote the expression of pro-inflammatory factors in calf hepatocytes. Cell Physiol Biochem. 2014;33(4):920-32.
Shi Z, Song Y, Gao X, Loor JJ, Aboragah A, Yu H, Fang Z, Zhu Y, Du X, Li X, Gao W, Liu G. Disruption of endoplasmic reticulum homeostasis exacerbates liver injury in clinically ketotic cows. J Dairy Sci. 2021;104(8):9130-41.
Shimada M, Hernandez-Gonzalez I, Gonzalez-Robayna I, Richards JS. Paracrine and autocrine regulation of epidermal growth factor-like factors in cumulus oocyte complexes and granulosa cells: key roles for prostaglandin synthase 2 and progesterone receptor. Mol Endocrinol. 2006;20(6):1352-65.
Shimazu T, Hirschey MD, Newman J, He W, Shirakawa K, Le Moan N, Grueter CA, Lim H, Saunders LR, Stevens RD, Newgard CB, Farese RV Jr, Cabo R, Ulrich S, Akassoglou K, Verdin E. Suppression of oxidative stress by β -hydroxybutyrate, an endogenous histone deacetylase inhibitor. Science. 2013;339(6116):211-4.
Song Y, Li X, Li Y, Li N, Shi X, Ding H, Zhang Y, Li X, Liu G, Wang Z. Non-esterified fatty acids activate the ROS-p38-p53/Nrf2 signaling pathway to induce bovine hepatocyte apoptosis
Stevenson JS, Banuelos S, Mendonça LGD. Transition dairy cow health is associated with first postpartum ovulation risk, metabolic status, milk production, rumination, and physical activity. J Dairy Sci. 2020;103(10):9573-86.
Sugiura K, Su YQ, Eppig JJ. Targeted suppression of
Sutton-McDowall ML, Wu LL, Purdey M, Abell AD, Goldys EM, MacMillan KL, Thompson JG, Robker RL. Nonesterified fatty acid-induced endoplasmic reticulum stress in cattle cumulus oocyte complexes alters cell metabolism and developmental competence. Biol Reprod. 2016;94(1):23.
Tagawa R, Kawano Y, Minami A, Nishiumi S, Yano Y, Yoshida M, Kodama Y. β-hydroxybutyrate protects hepatocytes against endoplasmic reticulum stress in a sirtuin 1-independent manner. Arch Biochem Biophys. 2019;663:220-7.
Tanghe S, van Soom A, Nauwynck H, Coryn M, de Kruif A. Minireview: functions of the cumulus oophorus during oocyte maturation, ovulation, and fertilization. Mol Reprod Dev. 2002;61(3):414-24.
Tatemoto H, Sakurai N, Muto N. Protection of porcine oocytes against apoptotic cell death caused by oxidative stress during
Tsuzuki Y, Ikeuchi K, Nabenishi H, Ashizawa K. Effect of β-hydroxybutyrate added to maturation medium on nuclear maturation of pig oocytes. J Mamm Ova Res. 2009;26(3):153-8.
Tunjung WA, Yokoo M, Hoshino Y, Miyake Y, Kadowaki A, Sato E. Biochemical and biophysical research communications effect of hyaluronan to inhibit caspase activation in porcine granulosa cells. Biochem Biophys Res Commun. 2009;382(1):160-4.
Valckx SD, van Hoeck V, Arias-Alvarez M, Maillo V, Lopez-Cardona AP, Gutierrez-Adan A, Berth M, Cortvrindt R, Bols PE, Leroy JL. Elevated non-esterified fatty acid concentrations during
Vigetti D, Rizzi M, Moretto P, Deleonibus S, Dreyfuss JM, Karousou E, Viola M, Clerici M, Hascall VC, Ramoni MF, De Luca G, Passi A. Glycosaminoglycans and glucose prevent apoptosis in 4-methylumbelliferone-treated human aortic smooth muscle cells. J Biol Chem. 2011;286(40):34497-503.
Wang Y, Lauer ME, Anand S, Mack JA, Maytin EV. Hyaluronan synthase 2 protects skin fibroblasts against apoptosis induced by environmental stress. J Biol Chem. 2014;289(46):32253-65.
Wullepit N, Hostens M, Ginneberge C, Fievez V, Opsomer G, Fremaut D, De Smet S. Influence of a marine algae supplementation on the oxidative status of plasma in dairy cows during the periparturient period. Prev Vet Med. 2012;103(4):298-303.
Yang X, Wu LL, Chura LR, Liang X, Lane M, Norman RJ, Robker RL. Exposure to lipid-rich follicular fluid is associated with endoplasmic reticulum stress and impaired oocyte maturation in cumulus-oocyte complexes. Fertil Steril. 2012;97(6):1438-43.
Yorimitsu T, Nair U, Yang Z, Klionsky DJ. Endoplasmic reticulum stress triggers autophagy. J Biol Chem. 2006;281(40):30299-304.
Youssef MA, El-Khodery SA, El-deeb WM, El-Amaiem WEEA. Ketosis in buffalo (
Zhang B, Li M, Yang W, Loor JJ, Wang S, Zhao Y, Guo H, Ma X, Xia C, Xu C. Orai calcium release-activated calcium modulator 1 (ORAI1) plays a role in endoplasmic reticulum stress in bovine mammary epithelial cells challenged with physiological levels of ketone bodies. J Dairy Sci. 2020;103(5):4691-701.
Submitted date:
09/19/2024
Accepted date:
02/12/2025
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