O-GlcNAc修饰水平变化对牛卵母细胞体外成熟的影响

doi:10.11843/j.issn.0366-6964.2022.11.012

Abstract

Abstract: The aim of this study was to explore the effect of altered O-GlcNAc modification on in vitro maturation (IVM) of bovine oocytes. Bovine in vitro-matured(IVM) oocytes were used to detect the distribution of OGT, OGA and O-GlcNAc proteins. Then cumulus-oocyte complexes were matured in IVM medium supplemented with 4 mmol·L^-1 OGT inhibitor BADGP or 100 μmol·L^-1 OGA inhibitor PUGNAc, respectively. The none supplementation group was used as control. The first polar body extrusion rate and subsequent embryonic development in vitro were detected, the O-GlcNAc level as well as the mRNA and protein expression levels of OGT, OGA, GFAT and TXNIP were detected by RT-qPCR and Western blot. Results showed that OGT and O-GlcNAc proteins were colocalized in the cytoplasm and nucleus of oocytes, while OGA and O-GlcNAc proteins were colocalized in the cytoplasm and primarily enriched at the cortex. Compared with control group, the first polar body extrusion rate ((52.8±5.1)% & (60.9±1.9)% vs. (70.8±5.4)%) and the blastocyst formation rate ((9.6±4.9)% & (10.0±5.8)% vs. (21.5±4.3)%) significantly reduced in BADGP and PUGNAc groups (P<0.05). BADGP treatment significantly reduced the expression of OGT, the level of O-GlcNAc modification in oocytes was down-regulated, and the expression of OGA was decreased; In the PUGNAc-treated group, the expression of OGA was significantly down-regulated, the modification level of O-GlcNAc was increased, and the protein expression of OGT was significantly decreased. Inhibition of OGT significantly up-regulated the expression of GFAT mRNA, a key rate-limiting enzyme in the hexosamine biosynthesis pathway, whereas inhibition of OGA significantly down-regulated the expression of GFAT mRNA. In addition, the altered level of O-GlcNAc modification significantly up-regulated the expression of TXNIP, a key factor in glucose regulation. The results indicated that changes in the level of O-GlcNAc modification would reduce the maturation and developmental ability of bovine oocytes in vitro, and oocytes responded to the fluctuation of O-GlcNAc modification levels by feedback-regulating the expressions of OGT, OGA, GFAT and TXNIP.

Key words: bovine, oocyte, O-GlcNAc modification, OGT, OGA

CLC Number:

S823.3

WANG Tengfei, FENG Zhiqiang, SUN Yawen, ZHAO Shanjiang, HAO Haisheng, ZOU Huiying, DU Weihua, ZHAO Xueming, ZHU Huabin, PANG Yunwei. Effect of Altered O-GlcNAc Modification on in vitro Maturation of Bovine Oocytes[J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(11): 3856-3865.

References 37

[1]	KANG M K, HAN S J.Post-transcriptional and post-translational regulation during mouse oocyte maturation[J].BMB Rep, 2011, 44(3):147-157.
[2]	WU Y, LI M, YANG M.Post-translational modifications in oocyte maturation and embryo development[J].Front Cell Dev Biol, 2021, 9:645318.
[3]	YANG X Y, QIAN K.Protein O-GlcNAcylation:emerging mechanisms and functions[J].Nat Rev Mol Cell Biol, 2017, 18(7):452-465.
[4]	HART G W, HOUSLEY M P, SLAWSON C.Cycling of O-linked β-N-acetylglucosamine on nucleocytoplasmic proteins[J].Nature, 2007, 446(7139):1017-1022.
[5]	HART G W.Nutrient regulation of signaling and transcription[J].J Biol Chem, 2019, 294(7):2211-2231.
[6]	SLAWSON C, DUNCAN F E.Sweet action:the dynamics of O-GlcNAcylation during meiosis in mouse oocytes[J].Mol Reprod Dev, 2015, 82(12):915.
[7]	MIURA T, KUME M, KAWAMURA T, et al.O-GlcNAc on PKCζ inhibits the FGF4-PKCζ-MEK-ERK1/2 pathway via inhibition of PKCζ phosphorylation in mouse embryonic stem cells[J].Stem Cell Rep, 2018, 10(1):272-286.
[8]	ZHOU L T, ROMAR R, PAVONE M E, et al.Disruption of O-GlcNAc homeostasis during mammalian oocyte meiotic maturation impacts fertilization[J].Mol Reprod Dev, 2019, 86(5):543-557.
[9]	SUTTON-MCDOWALL M L, MITCHELL M, CETICA P, et al.Glucosamine supplementation during in vitro maturation inhibits subsequent embryo development:possible role of the hexosamine pathway as a regulator of developmental competence[J].Biol Reprod, 2006, 74(5):881-888.
[10]	PANTALEON M, TAN H Y, KAFER G R, et al.Toxic effects of hyperglycemia are mediated by the hexosamine signaling pathway and O-linked glycosylation in early mouse embryos[J].Biol Reprod, 2010, 82(4):751-758.
[11]	FRANK L A, SUTTON-MCDOWALL M L, RUSSELL D L, et al.Effect of varying glucose and glucosamine concentration in vitro on mouse oocyte maturation and developmental competence[J].Reprod Fertil Dev, 2013, 25(8):1095-1104.
[12]	HART G W.Three decades of research on O-GlcNAcylation-a major nutrient sensor that regulates signaling, transcription and cellular metabolism[J].Front Endocrinol (Lausanne), 2014, 5:183.
[13]	TAN E P, DUNCAN F E, SLAWSON C.The sweet side of the cell cycle[J].Biochem Soc Trans, 2017, 45(2):313-322.
[14]	WEBSTER D M, TEO C F, SUN Y H, et al.O-GlcNAc modifications regulate cell survival and epiboly during zebrafish development[J].BMC Dev Biol, 2009, 9:28.
[15]	O'DONNELL N, ZACHARA N E, HART G W, et al.Ogt-dependent X-chromosome-linked protein glycosylation is a requisite modification in somatic cell function and embryo viability[J].Mol Cell Biol, 2004, 24(4):1680-1690.
[16]	YANG Y R, SONG M, LEE H, et al.O-GlcNAcase is essential for embryonic development and maintenance of genomic stability[J].Aging Cell, 2012, 11(3):439-448.
[17]	KEEMBIYEHETTY C.Disruption of O-GlcNAc cycling by deletion of O-GlcNAcase (Oga/Mgea5) changed gene expression pattern in mouse embryonic fibroblast (MEF) cells[J].Genom Data, 2015, 5:30-33.
[18]	MUHA V, AUTHIER F, SZOKE-KOVACS Z, et al.Loss of O-GlcNAcase catalytic activity leads to defects in mouse embryogenesis[J].J Biol Chem, 2021, 296:100439.
[19]	LEFEBVRE T, BAERT F, BODART J F, et al.Modulation of O-GlcNAc glycosylation during Xenopus oocyte maturation[J].J Cell Biochem, 2004, 93(5):999-1010.
[20]	DEHENNAUT V, LEFEBVRE T, SELLIER C, et al.O-linked N-acetylglucosaminyltransferase inhibition prevents G2/M transition in Xenopus laevis oocytes[J].J Biol Chem, 2007, 282(17):12527-12536.
[21]	DEHENNAUT V, HANOULLE X, BODART J F, et al.Microinjection of recombinant O-GlcNAc transferase potentiates Xenopus oocytes M-phase entry[J].Biochem Biophys Res Commun, 2008, 369(2):539-546.
[22]	ZHU Y, HART G W.Targeting O-GlcNAcylation to develop novel therapeutics[J].Mol Aspects Med, 2021, 79:100885.
[23]	FEHL C, HANOVER J A.Tools, tactics and objectives to interrogate cellular roles of O-GlcNAc in disease[J].Nat Chem Biol, 2022, 18(1):8-17.
[24]	SLAWSON C, ZACHARA N E, VOSSELLER K, et al.Perturbations in O-linked β-N-acetylglucosamine protein modification cause severe defects in mitotic progression and cytokinesis[J].J Biol Chem, 2005, 280(38):32944-32956.
[25]	ZHANG Z, TAN E P, VANDENHULL N J, et al.O-GlcNAcase expression is sensitive to changes in O-GlcNAc homeostasis[J].Front Endocrinol (Lausanne), 2014, 5:206.
[26]	LIN C H, LIAO C C, CHEN M Y, et al.Feedback regulation of O-GlcNAc transferase through translation control to maintain intracellular O-GlcNAc homeostasis[J].Int J Mol Sci, 2021, 22(7):3463.
[27]	WEISS M, ANDERLUH M, GOBEC M.Inhibition of O-GlcNAc transferase alters the differentiation and maturation process of human monocyte derived dendritic cells[J].Cells, 2021, 10(12):3312.
[28]	MA J F, WU C, HART G W.Analytical and biochemical perspectives of protein O-GlcNAcylation[J].Chem Rev, 2021, 121(3):1513-1581.
[29]	ZHANG H L, JIA Y W, COOPER J J, et al.Common variants in glutamine:fructose-6-phosphate amidotransferase 2 (GFPT2) gene are associated with type 2 diabetes, diabetic nephropathy, and increased GFPT2 mRNA levels[J].J Clin Endocrinol Metab, 2004, 89(2):748-755.
[30]	CHIARADONNA F, RICCIARDIELLO F, PALORINI R.The nutrient-sensing hexosamine biosynthetic pathway as the Hub of cancer metabolic rewiring[J].Cells, 2018, 7(6):53.
[31]	AKELLA N M, CIRAKU L, REGINATO M J.Fueling the fire:emerging role of the hexosamine biosynthetic pathway in cancer[J].BMC Biol, 2019, 17(1):52.
[32]	CHATHAM J C, YOUNG M E, ZHANG J H.Role of O-linked N-acetylglucosamine (O-GlcNAc) modification of proteins in diabetic cardiovascular complications[J].Curr Opin Pharmacol, 2021, 57:1-12.
[33]	GHOSH S K, BOND M R, LOVE D C, et al.Disruption of O-GlcNAc cycling in C.elegans perturbs nucleotide sugar pools and complex glycans[J].Front Endocrinol (Lausanne), 2014, 5:197.
[34]	JIANG X L, PANG Y W, ZHAO S J, et al.Thioredoxin-interacting protein regulates glucose metabolism and improves the intracellular redox state in bovine oocytes during in vitro maturation[J].Am J Physiol Endocrinol Metab, 2020, 318(3):E405-E416.
[35]	PERRONE L, DEVI T S, HOSOYA K I, et al.Inhibition of TXNIP expression in vivo blocks early pathologies of diabetic retinopathy[J].Cell Death Dis, 2010, 1(8):e65.
[36]	STOLTZMAN C A, KAADIGE M R, PETERSON C W, et al.Mondoa senses non-glucose sugars:regulation of thioredoxin-interacting protein (TXNIP) and the hexose transport curb[J].J Biol Chem, 2011, 286(44):38027-38034.
[37]	FILHOULAUD G, BENHAMED F, PAGESY P, et al.O-GlcNAcylation links TxNIP to inflammasome activation in pancreatic β cells[J].Front Endocrinol (Lausanne), 2019, 10:291.

Effect of Altered O-GlcNAc Modification on in vitro Maturation of Bovine Oocytes

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