犏牛和牦牛ESCO2基因的序列特征及其在睾丸中的表达对比分析

doi:10.11843/j.issn.0366-6964.2021.011.014

Abstract

Abstract: The aim of this study was to clone the establishment of sister chromatid cohesion N-acetyltransferase 2(ESCO2) gene, analyze its expression and localization in the testis at different developmental stages in cattle-yak and yak, and provide a theoretical basis for further study the role mechanism of ESCO2 in the male meiosis process. Healthy male cattle-yaks and yaks were used as experimental animals in this study, they were divided into fetal cattle group (5-6 months old), juvenile group (1-2 years old) and adult group (3-4 years old), with 3 animals in each group. The CDS region of ESCO2 gene of cattle-yak and yak were cloned by RT-PCR and its sequence characteristics were analyzed by bioinformatics softwares. qRT-PCR was used to detect the expression patterns of ESCO2 gene in different tissues of cattle-yak. The expression of ESCO2 mRNA in testes at different developmental stages of cattle-yak and yak were detected by qRT-PCR, the differences of cell location and expression of ESCO2 protein were detected by immunohistochemistry (IHC) staining. The results showed that the CDS region of ESCO2 genes in cattle-yak was 1 833 bp(MW198470), it encoded 610 amino acids. Compared with yak, the ESCO2 protein sequence of cattle-yak had more 19 amino acids at position 301-319 aa and there were 3 amino acid mutations. The cattle-yak and cattle had higher homology than other mammals based on the protein sequence of ESCO2. Interaction network showed that ESCO2 mainly interacted with SMC3, SMC1A, PDS5A, PDS5B, STAG2 and these proteins were related to sister chromatid condensation, meiotic cell cycle, DNA repair, cell division and chromosome remodeling. ESCO2 was expressed in all tissues of the cattle-yak, but its relative expression level in the testis was significantly higher than those in other tissues (P<0.05). In addition, the spatial expression of ESCO2 in testes of cattle-yak showed an upward trend with age, and the relative expression abundance of ESCO2 in cattle-yak at juvenile and adult stages was significantly lower than that of yak(P<0.05). IHC staining showed that meiosis of male cattle-yak was blocked in primary spermatocytes and ESCO2 protein was differentially expressed in primary spermatocytes between cattle-yak and yak. The research suggested that there was obvious difference in the sequence and expression pattern of ESCO2 between cattle-yak and yak, which may be one of reasons caused male sterility in cattle-yak, but the specific mechanism need further study.

Key words: cattle-yak, ESCO2, testis, meiosis, gene expression

CLC Number:

S823.85

MIN Xingyu, YANG Lixue, YANG Manzhen, HU Yulei, YU Hailing, YANG Luyu, LI Jian, XIONG Xianrong. Sequence Characteristics and Comparative Expression Analysis in Testis of ESCO2 Gene in Cattle-yak and Yak[J]. Acta Veterinaria et Zootechnica Sinica, 2021, 52(11): 3126-3136.

References 40

[1]	WU Y, ZHANG W X, ZUO F, et al. Comparison of mRNA expression from Y-chromosome X-degenerate region genes in taurine cattle, yaks and interspecific hybrid bulls[J].Anim Genet, 2019, 50(6):740-743.
[2]	XU C F, SHAH M A, MIPAM T, et al. Bovid microRNAs involved in the process of spermatogonia differentiation into spermatocytes[J].Int J Biol Sci, 2020, 16(2):239-250.
[3]	王泳杰, 王之盛, 胡瑞, 等. 不同品种肉牛产肉性能、牛肉营养品质及风味物质的比较[J].动物营养学报, 2019, 31(8):3621-3631.WANG Y J, WANG Z S, HU R, et al. Comparison of meat performance, nutritional quality and flavor substance in beef of different breeds cattle[J].Chinese Journal of Animal Nutrition, 2019, 31(8):3621-3631.(in Chinese)
[4]	QIU Q, ZHANG G J, MA T, et al. The yak genome and adaptation to life at high altitude[J].Nat Genet, 2012, 44(8):946-949.
[5]	阿果约达, 熊显荣, 王艳, 等. 犏牛雄性不育相关lncRNA的鉴定与分析[J].畜牧兽医学报, 2019, 50(3):551-561.AGUO Y D, XIONG X R, WANG Y, et al. Identification and analysis of long non-coding RNA associated with cattle-yak male infertility[J].Acta Veterinaria et Zootechnica Sinica, 2019, 50(3):551-561.(in Chinese)
[6]	ALOMER R M, DA SILVA E M L, CHEN J R, et al. Esco1 and Esco2 regulate distinct cohesin functions during cell cycle progression[J].Proc Natl Acad Sci U S A, 2017, 114(37):9906-9911.
[7]	BENDER D, DA SILVA E M L, CHEN J R, et al. Multivalent interaction of ESCO2 with the replication machinery is required for sister chromatid cohesion in vertebrates[J].Proc Natl Acad Sci U S A, 2020, 117(2):1081-1089.
[8]	LADURNER R, KREIDL E, IVANOV M P, et al. Sororin actively maintains sister chromatid cohesion[J].EMBO J, 2016, 35(6):635-653.
[9]	MFAREJ M G, SKIBBENS R V.An ever-changing landscape in Roberts syndrome biology:implications for macromolecular damage[J].PLoS Genet, 2020, 16(12):e1009219.
[10]	MCKAY M J, CRAIG J, KALITSIS P, et al. A Roberts syndrome individual with differential genotoxin sensitivity and a DNA damage response defect[J].Int J Radiat Oncol Biol Phys, 2019, 103(5):1194-1202.
[11]	GORDILLO M, VEGA H, TRAINER A H, et al. The molecular mechanism underlying Roberts syndrome involves loss of ESCO2 acetyltransferase activity[J].Hum Mol Genet, 2008, 17(14):2172-2180.
[12]	KOUZNETSOVA E, KANNO T, KARLBERG T, et al. Sister chromatid cohesion establishment factor ESCO1 operates by substrate-assisted catalysis[J].Structure, 2016, 24(5):789-796.
[13]	HOGARTH C A, MITCHELL D, EVANOFF R, et al. Identification and expression of potential regulators of the mammalian mitotic-to-meiotic transition[J].Biol Reprod, 2011, 84(1):34-42.
[14]	LI H, YOU L J, TIAN Y F, et al. DPAGT1-mediated protein N-Glycosylation is indispensable for oocyte and follicle development in mice[J].Adv Sci (Weinh), 2020, 7(14):2000531.
[15]	LALDINSANGI C, VIJAYAPRASADARAO K, RAJAKUMAR A, et al. Two-dimensional proteomic analysis of gonads of air-breathing catfish, Clarias batrachus after the exposure of endosulfan and malathion[J].Environ Toxicol Pharmacol, 2014, 37(3):1006-1014.
[16]	EVANS E B, HOGARTH C, EVANOFF R M, et al. Localization and regulation of murine Esco2 during male and female meiosis[J].Biol Reprod, 2012, 87(3):61.
[17]	LU Y J, CHEN Y, CUI Z K, et al. Distinct roles of cohesin acetyltransferases Esco1 and Esco2 in porcine oocyte meiosis I[J].Cell Cycle, 2019, 18(19):2481-2494.
[18]	LU Y J, DAI X X, ZHANG M Q, et al. Cohesin acetyltransferase Esco2 regulates SAC and kinetochore functions via maintaining H4K16 acetylation during mouse oocyte meiosis[J].Nucleic Acids Res, 2017, 45(16):9388-9397.
[19]	MCNICOLL F, KÜHNEL A, BISWAS U, et al. Meiotic sex chromosome cohesion and autosomal synapsis are supported by Esco2[J].Life Sci Alliance, 2020, 3(3):e201900564.
[20]	LUENSE L J, DONAHUE G, LIN-SHIAO E, et al. Gcn5-mediated histone acetylation governs nucleosome dynamics in spermiogenesis[J].Dev Cell, 2019, 51(6):745-758.e6.
[21]	AKSNES H, REE R, ARNESEN T.Co-translational, post-translational, and non-catalytic roles of N-terminal acetyltransferases[J]. Mol Cell, 2019, 73(6):1097-1114.
[22]	CHEN Y, ZHOU Y L, YIN H S.Recent advances in biosensor for histone acetyltransferase detection[J].Biosens Bioelectron, 2021, 175:112880.
[23]	RIVERA-COLÓN Y, MAGUIRE A, LISZCZAK G P, et al. Molecular basis for cohesin acetylation by establishment of sister chromatid cohesion N-acetyltransferase ESCO1[J].J Biol Chem, 2016, 291(51):26468-26477.
[24]	ALEXEEV V, IGOUCHEVA O, DOMASHENKO A, et al. Localized in vivo genotypic and phenotypic correction of the albino mutation in skin by RNA-DNA oligonucleotide[J].Nat Biotechnol, 2000, 18(1):43-47.
[25]	KOBLAN L W, ERDOS M R, WILSON C, et al. In vivo base editing rescues Hutchinson-Gilford progeria syndrome in mice[J].Nature, 2021, 589(7843):608-614.
[26]	PECKER L H, LANZKRON S.Sickle cell disease[J].Ann Intern Med, 2021, 174(1):ITC1-ITC16.
[27]	VEGA H, WAISFISZ Q, GORDILLO M, et al. Roberts syndrome is caused by mutations in ESCO2, a human homolog of yeast ECO1 that is essential for the establishment of sister chromatid cohesion[J].Nat Genet, 2005, 37(5):468-470.
[28]	CHENG H Z, ZHANG N G, PATI D.Cohesin subunit RAD21:from biology to disease[J].Gene, 2020, 758:144966.
[29]	ZHANG J, FENG C, SU H D, et al. The cohesin complex subunit ZmSMC3 participates in meiotic centromere pairing in maize[J].Plant Cell, 2020, 32(4):1323-1336.
[30]	AL-JOMAH N, MUKOLOLO L, ANJUM A, et al. Pds5A and Pds5B display non-redundant functions in mitosis and their loss triggers Chk1 activation[J].Front Cell Dev Biol, 2020, 8:531.
[31]	DEARDORFF M A, BANDO M, NAKATO R, et al. HDAC8 mutations in Cornelia de Lange syndrome affect the cohesin acetylation cycle[J].Nature, 2012, 489(7415):313-317.
[32]	KULESZEWICZ K, FU X W, KUDO N R.Cohesin loading factor Nipbl localizes to chromosome axes during mammalian meiotic prophase[J].Cell Div, 2013, 8(1):12.
[33]	FAGERBERG L, HALLSTRÖM B M, OKSVOLD P, et al. Analysis of the human tissue-specific expression by genome-wide integration of transcriptomics and antibody-based proteomics[J].Mol Cell Proteomics, 2014, 13(2):397-406.
[34]	YU Y, FUSCOE J C, ZHAO C, et al. A rat RNA-Seq transcriptomic BodyMap across 11 organs and 4 developmental stages[J]. Nat Commun, 2014, 5:3230.
[35]	CHEN H M, ZHANG L, HE W T, et al. ESCO2 knockdown inhibits cell proliferation and induces apoptosis in human gastric cancer cells[J].Biochem Biophys Res Commun, 2018, 496(2):475-481.
[36]	GUO X B, HUANG B, PAN Y H, et al. ESCO2 inhibits tumor metastasis via transcriptionally repressing MMP2 in colorectal cancer[J].Cancer Manag Res, 2018, 10:6157-6166.
[37]	LOU Y N, LIU W J, WANG C L, et al. Histological evaluation and Prdm9 expression level in the testis of sterile male cattle-yaks[J].Livest Sci, 2014, 160:208-213.
[38]	SATO Y, KURIWAKI R, HAGINO S, et al. Abnormal functions of Leydig cells in crossbred cattle-yak showing infertility[J]. Reprod Domest Anim, 2020, 55(2):209-216.
[39]	YAN P, XIANG L, GUO X, et al. The low expression of Dmrt7 is associated with spermatogenic arrest in cattle-yak[J].Mol Biol Rep, 2014, 41(11):7255-7263.
[40]	李波, 庄梦茹, 李娜, 等. 奶山羊ESCO2基因克隆及其功能的初步研究[J].农业生物技术学报, 2016, 24(2):176-185.LI B, ZHUANG M R, LI N, et al. Molecular cloning of ESCO2 gene and the preliminary study of its function in dairy goat (Capra hircus)[J].Journal of Agricultural Biotechnology, 2016, 24(2):176-185.(in Chinese)

Sequence Characteristics and Comparative Expression Analysis in Testis of ESCO2 Gene in Cattle-yak and Yak

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

References 40

Related Articles 15

Recommended Articles

Metrics

Comments

[1]	YANG Yang, YU Qian, LIU Yucheng, YANG Hua, ZHAO Zhuo, WANG Limin, ZHOU Ping, YANG Qingyong, DAI Rong. Identification and Tissue Expression Analysis of the Sheep MYL Gene Family [J]. Acta Veterinaria et Zootechnica Sinica, 2024, 55(4): 1551-1564.
[2]	KANG Jia, DUAN Xiangru, YIN Xuejiao, YANG Ruochen, LI Taichun, SHAN Xinyu, CHEN Meijing, ZHANG Yingjie, LIU Yueqin. Effects of Cysteine and Methionine on Secondary Hair Follicle Growth and Hair Dermal Papilla Cell Proliferation in vitro in Cashmere Goats [J]. Acta Veterinaria et Zootechnica Sinica, 2024, 55(2): 515-527.
[3]	ZHANG Ying, YUAN Ligang, CHEN Guojuan, ZHANG Fang, YANG Dapeng. Analysis of Differential Expression of ET-1/eNOS in the Development of Cryptorchidism in Yak [J]. Acta Veterinaria et Zootechnica Sinica, 2024, 55(1): 207-217.
[4]	HU Ting, ZHANG Yonghong, HOU Xiaolin, YAO Hua, CUI Defeng, PAN Zaozao, ZHANG Lingyu, ZHANG Jiaxi, WU Qiong. The Effects of Bisphenol A on Inflammation and Amino Acid Metabolism Pathways in Porcine Testis Sertoli Cells Based on Transcriptome Analysis [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(7): 2858-2871.
[5]	QING Enhua, TANG Bincheng, NIU Tian, WANG Junqi, CHEN Zhaoyan, HU Jiwei, HE Hua, LI Liang, WANG Jiwen, HU Shenqiang. Effects of Different Dry Rearing Systems on Histomorphology of Goose Testis and External Genitalia [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(7): 2872-2885.
[6]	SUN Junfeng, PAN Jianqiu, ZHANG Zhuoshen, JIANG Danli, SHENG Xu, CHEN Rong, XU Danning, TIAN Yunbo, HUANG Yunmao. The Expression Patterns of OPN5-TSH-DIO2/DIO3 and VIP-PRL in the Process of Repressing the Testicular Function of Male Shanma Duck under Short-day Photoperiod [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(5): 2001-2012.
[7]	CHEN Cancan, JIANG Jing, SUN Xiaoyan, REN Hangxing, LI Jie. Expression of AGRP Gene in Goat Tissue and Its Action Mechanism on Melanin Production [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(4): 1441-1451.
[8]	SHAO Jing, ZHANG Ying, TANG Yu, XU Baozeng. Research Progress of ERM Proteins in Mammalian Oocyte Maturation and Fertilization [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(11): 4477-4487.
[9]	JI Zhengyu, NI Mengru, ZHANG Zhaobo, ZHAO Gan, HUANG Zan, LI Pinghua, HUANG Ruihua, HOU Liming. Research on Adipogenic Capacity and Gene Expression Pattern of in Vitro FAPs Cells Derived from Longissimus Dorsi Muscle of Suhuai Pig [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(10): 4126-4142.
[10]	SANG Lei, CHEN Dongjin, SUN Shikun, GAO Chengfang, WANG Jinxiang, CHEN Yanfeng, XIE Xiping. Cloning and Expression of GnIH Gene and Its Effect on Reproductive Hormones Secretion of Young Male Rabbits [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(1): 201-212.
[11]	LIU Huijuan, ZHUANG Su, ZHANG Jiaqi, ZHOU Binbin, XIONG Wei, WANG Tian, WANG Chao. Effects of Dietary Supplementation of Different Levels of Rutin on Testicular Tissue in Mice under Heat Stress [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(8): 2586-2597.
[12]	LUORENG Zhuoma, WANG Jinpeng, JIAO Peng, LI Yanxia, DONG Yiwen, WEI Dawei, WNAG Xingping. Construction of Dairy Cow Mastitis Model and Analysis of mRNA Transcription Level of Inflammation Related Cytokine Genes [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(8): 2763-2772.
[13]	YU Yongtao, MAO Yanni, ZHAO Qingmei, LI Jinrong, BAI Xiaonan, XUE Jiaqi, ZHANG Haodong. Expression Pattern Analysis of Related Genes in SWN Gene Cluster of Alternaria oxytropis Mutated by Ethyl Methylate [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(4): 1241-1251.
[14]	LI Yan, LAN Tingying, PANG Bo, YANG Xiaonong, HUANG Jian. Expression of NLRP3 Inflammasome Signal Associated Genes in Canine Mammary Tumors and Clinical Significance [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(4): 1252-1258.
[15]	LIU Yue, XUE Xianglan, LI Xiaobo, JIANG Lin, PU Yabin, HE Xiaohong, MA Yuehui, ZHAO Qianjun. Research Progress of the Relationship between Chromatin Accessibility and Animal Embryo Development [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(3): 680-687.