Cloning and Tissue Expression Characteristics of Yak DDIT3 Gene

doi:10.7668/hbnxb.20192262

Abstract

Abstract: The objective of this study was to investigate the sequence and tissue expression characteristics of DNA damage inducible transcript 3(DDIT3) in female yaks. The yak DDIT3 gene was cloned by RT-PCR. The structure and function of DDIT3 protein were analyzed by bioinformatics software. The expression levels of DDIT3 gene in different tissues, and different reproductive organs and oocytes at different physiological stage of female yaks were detected by Real-time quantitative PCR(RT-qPCR). The results showed that the full-length CDS region of yak DDIT3 gene was 507 bp, which encoded 168 amino acids. Nucleotide sequence alignment showed that yak had the highest homology with bison(99.71%) and more than 88% homology with other species, indicating that DDIT3 gene was highly conservative in the process of evolution. The expression of DDIT3 gene in ovary was extremely significantly higher than that in heart, liver, kidney, spleen, lung, uterus and fallopian tube(P <0.01). In the ovary, the expression of DDIT3 gene was significantly higher during pregnancy than that during follicular phase, luteal phase and fetus stage(P <0.05), and it was significantly higher during luteal phase than that in fetus stage(P <0.05). In the uterus, the expression of DDIT3 was significantly higher than that in follicular stage and fetus stage(P <0.05). In oviduct, its expression was not significantly different at different physiological stages. The expression of DDIT3 gene in M Ⅱ stage oocytes was significantly higher than that in GV stage and M Ⅰ stage(P <0.05). Its expression in M Ⅱ granulosa cells was also significantly higher than that in GV stage and M Ⅰ stage(P <0.05). There was no significant difference in DDIT3 expression between oocytes and granulosa cells in GV stage and M Ⅰ stage. In conclusion, yak DDIT3 gene possible plays an important role in regulating ovary function and pregnancy maintenance, follicle development and maturation.

Key words: Bos grunniens, DDIT3 gene, RT-qPCR, Tissue expression, Ovary, Oocyte

CLC Number:

S813.1
Q78

WU Jianfei, LIU Yu, LI Heng, JING Tian, LU Jianyuan, ZI Xiangdong. Cloning and Tissue Expression Characteristics of Yak DDIT3 Gene[J]. ACTA AGRICULTURAE BOREALI-SINICA, 2021, 36(5): 216-225. doi: 10.7668/hbnxb.20192262.

/ / Recommend / Download Citations

URL: http://www.hbnxb.net/EN/10.7668/hbnxb.20192262

http://www.hbnxb.net/EN/Y2021/V36/I5/216

References

[1] Phillips M J, Voeltz G K. Structure and function of ER membrane contact sites with other organelles[J]. Nature Reviews Molecular Cell Biology, 2016, 17(2):69-82.doi:10.1038/nrm.2015.8.
[2] Hetz C, Zhang K, Kaufman R J. Mechanisms, regulation and functions of the unfolded protein response[J]. Nature Reviews Molecular Cell Biology, 2020, 21(8):421-438.doi:10.1038/s41580-020-0250-z.
[3] Sisinni L, Pietrafesa M, Lepore S, Maddalena F, Condelli V, Esposito F, Landriscina M. Endoplasmic reticulum stress and unfolded protein response in breast cancer:The balance between apoptosis and autophagy and its role in drug resistance[J]. International Journal of Molecular Sciences, 2019, 20(4):857.doi:10.3390/ijms20040857.
[4] Xue Q H, Li C H, Chen J, Guo H M, Li D Q, Wu X L. The protective effect of the endoplasmic reticulum stress-related factors BiP/GRP78 and CHOP/Gadd153 on noise-induced hearing loss in Guinea pigs[J]. Noise & Health, 2016, 18(84):247-255.doi:10.4103/1463-1741.192481.
[5] Averous J, Bruhat A, Jousse C, Carraro V, Thiel G, Fafournoux P. Induction of CHOP expression by amino acid limitation requires both ATF4 expression and ATF2 phosphorylation[J]. Journal of Biological Chemistry, 2004, 279(7):5288-5297.doi:10.1074/jbc.M311862200.
[6] Liu X G, Yue P, Zhou Z M, Khuri F R, Sun S Y. Death receptor regulation and celecoxib-induced apoptosis in human lung cancer cells[J]. Journal of the National Cancer Institute, 2004, 96(23):1769-1780.doi:10.1093/jnci/djh322.
[7] Gáll T, Balla G, Balla J. Heme, heme oxygenase, and endoplasmic reticulum stress-A new insight into the pathophysiology of vascular diseases[J]. International Journal of Molecular Sciences, 2019, 20(15):3675.doi:10.3390/ijms20153675.
[8] Pandey V K, Mathur A, Kakkar P. Emerging role of Unfolded Protein Response(UPR) mediated proteotoxic apoptosis in diabetes[J]. Life Sciences, 2019, 216(1):246-258.doi:10.1016/j.lfs.2018.11.041.
[9] Syc-Mazurek S B, Fernandes K A, Wilson M P, Shrager P, Libby R T. Together JUN and DDIT3(CHOP) control retinal ganglion cell death after axonal injury[J]. Molecular Neurodegeneration, 2017, 12(1):71.doi:10.1186/s13024-017-0214-8.
[10] Guzel E, Arlier S, Guzeloglu-Kayisli O, Tabak M S, Ekiz T, Semerci N, Larsen K, Schatz F, Lockwood C J, Kayisli U A. Endoplasmic reticulum stress and homeostasis in reproductive physiology and pathology[J]. International Journal of Molecular Sciences, 2017, 18(4):792.doi:10.3390/ijms18040792.
[11] Lin T, Lee J E, Kang J W, Shin H Y, Lee J B, Jin D I. Endoplasmic reticulum(ER) stress and unfolded protein response(UPR) in mammalian oocyte maturation and preimplantation embryo development[J]. International Journal of Molecular Sciences, 2019, 20(2):409.doi:10.3390/ijms20020409.
[12] Park H J, Park J Y, Kim J W, Yang S G, Jung J M, Kim M J, Kang M J, Cho Y H, Wee G, Yang H Y, Song B S, Kim S U, Koo D B. Melatonin improves the meiotic maturation of porcine oocytes by reducing endoplasmic reticulum stress during in vitro maturation[J]. Journal of Pineal Research, 2018, 64(2):e12458.doi:10.1111/jpi.12458.
[13] Zhao N, Liu X J, Li J T, Zhang L, Fu Y, Zhang Y J, Chen R X, Wei X Q, Wang R, Wang Y, Zhang J M. Endoplasmic reticulum stress inhibition is a valid therapeutic strategy in vitrifying oocytes[J]. Cryobiology, 2015, 70(1):48-52.doi:10.1016/j.cryobiol.2014.12.001.
[14] Park H J, Park S J, Koo D B, Lee S R, Kong I K, Ryoo J W, Park Y I, Chang K T, Lee D S. Progesterone production is affected by unfolded protein response(UPR) signaling during the luteal phase in mice[J]. Life Sciences, 2014, 113(1/2):60-67.doi:10.1016/j.lfs.2014.07.033.
[15] Yang Y Z, Sun M, Shan Y Y, Zheng X M, Ma H M, Ma W Z, Wang Z S, Pei X Y, Wang Y R. Endoplasmic reticulum stress-mediated apoptotic pathway is involved in corpus luteum regression in rats[J]. Reproductive Sciences, 2015, 22(5):572-584.doi:10.1177/1933719114553445.
[16] Ali I, Liu H X, Li Z S, Ma D X, Xu L J, Shah S Z A, Ullah O, Fang A Z. Reduced glutathione alleviates tunicamycin-induced endoplasmic reticulum stress in mouse preimplantation embryos[J]. The Journal of Reproduction and Development, 2018, 64(1):15-24.doi:10.1262/jrd.2017-055.
[17] Yoon S B, Choi S A, Sim B W, Kim J S, Mun S E, Jeong P S, Yang H J, Lee Y, Park Y H, Song B S, Kim Y H, Jeong K J, Huh J W, Lee S R, Kim S U, Chang K T. Developmental competence of bovine early embryos depends on the coupled response between oxidative and endoplasmic reticulum stress[J]. Biology of Reproduction, 2014, 90(5):104.doi:10.1095/biolreprod.113.113480.
[18] Takahashi N, Harada M, Hirota Y, Nose E, Azhary J M, Koike H, Kunitomi C, Yoshino O, Izumi G, Hirata T, Koga K, Wada-Hiraike O, Chang R J, Shimasaki S, Fujii T, Osuga Y. Activation of endoplasmic reticulum stress in granulosa cells from patients with polycystic ovary syndrome contributes to ovarian fibrosis[J]. Scientific Reports, 2017, 7(1):10824.doi:10.1038/s41598-017-11252-7.
[19] Jiang L L, Cui J Q, Zhang C L, Xie J K, Zhang S D, Fu D J, Duo W. Sigma-1 receptor is involved in diminished ovarian reserve possibly by influencing endoplasmic reticulum stress-mediated granulosa cells apoptosis[J]. Aging, 2020, 12(10):9041-9065.doi:10.18632/aging.103166.
[20] Qiu Q, Zhang G J, Ma T, Qian W B, Wang J Y, Ye Z Q, et al. The yak genome and adaptation to life at high altitude[J]. Nature Genetics, 2012, 44(8):946-949.doi:10.1038/ng.2343.
[21] Lan D L, Xiong X R, Huang C, Mipam T D, Li J. Toward understanding the genetic basis of yak ovary reproduction:A characterization and comparative analyses of estrus ovary transcriptiome in yak and cattle[J]. PLoS One, 2016, 11(4):e0152675.doi:10.1371/journal.pone.0152675.
[22] Xia Y, Wang Q, He X D, Chen Y, Jige M T, Zi X D. Cloning and expression analysis of the follicle-stimulating hormone receptor(FSHR) gene in the reproductive axis of female yaks(Bos grunniens)[J]. Domestic Animal Endocrinology, 2020, 70:106383.doi:10.1016/j.domaniend.2019.07.011.
[23] 字向东, 罗斌, 夏威, 郑玉才, 熊显荣, 李键, 钟金城, 朱江江, 张正帆.基于RNA-Seq技术的牦牛体外受精胚胎发育转录组分析[J].中国农业科学, 2018, 51(8):1577-1589.doi:10.3864/j.issn.0578-1752.2018.08.015.
Zi X D, Luo B, Xia W, Zheng Y C, Xiong X R, Li J, Zhong J C, Zhu J J, Zhang Z F. Transcriptomic analysis of IVF embryonic development in the yak(Bos grunniens) via RNA-Seq[J]. Scientia Agricultura Sinica, 2018, 51(8):1577-1589.
[24] 海卓, 熊显荣, 马鸿程, 黄向月, 闵星宇, 李键.牦牛KDM7A 表达谱分析及其在卵母细胞减数分裂进程中的表达[J].华北农学报, 2020, 35(6):217-224.doi:10.7668/hbnxb.20191191.
Hai Z, Xiong X R, Ma H C, Huang X Y, Min X Y, Li J. Analysis of KDM7A expression profile in yak and its expression in the process of oocyte meiosis[J]. Acta Agriculturae Boreali-Sinica, 2020, 35(6):217-224.
[25] 李鑫, 何小芳, 张浩, 郑建莹, 王雨雪, 林亚秋, 王永, 朱江江.山羊PHKG1 基因克隆及其表达特性分析[J].华北农学报, 2020, 35(4):195-202.doi:10.7668/hbnxb.20190880.
Li X, He X F, Zhang H, Zheng J Y, Wang Y X, Lin Y Q, Wang Y, Zhu J J. Cloning and expression analysis of PHKG1 gene in goat[J]. Acta Agriculturae Boreali-Sinica, 2020, 35(4):195-202.
[26] Kato H, Nishitoh H. Stress responses from the endoplasmic reticulum in cancer[J]. Frontiers in Oncology, 2015, 5:93.doi:10.3389/fonc.2015.00093.
[27] 李齐发, 李隐侠, 赵兴波, 潘增祥, 刘振山, 张庆波, 屈旭光, 宋大伟, 董丽艳, 李宁, 谢庄.牦牛线粒体DNA D-loop区序列测定及其在牛亚科中分类地位的研究[J].畜牧兽医学报, 2008, 39(1):1-6.doi:10.3321/j.issn:0366-6964.2008.01.001.
Li Q F, Li Y X, Zhao X B, Pan Z X, Liu Z S, Zhang Q B, Qu X G, Song D W, Dong L Y, Li N, Xie Z. Sequencing D-loop region of mitochondrial DNA in yak and study on its taxonomic status in bovinae[J]. Acta Veterinaria et Zootechnica Sinica, 2008, 39(1):1-6.
[28] 郭松长, 刘建全, 祁得林, 杨洁, 赵新全.牦牛的分类学地位及起源研究:mtDNAD-loop序列的分析[J].兽类学报, 2006, 26(4):325-330.doi:10.16829/j.slxb.2006.04.002.
Guo S C, Liu J Q, Qi D L, Yang J, Zhao X Q. Taxonomic placement and origin of yaks:Implications from analyses of mtDNA D-loop fragment sequences[J]. Acta Theriologica Sinica, 2006, 26(4):325-330.
[29] Yin D, Dong H, Wang T X, Hu Z Z, Cheng N N, Qu W M, Huang Z L. Glutamate activates the histaminergic tuberomammillary nucleus and increases wakefulness in rats[J]. Neuroscience, 2019, 413:86-98.doi:10.1016/j.neuroscience.2019.05.032.
[30] Chaudhari N, Dawalbhakta M, Nampoothiri L. GnRH dysregulation in polycystic ovarian syndrome(PCOS) is a manifestation of an altered neurotransmitter profile[J]. Reproductive Biology and Endocrinology, 2018, 16(1):37.doi:10.1186/s12958-018-0354-x.
[31] Fagerberg L, Hallström B M, Oksvold P, Kampf C, Djureinovic D, Odeberg J, et al. Analysis of the human tissue-specific expression by genome-wide integration of transcriptomics and antibody-based proteomics[J]. Molecular and Cellular Proteomics, 2014, 13(2):397-406.doi:10.1074/mcp.M113.035600.
[32] Berisha B, Schams D. Ovarian function in ruminants[J]. Domestic Animal Endocrinology, 2005, 29(2):305-317.doi:10.1016/j.domaniend.2005.02.035.
[33] Wray S, Prendergast C. The myometrium:From excitation to contractions and labour[J]. Advances in Experimental Medicine and Biology, 2019, 1124:233-263.doi:10.1007/978-981-13-5895-1_10.
[34] Monniaux D, Michel P, Postel M, Clément F. Multi-scale modelling of ovarian follicular development:From follicular morphogenesis to selection for ovulation[J]. Biology of the Cell, 2016, 108(6):149-160.doi:10.1111/boc.201500087.
[35] Harada M, Nose E, Takahashi N, Hirota Y, Hirata T, Yoshino O, Koga K, Fujii T, Osuga Y. Evidence of the activation of unfolded protein response in granulosa and cumulus cells during follicular growth and maturation[J]. Gynecological Endocrinology, 2015, 31(10):783-787.doi:10.3109/09513590.2015.1062862.
[36] Lin P F, Yang Y Z, Li X, Chen F L, Cui C C, Hu L Y, Li Q, Liu W, Jin Y P. Endoplasmic reticulum stress is involved in granulosa cell apoptosis during follicular atresia in goat ovaries[J]. Molecular Reproduction and Development, 2012, 79(6):423-432.doi:10.1002/mrd.22045.
[37] Park H J, Park S J, Koo D B, Kong I K, Kim M K, Kim J M, Choi M S, Park Y H, Kim S U, Chang K T, Park C K, Chae J I, Lee D S. Unfolding protein response signaling is involved in development, maintenance, and regression of the corpus luteum during the bovine estrous cycle[J]. Biochemical and Biophysical Research Communications, 2013, 441(2):344-350.doi:10.1016/j.bbrc.2013.10.056.
[38] Lin P F, Jin Y P, Lan X L, Yang Y Z, Chen F L, Wang N, Li X, Sun Y J, Wang A H. GRP78 expression and regulation in the mouse uterus during embryo implantation[J]. Journal of Molecular Histology, 2014, 45(3):259-268.doi:10.1007/s10735-013-9552-1.
[39] Liu A X, He W H, Yin L J, Lü P P, Zhang Y, Sheng J Z, Leung P C, Huang H F. Sustained endoplasmic reticulum stress as a cofactor of oxidative stress in decidual cells from patients with early pregnancy loss[J]. The Journal of Clinical Endocrinology & Metabolism, 2011, 96(3):493-497.doi:10.1210/jc.2010-2192.
[40] 韩杰, 熊显荣, 蔡雯祎, 杨显英, 阿果约达, 张燕红, 李键.牦牛KDM4A 基因克隆、组织表达谱及其在卵母细胞和颗粒细胞中的表达[J].畜牧兽医学报, 2018, 49(2):291-299.doi:10.11843/j.issn.0366-6964.2018.02.008.
Han J, Xiong X R, Cai W W, Yang X Y, A Guo Y D, Zhang Y H, Li J. Cloning of KDM4A gene and its expression in different tissues, oocyte and granulosa cell of yak[J]. Acta Veterinaria et Zootechnica Sinica, 2018, 49(2):291-299.
[41] Kang J T, Koo O J, Kwon D K, Park H J, Jang G, Kang S K, Lee B C.Effects of melatonin on in vitro maturation of porcine oocyte and expression of melatonin receptor RNA in cumulus and granulosa cells[J]. Journal of Pineal Research, 2009, 46(1):22-28.doi:10.1111/j.1600-079x.2008.00602.x.
[42] Latham K E.Endoplasmic reticulum stress signaling in mammalian oocytes and embryos:Life in balance[J]. International Review of Cell and Molecular Biology, 2015, 316:227-265.doi:10.1016/bs.ircmb.2015.01.005.
[43] Zhang J Y, Diao Y F, Oqani R K, Han R X, Jin D I. Effect of endoplasmic reticulum stress on porcine oocyte maturation and parthenogenetic embryonic development in vitro[J]. Biology of Reproduction, 2012, 86(4):128, 1-9.doi:10.1095/biolreprod.111.095059.
[44] 杨方晓, 李莲, 赵若含, 王根林.褪黑素对HT-2毒素诱导的牛卵巢颗粒细胞内质网应激与自噬的影响[J].南京农业大学学报, 2020, 43(1):143-150.doi:10.7685/jnau.201812028.
Yang F X, Li L, Zhao R H, Wang G L. Effects of melatonin on endoplasmic reticulum stress and autophagy in bovine ovarian granulosa cells induced by HT-2 toxin[J]. Journal of Nanjing Agricultural University, 2020, 43(1):143-150.

Please choose a citation manager

Content to export