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Journal of Assisted Reproduction and Genetics

Erschienen in:

04.12.2019 | Assisted Reproduction Technologies

Tauroursodeoxycholic acid (TUDCA) enhanced intracytoplasmic sperm injection (ICSI) embryo developmental competence by ameliorating endoplasmic reticulum (ER) stress and inhibiting apoptosis

verfasst von: Tengfei Deng, Juanke Xie, Hengtao Ge, Qi Liu, Xiaobing Song, Lin Hu, Li Meng, Cuilian Zhang

Erschienen in: Journal of Assisted Reproduction and Genetics | Ausgabe 1/2020

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Abstract

Purpose

The objective of this study was to examine the effect of tauroursodeoxycholic acid (TUDCA) on intracytoplasmic sperm injection (ICSI) embryos by evaluating endoplasmic reticulum (ER) stress, apoptosis, and embryo developmental competence in vitro and in vivo.

Methods

ER stress–associated genes and apoptosis-associated genes were measured and apoptosis index was analyzed. Embryo developmental competence was assessed in vitro and in vivo via the inner cell mass (ICM)/trophectoderm (TE) index, pregnancy and implantation rates, and birth rate.

Results

The relative mRNA and protein expression of binding immunoglobulin protein (BIP) was significantly higher in the ICSI embryo group without TUDCA treatment (ICSI-C) than in the in vitro fertilization (IVF) group and in the ICSI embryo group with TUDCA treatment (200 μM) (ICSI-T), while TUDCA ameliorated ER stress in ICSI embryos. Embryos in the ICSI-C group showed a higher apoptosis index than those in the IVF group and ICSI-T group, and there was no significant difference between the IVF group and ICSI-T group. TUDCA can significantly improve ICSI embryo developmental competence in vitro and in vivo based on the ICM/TE index, pregnancy and implantation rates, and birth rate.

Conclusion

ICSI embryos manifested high ER stress and high apoptosis, while TUDCA ameliorated ER stress and reduced apoptosis in ICSI embryos. TUDCA can significantly improve the developmental competence of ICSI embryos in vitro and in vivo. This study provides a new idea for improving the efficiency of ICSI, and it will also have a positive effect on the development of assisted reproduction technologies for humans and other animals.

Faddy MJ, Gosden MD, Gosden RG. A demographic projection of the contribution of assisted reproductive technologies to world population growth. Reprod Biomed Online. 2018;36:455–8.PubMed

Singh K, Jaiswal D. Human male infertility: a complex multifactorial phenotype. Reprod Sci. 2011;18:418–25.PubMed

Rubino P, Vigano P, Luddi A, Piomboni P. The ICSI procedure from past to future: a systematic review of the more controversial aspects. Hum Reprod Update. 2016;22:194–227.PubMed

Khoueiry R, Ibala-Romdhane S, Al-Khtib M, Blachere T, Lornage J, Guerin JF, et al. Abnormal methylation of KCNQ1OT1 and differential methylation of H19 imprinting control regions in human ICSI embryos. Zygote. 2013;21:129–38.PubMed

Tang L, Liu Z, Zhang R, Su C, Yang W, Yao Y, et al. Imprinting alterations in sperm may not significantly influence ART outcomes and imprinting patterns in the cord blood of offspring. PLoS One. 2017;12:e0187869.PubMedPubMedCentral

Choux C, Binquet C, Carmignac V, Bruno C, Chapusot C, Barberet J, et al. The epigenetic control of transposable elements and imprinted genes in newborns is affected by the mode of conception: ART versus spontaneous conception without underlying infertility. Hum Reprod. 2018;33:331–40.PubMed

Marchesi DE, Qiao J, Feng HL. Embryo manipulation and imprinting. Semin Reprod Med. 2012;30:323–34.PubMed

Chen M, Heilbronn LK. The health outcomes of human offspring conceived by assisted reproductive technologies (ART). J Dev Orig Health Dis. 2017;8:388–402.PubMed

Vlachopoulos C, Kosteria I, Sakka S, Gkourogianni A, Terentes-Printzios D, Koutagiar I, et al. PCSK9 and Lp(a) levels of children born after assisted reproduction technologies. J Assist Reprod Genet. 2019;36:1091–9.PubMed

10.

Cram DS, Song B, McLachlan RI, Trounson AO. CAG trinucleotide repeats in the androgen receptor gene of infertile men exhibit stable inheritance in female offspring conceived after ICSI. Mol Hum Reprod. 2000;6:861–6.PubMed

11.

Salamone DF, Canel NG, Rodriguez MB. Intracytoplasmic sperm injection in domestic and wild mammals. Reproduction. 2017;154:F111–24.PubMed

12.

Arias ME, Sanchez-Villalba E, Delgado A, Felmer R. Effect of transfection and co-incubation of bovine sperm with exogenous DNA on sperm quality and functional parameters for its use in sperm-mediated gene transfer. Zygote. 2017;25:85–97.PubMed

13.

Jo HT, Bang JI, Kim SS, Choi BH, Jin JI, Kim HL, et al. Production of female bovine embryos with sex-sorted sperm using intracytoplasmic sperm injection: efficiency and in vitro developmental competence. Theriogenology. 2014;81(675-82):e1.

14.

O’Neill CL, Chow S, Rosenwaks Z, Palermo GD. Development of ICSI. Reproduction. 2018;156:F51–8.PubMed

15.

Kimura Y, Yanagimachi R. Intracytoplasmic sperm injection in the mouse. Biol Reprod. 1995;52:709–20.PubMed

16.

Salgado RM, Brom-de-Luna JG, Resende HL, Canesin HS, Hinrichs K. Lower blastocyst quality after conventional vs. Piezo ICSI in the horse reflects delayed sperm component remodeling and oocyte activation. J Assist Reprod Genet. 2018;35:825–40.PubMedPubMedCentral

17.

Yu Y, Ding C, Wang E, Chen X, Li X, Zhao C, et al. Piezo-assisted nuclear transfer affects cloning efficiency and may cause apoptosis. Reproduction. 2007;133:947–54.PubMed

18.

Sampieri L, Di Giusto P, Alvarez C. CREB3 transcription factors: ER-Golgi stress transducers as hubs for cellular homeostasis. Front Cell Dev Biol. 2019;7:123.PubMedPubMedCentral

19.

Khan S, Komarya SK, Jena G. Phenylbutyrate and beta-cell function: contribution of histone deacetylases and ER stress inhibition. Epigenomics. 2017;9:711–20.PubMed

20.

Lee WS, Yoo WH, Chae HJ. ER stress and autophagy. Curr Mol Med. 2015;15:735–45.PubMed

21.

Qu P, Zhao Y, Wang R, Zhang Y, Li L, Fan J, et al. Extracellular vesicles derived from donor oviduct fluid improved birth rates after embryo transfer in mice. Reprod Fertil Dev. 2019;31:324–32.PubMed

22.

Qu P, Qing S, Liu R, Qin H, Wang W, Qiao F, et al. Effects of embryo-derived exosomes on the development of bovine cloned embryos. PLoS One. 2017;12:e0174535.PubMedPubMedCentral

23.

Qu P, Zuo Z, Liu Z, Niu Z, Zhang Y, Du Y, et al. Sperm-borne small RNA regulate alpha-tubulin acetylation and epigenetic modification of early bovine somatic cell nuclear transfer embryos. Mol Hum Reprod. 2019.

24.

Jia L, Ding B, Shen C, Luo S, Zhang Y, Zhou L, et al. Use of oocytes selected by brilliant cresyl blue staining enhances rabbit cloned embryo development in vitro. Zygote. 2019;27:166–72.PubMed

25.

Kelley RL, Gardner DK. In vitro culture of individual mouse preimplantation embryos: the role of embryo density, microwells, oxygen, timing and conditioned media. Reprod Biomed Online. 2017;34:441–54.PubMed

26.

Bradley J, Swann K. Mitochondria and lipid metabolism in mammalian oocytes and early embryos. Int J Dev Biol. 2019;63:93–103.PubMed

27.

Wu LL, Russell DL, Norman RJ, Robker RL. Endoplasmic reticulum (ER) stress in cumulus-oocyte complexes impairs pentraxin-3 secretion, mitochondrial membrane potential (DeltaPsi m), and embryo development. Mol Endocrinol. 2012;26:562–73.PubMedPubMedCentral

28.

Latham KE. Stress signaling in mammalian oocytes and embryos: a basis for intervention and improvement of outcomes. Cell Tissue Res. 2016;363:159–67.PubMed

29.

Luo S, Mao C, Lee B, Lee AS. GRP78/BiP is required for cell proliferation and protecting the inner cell mass from apoptosis during early mouse embryonic development. Mol Cell Biol. 2006;26:5688–97.PubMedPubMedCentral

30.

Lin T, Lee JE, Oqani RK, Kim SY, Cho ES, Jeong YD, et al. Tauroursodeoxycholic acid improves pre-implantation development of porcine SCNT embryo by endoplasmic reticulum stress inhibition. Reprod Biol. 2016;16:269–78.PubMed

31.

Ullah O, Li Z, Ali I, Xu L, Liu H, Jin HZ, et al. Pterostilbene exerts a protective effect via regulating tunicamycin-induced endoplasmic reticulum stress in mouse preimplantation embryos. In Vitro Cell Dev Biol Anim. 2019;55:82–93.PubMed

32.

Ali I, Liu HX, Zhong-Shu L, Dong-Xue M, Xu L, Shah SZA, et al. Reduced glutathione alleviates tunicamycin-induced endoplasmic reticulum stress in mouse preimplantation embryos. J Reprod Dev. 2018;64:15–24.PubMed

33.

Xie Y, Wang F, Puscheck EE, Rappolee DA. Pipetting causes shear stress and elevation of phosphorylated stress-activated protein kinase/jun kinase in preimplantation embryos. Mol Reprod Dev. 2007;74:1287–94.PubMed

34.

Park YR, Park HB, Kim MJ, Jung BD, Lee S, Park CK, et al. Effects of endoplasmic reticulum stress inhibitor treatment during the micromanipulation of somatic cell nuclear transfer in porcine oocytes. Dev Reprod. 2019;23:43–54.PubMedPubMedCentral

35.

Sano R, Reed JC. ER stress-induced cell death mechanisms. Biochim Biophys Acta. 2013;1833:3460–70.PubMed

36.

Lin T, Diao YF, Kang JW, Lee JE, Kim DK, Jin DI. Tauroursodeoxycholic acid improves the implantation and live-birth rates of mouse embryos. Reprod Biol. 2015;15:101–5.PubMed

37.

Mochizuki M, Miyagi K, Kishigami S. Optimizing treatment of tauroursodeoxycholic acid to improve embryonic development after in vitro maturation of cumulus-free oocytes in mice. PLoS One. 2018;13:e0202962.PubMedPubMedCentral

38.

Zhao N, Liu XJ, Li JT, Zhang L, Fu Y, Zhang YJ, et al. Endoplasmic reticulum stress inhibition is a valid therapeutic strategy in vitrifying oocytes. Cryobiology. 2015;70:48–52.PubMed

39.

Dicks N, Bohrer RC, Gutierrez K, Michalak M, Agellon LB, Bordignon V. Relief of endoplasmic reticulum stress enhances DNA damage repair and improves development of pre-implantation embryos. PLoS One. 2017;12:e0187717.PubMedPubMedCentral

40.

Li XX, Diao YF, Wei HJ, Wang SY, Cao XY, Zhang YF, et al. Tauroursodeoxycholic acid enhances the development of porcine embryos derived from in vitro-matured oocytes and evaporatively dried spermatozoa. Sci Rep. 2017;7:6773.PubMedPubMedCentral

41.

Wydooghe E, Vandaele L, Beek J, Favoreel H, Heindryckx B, De Sutter P, et al. Differential apoptotic staining of mammalian blastocysts based on double immunofluorescent CDX2 and active caspase-3 staining. Anal Biochem. 2011;416:228–30.PubMed

42.

Ilina IV, Khramova YV, Filatov MA, Sitnikov DS. Femtosecond laser is effective tool for zona pellucida engraving and tagging of preimplantation mammalian embryos. J Assist Reprod Genet. 2019;36:1251–61.PubMed

Titel: Tauroursodeoxycholic acid (TUDCA) enhanced intracytoplasmic sperm injection (ICSI) embryo developmental competence by ameliorating endoplasmic reticulum (ER) stress and inhibiting apoptosis
verfasst von: Tengfei Deng
Juanke Xie
Hengtao Ge
Qi Liu
Xiaobing Song
Lin Hu
Li Meng
Cuilian Zhang
Publikationsdatum: 04.12.2019
Verlag: Springer US
Erschienen in: Journal of Assisted Reproduction and Genetics / Ausgabe 1/2020
Print ISSN: 1058-0468
Elektronische ISSN: 1573-7330
DOI: https://doi.org/10.1007/s10815-019-01627-2

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Tauroursodeoxycholic acid (TUDCA) enhanced intracytoplasmic sperm injection (ICSI) embryo developmental competence by ameliorating endoplasmic reticulum (ER) stress and inhibiting apoptosis