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http://dx.doi.org/10.12717/DR.2017.21.4.407

Regulation of the Endoplasmic Reticulum Stress by BIP/GRP78 is involved in Meiotic Maturation of Porcine Oocytes In Vitro  

Park, Hyo-Jin (Dept. of Biotechnology, College of Engineering, Daegu University)
Park, Jae-Young (Dept. of Biotechnology, College of Engineering, Daegu University)
Kim, Jin-Woo (Dept. of Biotechnology, College of Engineering, Daegu University)
Yang, Seul-Gi (Dept. of Biotechnology, College of Engineering, Daegu University)
Jung, Jae-Min (Dept. of Biotechnology, College of Engineering, Daegu University)
Kim, Min-Ji (Dept. of Biotechnology, College of Engineering, Daegu University)
Park, Joung Jun (Animal Reproduction & Biotechnology Center, Myung-Poom Hanwoo Consulting)
Koo, Deog-Bon (Dept. of Biotechnology, College of Engineering, Daegu University)
Publication Information
Development and Reproduction / v.21, no.4, 2017 , pp. 407-415 More about this Journal
Abstract
In the present study, we investigated the role of binding immunoglobulin protein/glucose-regulated protein, 78-kDa (BIP/GRP78)-regulated endoplasmic reticulum (ER)-stress on meiotic maturation and cumulus cells expansion in porcine cumulus-oocyte complexes (COCs). Previously, it has been demonstrated that unfolded protein response (UPR)-related genes, such as molecules involved in ER-stress defense mechanisms, were expressed in matured oocytes and cumulus cells during in vitro maturation (IVM) of porcine oocytes. However, BIP/GRP78-mediated regulation of ER stress in porcine oocytes has not been reported. Firstly, we observed the effects of knockdown of BIP/GRP78 (an UPR initiation marker) using porcine-specific siRNAs (#909, #693, and #1570) on oocyte maturation. Among all siRNAs, siRNA #693 significantly reduced the protein levels of UPR marker proteins (BIP/GRP78, ATF4, and P90ATF6) in porcine COCs observed by Western blotting and immunofluorescence analysis. We also observed that the reduction of BIP/GRP78 levels by siRNA#693 significantly inhibited the meiotic maturation of oocytes (siRNA #693: $32.5{\pm}10.1%$ vs control: $77.8{\pm}5.3%$). In addition, we also checked the effect of ER-stress inhibitors, tauroursodeoxycholic acid (TUDCA, $200{\mu}M$) and melatonin ($0.1{\mu}M$), in BIP/GRP78-knockdown oocytes. TUDCA and melatonin treatment could restore the expression levels of ER-stress marker proteins (BIP/GRP78, $p-eIF2{\alpha}$, $eIF2{\alpha}$, ATF4, and P90ATF6) in siRNA #693-transfected matured COCs. In conclusion, these results demonstrated that BIP/GRP78-mediated regulation of UPR signaling and ER stress plays an important role in in vitro maturation of porcine oocytes.
Keywords
ER stress; BIP/GRP78; UPR; In vitro maturation; Porcine oocyte;
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1 Zhang JY, Diao YF, Kim HR, Jin DI (2012b) Inhibition of endoplasmic reticulum stress improves mouse embryo development. PloS one 7:e40433.   DOI
2 Zhang JY, Diao YF, Oqani RK, Han RX, Jin DI (2012a) Effect of endoplasmic reticulum stress on porcine oocyte maturation and parthenogenetic embryonic development in vitro. Biol Reprod 86:128.
3 Zhu J, Chen M, Chen N, Ma A, Zhu C, Zhao R, Jiang M, Zhou J, Ye L, Fu H, Zhang X (2015) Glycyrrhetinic acid induces G1 phase cell cycle arrest in human non-small cell lung cancer cells through endoplasmic reticulum stress pathway. Int J Oncol 46:981-988.   DOI
4 Yang Y, Lin P, Chen F, Wang A, Lan X, Song Y, Jin Y (2013) Luman recruiting factor regulates endoplasmic reticulum stress in mouse ovarian granulosa cell apoptosis. Theriogenology 79:633-639 e631-633.   DOI
5 Kim JW, Park HJ, Chae SK, Ahn JH, DO GY, Choo YK, Park JJ, Jung BD, Kim SU, Chang KT, Koo DB (2016) Ganglioside GD1a promotes oocyte maturation, furthers preimplantation development, and increases blastocyst quality in pigs. J Reprod Dev 62:249-255.   DOI
6 Agarwal A, Gupta S, Sharma RK (2005) Role of oxidative stress in female reproduction. Reprod Biol Endocrinol : RB&E 3:28.   DOI
7 Audouard C, Le Masson F, Charry C, Li Z, Christians ES (2011) Oocyte-targeted deletion reveals that hsp90b1 is needed for the completion of first mitosis in mouse zygotes. PloS one 6:e17109.   DOI
8 Carloni S, Albertini MC, Galluzzi L, Buonocore G, Proietti F, Balduini W (2014) Melatonin reduces endoplasmic reticulum stress and preserves sirtuin 1 expression in neuronal cells of newborn rats after hypoxia-ischemia. J Pineal Res 57:192-199.   DOI
9 Ellederova Z, Halada P, Man P, Kubelka M, Motlik J, Kovarova H (2004) Protein patterns of pig oocytes during in vitro maturation. Biol Reprod 71:1533-1539.   DOI
10 Farinola MA, Gown AM, Judson K, Ronnett BM, Barry TS, Movahedi-Lankarani S, Vang R (2007) Estrogen receptor alpha and progesterone receptor expression in ovarian adult granulosa cell tumors and Sertoli-Leydig cell tumors. Int J Gynecol Pathol 26:375-382.   DOI
11 Lin P, Yang Y, Li X, Chen F, Cui C, Hu L, Li Q, Liu W, Jin Y (2012) Endoplasmic reticulum stress is involved in granulosa cell apoptosis during follicular atresia in goat ovaries. Mol Reprod Dev 79:423-432.   DOI
12 Luo S, Mao C, Lee B, Lee AS (2006) GRP78/BiP is required for cell proliferation and protecting the inner cell mass from apoptosis during early mouse embryonic development. Mol Cell Biol 26:5688-5697.   DOI
13 Teske BF, Wek SA, Bunpo P, Cundiff JK, McClintick JN, Anthony TG, Wek RC (2011b) The eIF2 kinase PERK and the integrated stress response facilitate activation of ATF6 during endoplasmic reticulum stress. Mol Biol Cell 22:4390-4405.   DOI
14 Mukherjee A, Soto C (2011) Role of calcineurin in neurodegeneration produced by misfolded proteins and endoplasmic reticulum stress. Curr Opin Cell Biol 23:223-230.   DOI
15 Ozcan U, Yilmaz E, Ozcan L, Furuhashi M, Vaillancourt E, Smith RO, Gorgun CZ, Hotamisligil GS (2006) Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313:1137-1140.   DOI
16 Poston L, Igosheva N, Mistry HD, Seed PT, Shennan AH, Rana S, Karumanchi SA, Chappell LC (2011) Role of oxidative stress and antioxidant supplementation in pregnancy disorders. Am J Clin Nutr 94:1980S-1985S.   DOI
17 Raab MS, Breitkreutz I, Tonon G, Zhang J, Hayden PJ, Nguyen T, Fruehauf JH, Lin BK, Chauhan D, Hideshima T, Munshi NC, Anderson KC, Podar K (2009) Targeting PKC: a novel role for beta-catenin in ER stress and apoptotic signaling. Blood 113:1513-1521.
18 Teske BF, Baird TD, Wek RC (2011a) Methods for analyzing eIF2 kinases and translational control in the unfolded protein response. Methods in Enzymology 490:333-356.
19 Wang M, Wey S, Zhang Y, Ye R, Lee AS (2009) Role of the unfolded protein response regulator GRP78/BiP in development, cancer, and neurological disorders. Antioxid Redox Signal 11:2307-2316.   DOI
20 Wu J, Kaufman RJ (2006) From acute ER stress to physiological roles of the unfolded protein response. Cell Death Differ 13:374-384.   DOI
21 Wu LL, Russell DL, Norman RJ, Robker RL (2012) Endoplasmic reticulum (ER) stress in cumulus-oocyte complexes impairs pentraxin-3 secretion, mitochondrial membrane potential (DeltaPsi m), and embryo development. Mol Endocrinol 26:562-573.   DOI
22 Namba T, Kodama R (2015) Avarol induces apoptosis in pancreatic ductal adenocarcinoma cells by activating PERK-eIF2alpha-CHOP signaling. Mar Drugs 13:2376-2389.   DOI