Skip to main content

Advertisement

SpringerLink
Log in

The roles of endoplasmic reticulum stress response in female mammalian reproduction

  • Review
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Endoplasmic reticulum stress (ERS) activates a protective pathway, called the unfold protein response, for maintaining cellular homeostasis, but cellular apoptosis is triggered by excessive or persistent ERS. Several recent studies imply that the ERS response might have broader physiological roles in the various reproductive processes of female mammals, including embryo implantation, decidualization, preimplantation embryonic development, follicle atresia, and the development of the placenta. This review summarizes the existing data concerning the molecular and biological roles of the ERS response. The study of the functions of the ERS response in mammalian reproduction might provide novel insights into and an understanding of reproductive cell survival and apoptosis under physiological and pathological conditions. The ERS response is a novel signaling pathway for reproductive cell survival and apoptosis. Infertility might be a result of disturbing the ERS response during the process of female reproduction.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Abbreviations

ERS:

Endoplasmic reticulum stress

UPR:

Unfolded protein response

Grp78/Bip:

Glucose-regulated protein 78-kDa/immunoglobulin heavy chain binding protein in pre-B cells

ATF6α:

Activating transcription factor 6α

IRE1α:

Inositol requiring enzyme 1α

PERK:

Pancreatic ER kinase

CHOP:

C/EBP-homologous protein growth arrest and DNA damage-inducible gene 153 GADD153; DNA-damage inducible transcription 3 DDIT3

JNK:

c-Jun N-terminal kinase

eIF2α:

Eukaryotic initiation factor 2α

Xbp1(U):

Unspliced X-box binding protein

Xbp1(S):

Spliced X-box binding protein

References

  • Abraham T, Pin CL, Watson AJ (2012) Embryo collection induces transient activation of XBP1 arm of the ER stress response while embryo vitrification does not. Mol Hum Reprod 18:229–242

    Article  CAS  PubMed  Google Scholar 

  • Banerjee A, Padh H, Nivsarkar M (2009) Role of the calcium channel in blastocyst implantation: a novel contraceptive target. J Basic Clin Physiol Pharmacol 20:43–53

    Article  CAS  PubMed  Google Scholar 

  • Banerjee A, Padh H, Nivsarkar M (2011) Hormonal crosstalk with calcium channel blocker during implantation. Syst Biol Reprod Med 57:186–189

    Article  CAS  PubMed  Google Scholar 

  • Basar M, Bozkurt I, Guzeloglu-Kayisli O, Sozen B, Tekmen I, Schatz F, Arici A, Lockwood CJ, Kayisli UA (2014) Unfolded protein response prevents blastocyst formation during preimplantation embryo development in vitro. Fertil Steril 102:1777–1784

    Article  CAS  PubMed  Google Scholar 

  • Bernales S, McDonald KL, Walter P (2006) Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol 4:e423

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Bowen JM, Keyes PL, Warren JS, Townson DH (1996) Prolactin-induced regression of the rat corpus luteum: expression of monocyte chemoattractant protein-1 and invasion of macrophages. Biol Reprod 54:1120–1127

    Article  CAS  PubMed  Google Scholar 

  • Bowen-Shauver JM, Gibori G (2004) The corpus luteum of pregnancy. In: Leung PCK, Adashi EY (eds) The ovary. Elseiver/Academic Press, San Diego, pp 201–230

    Google Scholar 

  • Burton G, Yung HW, Cindrova-Davies T, Charnock-Jones D (2009) Placental endoplasmic reticulum stress and oxidative stress in the pathophysiology of unexplained intrauterine growth restriction and early onset preeclampsia. Placenta 30:43–48

    Article  PubMed Central  CAS  Google Scholar 

  • Carambula SF, Pru JK, Lynch MP, Matikainen T, Gonçalves PB, Flavell RA, Tilly JL, Rueda BR (2003) Prostaglandin F2alpha- and FAS-activating antibody induced regression of the corpus luteum involves caspase-8 and is defective in caspase-3 deficient mice. Reprod Biol Endocrinol 1:15

    Article  PubMed Central  PubMed  Google Scholar 

  • Choi JY, Jo MW, Lee EY, Yoon BK, Choi DS (2010) The role of autophagy in follicular development and atresia in rat granulosa cells. Fertil Steril 93:2532–2537

    Article  PubMed  Google Scholar 

  • Choi JY, Jo MW, Lee EY, Choi DS (2011) The role of autophagy in corpus luteum regression in the rat. Biol Reprod 85:465–472

    Article  CAS  PubMed  Google Scholar 

  • Choi JY, Jo MW, Lee EY, Choi DS (2013) AKT is involved in granulosa cell autophagy regulation via mTOR signaling during rat follicular development and atresia. Reproduction 147:73–80

    Article  PubMed  CAS  Google Scholar 

  • Choi KC, An BS, Yang H, Jeung EB (2011) Regulation and molecular mechanisms of calcium transport genes: do they play a role in calcium transport in the uterine endometrium? J Physiol Pharmacol 62:499–504

    CAS  PubMed  Google Scholar 

  • Dai R, Li J, Fu J, Chen Y, Yu L, Zhao X, Qian Y, Zhang H, Chen H, Ren Y, Su B, Luo T, Zhu J, Wang H (2012) Disturbance of Ca2+ homeostasis converts pro-Met into non-canonical tyrosine kinase p190MetNC in response to endoplasmic reticulum stress in MHCC97 cells. J Biol Chem 287:14586–14597

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dauffenbach LM, Khan SM, Yeh J (2003) Corpus luteum regression in the rat in vivo and in vitro studies of apoptotic mechanisms. J Med 34:87–100

    CAS  PubMed  Google Scholar 

  • Dey S, Lim H, Das SK, Reese J, Paria B, Daikoku T, Wang H (2004) Molecular cues to implantation. Endocr Rev 25:341–373

    Article  CAS  PubMed  Google Scholar 

  • Ellgaard L, Helenius A (2003) Quality control in the endoplasmic reticulum. Nat Rev Mol Cell Biol 4:181–191

    Article  CAS  PubMed  Google Scholar 

  • Fleming J, Fontanier N, Harries D, Rees W (1997) The growth arrest genes gas5, gas6, and CHOP-10 (gadd153) are expressed in the mouse preimplantation embryo. Mol Reprod Dev 48:310–316

    Article  CAS  PubMed  Google Scholar 

  • Fontanier-Razzaq N, McEvoy TG, Robinson JJ, Rees WD (2001) DNA damaging agents increase gadd153 (CHOP-10) messenger RNA levels in bovine preimplantation embryos cultured in vitro. Biol Reprod 64:1386–1391

    Article  CAS  PubMed  Google Scholar 

  • Fujita E, Kouroku Y, Isoai A, Kumagai H, Misutani A, Matsuda C, Hayashi YK, Momoi T (2007) Two endoplasmic reticulum-associated degradation (ERAD) systems for the novel variant of the mutant dysferlin: ubiquitin/proteasome ERAD(I) and autophagy/lysosome ERAD(II). Hum Mol Genet 16:618–629

    Article  CAS  PubMed  Google Scholar 

  • Fung TS, Liu DX (2014) Coronavirus infection, ER stress, apoptosis and innate immunity. Front Microbiol 5:296

    Article  PubMed Central  PubMed  Google Scholar 

  • Gao HJ, Zhu YM, He WH, Liu AX, Dong MY, Jin M, Sheng JZ, Huang HF (2012) Endoplasmic reticulum stress induced by oxidative stress in decidual cells: a possible mechanism of early pregnancy loss. Mol Biol Rep 39:9179–9186

    Article  CAS  PubMed  Google Scholar 

  • Gaytán F, Morales C, Bellido C, Aguilar R, Millán Y, Martín De Las Mulas J, Sánchez-Criado JE (2000) Progesterone on an oestrogen background enhances prolactin-induced apoptosis in regressing corpora lutea in the cyclic rat: possible involvement of luteal endothelial cell progesterone receptors. J Endocrinol 165:715–724

    Article  PubMed  Google Scholar 

  • Hao L, Vassena R, Wu G, Han Z, Cheng Y, Latham KE, Sapienza C (2009) The unfolded protein response contributes to preimplantation mouse embryo death in the DDK syndrome. Biol Reprod 80:944–953

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hasnain SZ, Lourie R, Das I, Chen AC, McGuckin MA (2012) The interplay between endoplasmic reticulum stress and inflammation. Immunol Cell Biol 90:260–270

    Article  CAS  PubMed  Google Scholar 

  • Hayashi K, Erikson DW, Tilford SA, Bany BM, Maclean JA, Rucker EB, Johnson GA, Spencer TE (2009) Wnt genes in the mouse uterus: potential regulation of implantation. Biol Reprod 80:989–1000

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hetz C, Thielen P, Matus S, Nassif M, Court F, Kiffin R, Martinez G, Cuervo AM, Brown RH, Glimcher LH (2009) XBP-1 deficiency in the nervous system protects against amyotrophic lateral sclerosis by increasing autophagy. Genes Dev 23:2294–2306

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hitomi J, Katayama T, Eguchi Y, Kudo T, Taniguchi M, Koyama Y, Manabe T, Yamagishi S, Bando Y, Imaizumi K, Tsujimoto Y, Tohyama M (2004) Involvement of caspase-4 in endoplasmic reticulum stress-induced apoptosis and Abeta-induced cell death. J Cell Biol 165:347–356

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hong D, Bai YP, Gao HC, Wang X, Li LF, Zhang GG, Hu CP (2014) Ox-LDL induces endothelial cell apoptosis via the LOX-1-dependent endoplasmic reticulum stress pathway. Atherosclerosis 235:310–317

    Article  CAS  PubMed  Google Scholar 

  • Huet-Hudson YM, Andrews GK, Dey SK (1989) Cell type-specific localization of c-myc protein in the mouse uterus: modulation by steroid hormones and analysis of the perimplantation period. Endocrinology 125:1683–1690

    Article  CAS  PubMed  Google Scholar 

  • Hughes FM, Gorospe WC (1991) Biochemical identification of apoptosis (programmed cell death) in granulosa cells: evidence for a potential mechanism underlying follicular atresia. Endocrinology 129:2415–2422

    Article  CAS  PubMed  Google Scholar 

  • Iwawaki T, Akai R, Yamanaka S, Kohno K (2009) Function of IRE1 alpha in the placenta is essential for placental development and embryonic viability. Proc Natl Acad Sci U S A 106:16657–16662

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jheng JR, Ho JY, Horng JT (2014) ER stress, autophagy, and RNA viruses. Front Microbiol 5:388

    Article  PubMed Central  PubMed  Google Scholar 

  • Jiang JY, Cheung C, Wang Y, Tsang BK (2003) Regulation of cell death and cell survival gene expression during ovarian follicular development and atresia. Front Biosci 8:222–237

    Article  Google Scholar 

  • Jolly P, Tisdall D, Heath D, Lun S, McNatty K (1994) Apoptosis in bovine granulosa cells in relation to steroid synthesis, cyclic adenosine 3’,5’-monophosphate response to follicle-stimulating hormone and luteinizing hormone, and follicular atresia. Biol Reprod 51:934–944

    Article  CAS  PubMed  Google Scholar 

  • Juengel JL, Garverick HA, Johnson AL, Youngquist RS, Smith MF (1993) Apoptosis during luteal regression in cattle. Endocrinology 132:249–254

    CAS  PubMed  Google Scholar 

  • Jung E, An B, Choi K, Jeung E (2012) Apoptosis- and endoplasmic reticulum stress-related genes were regulated by estrogen and progesterone in the uteri of calbindin-D(9k) and -D(28k) knockout mice. J Cell Biochem 113:194–203

    Article  CAS  PubMed  Google Scholar 

  • Kaufman RJ (1999) Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev 13:1211–1233

    Article  CAS  PubMed  Google Scholar 

  • Kaufman RJ (2002) Orchestrating the unfolded protein response in health and disease. J Clin Invest 110:1389–1398

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kawakami T, Yoshimi M, Kadota Y, Inoue M, Sato M, Suzuki S (2014) Prolonged endoplasmic reticulum stress alters placental morphology and causes low birth weight. Toxicol Appl Pharmacol 275:134–144

    Article  CAS  PubMed  Google Scholar 

  • Kim JS, Song BS, Lee KS, Kim DH, Kim SU, Choo YK, Chang KT, Koo DB (2012) Tauroursodeoxycholic acid enhances the pre-implantation embryo development by reducing apoptosis in pigs. Reprod Domest Anim 47:791–798

    Article  CAS  PubMed  Google Scholar 

  • Kim SK, Kim YK, Lee AS (1990) Expression of the glucoseregulated proteins (GRP94 and GRP78) in differentiated and undifferentiated mouse embryonic cells and the use of the GRP78 promoter as an expression system in embryonic cells. Differentiation 42:153–159

    Article  CAS  PubMed  Google Scholar 

  • Kimber SJ, Spanswick C (2000) Blastocyst implantation: the adhesion cascade. Semin Cell Dev Biol 11:77–92

    Article  CAS  PubMed  Google Scholar 

  • Kogure K, Nakamura K, Ikeda S, Kitahara Y, Nishimura T, Iwamune M, Minegishi T (2013) Glucose-regulated protein, 78-kilodalton is a modulator of luteinizing hormone receptor expression in luteinizing granulosa cells in rats. Biol Reprod 88:8

    Article  PubMed  CAS  Google Scholar 

  • Koumenis C (2006) ER stress, hypoxia tolerance and tumor progression. Curr Mol Med 6:55–69

    Article  CAS  PubMed  Google Scholar 

  • Lan X, Jin Y, Yang Y, Lin P, Hu L, Cui C, Li Q, Li X, Wang A (2013) Expression and localization of Luman RNA and protein during mouse implantation and decidualization. Theriogenology 80:138–144

    Article  CAS  PubMed  Google Scholar 

  • Lee KY, DeMayo FJ (2004) Animal models of implantation. Reproduction 128:679–695

    Article  CAS  PubMed  Google Scholar 

  • Lemus L, Goder V (2014) Regulation of endoplasmic reticulum-associated protein degradation (ERAD) by ubiquitin. Cells 3:824–847

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Li B, Yi P, Zhang B, Xu C, Liu Q, Pi Z, Xu X, Chevet E, Liu J (2011) Differences in endoplasmic reticulum stress signalling kinetics determine cell survival outcome through activation of MKP-1. Cell Signal 23:35–45

    Article  PubMed  CAS  Google Scholar 

  • Li C, Wei J, Li Y, He X, Zhou Q, Yan J, Zhang J, Liu Y, Liu Y, Shu HB (2013) Transmembrane protein 214 (TMEM214) mediates endoplasmic reticulum stress-induced caspase 4 enzyme activation and apoptosis. J Biol Chem 288:17908–17917

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lian IA, Løset M, Mundal SB, Fenstad MH, Johnson MP, Eide IP, Bjørge L, Freed KA, Moses EK, Austgulen R (2011) Increased endoplasmic reticulum stress in decidual tissue from pregnancies complicated by fetal growth restriction with and without pre-eclampsia. Placenta 32:823–829

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lim H, Song H, Paria B, Reese J, Das SK, Dey S (2002) Molecules in blastocyst implantation: uterine and embryonic perspectives. Vitam Horm 64:43–76

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Lin P, Chen F, Wang N, Wang X, Li X, Zhou J, Jin Y, Wang A (2013) CREBZF expression and hormonal regulation in the mouse uterus. Reprod Biol Endocrinol 11:110

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lin P, Jin Y, Lan X, Yang Y, Chen F, Wang N, Li X, Sun Y, Wang A (2014) GRP78 expression and regulation in the mouse uterus during embryo implantation. J Mol Histol 45:259–268

    Article  CAS  PubMed  Google Scholar 

  • Lipson KL, Fonseca SG, Urano F (2006) Endoplasmic reticulum stress-induced apoptosis and autoimmunity in diabetes. Curr Mol Med 6:71–77

    Article  CAS  PubMed  Google Scholar 

  • Liu AX, He WH, Yin LJ, Lv PP, Zhang Y, Sheng JZ, Leung PC, Huang HF (2011) Sustained endoplasmic reticulum stress as a cofactor of oxidative stress in decidual cells from patients with early pregnancy loss. J Clin Endocrinol Metab 96:E493–E497

    Article  CAS  PubMed  Google Scholar 

  • Liu XM, Ding GL, Jiang Y, Pan HJ, Zhang D, Wang TT, Zhang RJ, Shu J, Sheng JZ, Huang HF (2012) Down-regulation of S100A11, a calcium-binding protein, in human endometrium may cause reproductive failure. J Clin Endocrinol Metab 97:3672–3683

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liu Z, Yue K, Ma S, Sun X, Tan J (2003) Effects of pregnant mare serum gonadotropin (eCG) on follicle development and granulosa-cell apoptosis in the pig. Theriogenology 59:775–785

    Article  CAS  PubMed  Google Scholar 

  • Løset M, Mundal SB, Johnson MP, Fenstad MH, Freed KA, Lian IA, Eide IP, Bjørge L, Blangero J, Moses EK, Austgulen R (2011) A transcriptional profile of the decidua in preeclampsia. Am J Obstet Gynecol 204:84.e1-27

    PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Malhotra JD, Kaufman RJ (2007) The endoplasmic reticulum and the unfolded protein response. Semin Cell Dev Biol 18:716–731

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Manabe N, Goto Y, Matsuda-Minehata F, Inoue N, Maeda A, Sakamaki K, Miyano T (2004) Regulation mechanism of selective atresia in porcine follicles: regulation of granulosa cell apoptosis during atresia. J Reprod Dev 50:493

    Article  PubMed  Google Scholar 

  • Matsuda-Minehata F, Inoue N, Goto Y, Manabe N (2006) The regulation of ovarian granulosa cell death by pro- and anti-apoptotic molecules. J Reprod Dev 52:695–670

    Article  CAS  PubMed  Google Scholar 

  • Mei Y, Thompson MD, Cohen RA, Tong X (2013) Endoplasmic reticulum stress and related pathological processes. J Pharmacol Biomed Anal 1:1000107

    PubMed Central  PubMed  Google Scholar 

  • Moenner M, Pluquet O, Bouchecareilh M, Chevet E (2007) Integrated endoplasmic reticulum stress responses in cancer. Cancer Res 67:10631–10634

    Article  CAS  PubMed  Google Scholar 

  • Murdoch WJ (1995) Programmed cell death in preovulatory ovine follicles. Biol Reprod 53:8–12

    Article  CAS  PubMed  Google Scholar 

  • Nakatsukasa K, Kamura T, Brodsky JL (2014) Recent technical developments in the study of ER-associated degradation. Curr Opin Cell Biol 29:82–91

    Article  CAS  PubMed  Google Scholar 

  • Ogata M, Hino S, Saito A, Morikawa K, Kondo S, Kanemoto S, Murakami T, Taniguchi M, Tanii I, Yoshinaga K, Shiosaka S, Hammarback JA, Urano F, Imaizumi K (2006) Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol 26:9220–9231

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Oh J, Riek AE, Weng S, Petty M, Kim D, Colonna M, Cella M, Bernal-Mizrachi C (2012) Endoplasmic reticulum stress controls M2 macrophage differentiation and foam cell formation. J Biol Chem 287:11629–11641

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Park HJ, Park SJ, Koo DB, Kong IK, Kim MK, Kim JM, Choi MS, Park YH, Kim SU, Chang KT, Park CK, Chae JI, Lee DS (2013) Unfolding protein response signaling is involved in development, maintenance, and regression of the corpus luteum during the bovine estrous cycle. Biochem Biophys Res Commun 441:344–350

    Article  CAS  PubMed  Google Scholar 

  • Park HJ, Park SJ, Koo DB, Lee SR, Kong IK, Ryoo JW, Park YI, Chang KT, Lee DS (2014) Progesterone production is affected by unfolded protein response (UPR) signaling during the luteal phase in mice. Life Sci 113:60–67

    Article  CAS  PubMed  Google Scholar 

  • Park SW, Zhou Y, Lee J, Lee J, Ozcan U (2010) Sarco(endo)plasmic reticulum Ca2+−ATPase 2b is a major regulator of endoplasmic reticulum stress and glucose homeostasis in obesity. Proc Natl Acad Sci U S A 107:19320–19325

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Quirk SM, Harman RM, Huber SC, Cowan RG (2000) Responsiveness of mouse corpora luteal cells to Fas antigen (CD95)-mediated apoptosis. Biol Reprod 63:49–56

    Article  CAS  PubMed  Google Scholar 

  • Rajakoski E (1960) The ovarian follicular system in sexually mature heifers with special reference to seasonal, cyclical, and left-right variations. Acta Endocrinol Suppl (Copenh) 15:836–838

    Google Scholar 

  • Reid RJ, Heald PJ (1970) Uptake of (3H) leucine into proteins of rat uterus during early pregnancy. Biochim Biophys Acta 204:278–279

    Article  CAS  PubMed  Google Scholar 

  • Rueda BR, Wegner JA, Marion SL, Wahlen DD, Hoyer PB (1995) Internucleosomal DNA fragmentation in ovine luteal tissue associated with luteolysis: in vivo and in vitro analyses. Biol Reprod 52:305–312

    Article  CAS  PubMed  Google Scholar 

  • Rueda BR, Tilly KI, Botros IW, Jolly PD, Hansen TR, Hoyer PB, Tilly JL (1997) Increased bax and interleukin-1beta-converting enzyme messenger ribonucleic acid levels coincide with apoptosis in the bovine corpus luteum during structural regression. Biol Reprod 56:186–193

    Article  CAS  PubMed  Google Scholar 

  • Salminen A, Kauppinen A, Suuronen T, Kaarniranta K, Ojala J (2009) ER stress in Alzheimer’s disease: a novel neuronal trigger for inflammation and Alzheimer’s pathology. J Neuroinflammation 6:41

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Samali A, FitzGerald U, Deegan S, Gupta S (2010) Methods for monitoring endoplasmic reticulum stress and the unfolded protein response. Int J Cell Biol 2010:8303074

    Google Scholar 

  • Sheveleva EV, Landowski TH, Samulitis BK, Bartholomeusz G, Powis G, Dorr RT (2012) Imexon induces an oxidative endoplasmic reticulum stress response in pancreatic cancer cells. Mol Cancer Res 210:392–400

    Article  CAS  Google Scholar 

  • Shikone T, Yamoto M, Kokawa K, Yamashita K, Nishimori K, Nakano R (1996) Apoptosis of human corpora lutea during cyclic luteal regression and early pregnancy. J Clin Endocrinol Metab 81:2376–2380

    CAS  PubMed  Google Scholar 

  • Shimada Y, Kobayashi H, Kawagoe S, Aoki K, Kaneshiro E, Shimizu H, Eto Y, Ida H, Ohashi T (2011) Endoplasmic reticulum stress induces autophagy through activation of p38 MAPK in fibroblasts from Pompe disease patients carrying c. 546G > T mutation. Mol Genet Metab 104:566–573

    Article  CAS  PubMed  Google Scholar 

  • Siman R, Flood DG, Thinakaran G, Neumar RW (2001) Endoplasmic reticulum stress induced cysteine protease activation in cortical neurons: effect of an Alzheimer’s disease-linked presenilin-1 knock-in mutation. J Biol Chem 276:44736–44743

    Article  CAS  PubMed  Google Scholar 

  • Simmons D, Kennedy T (2000) Induction of glucose-regulated protein 78 in rat uterine glandular epithelium during uterine sensitization for the decidual cell reaction. Biol Reprod 62:1168–1176

    Article  CAS  PubMed  Google Scholar 

  • Simon-Szabó L, Kokas M, Mandl J, Kéri G, Csala M (2014) Metformin attenuates palmitate-induced endoplasmic reticulum stress, serine phosphorylation of IRS-1 and apoptosis in rat insulinoma cells. PLoS One 9:e9786816

    Article  CAS  Google Scholar 

  • Stocco C, Telleria C, Gibori G (2007) The molecular control of corpus luteum formation, function, and regression. Endocr Rev 28:117–149

    Article  CAS  PubMed  Google Scholar 

  • Stouffer RL (2004) The function and regulation of cell populations comprising the corpus luteum during the ovarian cycle. In: Leung PCK, Adashi EY (eds) The ovary. Elseiver/Academic Press, San Diego, pp 169–184

    Google Scholar 

  • Sugimoto M, Manabe N, Kimura Y, Myoumot A, Imai Y, Ohno H, Miyamoto H (1998) Ultrastructural changes in granulosa cells in porcine antral follicles undergoing atresia indicate apoptotic cell death. J Reprod Dev 144:7–14

    Article  Google Scholar 

  • Szegezdi E, Logue SE, Gorman AM, Samali A (2006) Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep 7:880–885

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Telleria CM, Goyeneche AA, Cavicchia JC, Stati AO, Deis RP (2001) Apoptosis induced by antigestagen RU486 in rat corpus luteum of pregnancy. Endocrine 15:147–155

    Article  CAS  PubMed  Google Scholar 

  • Terada N, Yamamoto R, Takada T, Miyake T, Terakawa N, Wakimoto H, Taniguchi H, Li W, Kitamura Y, Matsumoto K (1989) Inhibitory effect of progesterone on cell death of mouse uterine epithelium. J Steroid Biochem 33:1091–1096

    Article  CAS  PubMed  Google Scholar 

  • Tersey SA, Nishiki Y, Templin AT, Cabrera SM, Stull ND, Colvin SC (2012) Islet β-cell endoplasmic reticulum stress precedes the onset of type 1 diabetes in the nonobese diabetic mouse model. Diabetes 61:818–827

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tirasophon W, Welihinda AA, Kaufman RJ (1998) A stress response pathway from the endoplasmic reticulum to the nucleus requires a novel bifunctional protein kinase/endoribonuclease (Ire1p) in mammalian cells. Genes Dev 12:1812–1824

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Todd DJ, Lee A-H, Glimcher LH (2008) The endoplasmic reticulum stress response in immunity and autoimmunity. Nat Rev Immunol 8:663–674

    Article  CAS  PubMed  Google Scholar 

  • Tomita T (1960) One-side cross sterility between inbred strains of mice. Jpn J Genet 35:291

    Google Scholar 

  • Tong XM, Lin XN, Song T, Liu L, Zhang SY (2010) Calcium-binding protein S100P is highly expressed during the implantation window in human endometrium. Fertil Steril 94:1510–1518

    Article  CAS  PubMed  Google Scholar 

  • Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, Harding HP, Ron D (2000) Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287:664

    Article  CAS  PubMed  Google Scholar 

  • Wakasugi N (1973) Studies on fertility of DDK mice: reciprocal crosses between DDK and C57BL/6J strains and experimental transplantation of the ovary. J Reprod Fertil 33:283–291

    Article  CAS  PubMed  Google Scholar 

  • Wakasugi N (1974) A genetically determined incompatibility system between spermatozoa and eggs leading to embryonic death in mice. J Reprod Fertil 41:85–96

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Dey SK (2006) Roadmap to embryo implantation: clues from mouse models. Nat Rev Genet 7:185–199

    Article  PubMed  CAS  Google Scholar 

  • Wang Z, Wang H, Xu ZM, Ji YL, Chen YH, Zhang ZH, Zhang C, Meng XH, Zhao M, Xu DX (2012) Cadmium-induced teratogenicity: association with ROS-mediated endoplasmic reticulum stress in placenta. Toxicol Appl Pharmacol 259:236–247

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Jiang C, Chen W, Zhang G, Luo D, Cao Y, Wu J, Ding Y, Liu B (2014) Baicalein induces apoptosis and autophagy via endoplasmic reticulum stress in hepatocellular carcinoma cells. Biomed Res Int 2014:732516

    PubMed Central  PubMed  Google Scholar 

  • Watson ED, Cross JC (2005) Development of structures and transport functions in the mouse placenta. Physiology (Bethesda) 20:180–193

    Article  CAS  Google Scholar 

  • Wu LL, Dunning KR, Yang X, Russell DL, Lane M, Norman RJ, Robker RL (2010) High-fat diet causes lipotoxicity responses in cumulus-oocyte complexes and decreased fertilization rates. Endocrinology 151:5438–5445

    Article  CAS  PubMed  Google Scholar 

  • Xu C, Bailly-Maitre B, Reed JC (2005) Endoplasmic reticulum stress: cell life and death decisions. J Clin Invest 115:2656–2664

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yang ES, Bae JY, Kim TH, Kim YS, Suk K, Bae YC (2014) Involvement of endoplasmic reticulum stress response in orofacial inflammatory pain. Exp Neurobiol 23:372–380

    Article  PubMed Central  PubMed  Google Scholar 

  • Yang X, Wu LL, Chura LR, Liang X, Lane M, Norman RJ, Robker RL (2012) Exposure to lipid-rich follicular fluid is associated with endoplasmic reticulum stress and impaired oocyte maturation in cumulus-oocyte complexes. Fertil Steril 97:1438–1443

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Lin P, Chen F, Wang A, Lan X, Song Y, Jin Y (2013a) Luman recruiting factor regulates endoplasmic reticulum stress in mouse ovarian granulosa cell apoptosis. Theriogenology 79:633–639

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Jin Y, Martyn AC, Lin P, Song Y, Chen F, Hu L, Cui C, Li X, Li Q, Lu R, Wang A (2013b) Expression pattern implicates a potential role for luman recruitment factor in the process of implantation in uteri and development of preimplantation embryos in mice. J Reprod Dev 59:245–251

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yang Y, Sun M, Shan Y, Zheng X, Ma H, Ma W, Wang Z, Pei X, Wang Y (2014) Endoplasmic reticulum stress-mediated apoptotic pathway is involved in corpus luteum regression in rats. Reprod Sci 2014:pii,1933719114553445

    Google Scholar 

  • Yorimitsu T, Klionsky DJ (2007) Eating the endoplasmic reticulum: quality control by autophagy. Trends Cell Biol 17:279–285

    Article  CAS  PubMed  Google Scholar 

  • Yung HW, Calabrese S, Hynx D, Hemmings BA, Cetin I, Charnock-Jones DS, Burton G (2008) Evidence of placental translation inhibition and endoplasmic reticulum stress in the etiology of human intrauterine growth restriction. Am J Pathol 173:451–462

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang D, Ma C, Sun X, Xia H, Zhang W (2012) S100P expression in response to sex steroids during the implantation window in human endometrium. Reprod Biol Endocrinol 10:106

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang H, Wu F, Kong X, Yang J, Chen H, Deng L, Cheng Y, Ye L, Zhu S, Zhang X, Wang Z, Shi H, Fu X, Li X, Xu H, Lin L, Xiao J (2014) Nerve growth factor improves functional recovery by inhibiting endoplasmic reticulum stress-induced neuronal apoptosis in rats with spinal cord injury. J Transl Med 12:130

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Zhang J, Zhu G, Wang X, Xu B, Hu L (2007) Apoptosis and expression of protein TRAIL in granulosa cells of rats with polycystic ovarian syndrome. J Huazhong Univ Sci Technolog Med Sci 27:311–314

    Article  CAS  PubMed  Google Scholar 

  • Zhang JY, Diao YF, Kim HR, Jin DI (2012) Inhibition of endoplasmic reticulum stress improves mouse embryo development. PLoS One 7:e40433

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zheng YZ, Cao ZG, Hu X, Shao ZM (2014) The endoplasmic reticulum stress markers GRP78 and CHOP predict disease-free survival and responsiveness to chemotherapy in breast cancer. Breast Cancer Res Treat 145:349–358

    Article  CAS  PubMed  Google Scholar 

  • Zinszner H, Kuroda M, Wang X, Batchvarova N, Lightfoot RT, Remotti H, Stevens JL, Ron D (1998) CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev 12:982–995

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Key Laboratory of Fertility Preservation and Maintenance, Ministry of Education, Key Laboratory of Reproduction and Genetics in Ningxia, Department of Histology and Embryology, Ningxia Medical University, Yinchuan, Ningxia, 75004, People’s Republic of China

    Yanzhou Yang, Xiuying Pei & Yanrong Wang

  2. College of Life Science, Capital Normal University, Beijing, 100048, Peoples’ Republic of China

    Cheng Zhang

  3. Key Laboratory of Animal Biotechnology of the Ministry of Agriculture, College of Veterinary Medicine, Northwest A&F University, Yangling, Shaanxi, 712100, China

    Yaping Jin

Authors
  1. Yanzhou Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiuying Pei
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yaping Jin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yanrong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Cheng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Yanzhou Yang or Cheng Zhang.

Additional information

This work was supported by the Natural Science Foundation of China (no. 81260110); the open project of Key Laboratory of Fertility Preservation and Maintenance, Ministry of Education, Ningxia Medical University; Beijing Municipal Natural Science Foundation (no. 5142003); and the National Natural Science Foundation of China (no. 31300958).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, Y., Pei, X., Jin, Y. et al. The roles of endoplasmic reticulum stress response in female mammalian reproduction. Cell Tissue Res 363, 589–597 (2016). https://doi.org/10.1007/s00441-015-2212-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-015-2212-x

Keywords

Search

Navigation