Abstract
The glucose-regulated protein (GRP78) also referred to as immunoglobulin heavy chain binding protein (Bip) is one of the best characterized endoplasmic reticulum (ER) chaperone proteins, which belongs to the heat-shock protein (HSP) family. GRP78 as a central regulator of ER stress (ERS) plays many important roles in cell survival and apoptosis through controlling the activation of transmembrane ERS sensors: PKR-like ER-associated kinase (PERK), inositol requiring kinase 1 (IRE1), and activating transcription factor 6 (ATF6). Many studies have reported that GRP78 is involved in the physiological and pathological process in female reproduction, including follicular development, corpus luteum (CL), oviduct, uterus, embryo, preimplantation development, implantation/decidualization, and the placenta. The present review summarizes the biological or pathological roles and signaling mechanisms of GRP78 during the reproductive processes. Further study on the functions and mechanisms of GRP78 may provide new insight into mammalian reproduction, which not only enhance the understanding of the physiological roles but also support therapy target against infertility.
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- ATF6:
-
Activating transcription factor 6
- Bip:
-
Immunoglobulin heavy chain binding protein
- CHOP:
-
C/EBP-homologous protein/DNA damage-inducible transcript 3
- CL:
-
Corpus luteum
- eIF2α:
-
Eukaryotic translation initiation factor 2α
- ER:
-
Endoplasmic reticulum
- FSH:
-
Follicle stimulating hormone
- GnRH:
-
Gonadotropin-releasing hormone
- GRP78:
-
Glucose-regulated protein
- HSP:
-
heat-shock protein
- IRE1:
-
inositol requiring kinase 1
- JNK:
-
c-Jun N-terminal kinase
- LH:
-
Luteinizing hormone
- PERK:
-
PKR-like ER-associated kinase
- UPR:
-
Unfolded protein response
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
Arnaudeau S, Arboit P, Bischof P, Shin-ya K, Tomida A, Tsuruo T, Irion O, Cohen M (2009) Glucose-regulated protein 78: a new partner of p53 in trophoblast. Proteomics 9:5316–5327
Barnes JA, Smoak IW (2000) Glucose-regulated protein 78 (GRP78) is elevated in embryonic mouse heart and induced following hypoglycemic stress. Anat Embryol (Berl) 202:67–74
Barnes JA, Smoak IW, Branch S (1999) Expression of glucose-regulated proteins (GRP78 and GRP94) in hearts and fore-limb buds of mouse embryos exposed to hypoglycemia in vitro. Cell Stress Chaperones 4:250–258
Boilard M, Reyes-Moreno C, Lachance C, Massicotte L, Bailey JL, Sirard MA, Leclerc P (2004) Localization of the chaperone proteins GRP78 and HSP60 on the luminal surface of bovine oviduct epithelial cells and their association with spermatozoa. Biol Reprod 71:1879–1889
Borradaile NM, Han X, Harp JD, Gale SE, Ory DS, Schaffer JE (2006) Disruption of endoplasmic reticulum structure and integrity in lipotoxic cell death. J Lipid Res 47:2726–2737
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
Brewer JW, Cleveland JL, Hendershot LM (1997) A pathway distinct from the mammalian unfolded protein response regulates expression of endoplasmic reticulum chaperones in non-stressed cells. Embo J 16:7207–7216
Burton GJ, Yung HW, Cindrova-Davies T, Charnock-Jones DS (2009) Placental endoplasmic reticulum stress and oxidative stress in the pathophysiology of unexplained intrauterine growth restriction and early onset preeclampsia. Placenta 30(Suppl A): S43–S48
Canepa MJ, Ortega NM, Monteleone MC, Mucci N, Kaiser GG, Brocco M, Mutto A (2014) Expression profile of genes as indicators of developmental competence and quality of in vitro fertilization and somatic cell nuclear transfer bovine embryos. PLoS One 9:e108139
Carambula SF, Pru JK, Lynch MP, Matikainen T, Goncalves 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
Chevalier M, Rhee H, Elguindi EC, Blond SY (2000) Interaction of murine BiP/GRP78 with the DnaJ homologue MTJ1. J Biol Chem 275:19620–19627
Choi J, Jo M, Lee E, Choi D (2011) The role of autophagy in corpus luteum regression in the rat. Biol Reprod 85:465–472
Cree LM, Hammond ER, Shelling AN, Berg MC, Peek JC, Green MP (2015) Maternal age and ovarian stimulation independently affect oocyte mtDNA copy number and cumulus cell gene expression in bovine clones. Hum Reprod 30:1410–1420
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
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
De Feo VJ (1963) Temporal aspect of uterine sensitivity in the pseudopregnant or pregnant rat. Endocrinology 72:305–316
Dey SK, Lim H, Das SK, Reese J, Paria BC, Daikoku T, Wang H (2004) Molecular cues to implantation. Endocr Rev 25:341–373
Diakogiannaki E, Welters HJ, Morgan NG (2008) Differential regulation of the endoplasmic reticulum stress response in pancreatic beta-cells exposed to long-chain saturated and monounsaturated fatty acids. J Endocrinol 197:553–563
Ellington JE, Ignotz GG, Varner DD, Marcucio RS, Mathison P, Ball BA (1993) In vitro interaction between oviduct epithelial and equine sperm. Arch Androl 31:79–86
Ellington JE, Evenson DP, Wright RW Jr, Jones AE, Schneider CS, Hiss GA, Brisbois RS (1999a) Higher-quality human sperm in a sample selectively attach to oviduct (fallopian tube) epithelial cells in vitro. Fertil Steril 71:924–929
Ellington JE, Samper JC, Jones AE, Oliver SA, Burnett KM, Wright RW (1999b) In vitro interactions of cryopreserved stallion spermatozoa and oviduct (uterine tube) epithelial cells or their secretory products. Anim Reprod Sci 56:51–65
Espey LL, Richards JS (2002) Temporal and spatial patterns of ovarian gene transcription following an ovulatory dose of gonadotropin in the rat. Biol Reprod 67:1662–1670
Fazeli A, Affara NA, Hubank M, Holt WV (2004) Sperm-induced modification of the oviductal gene expression profile after natural insemination in mice. Biol Reprod 71:60–65
Feng C, He K, Zhang C, Su S, Li B, Li Y, Duan CY, Chen S, Chen R, Liu Y, Li H, Wei M, Xia X, Dai R (2014) JNK contributes to the tumorigenic potential of human cholangiocarcinoma cells through the mTOR pathway regulated GRP78 induction. PLoS One 9:e90388
Fischer B, Bavister BD (1993) Oxygen tension in the oviduct and uterus of rhesus monkeys, hamsters and rabbits. J Reprod Fertil 99:673–679
Fleming JV, Fontanier N, Harries DN, Rees WD (1997) The growth arrest genes gas5, gas6, and CHOP-10 (gadd153) are expressed in the mouse preimplantation embryo. Mol Reprod Dev 48:310–316
Fontanier-Razzaq NC, Hay SM, Rees WD (1999) Upregulation of CHOP-10 (gadd153) expression in the mouse blastocyst as a response to stress. Mol Reprod Dev 54:326–332
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
Fu J, Zhao L, Wang L, Zhu X (2015) Expression of markers of endoplasmic reticulum stress-induced apoptosis in the placenta of women with early and late onset severe pre-eclampsia. Taiwan J Obstet Gynecol 54:19–23
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
Gaytan F, Morales C, Bellido C, Aguilar R, Millan Y, Martin De Las Mulas J, Sanchez-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
Georgiou AS, Sostaric E, Wong CH, Snijders AP, Wright PC, Moore HD, Fazeli A (2005) Gametes alter the oviductal secretory proteome. Mol Cell Proteomics 4:1785–1796
Gonzalez-Gronow M, Selim MA, Papalas J, Pizzo SV (2009) GRP78: a multifunctional receptor on the cell surface. Antioxid Redox Signal 11:2299–2306
Gray PC, Vale W (2012) Cripto/GRP78 modulation of the TGF-beta pathway in development and oncogenesis. FEBS Lett 586:1836–1845
Gualtieri R, Boni R, Tosti E, Zagami M, Talevi R (2005) Intracellular calcium and protein tyrosine phosphorylation during the release of bovine sperm adhering to the fallopian tube epithelium in vitro. Reproduction 129:51–60
Guan S, Guo L, Zhang T, Zhu B, Wang X, Zhang C (2015) Effects of gonadotropin on Fas and/or FasL expression and proliferation in rat ovary. Theriogenology 83:21–29
Guzel E, Basar M, Ocak N, Arici A, Kayisli UA (2011) Bidirectional interaction between unfolded-protein-response key protein HSPA5 and estrogen signaling in human endometrium. Biol Reprod 85:121–127
Haas IG, Wabl M (1983) Immunoglobulin heavy chain binding protein. Nature 306:387–389
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
Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, Schapira M, Ron D (2000) Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 6:1099–1108
Hayashi K, Erikson DW, Tilford SA, Bany BM, Maclean JA 2nd, Rucker EB 3rd, Johnson GA, Spencer TE (2009) Wnt genes in the mouse uterus: potential regulation of implantation. Biol Reprod 80:989–1000
Hendershot LM (2004) The ER function BiP is a master regulator of ER function. Mt Sinai J Med 71:289–297
Hill JA (2001) Maternal-embryonic cross-talk. Ann NY Acad Sci 943:17–25
Hong M, Luo S, Baumeister P, Huang JM, Gogia RK, Li M, Lee AS (2004) Underglycosylation of ATF6 as a novel sensing mechanism for activation of the unfolded protein response. J Biol Chem 279:11354–11363
Huang HL, Wu JL, Chen MH, Hong JR (2011) Aquatic birnavirus-induced ER stress-mediated death signaling contribute to downregulation of Bcl-2 family proteins in salmon embryo cells. PLoS One 6:e22935
Hunter RH, Rodriguez-Martinez H (2004) Capacitation of mammalian spermatozoa in vivo, with a specific focus on events in the Fallopian tubes. Mol Reprod Dev 67:243–250
Ishikawa T, Okada T, Ishikawa-Fujiwara T, Todo T, Kamei Y, Shigenobu S, Tanaka M, Saito TL, Yoshimura J, Morishita S, Toyoda A, Sakaki Y, Taniguchi Y, Takeda S, Mori K (2013) ATF6alpha/beta-mediated adjustment of ER chaperone levels is essential for development of the notochord in medaka fish. Mol Biol Cell 24:1387–1395
Iwamune M, Nakamura K, Kitahara Y, Minegishi T (2014) MicroRNA-376a regulates 78-kilodalton glucose-regulated protein expression in rat granulosa cells. PLoS One 9:e108997
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 USA 106:16657–16662
Jiemtaweeboon S, Shirasuna K, Nitta A, Kobayashi A, Schuberth HJ, Shimizu T, Miyamoto A (2011) Evidence that polymorphonuclear neutrophils infiltrate into the developing corpus luteum and promote angiogenesis with interleukin-8 in the cow. Reprod Biol Endocrinol 9:79
Jing G, Wang JJ, Zhang SX (2012) ER stress and apoptosis: a new mechanism for retinal cell death. Exp Diabetes Res 2012:589589
Juengel JL, Garverick HA, Johnson AL, Youngquist RS, Smith MF (1993) Apoptosis during luteal regression in cattle. Endocrinology 132:249–254
Kaufman RJ (1999) Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev 13:1211–1233
Kaufman RJ (2002) Orchestrating the unfolded protein response in health and disease. J Clin Invest 110:1389–1398
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
Kayisli UA, Mahutte NG, Arici A (2002) Uterine chemokines in reproductive physiology and pathology. Am J Reprod Immunol 47:213–221
Kidson A, Schoevers E, Langendijk P, Verheijden J, Colenbrander B, Bevers M (2003) The effect of oviductal epithelial cell co-culture during in vitro maturation on sow oocyte morphology, fertilization and embryo development. Theriogenology 59:1889–1903
Kim SK, Kim YK, Lee AS (1990) Expression of the glucose-regulated 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
Kim R, Emi M, Tanabe K, Murakami S (2006) Role of the unfolded protein response in cell death. Apoptosis 11:5–13
Kim YN, Kim HK, Warda M, Kim N, Park WS, Prince Adel B, Jeong DH, Lee DS, Kim KT, Han J (2007) Toward a better understanding of preeclampsia: comparative proteomic analysis of preeclamptic placentas. Proteomics Clin Appl 1:1625–1636
Kimber SJ, Spanswick C (2000) Blastocyst implantation: the adhesion cascade. Semin Cell Dev Biol 11:77–92
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
Kohno K (2007) How transmembrane proteins sense endoplasmic reticulum stress. Antioxid Redox Signal 9:2295–2303
Koshiyama M, Konishi I, Nanbu K, Nanbu Y, Mandai M, Komatsu T, Yamamoto S, Mori T, Fujii S (1995) Immunohistochemical localization of heat shock proteins HSP70 and HSP90 in the human endometrium: correlation with sex steroid receptors and Ki-67 antigen expression. J Clin Endocrinol Metab 80:1106–1112
Lachance C, Bailey JL, Leclerc P (2007) Expression of Hsp60 and Grp78 in the human endometrium and oviduct, and their effect on sperm functions. Hum Reprod 22:2606–2614
Lai E, Teodoro T, Volchuk A (2007) Endoplasmic reticulum stress: signaling the unfolded protein response. Physiology (Bethesda) 22:193–201
Lane M, Gardner DK (2005) Understanding cellular disruptions during early embryo development that perturb viability and fetal development. Reprod Fertil Dev 17:371–378
Lee AS (2001) The glucose-regulated proteins: stress induction and clinical applications. Trends Biochem Sci 26:504–510
Lee AS (2005) The ER chaperone and signaling regulator GRP78/BiP as a monitor of endoplasmic reticulum stress. Methods 35:373–381
Lei K, Davis RJ (2003) JNK phosphorylation of Bim-related members of the Bcl2 family induces Bax-dependent apoptosis. Proc Natl Acad Sci USA 100:2432–2437
Li J, Ni M, Lee B, Barron E, Hinton DR, Lee AS (2008) The unfolded protein response regulator GRP78/BiP is required for endoplasmic reticulum integrity and stress-induced autophagy in mammalian cells. Cell Death Differ 15:1460–1471
Lian IA, Loset M, Mundal SB, Fenstad MH, Johnson MP, Eide IP, Bjorge 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
Lin P, Chen F, Yang Y, Song Y, Li X, Lan X, Jin Y, Wang A (2012a) GRP78 expression and immunohistochemical localization in the female reproductive tract of mice. Theriogenology 78:1824–1829
Lin P, Yang Y, Li X, Chen F, Cui C, Hu L, Li Q, Liu W, Jin Y (2012b) Endoplasmic reticulum stress is involved in granulosa cell apoptosis during follicular atresia in goat ovaries. Mol Reprod Dev 79:423–432
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
Little E, Ramakrishnan M, Roy B, Gazit G, Lee AS (1994) The glucose-regulated proteins (GRP78 and GRP94): functions, gene regulation, and applications. Crit Rev Eukaryot Gene Expr 4:1–18
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
Loset M, Mundal SB, Johnson MP, Fenstad MH, Freed KA, Lian IA, Eide IP, Bjorge L, Blangero J, Moses EK, Austgulen R (2011) A transcriptional profile of the decidua in preeclampsia. Am J Obstet Gynecol 204(84):e81–e27
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
Mahoney WC, Duksin D (1979) Biological activities of the two major components of tunicamycin. J Biol Chem 254:6572–6576
Marciniak SJ, Yun CY, Oyadomari S, Novoa I, Zhang Y, Jungreis R, Nagata K, Harding HP, Ron D (2004) CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev 18:3066–3077
Marin-Briggiler CI, Gonzalez-Echeverria MF, Munuce MJ, Ghersevich S, Caille AM, Hellman U, Corrigall VM, Vazquez-Levin MH (2010) Glucose-regulated protein 78 (Grp78/BiP) is secreted by human oviduct epithelial cells and the recombinant protein modulates sperm-zona pellucida binding. Fertil Steril 93:1574–1584
Mizrachi D, Segaloff DL (2004) Intracellularly located misfolded glycoprotein hormone receptors associate with different chaperone proteins than their cognate wild-type receptors. Mol Endocrinol 18:1768–1777
Ni M, Zhang Y, Lee AS (2011) Beyond the endoplasmic reticulum: atypical GRP78 in cell viability, signalling and therapeutic targeting. Biochem J 434:181–188
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 USA 107:19320–19325
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 (2013a) 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
Park SJ, Kim TS, Park CK, Lee SH, Kim JM, Lee KS, Lee IK, Park JW, Lawson MA, Lee DS (2013b) hCG-induced endoplasmic reticulum stress triggers apoptosis and reduces steroidogenic enzyme expression through activating transcription factor 6 in Leydig cells of the testis. J Mol Endocrinol 50:151–166
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
Patierno SR, Tuscano JM, Kim KS, Landolph JR, Lee AS (1987) Increased expression of the glucose-regulated gene encoding the Mr 78,000 glucose-regulated protein in chemically and radiation-transformed C3H 10 T1/2 mouse embryo cells. Cancer Res 47:6220–6224
Peng J, Gao K, Gao T, Lei Y, Han P, Xin H, An X, Cao B (2015) Expression and regulation of tissue inhibitors of metalloproteinases (TIMP1 and TIMP3) in goat oviduct. Theriogenology 84:1636–1643
Psychoyos A (1973) Hormonal control of ovoimplantation. Vitam Horm 31:201–256
Psychoyos A (1986) Uterine receptivity for nidation. Ann NY Acad Sci 476:36–42
Quinones QJ, de Ridder GG, Pizzo SV (2008) GRP78: a chaperone with diverse roles beyond the endoplasmic reticulum. Histol Histopathol 23:1409–1416
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
Rasheva VI, Domingos PM (2009) Cellular responses to endoplasmic reticulum stress and apoptosis. Apoptosis 14:996–1007
Ray S, Hou X, Zhou HE, Wang H, Das SK (2006) Bip is a molecular link between the phase I and phase II estrogenic responses in uterus. Mol Endocrinol 20:1825–1837
Redman CW, Sargent IL (2005) Latest advances in understanding preeclampsia. Science 308:1592–1594
Reese J, Das SK, Paria BC, Lim H, Song H, Matsumoto H, Knudtson KL, DuBois RN, Dey SK (2001) Global gene expression analysis to identify molecular markers of uterine receptivity and embryo implantation. J Biol Chem 276:44137–44145
Reid RJ, Heald PJ (1970) Uptake of (3H)leucine into proteins of rat uterus during early pregnancy. Biochim Biophys Acta 204:278–279
Reid RJ, Heald PJ (1971) Protein metabolism of the rat uterus during the oestrous cycle, pregnancy and pseudopregnancy, and as affected by an anti-implantation compounds, ICI 46,474. J Reprod Fertil 27:73–82
Repo JK, Pesonen M, Mannelli C, Vahakangas K, Loikkanen J (2014) Exposure to ethanol and nicotine induces stress responses in human placental BeWo cells. Toxicol Lett 224:264–271
Richards JS, Russell DL, Ochsner S, Espey LL (2002) Ovulation: new dimensions and new regulators of the inflammatory-like response. Annu Rev Physiol 64:69–92
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
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
Rutkowski DT, Kaufman RJ (2004) A trip to the ER: coping with stress. Trends Cell Biol 14:20–28
Sato M, Yao VJ, Arap W, Pasqualini R (2010) GRP78 signaling hub a receptor for targeted tumor therapy. Adv Genet 69:97–114
Shen J, Chen X, Hendershot L, Prywes R (2002) ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev Cell 3:99–111
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
Shiu RP, Pouyssegur J, Pastan I (1977) Glucose depletion accounts for the induction of two transformation-sensitive membrane proteinsin Rous sarcoma virus-transformed chick embryo fibroblasts. Proc Natl Acad Sci USA 74:3840–3844
Shore GC, Papa FR, Oakes SA (2011) Signaling cell death from the endoplasmic reticulum stress response. Curr Opin Cell Biol 23:143–149
Simmons DG, Kennedy TG (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
Sonderegger S, Yap J, Menkhorst E, Weston G, Stanton PG, Dimitriadis E (2011) Interleukin (IL)11 mediates protein secretion and modification in human extravillous trophoblasts. Hum Reprod 26:2841–2849
Sostaric E, Georgiou AS, Wong CH, Watson PF, Holt WV, Fazeli A (2006) Global profiling of surface plasma membrane proteome of oviductal epithelial cells. J Proteome Res 5:3029–3037
Stocco C, Telleria C, Gibori G (2007) The molecular control of corpus luteum formation, function, and regression. Endocr Rev 28:117–149
Szegezdi E, Macdonald DC, Ni Chonghaile T, Gupta S, Samali A (2009) Bcl-2 family on guard at the ER. Am J Physiol Cell Physiol 296:C941–C953
Tabibzadeh S, Broome J (1999) Heat shock proteins in human endometrium throughout the menstrual cycle. Infect Dis Obstet Gynecol 7:5–9
Tabibzadeh S, Kong QF, Satyaswaroop PG, Babaknia A (1996) Heat shock proteins in human endometrium throughout the menstrual cycle. Hum Reprod 11:633–640
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
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
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 287:664–666
Veerbeek JH, Tissot Van Patot MC, Burton GJ, Yung HW (2015) Endoplasmic reticulum stress is induced in the human placenta during labour. Placenta 36:88–92
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
Watson ED, Cross JC (2005) Development of structures and transport functions in the mouse placenta. Physiology (Bethesda) 20:180–193
Wiest DL, Burkhardt JK, Hester S, Hortsch M, Meyer DI, Argon Y (1990) Membrane biogenesis during B cell differentiation: most endoplasmic reticulum proteins are expressed coordinately. J Cell Biol 110:1501–1511
Wong MK, Nicholson CJ, Holloway AC, Hardy DB (2015) Maternal nicotine exposure leads to impaired disulfide bond formation and augmented endoplasmic reticulum stress in the rat placenta. PLoS One 10:e0122295
Wong MK, Holloway AC, Hardy DB (2016) Nicotine directly induces endoplasmic reticulum stress response in rat placental trophoblast giant cells. Toxicol Sci 151(1):23–34
Wu J, Kaufman RJ (2006) From acute ER stress to physiological roles of the Unfolded Protein Response. Cell Death Differ 13:374–384
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
Yan Z, Wei H, Ren C, Yuan S, Fu H, Lv Y, Zhu Y, Zhang T (2015) Gene expression of Hsps in normal and abnormal embryonic development of mouse hindlimbs. Hum Exp Toxicol 34:563–574
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
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–e633
Yang Y, Pei X, Jin Y, Wang Y, Zhang C (2015a) The roles of endoplasmic reticulum stress response in female mammalian reproduction. Cell Tissue Res 363:589–597
Yang Y, Sun M, Shan Y, Zheng X, Ma H, Ma W, Wang Z, Pei X, Wang Y (2015b) Endoplasmic reticulum stress-mediated apoptotic pathway is involved in corpus luteum regression in rats. Reprod Sci 22:572–584
Ye J, Rawson RB, Komuro R, Chen X, Dave UP, Prywes R, Brown MS, Goldstein JL (2000) ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol Cell 6:1355–1364
Yoshida H, Haze K, Yanagi H, Yura T, Mori K (1998) Identification of the cis-acting endoplasmic reticulum stress response element responsible for transcriptional induction of mammalian glucose-regulated proteins. Involvement of basic leucine zipper transcription factors. J Biol Chem 273:33741–33749
Young LE, Sinclair KD, Wilmut I (1998) Large offspring syndrome in cattle and sheep. Rev Reprod 3:155–163
Yung HW, Calabrese S, Hynx D, Hemmings BA, Cetin I, Charnock-Jones DS, Burton GJ (2008) Evidence of placental translation inhibition and endoplasmic reticulum stress in the etiology of human intrauterine growth restriction. Am J Pathol 173:451–462
Yung HW, Cox M, Tissot van Patot M, Burton GJ (2012) Evidence of endoplasmic reticulum stress and protein synthesis inhibition in the placenta of non-native women at high altitude. Faseb J 26:1970–1981
Yung HW, Atkinson D, Campion-Smith T, Olovsson M, Charnock-Jones DS, Burton GJ (2014) Differential activation of placental unfolded protein response pathways implies heterogeneity in causation of early- and late-onset pre-eclampsia. J Pathol 234:262–276
Zhang K, Wong HN, Song B, Miller CN, Scheuner D, Kaufman RJ (2005) The unfolded protein response sensor IRE1alpha is required at 2 distinct steps in B cell lymphopoiesis. J Clin Invest 115:268–281
Zhang C, Xia G, Tsang BK (2011) Interactions of thyroid hormone and FSH in the regulation of rat granulosa cell apoptosis. Front Biosci (Elite Ed) 3:1401–1413
Zhang C, Niu W, Wang Z, Wang X, Xia G (2012a) The effect of gonadotropin on glucose transport and apoptosis in rat ovary. PLoS One 7:e42406
Zhang D, Ma C, Sun X, Xia H, Zhang W (2012b) S100P expression in response to sex steroids during the implantation window in human endometrium. Reprod Biol Endocrinol 10:106
Zhang C, Wang X, Wang Z, Niu W, Zhu B, Xia G (2013) Effect of different culture systems and 3, 5, 3′-triiodothyronine/follicle-stimulating hormone on preantral follicle development in mice. PLoS One 8:e61947
Zhu Y, Zhou H, Zhu Y, Wan X, Zhu J, Zhang T (2012) Gene expression of Hsp70, Hsp90, and Hsp110 families in normal and abnormal embryonic development of mouse forelimbs. Drug Chem Toxicol 35:432–444
Zhu Y, Ren C, Wan X, Zhu Y, Zhu J, Zhou H, Zhang T (2013) Gene expression of Hsp70, Hsp90 and Hsp110 families in normal palate and cleft palate during mouse embryogenesis. Toxicol Ind Health 29:915–930
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
Acknowledgments
This work was supported by the National Natural Science Foundation of China (No. 31671555; No 31300958) and Beijing Natural Science Foundation (No.5142003). And this project was also supported by Scientific Research Program of Beijing Municipal Commission of Education (KM201610028011). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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Zhang, C. (2017). Roles of Grp78 in Female Mammalian Reproduction. In: MacPhee, D. (eds) The Role of Heat Shock Proteins in Reproductive System Development and Function. Advances in Anatomy, Embryology and Cell Biology, vol 222. Springer, Cham. https://doi.org/10.1007/978-3-319-51409-3_7
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