Current research progresses of endoplasmic reticulum stress, Wolframin protein and pregnancy-related diseases

doi:10.3877/cma.j.issn.1673-5250.2020.04.001

Endoplasmic reticulum stress (ERS) is the core of cellular stress response. It can be classified into acute ERS and chronic ERS depending on the duration of ERS. Besides, it also can be divided into unfolded protein reaction (UPR), endoplasmic reticulum overload response (EOR), and sterol-regulatory element binding protein (SREBP) according to the different inducements of ERS. Wolframin protein, an resident membrane glycoprotein of endoplasmic reticulum, plays a key role in regulating ERS to maintain endoplasmic reticulum homeostasis by affecting both gene transcription and protein translation. At present, researches on ERS are mainly focused on ischemia, hypoxia, glucose deficiency, lipid overload, calcium ion disorder, etc., while researches on Wolframin proteins are mainly focused on the typical diseases of Wolfram syndrome including diabetes mellitus, optic atrophy, and bipolar disorder. In the field of perinatal medicine, ERS is closely related to pregnancy-related complications. However, due to stagnation of methodology, there are few researches about ERS and pregnancy-related diseases, such as preeclampsia, gestational diabetes mellitus (GDM), intrahepatic cholestasis of pregnancy. Hence, we report the latest related research of the classification of ERS, the relationship between Wolframin proteins and ERS, the corresponding signaling pathways mediated by ERS, and corresponding regulatory role of Wolframin proteins in the above signaling pathways, in order to provide a new direction for the pathophysiological mechanism of pregnance-related diseases.

Key words: Endoplasmic reticulum, Endoplasmic reticulum stress, Wolfram syndrome, Wolframin protein

[1]	Xu C, Bailly-Maitre B, Reed JC. Endoplasmic reticulum stress: cell life and death decisions [J]. J Clin Invest, 2005, 115(10): 2656-2664. DOI: 10.1172/JCI26373.
[2]	Ozcan U, Cao Q, Yilmaz E, et al. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes [J]. Science, 2004, 306(5695): 457-461. DOI: 10.1126/science.1103160.
[3]	Malhotra JD, Kaufman RJ. Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword? [J]. Antioxid Redox Signal, 2007, 9(12): 2277-2293. DOI: 10.1089/ars.2007.1782.
[4]	Gardner BM, Pincus D, Gotthardt K, et al. Endoplasmic reticulum stress sensing in the unfolded protein response [J]. Cold Spring Harb Perspect Biol, 2013, 5(3): a013169. DOI: 10.1101/cshperspect.a013169.
[5]	Rutkowski DT, Kaufman RJ. That which does not kill me makes me stronger: adapting to chronic ER stress [J]. Trends Biochem Sci, 2007, 32(10): 469-476. DOI: 10.1016/j.tibs.2007.09.003.
[6]	马孝甜. 内质网应激介导的滋养细胞凋亡与子痫前期的发病关系的研究[D]. 南京：南京医科大学，2011.
[7]	Hammadi M, Oulidi A, Gackière F, et al. Modulation of ER stress and apoptosis by endoplasmic reticulum calcium leak via translocon during unfolded protein response: involvement of GRP78 [J]. FASEB J, 2013, 27(4): 1600-1609. DOI: 10.1096/fj.12-218875.
[8]	Wu J, Kaufman RJ. From acute ER stress to physiological roles of the unfolded protein response [J]. Cell Death Differ, 2006, 13(3): 374-384. DOI: 10.1038/sj.cdd.4401840.
[9]	Szegezdi E, Logue SE, Gorman AM, et al. Mediators of endoplasmic reticulum stress-induced apoptosis [J]. EMBO Rep, 2006, 7(9): 880-885. DOI: 10.1038/sj.embor.7400779.
[10]	Sarcinelli C, Dragic H, Piecyk M, et al. ATF4-dependent NRF2 transcriptional regulation promotes antioxidant protection during endoplasmic reticulum stress [J]. Cancers (Basel), 2020, 12(3): 569. DOI: 10.3390/cancers12030569.
[11]	Liu Z, Lv Y, Zhao N, et al. Protein kinase R-like ER kinase and its role in endoplasmic reticulum stress-decided cell fate [J]. Cell Death Dis, 2015, 6(7): e1822. DOI: 10.1038/cddis.2015.183.
[12]	Civelek M, Manduchi E, Riley RJ, et al. Chronic endoplasmic reticulum stress activates unfolded protein response in arterial endothelium in regions of susceptibility to atherosclerosis [J]. Circ Res, 2009, 105(5): 453-461. DOI: 10.1161/CIRCRESAHA.109.203711.
[13]	Haze K, Okada T, Yoshida H, et al. Identification of the G13 (cAMP-response-element-binding protein-related protein) gene product related to activating transcription factor 6 as a transcriptional activator of the mammalian unfolded protein response [J]. Biochem J, 2001, 355(Pt 1): 19-28. DOI: 10.1042/0264-6021:3550019.
[14]	Tabas I, Ron D. Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress [J]. Nat Cell Biol, 2011, 13(3): 184-190. DOI: 10.1038/ncb0311-184.
[15]	Sun H, Wei G, Liu H, et al. Inhibition of XBP1s ubiquitination enhances its protein stability and improves glucose homeostasis [J]. Metabolism, 2020, 105: 154046. DOI: 10.1016/j.metabol.2019.154046.
[16]	Sicari D, Delaunay-Moisan A, Combettes L, et al. A guide to assessing endoplasmic reticulum homeostasis and stress in mammalian systems [J]. FEBS J, 2020, 287(1): 27-42. DOI: 10.1111/febs.15107.
[17]	Lin JH, Li H, Yasumura D, et al. IRE1 signaling affects cell fate during the unfolded protein response [J]. Science, 2007, 318(5852): 944-949. DOI: 10.1126/science.1146361.
[18]	Díaz-Hung ML, Martínez G, Hetz C. Emerging roles of the unfolded protein response (UPR) in the nervous system: a link with adaptive behavior to environmental stress? [J]. Int Rev Cell Mol Biol, 2020, 350(1): 29-61. DOI: 10.1016/bs.ircmb.2020.01.004.
[19]	Kaufman RJ. Orchestrating the unfolded protein response in health and disease [J]. J Clin Invest, 2002, 110(10): 1389-1398. DOI: 10.1172/JCI16886.
[20]	Kumar R, Azam S, Sullivan JM, et al. Brain ischemia and reperfusion activates the eukaryotic initiation factor 2alpha kinase, PERK [J]. J Neurochem, 2001, 77(5): 1418-1421. DOI: 10.1046/j.1471-4159.2001.00387.x.
[21]	Lin JH, Walter P, Yen TS. Endoplasmic reticulum stress in disease pathogenesis [J]. Annu Rev Pathol, 2008, 3: 399-425. DOI: 10.1146/annurev.pathmechdis.3.121806.151434.
[22]	Li Y, Guo Y, Tang J, et al. New insights into the roles of CHOP-induced apoptosis in ER stress [J]. Acta Biochim Biophys Sin (Shanghai), 2015, 47(2): 146-147. DOI: 10.1093/abbs/gmu128.
[23]	Szegezdi E, Fitzgerald U, Samali A. Caspase-12 and ER-stress-mediated apoptosis: the story so far [J]. Ann N Y Acad Sci, 2003, 1010(1): 186-194. DOI: 10.1196/annals.1299.032.
[24]	Inoue H, Tanizawa Y, Wasson J, et al. A gene encoding a transmembrane protein is mutated in patients with diabetes mellitus and optic atrophy (Wolfram syndrome) [J]. Nat Genet, 1998, 20(2): 143-148. DOI: 10.1038/2441.
[25]	Morikawa S, Tajima T, Nakamura A, et al. A novel heterozygous mutation of the WFS1 gene leading to constitutive endoplasmic reticulum stress is the cause of Wolfram syndrome [J]. Pediatr Diabetes, 2017, 18(8): 934-941. DOI: 10.1111/pedi.12513.
[26]	Ivask M, Hugill A, Kõks S. RNA-sequencing of WFS1-deficient pancreatic islets [J]. Physiol Rep, 2016, 4(7): e12750. DOI: 10.14814/phy2.12750.
[27]	Yamaguchi S, Ishihara H, Tamura A, et al. Endoplasmic reticulum stress and N-glycosylation modulate expression of WFS1 protein [J]. Biochem Biophys Res Commun, 2004, 325(1): 250-256. DOI: 10.1016/j.bbrc.2004.10.017.
[28]	De Falco M, Manente L, Lucariello A, et al. Localization and distribution of wolframin in human tissues [J]. Front Biosci (Elite Ed), 2012, 4: 1986-1998. DOI: 10.2741/519.
[29]	Kovacs-Nagy R, Elek Z, Szekely A, et al. Association of aggression with a novel microRNA binding site polymorphism in the wolframin gene [J]. Am J Med Genet B Neuropsychiatr Genet, 2013, 162B(4): 404-412. DOI: 10.1002/ajmg.b.32157.
[30]	Kakiuchi C, Ishigaki S, Oslowski CM, et al. Valproate, a mood stabilizer, induces WFS1 expression and modulates its interaction with ER stress protein GRP94 [J]. PLoS One, 2009, 4(1): e4134. DOI: 10.1371/journal.pone.0004134.
[31]	Ueda K, Kawano J, Takeda K, et al. Endoplasmic reticulum stress induces WFS1 gene expression in pancreatic beta-cells via transcriptional activation [J]. Eur J Endocrinol, 2005, 153(1): 167-176. DOI: 10.1530/eje.1.01945.
[32]	Yamada T, Ishihara H, Tamura A, et al. WFS1-deficiency increases endoplasmic reticulum stress, impairs cell cycle progression and triggers the apoptotic pathway specifically in pancreatic beta-cells [J]. Hum Mol Genet, 2006, 15(10): 1600-1609. DOI: 10.1093/hmg/ddl081.
[33]	Fonseca SG, Fukuma M, Lipson KL, et al. WFS1 is a novel component of the unfolded protein response and maintains homeostasis of the endoplasmic reticulum in pancreatic beta-cells [J]. J Biol Chem, 2005, 280(47): 39609-39615. DOI: 10.1074/jbc.M507426200.
[34]	Fonseca SG, Ishigaki S, Oslowski CM, et al. Wolfram syndrome 1 gene negatively regulates ER stress signaling in rodent and human cells [J]. J Clin Invest, 2010, 120(3): 744-755. DOI: 10.1172/JCI39678.
[35]	Fonseca SG, Burcin M, Gromada J, et al. Endoplasmic reticulum stress in beta-cells and development of diabetes [J]. Curr Opin Pharmacol, 2009, 9(6): 763-770. DOI: 10.1016/j.coph.2009.07.003.
[36]	Kõks S, Soomets U, Paya-Cano JL, et al. WFS1 gene deletion causes growth retardation in mice and interferes with the growth hormone pathway [J]. Physiol Genomics, 2009, 37(3): 249-259. DOI: 10.1152/physiolgenomics.90407.2008.
[37]	Huopio H, Cederberg H, Vangipurapu J, et al. Association of risk variants for type 2 diabetes and hyperglycemia with gestational diabetes [J]. Eur J Endocrinol, 2013, 169(3): 291-297. DOI: 10.1530/EJE-13-0286.
[38]	De Franco E, Flanagan SE, Yagi T, et al. Dominant ER stress-inducing WFS1 mutations underlie a genetic syndrome of neonatal/infancy-onset diabetes, congenital sensorineural deafness, and congenital cataracts [J]. Diabetes, 2017, 66(7): 2044-2053. DOI: 10.2337/db16-1296.
[39]	Noormets K, Kõks S, Kavak A, et al. Male mice with deleted Wolframin (Wfs1) gene have reduced fertility [J]. Reprod Biol Endocrinol, 2009, 7：82. DOI: 10.1186/1477-7827-7-82.
[40]	Karna KK, Shin YS, Choi BR, et al. The Role of endoplasmic reticulum stress response in male reproductive physiology and pathology: a review[J]. World J Mens Health, 2019. DOI: 10.5534/wjmh.190038.
[41]	Domènech E, Kruyer H, Gómez C, et al. First prenatal diagnosis for Wolfram syndrome by molecular analysis of the WFS1 gene [J]. Prenat Diagn, 2004, 24(10): 787-789. DOI: 10.1002/pd.982.
[42]	Rugolo S, Mirabella D, Palumbo MA, et al. Complete Wolfram syndrome and successful pregnancy [J]. Eur J Obstet Gynecol Reprod Biol, 2002, 105(2): 192-193. DOI: 10.1016/s0301-2115(02)00150-1.
[43]	Lucariello A, Perna A, Sellitto C, et al. Modulation of wolframin expression in human placenta during pregnancy: comparison among physiological and pathological states [J]. Biomed Res Int, 2014, 2014: 985478. DOI: 10.1155/2014/985478.
[44]	Xu T, Zhou Z, Liu N, et al. Disrupted compensatory response mediated by Wolfram syndrome 1 protein and corticotrophin-releasing hormone family peptides in early-onset intrahepatic cholestasis pregnancy [J]. Placenta, 2019, 83(1): 63-71. DOI: 10.1016/j.placenta.2019.06.378.
[45]	WFS1 is prognostic, high expression is favourable in endometrial cancer [EB/OL]. [2020-01-11]. URL
[46]	Berchuck A, Iversen ES, Lancaster JM, et al. Patterns of gene expression that characterize long-term survival in advanced stage serous ovarian cancers [J]. Clin Cancer Res, 2005, 11(10): 3686-3696. DOI: 10.1158/1078-0432.CCR-04-2398.
[47]	Chao S, Xiao JL, Haizhen W, et al. Lithocholic acid activates mTOR signaling inducing endoplasmic reticulum stress in placenta during intrahepatic cholestasis of pregnancy [J]. Life Sci, 2019, 218(2): 300-307. DOI: 10.1016/j.lfs.2018.12.050.

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