Genome-wide analysis of tunicamycin-induced endoplasmic reticulum stress response and the protective effect of endoplasmic reticulum inhibitors in neonatal rat cardiomyocytes

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• 作者：Chun-Lei Liu ; Wu Zhong ; Yun-Yun He ; Xin Li ; Song Li…
• 关键词：Endoplasmic reticulum stress ; RNA ; seq ; UPR ; Cardiomyopathy
• 刊名：Molecular and Cellular Biochemistry
• 出版年：2016
• 出版时间：February 2016
• 年：2016
• 卷：413
• 期：1-2
• 页码：57-67
• 全文大小：1,120 KB
• 参考文献：1.Yuan L, Cao Y, Knöchel W (2007) Endoplasmic reticulum stress induced by tunicamycin disables germ layer formation in Xenopus laevis embryos. Dev Dynam 236(10):2844–2851CrossRef
  2.Boyce M, Yuan J (2006) Cellular response to endoplasmic reticulum stress: a matter of life or death. Cell Death Differ 13(3):363–373CrossRef PubMed
  3.Minamino T, Komuro I, Kitakaze M (2010) Endoplasmic reticulum stress as a therapeutic target in cardiovascular disease. Circ Res 107(9):1071–1082CrossRef PubMed
  4.Deng Q, Xu C, Wang R, Zheng J, Li S, Jin Q, Yang Y (2015) TN-2 Ameliorates tunicamycin-induced mitochondria and endoplasmic reticulum stress-associated apoptosis in rat dorsal root ganglion neurons. J Mol Neurosci 57(2):314CrossRef PubMed
  5.Quan X, Wang J, Liang C, Zheng H, Zhang L (2015) Melatonin inhibits tunicamycin-induced endoplasmic reticulum stress and insulin resistance in skeletal muscle cells. Biochem Biophys Res Commun 463(4):1102–1107CrossRef PubMed
  6.Hwang HJ, Jung TW, Ryu JY, Hong HC, Choi HY, Seo JA, Kim SG, Kim NH, Choi KM, Choi DS, Baik SH, Yoo HJ (2014) Dipeptidyl petidase-IV inhibitor (gemigliptin) inhibits tunicamycin-induced endoplasmic reticulum stress, apoptosis and inflammation in H9c2 cardiomyocytes. Mol Cell Endocrinol 392(1–2):1–7CrossRef PubMed
  7.Shen M, Wang L, Guo X, Xue Q, Huo C, Li X, Fan L, Wang X (2015) A novel endoplasmic reticulum stress induced apoptosis model using tunicamycin in primary cultured neonatal rat cardiomyocytes. Mol Med Rep 12(4):5149–5154PubMed
  8.Boyce M, Bryant KF, Jousse C, Long K, Harding HP, Scheuner D, Kaufman RJ, Ma D, Coen DM, Ron D, Yuan J (2005) A selective inhibitor of eIF2alpha dephosphorylation protects cells from ER stress. Science 307(5711):935–939CrossRef PubMed
  9.Huang X, Chen Y, Zhang H, Ma Q, Zhang YW, Xu H (2012) Salubrinal attenuates beta-amyloid-induced neuronal death and microglial activation by inhibition of the NF-kappaB pathway. Neurobiol Aging 33(5):1007.e9-17PubMed
  10.Ladriere L, Igoillo-Esteve M, Cunha DA, Brion JP, Bugliani M, Marchetti P, Eizirik DL, Cnop M (2010) Enhanced signaling downstream of ribonucleic Acid-activated protein kinase-like endoplasmic reticulum kinase potentiates lipotoxic endoplasmic reticulum stress in human islets. J Clin Endocr Metab 95(3):1442–1449CrossRef PubMed
  11.Liu CL, Li X, Hu GL, Li RJ, He YY, Zhong W, Li S, He KL, Wang LL (2012) Salubrinal protects against tunicamycin and hypoxia induced cardiomyocyte apoptosis via the PERK-eIF2alpha signaling pathway. J Geriatr Cardiol 9(3):258–268PubMedCentral CrossRef PubMed
  12.Liu J, He KL, Li X, Li RJ, Liu CL, Zhong W, Li S (2012) SAR, cardiac myocytes protection activity and 3D-QSAR studies of salubrinal and its potent derivatives. Curr Med Chem 19(1):1–8CrossRef
  13.Liu CL, He YY, Li X, Li RJ, He KL, Wang LL (2014) Inhibition of serine/threonine protein phosphatase PP1 protects cardiomyocytes from tunicamycin-induced apoptosis and I/R through the upregulation of p-eIF2alpha. Int J Mol Med 33(3):499–506PubMedCentral PubMed
  14.Farber CR (2013) systems-level analysis of genome-wide association data. G3-Genes Genom Genet 3:119–129
  15.Streets AM, Zhang X, Cao C, Pang Y, Wu X, Xiong L, Yang L, Fu Y, Zhao L, Tang F, Huang Y (2014) Microfluidic single-cell whole-transcriptome sequencing. P Natl Acad Sci USA 111(19):7048–7053CrossRef
  16.da Huang W, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4(1):44–57CrossRef
  17.Jonikas MC, Collins SR, Denic V, Oh E, Quan EM, Schmid V, Weibezahn J, Schwappach B, Walter P, Weissman JS, Schuldiner M (2009) Comprehensive characterization of genes required for protein folding in the endoplasmic reticulum. Science 323(5922):1693–1697PubMedCentral CrossRef PubMed
  18.Dombroski BA, Nayak RR, Ewens KG, Ankener W, Cheung VG, Spielman RS (2010) Gene expression and genetic variation in response to endoplasmic reticulum stress in human cells. Am J Hum Genet 86(5):719–729PubMedCentral CrossRef PubMed
  19.Chow CY, Wolfner MF, Clark AG (2013) Using natural variation in Drosophila to discover previously unknown endoplasmic reticulum stress genes. Proc Natl Acad Sci USA 110(22):9013–9018PubMedCentral CrossRef PubMed
  20.Fan F, Ma G, Li J, Liu Q, Benz JP, Tian C, Ma Y (2015) Genome-wide analysis of the endoplasmic reticulum stress response during lignocellulase production in Neurospora crassa. Biotechnol Biofuels 8:66PubMedCentral CrossRef PubMed
  21.Teske BF, Wek S, Bunpo P, Cundiff JK, McClintick JN, Anthony TG, Wek RC (2011) The eIF2 kinase PERK and the integrated stress response facilitate activation of ATF6 during endoplasmic reticulum stress. Mol Biol Cell 22(15):4390–4405PubMedCentral CrossRef PubMed
  22.Cechowska-Pasko M, Surazynski A, Bankowski E (2009) The effect of glucose deprivation on collagen synthesis in fibroblast cultures. Mol Cell Biochem 327(1–2):211–218CrossRef PubMed
  23.Riezzo I, Neri M, De Stefano F, Fulcheri E, Ventura F, Pomara C, Rabozzi R, Turillazzi E, Fineschi V (2010) The timing of perinatal hypoxia/ischemia events in term neonates: a retrospective autopsy study. HSPs, ORP-150 and COX2 are reliable markers to classify acute, perinatal events. Diagn Pathol 5:49PubMedCentral CrossRef PubMed
  24.Kim TY, Kim E, Yoon SK, Yoon JB (2008) Herp enhances ER-associated protein degradation by recruiting ubiquilins. Biochem Biophys Res Commun 369(2):741–746CrossRef PubMed
  25.Apostolou A, Shen Y, Liang Y, Luo J, Fang S (2008) Armet, a UPR-upregulated protein, inhibits cell proliferation and ER stress-induced cell death. Exp Cell Res 314(13):2454–2467CrossRef PubMed
  26.Cai S, Bulus N, Fonseca-Siesser PM, Chen D, Hanks SK, Pozzi A, Zent R (2005) CD98 modulates integrin beta1 function in polarized epithelial cells. J Cell Sci 118(Pt 5):889–899CrossRef PubMed
  27.Oh-hashi K, Kanamori Y, Hirata Y, Kiuchi K (2014) Characterization of V-ATPase inhibitor-induced secretion of cysteine-rich with EGF-like domains 2. Cell Biol Toxicol 30(3):127–136CrossRef PubMed
  28.Hartley CL, Edwards S, Mullan L, Bell PA, Fresquet M, Boot-Handford RP, Briggs MD (2013) Armet/Manf and Creld2 are components of a specialized ER stress response provoked by inappropriate formation of disulphide bonds: implications for genetic skeletal diseases. Hum Mol Genet 22(25):5262–5275PubMedCentral CrossRef PubMed
  29.Fukuda S, Sumii M, Masuda Y, Takahashi M, Koike N, Teishima J, Yasumoto H, Itamoto T, Asahara T, Dohi K, Kamiya K (2001) Murine and human SDF2L1 is an endoplasmic reticulum stress-inducible gene and encodes a new member of the Pmt/rt protein family. Biochem Biophys Res Commun 280(1):407–414CrossRef PubMed
  30.Tiwari A, Schuiki I, Zhang L, Allister EM, Wheeler MB, Volchuk A (2013) SDF2L1 interacts with the ER-associated degradation machinery and retards the degradation of mutant proinsulin in pancreatic beta-cells. J Cell Sci 126(Pt 9):1962–1968CrossRef PubMed
  31.He YY, Liu CL, Li X, Zhong W, Li S, He KL, Wang LL (2014) Effects of PP1-12, a novel protein phosphatase-1 inhibitor, on ventricular function and remodeling after myocardial infarction in rats. J Cardiovasc Pharm 64(4):360–367CrossRef
  
• 作者单位：Chun-Lei Liu (1)
  Wu Zhong (2)
  Yun-Yun He (1)
  Xin Li (1)
  Song Li (1) (2)
  Kun-Lun He (1)
  
  1. Department of Geriatric Cardiology, The General Hospital of Chinese People’s Liberation Army, NO. 28, Fuxing Road, Haidian District, Beijing, 100853, China
  2. Beijing Institute of Pharmacology and Toxicology, NO. 27, Taiping Road, Haidian District, Beijing, 100850, China
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Biochemistry
  Medical Biochemistry
  Oncology
  Cardiology
  
• 出版者：Springer Netherlands
• ISSN：1573-4919

文摘

Tunicamycin (TM) is an inducer of endoplasmic reticulum (ER) stress. However, which genes related to ER stress was induced in cardiomyocytes on a genome-wide scale remains poorly understood. Salubrinal and its derivatives are ER stress inhibitors. However, the cellular protection mechanisms remain unresolved. Neonatal rat cardiomyocytes were cultured from ventricles of one-day-old Wistar rats. Cells were exposed to salubrinal, its derivatives (PP1-12, PP1-24) or vehicle followed by TM treatment at different times. Total RNA was isolated from cells for RNA-sequencing analysis. The expressions of 189, 182, 556, 860, and 1314 genes were changed in cells exposed to TM for 1, 3, 6, 12, and 24 h. Five well-known UPR genes (Hspa5, Hsp90b1, Calr, Ddit3, and Atf4) were significantly increased in a time-dependent manner. Six not well-known genes (Hyou1, Herpud1, Manf, Creld2, Sdf2l1, and Slc3a2) were highlighted to be involved in ER stress. Compared with TM-only treated cells, the expressions of 36 genes upregulated by TM and 74 genes downregulated by TM were reversed by salubrinal. In comparison, 121 genes upregulated by TM and 92 genes downregulated by TM were reversed by PP1-12. Most genes altered by salubrinal are in the category of transcription (1 h) and cell cycle (24 h). Most genes altered by PP1-12 are in the category of response to ER stress (3 h) and cell cycle (24 h). Our findings help elucidate the mechanism for TM treatment and may be useful for future drug screens involved in ER stress. Keywords Endoplasmic reticulum stress RNA-seq UPR Cardiomyopathy