Identification and Functional Characterization of Hypoxia-Induced Endoplasmic Reticulum Stress Regulating lncRNA (HypERlnc) in Pericytes

Circulation Research

Volumn 121, Issue 4, 2017, Pages 368-375

  Bischoff, Florian C ^a,b,d   Werner, Astrid ^a,b   John, David ^a,d   Boeckel, Jes Niels ^c,d   Melissari, Maria Theodora ^a   Grote, Phillip ^a   Glaser, Simone F ^a,b   Demolli, Shemsi ^a,d   Uchida, Shizuka ^a,d,e   Michalik, Katharina M ^a   Meder, Benjamin ^c,d   Katus, Hugo A ^c,d   Haas, Jan ^c,d   Chen, Wei ^d,f,g   Pullamsetti, Soni S ^h,i   Seeger, Werner ^h,i   Zeiher, Andreas M ^b,d   Dimmeler, Stefanie ^a,d   Zehendner, Christoph M ^a,b,d  

^a GOETHE UNIVERSITY MEDICAL SCHOOL   (Germany)

^b GOETHE UNIVERSITY   (Germany)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^e UNIVERSITY OF LOUISVILLE   (United States)

^f MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^g SOUTHERN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^h MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

ⁱ JUSTUS LIEBIG UNIVERSITY GIESSEN   (Germany)

Author keywords

cardiovascular diseases; heart diseases; pericytes; pulmonary heart disease; RNA, long noncoding

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; ALPHA SMOOTH MUSCLE ACTIN; DESMIN; GLUCOSE REGULATED PROTEIN 78; LONG UNTRANSLATED RNA; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PROTEIN IRE1; PROTEIN IRE1ALPHA; PROTEIN NG2; PROTEOGLYCAN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; CAPILLARY ENDOTHELIAL CELL; CARDIOVASCULAR DISEASE; CELL DEDIFFERENTIATION; CELL HYPOXIA; CELL PERMEABILIZATION; CELL PROLIFERATION; CELL VIABILITY; COCULTURE; CONTROLLED STUDY; DOWN REGULATION; ENDOPLASMIC RETICULUM STRESS; ENDOTHELIUM CELL; GENE EXPRESSION; GENE ONTOLOGY; GENE SILENCING; HEART FAILURE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; IN VITRO STUDY; MARKER GENE; PERICYTE; PRIORITY JOURNAL; PULMONARY HYPERTENSION; RNA SEQUENCE; TRANSCRIPTION INITIATION; UPREGULATION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; GENETICS; METABOLISM; MOUSE; NUCLEOTIDE SEQUENCE; PATHOLOGY; PHYSIOLOGY; RANDOMIZATION; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALS; BASE SEQUENCE; CELL HYPOXIA; COCULTURE TECHNIQUES; ENDOPLASMIC RETICULUM STRESS; ENDOTHELIAL CELLS; HEART FAILURE; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; HYPERTENSION, PULMONARY; MICE; MICE, INBRED C57BL; PERICYTES; RANDOM ALLOCATION; RNA, LONG NONCODING;

EID: 85020524679     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.116.310531     Document Type: Article

References (28)

1. Lindahl P, Johansson BR, Levéen P, Betsholtz C. Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science. 1997;277:242-245.
2. Bjarnegård M, Enge M, Norlin J, Gustafsdottir S, Fredriksson S, Abramsson A, Takemoto M, Gustafsson E, Fässler R, Betsholtz C. Endotheliumspecific ablation of PDGFB leads to pericyte loss and glomerular, cardiac and placental abnormalities. Development. 2004;131:1847-1857. doi: 10.1242/dev.01080.
3. Armulik A, Genové G, Mäe M, Nisancioglu MH, Wallgard E, Niaudet C, He L, Norlin J, Lindblom P, Strittmatter K, Johansson BR, Betsholtz C. Pericytes regulate the blood-brain barrier. Nature. 2010;468:557-561. doi: 10.1038/nature09522.
4. Göritz C, Dias DO, Tomilin N, Barbacid M, Shupliakov O, Frisén J. A pericyte origin of spinal cord scar tissue. Science. 2011;333:238-242. doi: 10.1126/science.1203165.
5. Zehendner CM, Sebastiani A, Hugonnet A, Bischoff F, Luhmann HJ, Thal SC. Traumatic brain injury results in rapid pericyte loss followed by reactive pericytosis in the cerebral cortex. Sci Rep. 2015;5:13497. doi: 10.1038/srep13497.
6. Ricard N, Tu L, Le Hiress M, Huertas A, Phan C, Thuillet R, Sattler C, Fadel E, Seferian A, Montani D, Dorfmüller P, Humbert M, Guignabert C. Increased pericyte coverage mediated by endothelial-derived fibroblast growth factor-2 and interleukin-6 is a source of smooth muscle-like cells in pulmonary hypertension. Circulation. 2014;129:1586-1597. doi: 10.1161/CIRCULATIONAHA.113.007469.
7. Uchida S, Dimmeler S. Long noncoding RNAs in cardiovascular diseases. Circ Res. 2015;116:737-750. doi: 10.1161/CIRCRESAHA.116.302521.
8. Boon RA, Jaé N, Holdt L, Dimmeler S. Long noncoding RNAs: from clinical genetics to therapeutic targets? J Am Coll Cardiol. 2016;67:1214-1226. doi: 10.1016/j.jacc.2015.12.051.
9. Michalik KM, You X, Manavski Y, Doddaballapur A, Zörnig M, Braun T, John D, Ponomareva Y, Chen W, Uchida S, Boon RA, Dimmeler S. Long noncoding RNA MALAT1 regulates endothelial cell function and vessel growth. Circ Res. 2014;114:1389-1397. doi: 10.1161/ CIRCRESAHA.114.303265.
10. Bell RD, Long X, Lin M, Bergmann JH, Nanda V, Cowan SL, Zhou Q, Han Y, Spector DL, Zheng D, Miano JM. Identification and initial functional characterization of a human vascular cell-enriched long noncoding RNA. Arterioscler Thromb Vasc Biol. 2014;34:1249-1259. doi: 10.1161/ ATVBAHA.114.303240.
11. Sallam T, Jones MC, Gilliland T, Zhang L, Wu X, Eskin A, Sandhu J, Casero D, Vallim TQ, Hong C, Katz M, Lee R, Whitelegge J, Tontonoz P. Feedback modulation of cholesterol metabolism by the lipid-responsive non-coding RNA LeXis. Nature. 2016;534:124-128. doi: 10.1038/ nature17674.
12. Viereck J, Kumarswamy R, Foinquinos A, et al. Long noncoding RNA Chast promotes cardiac remodeling. Sci Transl Med. 2016;8:326ra22. doi: 10.1126/scitranslmed.aaf1475.
13. Nees S, Weiss DR, Senftl A, Knott M, Förch S, Schnurr M, Weyrich P, Juchem G. Isolation, bulk cultivation, and characterization of coronary microvascular pericytes: the second most frequent myocardial cell type in vitro. Am J Physiol Heart Circ Physiol. 2012;302:H69-H84. doi: 10.1152/ ajpheart.00359.2011.
14. Lin J, Zhang X, Xue C, Zhang H, Shashaty MG, Gosai SJ, Meyer N, Grazioli A, Hinkle C, Caughey J, Li W, Susztak K, Gregory BD, Li M, Reilly MP. The long noncoding RNA landscape in hypoxic and inflammatory renal epithelial injury. Am J Physiol Renal Physiol. 2015;309:F901- F913. doi: 10.1152/ajprenal.00290.2015.
15. Yang L, Duff MO, Graveley BR, Carmichael GG, Chen LL. Genomewide characterization of non-polyadenylated RNAs. Genome Biol. 2011;12:R16. doi: 10.1186/gb-2011-12-2-r16.
16. Kassan M, Galán M, Partyka M, Saifudeen Z, Henrion D, Trebak M, Matrougui K. Endoplasmic reticulum stress is involved in cardiac damage and vascular endothelial dysfunction in hypertensive mice. Arterioscler Thromb Vasc Biol. 2012;32:1652-1661. doi: 10.1161/ ATVBAHA.112.249318.
17. Minamino T, Komuro I, Kitakaze M. Endoplasmic reticulum stress as a therapeutic target in cardiovascular disease. Circ Res. 2010;107:1071-1082. doi: 10.1161/CIRCRESAHA.110.227819.
18. Baumeister P, Luo S, Skarnes WC, Sui G, Seto E, Shi Y, Lee AS. Endoplasmic reticulum stress induction of the Grp78/BiP promoter: activating mechanisms mediated by YY1 and its interactive chromatin modifiers. Mol Cell Biol. 2005;25:4529-4540. doi: 10.1128/ MCB.25.11.4529-4540.2005.
19. Okada K, Minamino T, Tsukamoto Y, et al. Prolonged endoplasmic reticulum stress in hypertrophic and failing heart after aortic constriction: possible contribution of endoplasmic reticulum stress to cardiac myocyte apoptosis. Circulation. 2004;110:705-712. doi: 10.1161/01. CIR.0000137836.95625.D4.
20. Battson ML, Lee DM, Gentile CL. Endoplasmic reticulum stress and the development of endothelial dysfunction. Am J Physiol Heart Circ Physiol. 2017;312:H355-H367. doi: 10.1152/ajpheart.00437.2016.
21. Prola A, Silva JP, Guilbert A, et al. SIRT1 protects the heart from ER stress-induced cell death through eIF2α deacetylation. Cell Death Differ. 2017;24:343-356. doi: 10.1038/cdd.2016.138.
22. Kato M, Wang M, Chen Z, Bhatt K, Oh HJ, Lanting L, Deshpande S, Jia Y, Lai JY, O'Connor CL, Wu Y, Hodgin JB, Nelson RG, Bitzer M, Natarajan R. An endoplasmic reticulum stress-regulated lncRNA hosting a microRNA megacluster induces early features of diabetic nephropathy. Nat Commun. 2016;7:12864. doi: 10.1038/ncomms12864.
23. Chen RP, Huang ZL, Liu LX, Xiang MQ, Li GP, Feng JL, Liu B, Wu LF. Involvement of endoplasmic reticulum stress and p53 in lncRNA MEG3-induced human hepatoma HepG2 cell apoptosis. Oncol Rep. 2016;36:1649-1657. doi: 10.3892/or.2016.4919.
24. Su S, Liu J, He K, Zhang M, Feng C, Peng F, Li B, Xia X. Overexpression of the long noncoding RNA TUG1 protects against cold-induced injury of mouse livers by inhibiting apoptosis and inflammation. FEBS J. 2016;283:1261-1274. doi: 10.1111/febs.13660.
25. Bertolotti A, Zhang Y, Hendershot LM, Harding HP, Ron D. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol. 2000;2:326-332. doi: 10.1038/35014014.
26. Tsang KY, Chan D, Bateman JF, Cheah KS. In vivo cellular adaptation to ER stress: survival strategies with double-edged consequences. J Cell Sci. 2010;123:2145-2154. doi: 10.1242/jcs.068833.
27. Swayze EE, Siwkowski AM, Wancewicz EV, Migawa MT, Wyrzykiewicz TK, Hung G, Monia BP, Bennett CF. Antisense oligonucleotides containing locked nucleic acid improve potency but cause significant hepatotoxicity in animals. Nucleic Acids Res. 2007;35:687-700. doi: 10.1093/nar/ gkl1071.
28. Zhu M, Goetsch SC, Wang Z, Luo R, Hill JA, Schneider J, Morris SM Jr, Liu ZP. FoxO4 promotes early inflammatory response upon myocardial infarction via endothelial Arg1. Circ Res. 2015;117:967-977. doi: 10.1161/CIRCRESAHA.115.306919.