Ginkgolide K protects the heart against endoplasmic reticulum stress injury by activating the inositol-requiring enzyme 1α/X box-binding protein-1 pathway

British Journal of Pharmacology

Volumn , Issue , 2016, Pages 2402-2418

  Wang, Shoubao ^a,c   Wang, Zhenzhong ^b   Fan, Qiru ^b,d   Guo, Jing ^a   Galli, Gina ^a   Du, Guanhua ^c   Wang, Xin ^a   Xiao, Wei ^b  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b State Key Laboratory of New tech for Chinese Medicine Pharmaceutical Process   (China)

^c INSTITUTE OF MATERIA MEDICA   (China)

^d CHINA PHARMACEUTICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ACTIVATING TRANSCRIPTION FACTOR 6; APOPTOSIS SIGNAL REGULATING KINASE 1; BECLIN 1; CASPASE 3; CCAAT ENHANCER BINDING PROTEIN; CYTOCHROME C; GINKGOLIDE; GINKGOLIDE K; GLUCOSE REGULATED PROTEIN 78; HYDROGEN PEROXIDE; INOSITOL REQUIRING ENZYME 1 ALPHA; MICROTUBULE ASSOCIATED PROTEIN 1; MICROTUBULE ASSOCIATED PROTEIN 1 LIGHT CHAIN 3 TYPE 2; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN IRE1; PROTEIN P62; STRESS ACTIVATED PROTEIN KINASE; THAPSIGARGIN; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; TUNICAMYCIN; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1;

ACUTE HEART INFARCTION; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; CARDIAC MUSCLE CELL; CELL DEATH; CELL EXPANSION; CELL PROTECTION; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; DRUG EFFECT; DRUG MECHANISM; ECHOCARDIOGRAPHY; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HEART FUNCTION; HEART INFARCTION SIZE; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSMISSION ELECTRON MICROSCOPY; UBIQUITINATION; UNFOLDED PROTEIN RESPONSE;

EID: 84978791413     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.13516     Document Type: Article

References (60)

1. Alexander SPH, Fabbro D, Kelly E, Marrion N, Peters JA, Benson HE et al. (2015a). The Concise Guide to PHARMACOLOGY 2015/16: Enzymes. Br J Pharmacol 172: 6024–6109.
2. Alexander SPH, Kelly E, Marrion N, Peters JA, Benson HE, Faccenda E et al. (2015b). The Concise Guide to PHARMACOLOGY 2015/16: Overview. Br J Pharmacol 172: 5729–5143.
3. Amm I, Sommer T, Wolf DH (2014). Protein quality control and elimination of protein waste: the role of the ubiquitin-proteasome system. Biochim Biophys Acta 1843: 182–196.
4. Bouchecareilh M, Higa A, Fribourg S, Moenner M, Chevet E (2011). Peptides derived from the bifunctional kinase/RNase enzyme IRE1α modulate IRE1α activity and protect cells from endoplasmic reticulum stress. FASEB J 25: 3115–3129.
5. Bravo R, Parra V, Gatica D, Rodriguez AE, Torrealba N, Paredes F et al. (2013). Endoplasmic reticulum and the unfolded protein response: dynamics and metabolic integration. Int Rev Cell Mol Biol 301: 215–290.
6. Byrd AE, Brewer JW (2013). Micro(RNA)managing endoplasmic reticulum stress. IUBMB Life 65: 373–381.
7. Chen YN, Brandizzi F (2013). IRE1: ER stress sensor and cell fate executor. Trends Cell Biol 23: 547–555.
8. Chistiakov DA, Sobenin IA, Orekhov AN, Bobryshev YV (2014). Role of endoplasmic reticulum stress in atherosclerosis and diabetic macrovascular complications. Biomed Res Int 2014: 610140.
9. Christianson JC, Ye Y (2014). Cleaning up in the endoplasmic reticulum: ubiquitin in charge. Nat Struct Mol Biol 21: 325–335.
10. Curtis MJ, Bond RA, Spina D, Ahluwalia A, Alexander SP, Giembycz MA et al. (2015). Experimental design and analysis and their reporting: new guidance for publication in BJP. Br J Pharmacol 172: 3461–3471.
11. Dickhout JG, Carlisle RE, Austin RC (2011). Interrelationship between cardiac hypertrophy, heart failure, and chronic kidney disease: endoplasmic reticulum stress as a mediator of pathogenesis. Circ Res 108: 629–642.
12. DuRose JB, Tam AB, Niwa M (2006). Intrinsic capacities of molecular sensors of the unfolded protein response to sense alternate forms of endoplasmic reticulum stress. Mol Biol Cell 17: 3095–3107.
13. Fan ZY, Liu XG, Guo RZ, Dong X, Gao W, Li P et al. (2015). Pharmacokinetic studies of ginkgolide K in rat plasma and tissues after intravenous administration using ultra-high performance liquid chromatography–tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 988: 1–7.
14. Gao E, Lei YH, Shang X, Huang ZM, Zuo L, Boucher M et al. (2010). A novel and efficient model of coronary artery ligation and myocardial infarction in the mouse. Circ Res 107: 1445–1453.
15. Ghosh R, Wang L, Wang ES, Perera BG, Igbaria A, Morita S et al. (2014). Allosteric inhibition of the IRE1alpha RNase preserves cell viability and function during endoplasmic reticulum stress. Cell 158: 534–548.
16. Groenendyk J, Agellon LB, Michalak M (2013). Coping with endoplasmic reticulum stress in the cardiovascular system. Annu Rev Physiol 75: 49–67.
17. Han D, Lerner AG, Vande Walle L, Upton JP, Xu W, Hagen A et al. (2009). IRE1alpha kinase activation modes control alternate endoribonuclease outputs to determine divergent cell fates. Cell 138: 562–575.
18. Hollien J, Lin JH, Li H, Stevens N, Walter P, Weissman JS (2009). Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J Cell Biol 186: 323–331.
19. Hosoi T, Korematsu K, Horie N, Suezawa T, Okuma Y, Nomura Y et al. (2012). Inhibition of casein kinase 2 modulates XBP1–GRP78 arm of unfolded protein responses in cultured glial cells. PLoS One 7: e40144.
20. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG (2010). Animal research: reporting in vivo experiments: the ARRIVE guidelines. Br J Pharmacol 160: 1577–1579.
21. Kimura TE, Jin J, Zi M, Prehar S, Liu W, Oceandy D et al. (2010). Targeted deletion of the extracellular signal-regulated protein kinase 5 attenuates hypertrophic response and promotes pressure overload-induced apoptosis in the heart. Circ Res 106: 961–970.
22. Koltai M, Tosaki A, Hosford D, Braquet P (1989). Ginkgolide B protects isolated hearts against arrhythmias induced by ischemia but not reperfusion. Eur J Pharmacol 164: 293–302.
23. Lee AH, Iwakoshi NN, Glimcher LH (2003). XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol 23: 7448–7459.
24. Liu X, Yan Y, Bao L, Chen B, Zhao Y, Qi R (2014). Ginkgolide B inhibits platelet release by blocking Syk and p38 MAPK phosphorylation in thrombin-stimulated platelets. Thromb Res 134: 1066–1073.
25. Liu X, Zhao G, Yan Y, Bao L, Chen B, Qi R (2012). Ginkgolide B reduces atherogenesis and vascular inflammation in ApoE(−/−) mice. PLoS One 7: e36237.
26. Luo T, Kim JK, Chen B, Abdel-Latif A, Kitakaze M, Yan L (2015). Attenuation of ER stress prevents post-infarction-induced cardiac rupture and remodeling by modulating both cardiac apoptosis and fibrosis. Chem Biol Interact 225: 90–98.
27. Ma S, Liu H, Jiao H, Wang L, Chen L, Liang J et al. (2012a). Neuroprotective effect of ginkgolide K on glutamate-induced cytotoxicity in PC 12 cells via inhibition of ROS generation and Ca(2+) influx. Neurotoxicology 33: 59–69.
28. Ma S, Liu X, Xun Q, Zhang X (2014). Neuroprotective effect of ginkgolide K against H2O2-induced PC12 cell cytotoxicity by ameliorating mitochondrial dysfunction and oxidative stress. Biol Pharm Bull 37: 217–225.
29. Ma S, Yin H, Chen L, Liu H, Zhao M, Zhang X (2012b). Neuroprotective effect of ginkgolide K against acute ischemic stroke on middle cerebral ischemia occlusion in rats. J Nat Med 66: 25–31.
30. Maclennan KM, Darlington CL, Smith PF (2002). The CNS effects of Ginkgo biloba extracts and ginkgolide B. Prog Neurobiol 67: 235–257.
31. Margariti A, Li H, Chen T, Martin D, Vizcay-Barrena G, Alam S et al. (2013). XBP1 mRNA splicing triggers an autophagic response in endothelial cells through BECLIN-1 transcriptional activation. J Biol Chem 288: 859–872.
32. Maurel M, Dejeans N, Taouji S, Chevet E, Grosset CF (2013). MicroRNA-1291-mediated silencing of IRE1α enhances glypican-3 expression. RNA 19: 778–788.
33. McAlpine CS, Werstuck GH (2013). The development and progression of atherosclerosis: evidence supporting a role for endoplasmic reticulum (ER) stress signaling. Cardiovasc Hematol Disord Drug Targets 13: 158–164.
34. McGrath JC, Lilley E (2015). Implementing guidelines on reporting research using animals (ARRIVE etc.): new requirements for publication in BJP. Br J Pharmacol 172: 3189–3193.
35. Mendez R, Zheng Z, Fan Z, Rajagopalan S, Sun Q, Zhang K (2013). Exposure to fine airborne particulate matter induces macrophage infiltration, unfolded protein response, and lipid deposition in white adipose tissue. Am J Transl Res 5: 224–234.
36. Mitra A, Basak T, Datta K, Naskar S, Sengupta S, Sarkar S (2013). Role of alpha-crystallin B as a regulatory switch in modulating cardiomyocyte apoptosis by mitochondria or endoplasmic reticulum during cardiac hypertrophy and myocardial infarction. Cell Death Dis 4: e582.
37. Mizushima N, Yoshimori T (2007). How to interpret LC3 immunoblotting. Autophagy 3: 542–545.
38. Montes P, Ruiz-Sanchez E, Rojas C, Rojas P (2015). Ginkgo biloba Extract 761: a review of basic studies and potential clinical use in psychiatric disorders. CNS Neurol Disord Drug Targets 14: 132–149.
39. Nadanaka S, Okada T, Yoshida H, Mori K (2007). Role of disulfide bridges formed in the luminal domain of ATF6 in sensing endoplasmic reticulum stress. Mol Cell Biol 27: 1027–1043.
40. Oikawa D, Kimata Y, Kohno K, Iwawaki T (2009). Activation of mammalian IRE1alpha upon ER stress depends on dissociation of BiP rather than on direct interaction with unfolded proteins. Exp Cell Res 315: 2496–2504.
41. Oikawa D, Kitamura A, Kinjo M, Iwawaki T (2012). Direct association of unfolded proteins with mammalian ER stress sensor, IRE1beta. PLoS One 7: e51290.
42. Oono K, Yoneda T, Manabe T, Yamagishi S, Matsuda S, Hitomi J et al. (2004). JAB1 participates in unfolded protein responses by association and dissociation with IRE1. Neurochem Int 45: 765–772.
43. Pietri S, Maurelli E, Drieu K, Culcasi M (1997). Cardioprotective and anti-oxidant effects of the terpenoid constituents of Ginkgo biloba extract (EGb 761). J Mol Cell Cardiol 29: 733–742.
44. Reinstein E, Frentz S, Morgan T, Garcia-Minaur S, Leventer RJ, McGillivray G et al. (2013). Vascular and connective tissue anomalies associated with X-linked periventricular heterotopia due to mutations in filamin A. Eur J Hum Genet: EJHG 21: 494–502.
45. Southan C, Sharman JL, Benson HE, Faccenda E, Pawson AJ, Alexander SPH et al. (2016). The IUPHAR/BPS Guide to PHARMACOLOGY in 2016: towards curated quantitative interactions between 1300 protein targets and 6000 ligands. Nucl Acids Res 44 (Database Issue): D1054–D1068.
46. Sozen E, Karademir B, Ozer NK (2015). Basic mechanisms in endoplasmic reticulum stress and relation to cardiovascular diseases. Free Radic Biol Med 78: 30–41.
47. Su H, Wang X (2010). The ubiquitin-proteasome system in cardiac proteinopathy: a quality control perspective. Cardiovasc Res 85: 253–262.
48. Szegezdi E, Logue SE, Gorman AM, Samali A (2006). Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep 7: 880–885.
49. Tam AB, Koong AC, Niwa M (2014). Ire1 has distinct catalytic mechanisms for XBP1/HAC1 splicing and RIDD. Cell Rep 9: 850–858.
50. Tosaki A, Pali T, Droy-Lefaix MT (1996). Effects of Ginkgo biloba extract and preconditioning on the diabetic rat myocardium. Diabetologia 39: 1255–1262.
51. Tsukumo Y, Tomida A, Kitahara O, Nakamura Y, Asada S, Mori K et al. (2007). Nucleobindin 1 controls the unfolded protein response by inhibiting ATF6 activation. J Biol Chem 282: 29264–29272.
52. Varga E, Bodi A, Ferdinandy P, Droy-Lefaix MT, Blasig IE, Tosaki A (1999). The protective effect of EGb 761 in isolated ischemic/reperfused rat hearts: a link between cardiac function and nitric oxide production. J Cardiovasc Pharmacol 34: 711–717.
53. Vekich JA, Belmont PJ, Thuerauf DJ, Glembotski CC (2012). Protein disulfide isomerase-associated 6 is an ATF6-inducible ER stress response protein that protects cardiac myocytes from ischemia/reperfusion-mediated cell death. J Mol Cell Cardiol 53: 259–267.
54. Wang ZH, Liu JL, Wu L, Yu Z, Yang HT (2014). Concentration-dependent wrestling between detrimental and protective effects of H2O2 during myocardial ischemia/reperfusion. Cell Death Dis 5: e1297.
55. Wei J, Hendershot LM (1996). Protein folding and assembly in the endoplasmic reticulum. EXS 77: 41–55.
56. Wiseman RL, Zhang Y, Lee KP, Harding HP, Haynes CM, Price J et al. (2010). Flavonol activation defines an unanticipated ligand-binding site in the kinase-RNase domain of IRE1. Mol Cell 38: 291–304.
57. Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K (2001). XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107: 881–891.
58. Zhang L, Chen X, Sharma P, Moon M, Sheftel AD, Dawood F et al. (2014). HACE1-dependent protein degradation provides cardiac protection in response to haemodynamic stress. Nat Commun 5: 3430.
59. Zhang S, Chen B, Wu W, Bao L, Qi R (2011). Ginkgolide B reduces inflammatory protein expression in oxidized low-density lipoprotein-stimulated human vascular endothelial cells. J Cardiovasc Pharmacol 57: 721–727.
60. Zhao X, Yao H, Yin HL, Zhu QL, Sun JL, Ma W et al. (2013). Ginkgo biloba extract and ginkgolide antiarrhythmic potential by targeting hERG and ICa-L channel. J Pharmacol Sci 123: 318–327.