Salidroside stimulates mitochondrial biogenesis and protects against H 2O2-induced endothelial dysfunction

Oxidative Medicine and Cellular Longevity

Volumn 2014, Issue , 2014, Pages

  Xing, Shasha ^a,b   Yang, Xiaoyan ^a,b   Li, Wenjing ^a,b   Bian, Fang ^a,b   Wu, Dan ^a,b   Chi, Jiangyang ^a,b   Xu, Gao ^a,b   Zhang, Yonghui ^a,b   Jin, Si ^a,b  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b Key Laboratory for Drug Target Researches and Pharmacodynamic Evaluation of Hubei Province   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANTS; CYTOLOGY; ENDOTHELIAL CELLS; NITRIC OXIDE; OXYGEN; TRANSCRIPTION FACTORS;

ENDOTHELIAL DYSFUNCTION; ENDOTHELIAL NITRIC-OXIDE SYNTHASE (ENOS); HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; MITOCHONDRIAL BIOGENESIS; MITOCHONDRIAL DYSFUNCTION; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL TRANSCRIPTION FACTOR; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR;

MITOCHONDRIA;

ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUCOSIDE; HYDROGEN PEROXIDE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PHENOL DERIVATIVE; PPARGC1A PROTEIN, RAT; PROTEIN KINASE B; SALIDROSIDE; TRANSCRIPTION FACTOR;

ANIMAL; ANTAGONISTS AND INHIBITORS; AORTA; CELL CULTURE; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; HUMAN; METABOLISM; MITOCHONDRION; RAT; RHODIOLA; TOXICITY; UMBILICAL VEIN ENDOTHELIAL CELL; WISTAR RAT;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; AORTA; CELL SURVIVAL; CELLS, CULTURED; GLUCOSIDES; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; HYDROGEN PEROXIDE; MITOCHONDRIA; NF-KAPPA B; NITRIC OXIDE SYNTHASE TYPE III; PHENOLS; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, WISTAR; RHODIOLA; TRANSCRIPTION FACTORS;

EID: 84901380033     PISSN: 19420900     EISSN: 19420994     Source Type: Journal    
DOI: 10.1155/2014/904834     Document Type: Article

References (80)

1. Makarenko V. V., Usatyuk P. V., Yuan G., Lee M. M., Nanduri J., Natarajan V., Kumar G. K., Prabhakar N. R., Intermittent hypoxia-induced Endothelial barrier Dysfunction requires ROS-dependent MAP kinase activation. American Journal of Physiology Cell Physiology 2014 10.1152/ajpcell.00313.2013
2. Hermida N., Balligand J. L., Low-density lipoprotein-cholesterol-induced endothelial dysfunction and oxidative stress: the role of statins. Antioxidants & Redox Signaling 2013 20 8 1216 1237 10.1089/ars.2013.5537
3. Wang S., Zhang M., Liang B., Xu J., Xie Z., Liu C., Viollet B., Yan D., Zou M.-H., AMPK α 2 deletion causes aberrant expression and activation of NAD(P)H oxidase and consequent endothelial dysfunction in vivo: role of 26S proteasomes. Circulation Research 2010 106 6 1117 1128 2-s2.0-77950989801 10.1161/CIRCRESAHA.109.212530
4. Sena C. M., Pereira A. M., Seica R., Endothelial dysfunction-a major mediator of diabetic vascular disease. Biochimica et Biophysica Acta 2013 1832 12 2216 2231
5. Moens A. L., Kietadisorn R., Lin J. Y., Kass D., Targeting endothelial and myocardial dysfunction with tetrahydrobiopterin. Journal of Molecular and Cellular Cardiology 2011 51 4 559 563 2-s2.0-79960803194 10.1016/j.yjmcc.2011. 03.009
6. Dromparis P., Michelakis E. D., Mitochondria in vascular health and disease. Annual Review of Physiology 2013 75 95 126
7. Marzetti E., Csiszar A., Dutta D., Balagopal G., Calvani R., Leeuwenburgh C., Role of mitochondrial dysfunction and altered autophagy in cardiovascular aging and disease: from mechanisms to therapeutics. American Journal of Physiology-Heart and Circulatory Physiology 2013 305 4 H459 H476
8. Mercer J. R., Mitochondrial bioenergetics and therapeutic intervention in cardiovascular disease. Pharmacology & Therapeutics 2014 141 1 13 20
9. Poyton R. O., Ball K. A., Castello P. R., Mitochondrial generation of free radicals and hypoxic signaling. Trends in Endocrinology and Metabolism 2009 20 7 332 340 2-s2.0-69849097192 10.1016/j.tem.2009.04.001
10. Thomas S. R., Witting P. K., Drummond G. R., Redox control of endothelial function and dysfunction: molecular mechanisms and therapeutic opportunities. Antioxidants & Redox Signaling 2008 10 10 1713 1765 2-s2.0-49849084827 10.1089/ars.2008.2027
11. Sorbara M. T., Girardin S. E., Mitochondrial ROS fuel the inflammasome. Cell Research 2011 21 4 558 560 2-s2.0-79954421862 10.1038/cr.2011.20
12. Banfi C., Brioschi M., Barbieri S. S., Eligini S., Barcella S., Tremoli E., Colli S., Mussoni L., Mitochondrial reactive oxygen species: a common pathway for PAR1- and PAR2-mediated tissue factor induction in human endothelial cells. Journal of Thrombosis and Haemostasis 2009 7 1 206 216 2-s2.0-57749187104 10.1111/j.1538-7836.2008.03204.x
13. 2 production promotes endothelial NF- B activation in aged rat arteries. American Journal of Physiology-Heart and Circulatory Physiology 2007 293 1 H37 H47 2-s2.0-34547178903 10.1152/ajpheart.01346.2006 (Pubitemid 47108162)
14. Addabbo F., Ratliff B., Park H.-C., Kuo M.-C., Ungvari Z., Ciszar A., Krasnikof B., Sodhi K., Zhang F., Nasjletti A., Goligorsky M. S., The krebs cycle and mitochondrial mass are early victims of endothelial dysfunction: proteomic approach. American Journal of Pathology 2009 174 1 34 43 2-s2.0-58249098409 10.2353/ajpath.2009.080650
15. Davidson S. M., Duchen M. R., Endothelial mitochondria: contributing to vascular function and disease. Circulation Research 2007 100 8 1128 1141 2-s2.0-34247598856 10.1161/01.RES.0000261970.18328.1d (Pubitemid 46684126)
16. Kluge M. A., Fetterman J. L., Vita J. A., Mitochondria and endothelial function. Circulation Research 2013 112 8 1171 1188
17. Krishnan K. J., Reeve A. K., Samuels D. C., Chinnery P. F., Blackwood J. K., Taylor R. W., Wanrooij S., Spelbrink J. N., Lightowlers R. N., Turnbull D. M., What causes mitochondrial DNA deletions in human cells? Nature Genetics 2008 40 3 275 279 2-s2.0-39749124232 10.1038/ng.f.94 (Pubitemid 351311775)
18. Rosca M. G., Hoppel C. L., Mitochondria in heart failure. Cardiovascular Research 2010 88 1 40 50 2-s2.0-77956586695 10.1093/cvr/cvq240
19. Halestrap A. P., Calcium, mitochondria and reperfusion injury: a pore way to die. Biochemical Society Transactions 2006 34, part 2 232 237 2-s2.0-33645994183 10.1042/BST20060232
20. Gutierrez J., Ballinger S. W., Darley-Usmar V. M., Landar A., Free radicals, mitochondria, and oxidized lipids: the emerging role in signal transduction in vascular cells. Circulation Research 2006 99 9 924 932 2-s2.0-33750475625 10.1161/01.RES.0000248212.86638.e9 (Pubitemid 44657795)
21. Ungvari Z., Labinskyy N., Gupte S., Chander P. N., Edwards J. G., Csiszar A., Dysregulation of mitochondrial biogenesis in vascular endothelial and smooth muscle cells of aged rats. American Journal of Physiology-Heart and Circulatory Physiology 2008 294 5 H2121 H2128 2-s2.0-44949220235 10.1152/ajpheart.00012.2008
22. Blake R., Trounce I. A., Mitochondrial dysfunction and complications associated with diabetes. Biochimica et Biophysica Acta 2014 1840 4 1404 1412 10.1016/j.bbagen.2013.11.007
23. Scarpulla R. C., Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network. Biochimica et Biophysica Acta 2011 1813 7 1269 1278 2-s2.0-79957960940 10.1016/j.bbamcr.2010.09.019
24. Patten I. S., Arany Z., PGC-1 coactivators in the cardiovascular system. Trends in Endocrinology and Metabolism 2012 23 2 90 97 2-s2.0-84856470679 10.1016/j.tem.2011.09.007
25. Scarpulla R. C., Nuclear control of respiratory chain expression by nuclear respiratory factors and PGC-1-related coactivator. Annals of the New York Academy of Sciences 2008 1147 321 334 2-s2.0-57649148823 10.1196/annals.1427.006
26. Santos J. M., Tewari S., Goldberg A. F. X., Kowluru R. A., Mitochondrial biogenesis and the development of diabetic retinopathy. Free Radical Biology and Medicine 2011 51 10 1849 1860 2-s2.0-80054717662 10.1016/j.freeradbiomed.2011. 08.017
27. Xu Q., Xia P., Li X., Wang W., Liu Z., Gao X., Tetramethylpyrazine ameliorates high glucose-induced endothelial dysfunction by increasing mitochondrial biogenesis. PLoS ONE 2014 9 2 e88243
28. Panossian A., Wagner H., Stimulating effect of adaptogens: an overview with particular reference to their efficacy following single dose administration. Phytotherapy Research 2005 19 10 819 838 2-s2.0-27944504357 10.1002/ptr.1751 (Pubitemid 41670526)
29. Qian E. W., Ge D. T., Kong S.-K., Salidroside promotes erythropoiesis and protects erythroblasts against oxidative stress by up-regulating glutathione peroxidase and thioredoxin. Journal of Ethnopharmacology 2011 133 2 308 314 2-s2.0-78651400173 10.1016/j.jep.2010.09.025
30. Li X., Sipple J., Pang Q., Du W., Salidroside stimulates DNA repair enzyme Parp-1 activity in mouse HSC maintenance. Blood 2012 119 18 4162 4173
31. Leung S. B., Zhang H., Lau C. W., Huang Y., Lin Z., Salidroside improves homocysteine-induced endothelial dysfunction by reducing oxidative stress. Evidence-Based Complementary and Alternative Medicine 2013 2013 8 10.1155/2013/679635 679635
32. Williams J. R., The declaration of Helsinki and public health. Bulletin of the World Health Organization 2008 86 650 652 10.2471/BLT.08.050955
33. Jaffe E. A., Nachman R. L., Becker C. G., Minick C. R., Culture of human endothelial cells derived from umbilical veins. Identification by morphologic and immunologic criteria. The Journal of Clinical Investigation 1973 52 11 2745 2756 2-s2.0-0015822275
34. Bai Y., Suzuki A. K., Sagai M., The cytotoxic effects of diesel exhaust particles on human pulmonary artery endothelial cells in vitro: role of active oxygen species. Free Radical Biology and Medicine 2001 30 5 555 562 2-s2.0-0035283005 10.1016/S0891-5849(00)00499-8 (Pubitemid 32162962)
35. Song S., Zhou F., Chen W. R., Xing D., PDT-induced HSP70 externalization up-regulates NO production via TLR2 signal pathway in macrophages. FEBS Letters 2013 587 2 128 135
36. Dasuri K., Ebenezer P., Fernandez-Kim S. O., Zhang L., Gao Z., Bruce-Keller A. J., Freeman L. R., Keller J. N., Role of physiological levels of 4-hydroxynonenal on adipocyte biology: implications for obesity and metabolic syndrome. Free Radical Research 2013 47 1 8 19
37. Jin S., Lu D., Ye S., Ye H., Zhu L., Feng Z., Liu S., Wang D., Hu Q., A simplified probe preparation for ELISA-based NF- B activity assay. Journal of Biochemical and Biophysical Methods 2005 65 1 20 29 2-s2.0-27644558279 10.1016/j.jbbm.2005.08.006 (Pubitemid 41562867)
38. Zhang Y., Yang X., Bian F., TNF- α promotes early atherosclerosis by increasing transcytosis of LDL across endothelial cells: crosstalk between NF- B and PPAR- γ Journal of Molecular and Cellular Cardiology 2014 72 85 94
39. 2/NF- B pathway in bronchial epithelial cells. American Journal of Physiology-Cell Physiology 2011 301 1 C171 C180 2-s2.0-79959816106 10.1152/ajpcell.00363.2010
40. Zhou R., Yazdi A. S., Menu P., Tschopp J., A role for mitochondria in NLRP3 inflammasome activation. Nature 2011 469 7329 221 226 2-s2.0-78651393239 10.1038/nature09663
41. Parra V., Eisner V., Chiong M., Criollo A., Moraga F., Garcia A., Härtel S., Jaimovich E., Zorzano A., Hidalgo C., Lavandero S., Changes in mitochondrial dynamics during ceramide-induced cardiomyocyte early apoptosis. Cardiovascular Research 2008 77 2 387 397 2-s2.0-38849095253 10.1093/cvr/cvm029 (Pubitemid 351197639)
42. Reers M., Smith T. W., Chen L. B., J-aggregate formation of a carbocyanine as a quantitative fluorescent indicator of membrane potential. Biochemistry 1991 30 18 4480 4486 2-s2.0-0025830873
43. Collins T., Biology of disease: endothelial nuclear factor- B and the initiation of the atherosclerotic lesion. Laboratory Investigation 1993 68 5 499 508 2-s2.0-0027193894 (Pubitemid 23171848)
44. Schulz E., Gori T., Münzel T., Oxidative stress and endothelial dysfunction in hypertension. Hypertension Research 2011 34 6 665 673 2-s2.0-79958132625 10.1038/hr.2011.39
45. Giacco F., Brownlee M., Oxidative stress and diabetic complications. Circulation Research 2010 107 9 1058 1070 2-s2.0-78349297565 10.1161/CIRCRESAHA.110.223545
46. Briasoulis A., Tousoulis D., Androulakis E. S., Papageorgiou N., Latsios G., Stefanadis C., Endothelial dysfunction and atherosclerosis: focus on novel therapeutic approaches. Recent Patents on Cardiovascular Drug Discovery 2012 7 1 21 32 2-s2.0-84857751950 10.2174/157489012799362386
47. Xu M. C., Shi H. M., Wang H., Gao X. F., Salidroside protects against hydrogen peroxide-induced injury in HUVECs via the regulation of REDD1 and mTOR activation. Molecular Medicine Reports 2013 8 1 147 153
48. Yung L. M., Leung F. P., Yao X., Chen Z.-Y., Huang Y., Reactive oxygen species in vascular wall. Cardiovascular and Hematological Disorders-Drug Targets 2006 6 1 1 19 2-s2.0-33744501251 (Pubitemid 43803123)
49. Félétou M., Vanhoutte P. M., Endothelial dysfunction: a multifaceted disorder. American Journal of Physiology-Heart and Circulatory Physiology 2006 291 3 H985 H1002 2-s2.0-33748421398 10.1152/ajpheart.00292.2006 (Pubitemid 44343640)
50. Fujimoto S., Asano T., Sakai M., Sakurai K., Takagi D., Yoshimoto N., Itoh T., Mechanisms of hydrogen peroxide-induced relaxation in rabbit mesenteric small artery. European Journal of Pharmacology 2001 412 3 291 300 2-s2.0-0035793326 10.1016/S0014-2999(00)00940-7 (Pubitemid 32144945)
51. 2+ and other cellular metabolites. General Pharmacology 1999 33 4 325 336 2-s2.0-0032827847 10.1016/S0306-3623(99)00019-1 (Pubitemid 29465739)
52. Ellis A., Pannirselvam M., Anderson T. J., Triggle C. R., Catalase has negligible inhibitory effects on endothelium-dependent relaxations in mouse isolated aorta and small mesenteric artery. British Journal of Pharmacology 2003 140 7 1193 1200 2-s2.0-0345797830 10.1038/sj.bjp.0705549 (Pubitemid 38117423)
53. Zembowicz A., Hatchett R. J., Jakubowski A. M., Gryglewski R. J., Involvement of nitric oxide in the endothelium-dependent relaxation induced by hydrogen peroxide in the rabbit aorta. British Journal of Pharmacology 1993 110 1 151 158 2-s2.0-0027281566 (Pubitemid 23257772)
54. Cai H., Li Z., Dikalov S., Holland S. M., Hwang J., Jo H., Dudley S. C. Jr., Harrison D. G., NAD(P)H oxidase-derived hydrogen peroxide mediates endothelial nitric oxide production in response to angiotensin II. The Journal of Biological Chemistry 2002 277 50 48311 48317 2-s2.0-0037073677 10.1074/jbc.M208884200 (Pubitemid 35470785)
55. Wong C. M., Yung L. M., Leung F. P., Tsang S.-Y., Au C. L., Chen Z.-Y., Yao X., Cheng C. H. K., Lau C.-W., Gollasch M., Huang Y., Raloxifene protects endothelial cell function against oxidative stress. British Journal of Pharmacology 2008 155 3 326 334 2-s2.0-52949136618 10.1038/bjp.2008.262
56. Dimmeler S., Zeiher A. M., Nitric oxide-an endothelial cell survival factor. Cell Death and Differentiation 1999 6 10 964 968 2-s2.0-0032750425 (Pubitemid 29520797)
57. Wong W. T., Wong S. L., Tian X. Y., Huang Y., Endothelial dysfunction: the common consequence in diabetes and hypertension. Journal of Cardiovascular Pharmacology 2010 55 4 300 307 2-s2.0-77951737282 10.1097/FJC.0b013e3181d7671c
58. Niu X.-F., Smith C. W., Kubes P., Intracellular oxidative stress induced by nitric oxide synthesis inhibition increases endothelial cell adhesion to neutrophils. Circulation Research 1994 74 6 1133 1140 2-s2.0-0028304674 (Pubitemid 24176908)
59. Cai H., Li Z., Davis M. E., Kanner W., Harrison D. G., Dudley S. C. Jr., Akt-dependent phosphorylation of serine 1179 and mitogen-activated protein kinase kinase/extracellular signal-regulated kinase 1/2 cooperatively mediate activation of the endothelial nitric-oxide synthase by hydrogen peroxide. Molecular Pharmacology 2003 63 2 325 331 2-s2.0-0037310339 10.1124/mol.63.2.325 (Pubitemid 36158367)
60. Xia Z., Liu M., Wu Y., Sharma V., Luo T., Ouyang J., McNeill J. H., N-acetylcysteine attenuates TNF- α -induced human vascular endothelial cell apoptosis and restores eNOS expression. European Journal of Pharmacology 2006 550 1-3 134 142 2-s2.0-33749992417 10.1016/j.ejphar.2006.08.044 (Pubitemid 44572264)
61. Mohan S., Hamuro M., Sorescu G. P., Koyoma K., Sprague E. A., Jo H., Valente A. J., Prihoda T. J., Natarajan M., I B α -dependent regulation of low-shear flow-induced NF- B activity: role of nitric oxide. American Journal of Physiology-Cell Physiology 2003 284 4 C1039 C1047 2-s2.0-0037376624 (Pubitemid 36336960)
62. Matthews J. R., Botting C. H., Panico M., Morris H. R., Hay R. T., Inhibition of NF- B DNA binding by nitric oxide. Nucleic Acids Research 1996 24 12 2236 2242 2-s2.0-0029666293 10.1093/nar/24.12.2236 (Pubitemid 26193585)
63. Pineda-Molina E., Klatt P., Vázquez J., Marina A., García de Lacoba M., Pérez-Sala D., Lamas S., Glutathionylation of the p50 subunit of NF- B: a mechanism for redox-induced inhibition of DNA binding. Biochemistry 2001 40 47 14134 14142 2-s2.0-0035960648 10.1021/bi011459o (Pubitemid 33081616)
64. 2 and TNF α. Differences between in vivo and in vitro effects. FEBS Letters 1997 416 3 381 386 2-s2.0-0030692009 10.1016/S0014-5793(97)01244-1 (Pubitemid 27475402)
65. Oliveira-Marques V., Marinho H. S., Cyrne L., Antunes F., Role of hydrogen peroxide in NF- B activation: from inducer to modulator. Antioxidants & Redox Signaling 2009 11 9 2223 2243 2-s2.0-68949215885 10.1089/ars.2009.2601
66. Hasegawa Y., Saito T., Ogihara T., Ishigaki Y., Yamada T., Imai J., Uno K., Gao J., Kaneko K., Shimosawa T., Asano T., Fujita T., Oka Y., Katagiri H., Blockade of the nuclear factor- B pathway in the endothelium prevents insulin resistance and prolongs life spans. Circulation 2012 125 9 1122 1133 2-s2.0-84857914467 10.1161/CIRCULATIONAHA.111.054346
67. Nisoli E., Carruba M. O., Nitric oxide and mitochondrial biogenesis. Journal of Cell Science 2006 119, part 14 2855 2862 2-s2.0-33746841367 10.1242/jcs.03062 (Pubitemid 44177863)
68. Nisoli E., Clementi E., Paolucci C., Cozzi V., Tonello C., Sciorati C., Bracale R., Valerio A., Francolini M., Moncada S., Carruba M. O., Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science 2003 299 5608 896 899 2-s2.0-0347579845 10.1126/science.1079368 (Pubitemid 36182449)
69. Álvarez-Guardia D., Palomer X., Coll T., Davidson M. M., Chan T. O., Feldman A. M., Laguna J. C., Vázquez-Carrera M., The p65 subunit of NF-B binds to PGC-1, linking inflammation and metabolic disturbances in cardiac cells. Cardiovascular Research 2010 87 3 449 458 2-s2.0-77954775834 10.1093/cvr/cvq080
70. Kim H.-J., Park K.-G., Yoo E.-K., Kim Y.-H., Kim Y.-N., Kim H.-S., Kim H. T., Park J.-Y., Lee K.-U., Jang W. G., Kim J.-G., Kim B.-W., Lee I.-K., Effects of PGC-1 α on TNF- α -induced MCP-1 and VCAM-1 expression and NF- B activation in human aortic smooth muscle and endothelial cells. Antioxidants & Redox Signaling 2007 9 3 301 307 2-s2.0-33846463967 10.1089/ars.2006.1456 (Pubitemid 46150964)
71. Csiszar A., Labinskyy N., Pinto J. T., Ballabh P., Zhang H., Losonczy G., Pearson K., De Cabo R., Pacher P., Zhang C., Ungvari Z., Resveratrol induces mitochondrial biogenesis in endothelial cells. American Journal of Physiology-Heart and Circulatory Physiology 2009 297 1 H13 H20 2-s2.0-67650091375 10.1152/ajpheart.00368.2009
72. Schilling J., Lai L., Sambandam N., Dey C. E., Leone T. C., Kelly D. P., Toll-like receptor-mediated inflammatory signaling reprograms cardiac energy metabolism by repressing peroxisome proliferator-activated receptor γ coactivator-1 signaling. Circulation: Heart Failure 2011 4 4 474 482 2-s2.0-80052785073 10.1161/CIRCHEARTFAILURE.110.959833
73. Won J. C., Park J.-Y., Kim Y. M., Koh E. H., Seol S., Jeon B. H., Han J., Kim J. R., Park T.-S., Choi C. S., Lee W. J., Kim M.-S., Lee I.-K., Youn J. H., Lee K.-U., Peroxisome proliferator-activated receptor- γ coactivator 1- α overexpression prevents endothelial apoptosis by increasing ATP/ADP translocase activity. Arteriosclerosis, Thrombosis, and Vascular Biology 2010 30 2 290 297 2-s2.0-75149184537 10.1161/ATVBAHA.109.198721
74. Valle I., Álvarez-Barrientos A., Arza E., Lamas S., Monsalve M., PGC-1 α regulates the mitochondrial antioxidant defense system in vascular endothelial cells. Cardiovascular Research 2005 66 3 562 573 2-s2.0-19444365211 10.1016/j.cardiores.2005.01.026 (Pubitemid 40725768)
75. Ali F., Ali N. S., Bauer A., Boyle J. J., Hamdulay S. S., Haskard D. O., Randi A. M., Mason J. C., PPAR σ and PGC1 α act cooperatively to induce haem oxygenase-1 and enhance vascular endothelial cell resistance to stress. Cardiovascular Research 2010 85 4 701 710 2-s2.0-76749083354 10.1093/cvr/cvp365
76. Cai H., Hydrogen peroxide regulation of endothelial function: origins, mechanisms, and consequences. Cardiovascular Research 2005 68 1 26 36 2-s2.0-24344499139 10.1016/j.cardiores.2005.06.021 (Pubitemid 41253553)
77. Liu Y.-M., Jiang B., Bao Y.-M., An L.-J., Protocatechuic acid inhibits apoptosis by mitochondrial dysfunction in rotenone-induced PC12 cells. Toxicology in Vitro 2008 22 2 430 437 2-s2.0-38549155074 10.1016/j.tiv.2007.10. 012
78. Huang H., Manton K. G., The role of oxidative damage in mitochondria during aging: a review. Frontiers in Bioscience 2004 9 1100 1117 2-s2.0-2442685843 (Pubitemid 39060832)
79. Yakes F. M., van Houten B., Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proceedings of the National Academy of Sciences of the United States of America 1997 94 2 514 519 2-s2.0-0031032817 10.1073/pnas.94.2.514 (Pubitemid 27053665)
80. Hill B. G., Benavides G. A., Lancaster J. R. Jr., Ballinger S., Dell'Italia L., Jianhua Z., Darley-Usmar V. M., Integration of cellular bioenergetics with mitochondrial quality control and autophagy. Biological Chemistry 2012 393 12 1485 1512