Mitochondria and aging in the vascular system

Journal of Molecular Medicine

Volumn 88, Issue 10, 2010, Pages 1021-1027

  Ungvari, Zoltan ^a   Sonntag, William E ^a   Csiszar, Anna ^a  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

Author keywords

Aging; Endothelium; Mitochondria

Indexed keywords

ANTIOXIDANT; GROWTH HORMONE; REACTIVE OXYGEN METABOLITE; SOMATOMEDIN C;

AGING; APOPTOSIS; CALORIC RESTRICTION; CARDIOVASCULAR SYSTEM; CHRONIC INFLAMMATION; MITOCHONDRION; OXIDATIVE STRESS; REVIEW; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIUM; VASCULITIS;

AGING; BLOOD VESSELS; ENDOTHELIUM; HUMANS; INFLAMMATION; MITOCHONDRIA; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; VASCULAR DISEASES;

EID: 78149416510     PISSN: 09462716     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00109-010-0667-5     Document Type: Review

References (61)

1. D Harman 1972 The biologic clock: the mitochondria? J Am Geriatr Soc 20 145 147 1:STN:280:DyaE387lsVCmug%3D%3D 5016631
2. A Csiszar M Wang EG Lakatta ZI Ungvari 2008 Inflammation and endothelial dysfunction during aging: role of NF-{kappa}B J Appl Physiol 105 1333 1341 10.1152/japplphysiol.90470.2008 1:CAS:528:DC%2BD1cXht1KqurzK 10.1152/japplphysiol.90470.2008 18599677
3. ZI Ungvari N Labinskyy SA Gupte PN Chander JG Edwards A Csiszar 2008 Dysregulation of mitochondrial biogenesis in vascular endothelial and smooth muscle cells of aged rats Am J Physiol Heart Circ Physiol 294 H2121 H2128 1:CAS:528:DC%2BD1cXmtVWgurk%3D 10.1152/ajpheart.00012.2008 18326800
4. ZI Ungvari Z Orosz N Labinskyy A Rivera Z Xiangmin KE Smith A Csiszar 2007 Increased mitochondrial H2O2 production promotes endothelial NF-kB activation in aged rat arteries Am J Physiol Heart Circ Physiol 293 H37 H47 1:CAS:528:DC%2BD2sXovVyitLo%3D 10.1152/ajpheart.01346.2006 17416599 (Pubitemid 47108162)
5. A Csiszar Z Ungvari A Koller JG Edwards G Kaley 2003 Aging-induced proinflammatory shift in cytokine expression profile in rat coronary arteries FASEB J 17 1183 1185 1:CAS:528:DC%2BD3sXktl2jsL8%3D 12709402
6. DF Dai PS Rabinovitch 2009 Cardiac aging in mice and humans: the role of mitochondrial oxidative stress Trends Cardiovasc Med 19 213 220 10.1016/j.tcm.2009.12.004 1:CAS:528:DC%2BC3cXksFGms7c%3D 10.1016/j.tcm.2009.12. 004 20382344
7. S Phaneuf C Leeuwenburgh 2002 Cytochrome c release from mitochondria in the aging heart: a possible mechanism for apoptosis with age Am J Physiol Regul Integr Comp Physiol 282 R423 R430 1:CAS:528:DC%2BD38XhtFCqurs%3D 11792651
8. WE Sonntag CD Lynch PT Cooney PM Hutchins 1997 Decreases in cerebral microvasculature with age are associated with the decline in growth hormone and insulin-like growth factor 1 Endocrinology 138 3515 3520 1:CAS:528: DyaK2sXkslSgsbo%3D 10.1210/en.138.8.3515 9231806 (Pubitemid 27345707)
9. Q Gao X Zhao M Ahmad MS Wolin 2009 Mitochondrial-derived hydrogen peroxide inhibits relaxation of bovine coronary arterial smooth muscle to hypoxia through stimulation of ERK MAP kinase Am J Physiol Heart Circ Physiol 297 H2262 H2269 10.1152/ajpheart.00817.2009 1:CAS:528:DC%2BD1MXhsFOltLfO 10.1152/ajpheart.00817.2009 19855056
10. M Wang RE Monticone EG Lakatta 2010 Arterial aging: a journey into subclinical arterial disease Curr Opin Nephrol Hypertens 19 201 207 10.1097/MNH.0b013e3283361c0b 1:CAS:528:DC%2BC3cXht1CnurjO 10.1097/MNH. 0b013e3283361c0b 20040868
11. B van der Loo R Labugger JN Skepper M Bachschmid J Kilo JM Powell M Palacios-Callender JD Erusalimsky T Quaschning T Malinski D Gygi V Ullrich TF Lüscher 2000 Enhanced peroxynitrite formation is associated with vascular aging J Exp Med 192 1731 1744 10.1084/jem.192.12.1731 11120770 (Pubitemid 32049766)
12. A Csiszar N Labinskyy R Jimenez JT Pinto P Ballabh G Losonczy KJ Pearson R de Cabo Z Ungvari 2009 Anti-oxidative and anti-inflammatory vasoprotective effects of caloric restriction in aging: role of circulating factors and SIRT1 Mech Ageing Dev 10.1016/j.mad.2009.06.004 19549533
13. Z Ungvari C Parrado-Fernandez A Csiszar R de Cabo 2008 Mechanisms underlying caloric restriction and lifespan regulation: implications for vascular aging Circ Res 102 519 528 1:CAS:528:DC%2BD1cXjtVeru70%3D 10.1161/CIRCRESAHA.107.168369 18340017 (Pubitemid 351416750)
14. C Napoli I Martin-Padura F de Nigris M Giorgio G Mansueto P Somma M Condorelli G Sica G De Rosa P Pelicci 2003 Deletion of the p66Shc longevity gene reduces systemic and tissue oxidative stress, vascular cell apoptosis, and early atherogenesis in mice fed a high-fat diet Proc Natl Acad Sci USA 100 2112 2116 10.1073/pnas.0336359100 1:CAS:528:DC%2BD3sXhsFGrtrk%3D 10.1073/pnas. 0336359100 12571362 (Pubitemid 36254582)
15. P Francia C delli Gatti M Bachschmid I Martin-Padura C Savoia E Migliaccio PG Pelicci M Schiavoni TF Luscher M Volpe F Cosentino 2004 Deletion of p66shc gene protects against age-related endothelial dysfunction Circulation 110 2889 2895 1:CAS:528:DC%2BD2cXptVejs70%3D 10.1161/01.CIR.0000147731.24444.4D 15505103 (Pubitemid 39473614)
16. GG Camici F Cosentino FC Tanner TF Luscher 2008 The role of p66Shc deletion in age-associated arterial dysfunction and disease states J Appl Physiol 105 1628 1631 10.1152/japplphysiol.90579.2008 1:CAS:528: DC%2BD1cXhsVOqsrfJ 10.1152/japplphysiol.90579.2008 18772327
17. T Yamamori AR White I Mattagajasingh FA Khanday A Haile B Qi BH Jeon A Bugayenko K Kasuno DE Berkowitz K Irani 2005 P66shc regulates endothelial NO production and endothelium-dependent vasorelaxation: implications for age-associated vascular dysfunction J Mol Cell Cardiol 39 992 995 10.1016/j.yjmcc.2005.09.003 1:CAS:528:DC%2BD2MXht1Sqt73O 10.1016/j.yjmcc.2005. 09.003 16242150 (Pubitemid 41572332)
18. TA Elhadd TA Abdu J Oxtoby G Kennedy M McLaren R Neary JJ Belch RN Clayton 2001 Biochemical and biophysical markers of endothelial dysfunction in adults with hypopituitarism and severe GH deficiency J Clin Endocrinol Metab 86 4223 4232 1:CAS:528:DC%2BD3MXmvFCktbk%3D 10.1210/jc.86.9.4223 11549653 (Pubitemid 32848539)
19. A Csiszar N Labinskyy V Perez FA Recchia A Podlutsky P Mukhopadhyay G Losonczy P Pacher SN Austad A Bartke Z Ungvari 2008 Endothelial function and vascular oxidative stress in long-lived GH/IGF-deficient Ames dwarf mice Am J Physiol Heart Circ Physiol 295 H1882 H1894 10.1152/ajpheart.412.2008 1:CAS:528:DC%2BD1cXhsVWktb%2FJ 10.1152/ajpheart.412.2008 18757483
20. EJ Rivera A Goldin N Fulmer R Tavares JR Wands SM de la Monte 2005 Insulin and insulin-like growth factor expression and function deteriorate with progression of Alzheimer's disease: link to brain reductions in acetylcholine J Alzheimers Dis 8 247 268 1:CAS:528:DC%2BD2MXht1ynsLjF 16340083
21. C Lopez-Lopez MO Dietrich F Metzger H Loetscher I Torres-Aleman 2007 Disturbed cross talk between insulin-like growth factor I and AMP-activated protein kinase as a possible cause of vascular dysfunction in the amyloid precursor protein/presenilin 2 mouse model of Alzheimer's disease J Neurosci 27 824 831 1:CAS:528:DC%2BD2sXhs1Wrtrw%3D 10.1523/JNEUROSCI.4345-06.2007 17251422 (Pubitemid 46174501)
22. L Groban NA Pailes CD Bennett CS Carter MC Chappell DW Kitzman WE Sonntag 2006 Growth hormone replacement attenuates diastolic dysfunction and cardiac angiotensin II expression in senescent rats J Gerontol A Biol Sci Med Sci 61 28 35 16456192
23. AS Khan DC Sane T Wannenburg WE Sonntag 2002 Growth hormone, insulin-like growth factor-1 and the aging cardiovascular system Cardiovasc Res 54 25 35 1:CAS:528:DC%2BD38XivF2ru7w%3D 10.1016/S0008-6363(01)00533-8 12062358 (Pubitemid 34327932)
24. WE Sonntag C Lynch P Thornton A Khan S Bennett R Ingram 2000 The effects of growth hormone and IGF-1 deficiency on cerebrovascular and brain ageing J Anat 197 Pt 4 575 585 1:CAS:528:DC%2BD3MXps1Wmsw%3D%3D 10.1017/S002187829900713X 11197531 (Pubitemid 32051538)
25. JE Puche M Garcia-Fernandez J Muntane J Rioja S Gonzalez-Baron I Castilla Cortazar 2008 Low doses of insulin-like growth factor-I induce mitochondrial protection in aging rats Endocrinology 149 2620 2627 10.1210/en.2007-1563 1:CAS:528:DC%2BD1cXht1Gmsb7F 10.1210/en.2007-1563 18276748 (Pubitemid 351574499)
26. A Csiszar N Labinskyy A Podlutsky PM Kaminski MS Wolin C Zhang P Mukhopadhyay P Pacher F Hu R de Cabo P Ballabh Z Ungvari 2008 Vasoprotective effects of resveratrol and SIRT1: attenuation of cigarette smoke-induced oxidative stress and proinflammatory phenotypic alterations Am J Physiol Heart Circ Physiol 294 H2721 H2735 1:CAS:528:DC%2BD1cXnsVaktL0%3D 10.1152/ajpheart. 00235.2008 18424637
27. A Benigni D Corna C Zoja A Sonzogni R Latini M Salio S Conti D Rottoli L Longaretti P Cassis M Morigi TM Coffman G Remuzzi 2009 Disruption of the Ang II type 1 receptor promotes longevity in mice J Clin Invest 119 524 530 10.1172/JCI36703 1:CAS:528:DC%2BD1MXivF2kt7k%3D 10.1172/JCI36703 19197138
28. AE Dikalova AT Bikineyeva K Budzyn RR Nazarewicz L McCann W Lewis DG Harrison SI Dikalov 2010 Therapeutic targeting of mitochondrial superoxide in hypertension Circ Res 10.1161/CIRCRESAHA.109.214601 20448215
29. N Labinskyy P Mukhopadhyay J Toth G Szalai M Veres G Losonczy JT Pinto P Pacher P Ballabh A Podlutsky SN Austad A Csiszar Z Ungvari 2009 Longevity is associated with increased vascular resistance to high glucose-induced oxidative stress and inflammatory gene expression in Peromyscus leucopus Am J Physiol Heart Circ Physiol 296 H946 H956 10.1152/ajpheart.00693.2008 1:CAS:528:DC%2BD1MXkvVygsbs%3D 10.1152/ajpheart.00693.2008 19181967
30. G Lopez-Lluch PM Irusta P Navas R de Cabo 2008 Mitochondrial biogenesis and healthy aging Exp Gerontol 43 813 819 10.1016/j.exger.2008.06.014 1:CAS:528:DC%2BD1cXhtVart7rJ 10.1016/j.exger.2008.06.014 18662766
31. EM Burns TW Kruckeberg LE Comerford MT Buschmann 1979 Thinning of capillary walls and declining numbers of endothelial mitochondria in the cerebral cortex of the aging primate, Macaca nemestrina J Gerontol 34 642 650 1:STN:280:DyaE1M3ktVWgug%3D%3D 112144
32. EM Burns TW Kruckeberg PK Gaetano 1981 Changes with age in cerebral capillary morphology Neurobiol Aging 2 283 291 1:STN:280:DyaL387kvVOqsA%3D%3D 10.1016/0197-4580(81)90037-3 7335147 (Pubitemid 12152575)
33. G Lopez-Lluch N Hunt B Jones M Zhu H Jamieson S Hilmer MV Cascajo J Allard DK Ingram P Navas R de Cabo 2006 Calorie restriction induces mitochondrial biogenesis and bioenergetic efficiency Proc Natl Acad Sci USA 103 1768 1773 1:CAS:528:DC%2BD28Xhslehtrs%3D 10.1073/pnas.0510452103 16446459 (Pubitemid 43228768)
34. E Nisoli C Tonello A Cardile V Cozzi R Bracale L Tedesco S Falcone A Valerio O Cantoni E Clementi S Moncada MO Carruba 2005 Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS Science 310 314 317 1:CAS:528:DC%2BD2MXhtV2hurvO 10.1126/science.1117728 16224023 (Pubitemid 41457197)
35. F Addabbo B Ratliff HC Park MC Kuo Z Ungvari A Csiszar B Krasnikov K Sodhi F Zhang A Nasjletti MS Goligorsky 2009 The Krebs cycle and mitochondrial mass are early victims of endothelial dysfunction: proteomic approach Am J Pathol 174 34 43 10.2353/ajpath.2009.080650 1:CAS:528:DC%2BD1MXhslOlurY%3D 10.2353/ajpath.2009.080650 19095954
36. RM Reznick H Zong J Li K Morino IK Moore HJ Yu ZX Liu J Dong KJ Mustard SA Hawley D Befroy M Pypaert DG Hardie LH Young GI Shulman 2007 Aging-associated reductions in AMP-activated protein kinase activity and mitochondrial biogenesis Cell Metab 5 151 156 10.1016/j.cmet.2007.01.008 1:CAS:528: DC%2BD2sXitlSqtrk%3D 10.1016/j.cmet.2007.01.008 17276357 (Pubitemid 46172924)
37. P Echave G Machado-da-Silva RS Arkell MR Duchen J Jacobson R Mitter AC Lloyd 2009 Extracellular growth factors and mitogens cooperate to drive mitochondrial biogenesis J Cell Sci 122 4516 4525 10.1242/jcs.049734 1:CAS:528:DC%2BC3cXntFyhug%3D%3D 10.1242/jcs.049734 19920079
38. H Chen A Chomyn DC Chan 2005 Disruption of fusion results in mitochondrial heterogeneity and dysfunction J Biol Chem 280 26185 26192 10.1074/jbc.M503062200 1:CAS:528:DC%2BD2MXlvFymt7s%3D 10.1074/jbc.M503062200 15899901 (Pubitemid 41022214)
39. M Jendrach S Pohl M Voth A Kowald P Hammerstein J Bereiter-Hahn 2005 Morpho-dynamic changes of mitochondria during ageing of human endothelial cells Mech Ageing Dev 126 813 821 10.1016/j.mad.2005.03.002 1:CAS:528: DC%2BD2MXktVKqtr8%3D 10.1016/j.mad.2005.03.002 15888336 (Pubitemid 40693304)
40. A Makino BT Scott WH Dillmann 2010 Mitochondrial fragmentation and superoxide anion production in coronary endothelial cells from a mouse model of type 1 diabetes Diabetologia 10.1007/s00125-010-1770-4 in press
41. NJ Linford RP Beyer K Gollahon RA Krajcik VL Malloy V Demas GC Burmer PS Rabinovitch 2007 Transcriptional response to aging and caloric restriction in heart and adipose tissue Aging Cell 6 673 688 10.1111/j.1474-9726.2007.00319.x 1:CAS:528:DC%2BD2sXhtFeksLfO 10.1111/j.1474-9726.2007.00319.x 17874999 (Pubitemid 47400049)
42. DE Harrison R Strong ZD Sharp JF Nelson CM Astle K Flurkey NL Nadon JE Wilkinson K Frenkel CS Carter M Pahor MA Javors E Fernandez RA Miller 2009 Rapamycin fed late in life extends lifespan in genetically heterogeneous mice Nature 460 392 395 10.1038/nature08221 1:CAS:528:DC%2BD1MXotlSgtLg%3D 19587680
43. Y Zou S Yoon KJ Jung CH Kim TG Son MS Kim YJ Kim J Lee BP Yu HY Chung 2006 Upregulation of aortic adhesion molecules during aging J Gerontol 61 232 244
44. AJ Donato AD Black KL Jablonski LB Gano DR Seals 2008 Aging is associated with greater nuclear NFkappaB, reduced IkappaBalpha, and increased expression of proinflammatory cytokines in vascular endothelial cells of healthy humans Aging Cell 7 805 812 10.1111/j.1474-9726.2008.00438.x 1:CAS:528: DC%2BD1cXhsFemtrfF 10.1111/j.1474-9726.2008.00438.x 18782346 (Pubitemid 352749435)
45. AJ Donato I Eskurza AE Silver AS Levy GL Pierce PE Gates DR Seals 2007 Direct evidence of endothelial oxidative stress with aging in humans: relation to impaired endothelium-dependent dilation and upregulation of nuclear factor-kappaB Circ Res 100 1659 1666 1:CAS:528:DC%2BD2sXmtVGjtbg%3D 10.1161/01.RES.0000269183.13937.e8 17478731 (Pubitemid 46897269)
46. L Hajra AI Evans M Chen SJ Hyduk T Collins MI Cybulsky 2000 The NF-kappa B signal transduction pathway in aortic endothelial cells is primed for activation in regions predisposed to atherosclerotic lesion formation Proc Natl Acad Sci USA 97 9052 9057 1:CAS:528:DC%2BD3cXls12ksr8%3D 10.1073/pnas.97.16.9052 10922059 (Pubitemid 30626672)
47. I Mattagajasingh CS Kim A Naqvi T Yamamori TA Hoffman SB Jung J DeRicco K Kasuno K Irani 2007 SIRT1 promotes endothelium-dependent vascular relaxation by activating endothelial nitric oxide synthase Proc Natl Acad Sci USA 104 14855 14860 1:CAS:528:DC%2BD2sXhtVOnsLrL 10.1073/pnas.0704329104 17785417 (Pubitemid 350003232)
48. A Csiszar N Labinskyy R Jimenez JT Pinto P Ballabh G Losonczy KJ Pearson R de Cabo Z Ungvari 2009 Anti-oxidative and anti-inflammatory vasoprotective effects of caloric restriction in aging: role of circulating factors and SIRT1 Mech Ageing Dev 130 518 527 10.1016/j.mad.2009.06.004 1:CAS:528: DC%2BD1MXptVShtrY%3D 10.1016/j.mad.2009.06.004 19549533
49. K Shinmura K Tamaki K Saito Y Nakano T Tobe R Bolli 2007 Cardioprotective effects of short-term caloric restriction are mediated by adiponectin via activation of AMP-activated protein kinase Circulation 116 2809 2817 10.1161/CIRCULATIONAHA.107.725697 1:CAS:528:DC%2BD1cXosVyisA%3D%3D 10.1161/CIRCULATIONAHA.107.725697 18040027 (Pubitemid 350291223)
50. KJ Pearson JA Baur KN Lewis L Peshkin NL Price N Labinskyy WR Swindell D Kamara RK Minor E Perez HA Jamieson Y Zhang SR Dunn K Sharma N Pleshko LA Woollett A Csiszar Y Ikeno D Le Couteur PJ Elliott KG Becker P Navas DK Ingram NS Wolf Z Ungvari DA Sinclair R de Cabo 2008 Resveratrol delays age-related deterioration and mimics transcriptional aspects of dietary restriction without extending life span Cell Metab 8 157 168 1:CAS:528:DC%2BD1cXpvVKrs74%3D 10.1016/j.cmet.2008.06.011 18599363
51. ZI Ungvari N Labinskyy P Mukhopadhyay JT Pinto Z Bagi P Ballabh C Zhang P Pacher A Csiszar 2009 Resveratrol attenuates mitochondrial oxidative stress in coronary arterial endothelial cells Am J Physiol Heart Circ Physiol 10.1152/ajpheart.00375.2009
52. A Csiszar N Labinskyy JT Pinto P Ballabh H Zhang G Losonczy K Pearson R de Cabo P Pacher C Zhang Z Ungvari 2009 Resveratrol induces mitochondrial biogenesis in endothelial cells Am J Physiol Heart Circ Physiol 297 H13 H20 10.1152/ajpheart.00368.2009 1:CAS:528:DC%2BD1MXovVKisL0%3D 10.1152/ajpheart. 00368.2009 19429820
53. Z Ungvari N Labinskyy P Mukhopadhyay JT Pinto Z Bagi P Ballabh C Zhang P Pacher A Csiszar 2009 Resveratrol attenuates mitochondrial oxidative stress in coronary arterial endothelial cells Am J Physiol Heart Circ Physiol 297 H1876 H1881 10.1152/ajpheart.00375.2009 1:CAS:528:DC%2BD1MXhsValsbjE 10.1152/ajpheart.00375.2009 19749157
54. Ungvari Z, Bagi Z, Feher A, Recchia FA, Sonntag WE, Pearson K, de Cabo R, Csiszar A (2010) Resveratrol confers endothelial protection via activation of the antioxidant transcription factor Nrf2 Am J Physiol Heart Circ Physiol: in press
55. M Lagouge C Argmann Z Gerhart-Hines H Meziane C Lerin F Daussin N Messadeq J Milne P Lambert P Elliott B Geny M Laakso P Puigserver J Auwerx 2006 Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha Cell 127 1109 1122 1:CAS:528:DC%2BD2sXhs1egsQ%3D%3D 10.1016/j.cell.2006.11.013 17112576 (Pubitemid 44894520)
56. M Quintero SL Colombo A Godfrey S Moncada 2006 Mitochondria as signaling organelles in the vascular endothelium Proc Natl Acad Sci USA 103 5379 5384 10.1073/pnas.0601026103 1:CAS:528:DC%2BD28Xjslaqu74%3D 10.1073/pnas.0601026103 16565215
57. A Csiszar Z Ungvari JG Edwards PM Kaminski MS Wolin A Koller G Kaley 2002 Aging-induced phenotypic changes and oxidative stress impair coronary arteriolar function Circ Res 90 1159 1166 1:CAS:528:DC%2BD38XkvV2gsLs%3D 10.1161/01.RES.0000020401.61826.EA 12065318 (Pubitemid 34786900)
58. P Pacher JS Beckman L Liaudet 2007 Nitric oxide and peroxynitrite in health and disease Physiol Rev 87 315 424 1:CAS:528:DC%2BD2sXitVagsr8%3D 10.1152/physrev.00029.2006 17237348 (Pubitemid 46217686)
59. T Radovits L Seres D Gero LN Lin CJ Beller SH Chen J Zotkina I Berger JT Groves C Szabo G Szabo 2007 The peroxynitrite decomposition catalyst FP15 improves ageing-associated cardiac and vascular dysfunction Mech Ageing Dev 128 173 181 10.1016/j.mad.2006.09.005 1:CAS:528:DC%2BD2sXntlegtg%3D%3D 10.1016/j.mad.2006.09.005 17116320 (Pubitemid 46109011)
60. S Someya J Xu K Kondo D Ding RJ Salvi T Yamasoba PS Rabinovitch R Weindruch C Leeuwenburgh M Tanokura TA Prolla 2009 Age-related hearing loss in C57BL/6J mice is mediated by Bak-dependent mitochondrial apoptosis Proc Natl Acad Sci USA 106 19432 19437 10.1073/pnas.0908786106 1:CAS:528: DC%2BD1MXhsFGns7jK 10.1073/pnas.0908786106 19901338
61. AR Smith F Visioli B Frei TM Hagen 2008 Lipoic acid significantly restores, in rats, the age-related decline in vasomotion Br J Pharmacol 153 1615 1622 10.1038/bjp.2008.28 1:CAS:528:DC%2BD1cXksFymsLw%3D 10.1038/bjp.2008.28 18297110 (Pubitemid 351535993)