Macromolecular Degradation Systems and Cardiovascular Aging

Circulation Research

Volumn 118, Issue 10, 2016, Pages 1577-1592

  Nakayama, Hiroyuki ^a   Nishida, Kazuhiko ^b   Otsu, Kinya ^b  

^a OSAKA UNIVERSITY   (Japan)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

aging; autophagy; inflammation; proteasome endopeptidase complex; ubiquitin

Indexed keywords

ANGIOTENSIN II; CYSTEINE PROTEINASE; CYTOKINE; NUCLEIC ACID; PROTEASOME; PROTEIN; REACTIVE OXYGEN METABOLITE; UBIQUITIN;

AGING; ARTERIAL STIFFNESS; AUTOPHAGY; CARDIAC MUSCLE; CARDIOVASCULAR DISEASE; CARDITIS; DIASTOLIC DYSFUNCTION; DYNAMICS; EXPERIMENTAL MODEL; HUMAN; INFLAMMATION; MACROMOLECULE; NONHUMAN; PATHOPHYSIOLOGY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN SYNTHESIS; REVIEW; SENESCENCE; SIGNAL TRANSDUCTION; STEADY STATE; VASCULARIZATION; ANIMAL; CORONARY BLOOD VESSEL; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PATHOLOGY;

AGING; ANIMALS; AUTOPHAGY; CORONARY VESSELS; HUMANS; MYOCARDIUM; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS;

EID: 84968928069     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.115.307495     Document Type: Review

References (171)

1. Prince MJ, Wu F, Guo Y, Gutierrez Robledo LM, O'Donnell M, Sullivan R, Yusuf S. The burden of disease in older people and implications for health policy and practice. Lancet. 2015;385:549-562. doi: 10. 1016/ S0140-6736(14)61347-7.
2. Lakatta EG. So! What's aging? Is cardiovascular aging a disease? J Mol Cell Cardiol. 2015;83:1-13. doi: 10. 1016/j. yjmcc. 2015. 04. 005.
3. Wang M, Shah AM. Age-associated pro-inflammatory remodeling and functional phenotype in the heart and large arteries. J Mol Cell Cardiol. 2015;83:101-111. doi: 10. 1016/j. yjmcc. 2015. 02. 004.
4. de Cavanagh EM, Inserra F, Ferder L. Angiotensin II blockade: how its molecular targets may signal to mitochondria and slow aging. Coincidences with calorie restriction and mTOR inhibition. Am J Physiol Heart Circ Physiol. 2015;309:H15-H44. doi: 10. 1152/ ajpheart. 00459. 2014.
5. Kuilman T, Michaloglou C, Mooi WJ, Peeper DS. The essence of senescence. Genes Dev. 2010;24:2463-2479. doi: 10. 1101/gad. 1971610.
6. Vajapey R, Rini D, Walston J, Abadir P. The impact of age-related dysregulation of the angiotensin system on mitochondrial redox balance. Front Physiol. 2014;5:439. doi: 10. 3389/fphys. 2014. 00439.
7. Aubert G, Lansdorp PM. Telomeres and aging. Physiol Rev. 2008;88:557-579. doi: 10. 1152/physrev. 00026. 2007.
8. Kovacic JC, Moreno P, Nabel EG, Hachinski V, Fuster V. Cellular senescence, vascular disease, and aging: part 2 of a 2-part review: clinical vascular disease in the elderly. Circulation. 2011;123:1900-1910. doi: 10. 1161/CIRCULATIONAHA. 110. 009118.
9. Rueckschloss U, Villmow M, Klöckner U. NADPH oxidase-derived superoxide impairs calcium transients and contraction in aged murine ventricular myocytes. Exp Gerontol. 2010;45:788-796. doi: 10. 1016/j. exger. 2010. 05. 002.
10. Harman D. Free radical theory of aging: An update: increasing the functional life span. Ann N Y Acad Sci. 2006;1067:10-21. doi: 10. 1196/ annals. 1354. 003.
11. Newgard CB, Sharpless NE. Coming of age: molecular drivers of aging and therapeutic opportunities. J Clin Invest. 2013;123:946-950. doi: 10. 1172/JCI68833.
12. Coppé JP, Desprez PY, Krtolica A, Campisi J. The senescence-associated secretory phenotype: The dark side of tumor suppression. Annu Rev Pathol. 2010;5:99-118. doi: 10. 1146/annurev-pathol-121808-102144.
13. Larsson NG. Somatic mitochondrial DNA mutations in mammalian aging. Annu Rev Biochem. 2010;79:683-706. doi: 10. 1146/ annurev-biochem-060408-093701.
14. Van Raamsdonk JM, Hekimi S. Deletion of the mitochondrial superoxide dismutase sod-2 extends lifespan in Caenorhabditis elegans. PLoS Genet. 2009;5:e1000361. doi: 10. 1371/journal. pgen. 1000361.
15. Van Raamsdonk JM, Hekimi S. Superoxide dismutase is dispensable for normal animal lifespan. Proc Natl Acad Sci U S A. 2012;109:5785-5790. doi: 10. 1073/pnas. 1116158109.
16. Kawanishi S, Hiraku Y, Oikawa S. Mechanism of guanine-specific DNA damage by oxidative stress and its role in carcinogenesis and aging. Mutat Res. 2001;488:65-76.
17. Richter T, von Zglinicki T. A continuous correlation between oxidative stress and telomere shortening in fibroblasts. Exp Gerontol. 2007;42:1039-1042. doi: 10. 1016/j. exger. 2007. 08. 005.
18. Braidy N, Guillemin GJ, Mansour H, Chan-Ling T, Poljak A, Grant R. Age related changes in NAD+ metabolism oxidative stress and Sirt1 activity in wistar rats. PLoS One. 2011;6:e19194. doi: 10. 1371/journal. pone. 0019194.
19. Harrison DE, Strong R, Sharp ZD, Nelson JF, Astle CM, Flurkey K, Nadon NL, Wilkinson JE, Frenkel K, Carter CS, Pahor M, Javors MA, Fernandez E, Miller RA. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature. 2009;460:392-395. doi: 10. 1038/ nature08221.
20. Howitz KT, Bitterman KJ, Cohen HY, Lamming DW, Lavu S, Wood JG, Zipkin RE, Chung P, Kisielewski A, Zhang LL, Scherer B, Sinclair DA. Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature. 2003;425:191-196. doi: 10. 1038/nature01960.
21. Wood JG, Rogina B, Lavu S, Howitz K, Helfand SL, Tatar M, Sinclair D. Sirtuin activators mimic caloric restriction and delay ageing in metazoans. Nature. 2004;430:686-689. doi: 10. 1038/nature02789.
22. Franceschi C, Bonafè M, Valensin S, Olivieri F, De Luca M, Ottaviani E, De Benedictis G. Inflamm-aging. An evolutionary perspective on immunosenescence. Ann N Y Acad Sci. 2000;908:244-254.
23. Laplante M, Sabatini DM. mTOR signaling in growth control and disease. Cell. 2012;149:274-293. doi: 10. 1016/j. cell. 2012. 03. 017.
24. Vellai T, Takacs-Vellai K, Zhang Y, Kovacs AL, Orosz L, Müller F. Genetics: influence of TOR kinase on lifespan in C. elegans. Nature. 2003;426:620. doi: 10. 1038/426620a.
25. Chen AT, Guo C, Dumas KJ, Ashrafi K, Hu PJ. Effects of Caenorhabditis elegans sgk-1 mutations on lifespan, stress resistance, and DAF-16/FoxO regulation. Aging Cell. 2013;12:932-940. doi: 10. 1111/acel. 12120.
26. Kapahi P, Zid BM, Harper T, Koslover D, Sapin V, Benzer S. Regulation of lifespan in Drosophila by modulation of genes in the TOR signaling pathway. Curr Biol. 2004;14:885-890. doi: 10. 1016/j. cub. 2004. 03. 059.
27. Arnold CR, Wolf J, Brunner S, Herndler-Brandstetter D, Grubeck-Loebenstein B. Gain and loss of T cell subsets in old age-age-related reshaping of the T cell repertoire. J Clin Immunol. 2011;31:137-146. doi: 10. 1007/s10875-010-9499-x.
28. Kogut I, Scholz JL, Cancro MP, Cambier JC. B cell maintenance and function in aging. Semin Immunol. 2012;24:342-349. doi: 10. 1016/j. smim. 2012. 04. 004.
29. Fagiolo U, Cossarizza A, Scala E, Fanales-Belasio E, Ortolani C, Cozzi E, Monti D, Franceschi C, Paganelli R. Increased cytokine production in mononuclear cells of healthy elderly people. Eur J Immunol. 1993;23:2375-2378. doi: 10. 1002/eji. 1830230950.
30. Olsson J, Wikby A, Johansson B, Löfgren S, Nilsson BO, Ferguson FG. Age-related change in peripheral blood T-lymphocyte subpopulations and cytomegalovirus infection in the very old: The Swedish longitudinal OCTO immune study. Mech Ageing Dev. 2000;121:187-201.
31. Sikora E, Arendt T, Bennett M, Narita M. Impact of cellular senescence signature on ageing research. Ageing Res Rev. 2011;10:146-152. doi: 10. 1016/j. Arr. 2010. 10. 002.
32. Shaw AC, Goldstein DR, Montgomery RR. Age-dependent dysregulation of innate immunity. Nat Rev Immunol. 2013;13:875-887. doi: 10. 1038/ nri3547.
33. Miyake K. Innate immune sensing of pathogens and danger signals by cell surface Toll-like receptors. Semin Immunol. 2007;19:3-10. doi: 10. 1016/j. smim. 2006. 12. 002.
34. Cannizzo ES, Clement CC, Sahu R, Follo C, Santambrogio L. Oxidative stress, inflamm-aging and immunosenescence. J Proteomics. 2011;74:2313-2323. doi: 10. 1016/j. jprot. 2011. 06. 005.
35. Chávez-Sánchez L, Madrid-Miller A, Chávez-Rueda K, Legorreta-Haquet MV, Tesoro-Cruz E, Blanco-Favela F. Activation of TLR2 and TLR4 by minimally modified low-density lipoprotein in human macrophages and monocytes triggers the inflammatory response. Hum Immunol. 2010;71:737-744. doi: 10. 1016/j. humimm. 2010. 05. 005.
36. Chen GY, Nuñez G. Sterile inflammation: sensing and reacting to damage. Nat Rev Immunol. 2010;10:826-837. doi: 10. 1038/nri2873.
37. Panda A, Qian F, Mohanty S, van Duin D, Newman FK, Zhang L, Chen S, Towle V, Belshe RB, Fikrig E, Allore HG, Montgomery RR, Shaw AC. Age-associated decrease in TLR function in primary human dendritic cells predicts influenza vaccine response. J Immunol. 2010;184:2518-2527. doi: 10. 4049/jimmunol. 0901022.
38. Jing Y, Shaheen E, Drake RR, Chen N, Gravenstein S, Deng Y. Aging is associated with a numerical and functional decline in plasmacytoid dendritic cells, whereas myeloid dendritic cells are relatively unaltered in human peripheral blood. Hum Immunol. 2009;70:777-784. doi: 10. 1016/j. humimm. 2009. 07. 005.
39. Jylhävä J, Kotipelto T, Raitala A, Jylhä M, Hervonen A, Hurme M. Aging is associated with quantitative and qualitative changes in circulating cellfree DNA: The Vitality 90+ study. Mech Ageing Dev. 2011;132:20-26. doi: 10. 1016/j. mad. 2010. 11. 001.
40. Jylhävä J, Jylhä M, Lehtimäki T, Hervonen A, Hurme M. Circulating cellfree DNA is associated with mortality and inflammatory markers in nonagenarians: The Vitality 90+ Study. Exp Gerontol. 2012;47:372-378. doi: 10. 1016/j. exger. 2012. 02. 011.
41. Salminen A, Kauppinen A, Kaarniranta K. Emerging role of NF-?B signaling in the induction of senescence-associated secretory phenotype (SASP). Cell Signal. 2012;24:835-845. doi: 10. 1016/j. cellsig. 2011. 12. 006.
42. Zhang Q, Raoof M, Chen Y, Sumi Y, Sursal T, Junger W, Brohi K, Itagaki K, Hauser CJ. Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature. 2010;464:104-107. doi: 10. 1038/nature08780.
43. Pinti M, Cevenini E, Nasi M, De Biasi S, Salvioli S, Monti D, Benatti S, Gibellini L, Cotichini R, Stazi MA, Trenti T, Franceschi C, Cossarizza A. Circulating mitochondrial DNA increases with age and is a familiar trait: Implications for "inflamm-aging". Eur J Immunol. 2014;44:1552-1562. doi: 10. 1002/eji. 201343921.
44. Oka T, Hikoso S, Yamaguchi O, Taneike M, Takeda T, Tamai T, Oyabu J, Murakawa T, Nakayama H, Nishida K, Akira S, Yamamoto A, Komuro I, Otsu K. Mitochondrial DNA that escapes from autophagy causes inflammation and heart failure. Nature. 2012;485:251-255. doi: 10. 1038/ nature10992.
45. Vandanmagsar B, Youm YH, Ravussin A, Galgani JE, Stadler K, Mynatt RL, Ravussin E, Stephens JM, Dixit VD. The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat Med. 2011;17:179-188. doi: 10. 1038/nm. 2279.
46. Mori MA, Raghavan P, Thomou T, Boucher J, Robida-Stubbs S, Macotela Y, Russell SJ, Kirkland JL, Blackwell TK, Kahn CR. Role of microRNA processing in adipose tissue in stress defense and longevity. Cell Metab. 2012;16:336-347. doi: 10. 1016/j. cmet. 2012. 07. 017.
47. Barrett AJ, Rawlings ND. 'Species' of peptidases. Biol Chem. 2007;388:1151-1157. doi: 10. 1515/BC. 2007. 151.
48. Goll DE, Thompson VF, Li H, Wei W, Cong J. The calpain system. Physiol Rev. 2003;83:731-801. doi: 10. 1152/physrev. 00029. 2002.
49. Taneike M, Mizote I, Morita T, et al. Calpain protects the heart from hemodynamic stress. J Biol Chem. 2011;286:32170-32177. doi: 10. 1074/ jbc. M111. 248088.
50. Ono Y, Sorimachi H. Calpains: An elaborate proteolytic system. Biochim Biophys Acta. 2012;1824:224-236. doi: 10. 1016/j. bbapap. 2011. 08. 005.
51. Averna M, De Tullio R, Salamino F, Minafra R, Pontremoli S, Melloni E. Age-dependent degradation of calpastatin in kidney of hypertensive rats. J Biol Chem. 2001;276:38426-38432. doi: 10. 1074/jbc. M101936200.
52. Budihardjo I, Oliver H, Lutter M, Luo X, Wang X. Biochemical pathways of caspase activation during apoptosis. Annu Rev Cell Dev Biol. 1999;15:269-290. doi: 10. 1146/annurev. cellbio. 15. 1. 269.
53. Rohn TT. The role of caspases in Alzheimer's disease; potential novel therapeutic opportunities. Apoptosis. 2010;15:1403-1409. doi: 10. 1007/ s10495-010-0463-2.
54. Shalini S, Dorstyn L, Dawar S, Kumar S. Old, new and emerging functions of caspases. Cell Death Differ. 2015;22:526-539. doi: 10. 1038/ cdd. 2014. 216.
55. Martinon F, Tschopp J. Inflammatory caspases and inflammasomes: master switches of inflammation. Cell Death Differ. 2007;14:10-22. doi: 10. 1038/sj. cdd. 4402038.
56. Rawlings ND, Barrett AJ, Bateman A. MEROPS: The database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res. 2012;40:D343-D350. doi: 10. 1093/nar/gkr987.
57. Turk B, Turk D, Turk V. Lysosomal cysteine proteases: more than scavengers. Biochim Biophys Acta. 2000;1477:98-111.
58. Brix K, Dunkhorst A, Mayer K, Jordans S. Cysteine cathepsins: cellular roadmap to different functions. Biochimie. 2008;90:194-207. doi: 10. 1016/j. biochi. 2007. 07. 024.
59. Pišlar A, Kos J. Cysteine cathepsins in neurological disorders. Mol Neurobiol. 2014;49:1017-1030. doi: 10. 1007/s12035-013-8576-6.
60. Conus S, Simon HU. Cathepsins: key modulators of cell death and inflammatory responses. Biochem Pharmacol. 2008;76:1374-1382. doi: 10. 1016/j. bcp. 2008. 07. 041.
61. Nakanishi H, Tominaga K, Amano T, Hirotsu I, Inoue T, Yamamoto K. Age-related changes in activities and localizations of cathepsins D, E, B, and L in the rat brain tissues. Exp Neurol. 1994;126:119-128. doi: 10. 1006/exnr. 1994. 1048.
62. Bhattacharyya S, Yu H, Mim C, Matouschek A. Regulated protein turnover: snapshots of the proteasome in action. Nat Rev Mol Cell Biol. 2014;15:122-133. doi: 10. 1038/nrm3741.
63. Glickman MH, Ciechanover A. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev. 2002;82:373-428. doi: 10. 1152/physrev. 00027. 2001.
64. Hinz M, Scheidereit C. The I?B kinase complex in NF-?B regulation and beyond. EMBO Rep. 2014;15:46-61. doi: 10. 1002/embr. 201337983.
65. Hikoso S, Yamaguchi O, Nakano Y, et al. The I{kappa}B kinase {beta}/ nuclear factor {kappa}B signaling pathway protects the heart from hemodynamic stress mediated by the regulation of manganese superoxide dismutase expression. Circ Res. 2009;105:70-79. doi: 10. 1161/ CIRCRESAHA. 108. 193318.
66. Ronnebaum SM, Patterson C, Schisler JC. Minireview: hey U(PS): metabolic and proteolytic homeostasis linked via AMPK and the ubiquitin proteasome system. Mol Endocrinol. 2014;28:1602-1615. doi: 10. 1210/ me. 2014-1180.
67. Teixeira LK, Reed SI. Ubiquitin ligases and cell cycle control. Annu Rev Biochem. 2013;82:387-414. doi: 10. 1146/ annurev-biochem-060410-105307.
68. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell. 1999;96:857-868.
69. Pickering AM, Koop AL, Teoh CY, Ermak G, Grune T, Davies KJ. The immunoproteasome, the 20S proteasome and the PA28 proteasome regulator are oxidative-stress-adaptive proteolytic complexes. Biochem J. 2010;432:585-594. doi: 10. 1042/BJ20100878.
70. Vilchez D, Morantte I, Liu Z, Douglas PM, Merkwirth C, Rodrigues AP, Manning G, Dillin A. RPN-6 determines C. elegans longevity under proteotoxic stress conditions. Nature. 2012;489:263-268. doi: 10. 1038/nature11315.
71. Chondrogianni N, Gonos ES. Proteasome function determines cellular homeostasis and the rate of aging. Adv Exp Med Biol. 2010;694:38-46.
72. Ding Q, Dimayuga E, Keller JN. Proteasome regulation of oxidative stress in aging and age-related diseases of the CNS. Antioxid Redox Signal. 2006;8:163-172. doi: 10. 1089/ars. 2006. 8. 163.
73. Pickering AM, Lehr M, Miller RA. Lifespan of mice and primates correlates with immunoproteasome expression. J Clin Invest. 2015;125:2059-2068. doi: 10. 1172/JCI80514.
74. Shringarpure R, Grune T, Mehlhase J, Davies KJ. Ubiquitin conjugation is not required for the degradation of oxidized proteins by proteasome. J Biol Chem. 2003;278:311-318. doi: 10. 1074/jbc. M206279200.
75. Farout L, Friguet B. Proteasome function in aging and oxidative stress: implications in protein maintenance failure. Antioxid Redox Signal. 2006;8:205-216. doi: 10. 1089/ars. 2006. 8. 205.
76. Bence NF, Sampat RM, Kopito RR. Impairment of the ubiquitin-proteasome system by protein aggregation. Science. 2001;292:1552-1555. doi: 10. 1126/science. 292. 5521. 1552.
77. Mizushima N, Komatsu M. Autophagy: renovation of cells and tissues. Cell. 2011;147:728-741. doi: 10. 1016/j. cell. 2011. 10. 026.
78. Wu H, Chen S, Ammar AB, Xu J, Wu Q, Pan K, Zhang J, Hong Y. Crosstalk between macroautophagy and chaperone-mediated autophagy: implications for the treatment of neurological diseases. Mol Neurobiol. 2015;52:1284-1296. doi: 10. 1007/s12035-014-8933-0.
79. Arias E, Cuervo AM. Chaperone-mediated autophagy in protein quality control. Curr Opin Cell Biol. 2011;23:184-189. doi: 10. 1016/j. ceb. 2010. 10. 009.
80. Nishida K, Taneike M, Otsu K. The role of autophagic degradation in the heart. J Mol Cell Cardiol. 2015;78:73-79. doi: 10. 1016/j. yjmcc. 2014. 09. 029.
81. Leon LJ, Gustafsson AB. Staying young at heart: Autophagy and adaptation to cardiac aging [published online ahead of print November 5, 2015]. J Mol Cell Cardiol. 2015. doi: 10. 1016/j. yjmcc. 2015. 11. 006. http://www. jmmc-online. com/article/S0022-2828(15)30111-5/abstract.
82. Napirei M, Ricken A, Eulitz D, Knoop H, Mannherz HG. Expression pattern of the deoxyribonuclease 1 gene: lessons from the Dnase1 knockout mouse. Biochem J. 2004;380:929-937. doi: 10. 1042/BJ20040046.
83. Evans CJ, Aguilera RJ. DNase II: genes, enzymes and function. Gene. 2003;322:1-15.
84. Kavanagh D, Spitzer D, Kothari PH, Shaikh A, Liszewski MK, Richards A, Atkinson JP. New roles for the major human 3'-5' exonuclease TREX1 in human disease. Cell Cycle. 2008;7:1718-1725.
85. Yang YG, Lindahl T, Barnes DE. Trex1 exonuclease degrades ssDNA to prevent chronic checkpoint activation and autoimmune disease. Cell. 2007;131:873-886. doi: 10. 1016/j. cell. 2007. 10. 017.
86. Ahn J, Ruiz P, Barber GN. Intrinsic self-DNA triggers inflammatory disease dependent on STING. J Immunol. 2014;193:4634-4642. doi: 10. 4049/jimmunol. 1401337.
87. Licatalosi DD, Darnell RB. RNA processing and its regulation: global insights into biological networks. Nat Rev Genet. 2010;11:75-87. doi: 10. 1038/nrg2673.
88. Arribas-Layton M, Wu D, Lykke-Andersen J, Song H. Structural and functional control of the eukaryotic mRNA decapping machinery. Biochim Biophys Acta. 2013;1829:580-589. doi: 10. 1016/j. bbagrm. 2012. 12. 006.
89. Chlebowski A, Lubas M, Jensen TH, Dziembowski A. RNA decay machines: The exosome. Biochim Biophys Acta. 2013;1829:552-560. doi: 10. 1016/j. bbagrm. 2013. 01. 006.
90. Nagarajan VK, Jones CI, Newbury SF, Green PJ. XRN 5'?3' exoribonucleases: structure, mechanisms and functions. Biochim Biophys Acta. 2013;1829:590-603. doi: 10. 1016/j. bbagrm. 2013. 03. 005.
91. Dreyfuss G, Kim VN, Kataoka N. Messenger-RNA-binding proteins and the messages they carry. Nat Rev Mol Cell Biol. 2002;3:195-205. doi: 10. 1038/nrm760.
92. Uehata T, Akira S. mRNA degradation by the endoribonuclease Regnase-1/ ZC3H12a/MCPIP-1. Biochim Biophys Acta. 2013;1829:708-713. doi: 10. 1016/j. bbagrm. 2013. 03. 001.
93. Lee S, Choi E, Cha MJ, Park AJ, Yoon C, Hwang KC. Impact of miRNAs on cardiovascular aging. J Geriatr Cardiol. 2015;12:569-574. doi: 10. 11909/j. issn. 1671-5411. 2015. 05. 011.
94. Donato AJ, Morgan RG, Walker AE, Lesniewski LA. Cellular and molecular biology of aging endothelial cells. J Mol Cell Cardiol. 2015;89:122-135. doi: 10. 1016/j. yjmcc. 2015. 01. 021.
95. Minamino T, Miyauchi H, Yoshida T, Ishida Y, Yoshida H, Komuro I. Endothelial cell senescence in human atherosclerosis: role of telomere in endothelial dysfunction. Circulation. 2002;105:1541-1544.
96. Liu Y, Drozdov I, Shroff R, Beltran LE, Shanahan CM. Prelamin A accelerates vascular calcification via activation of the DNA damage response and senescence-associated secretory phenotype in vascular smooth muscle cells. Circ Res. 2013;112:e99-109. doi: 10. 1161/ CIRCRESAHA. 111. 300543.
97. Seidler S, Zimmermann HW, Bartneck M, Trautwein C, Tacke F. Agedependent alterations of monocyte subsets and monocyte-related chemokine pathways in healthy adults. BMC Immunol. 2010;11:30. doi: 10. 1186/1471-2172-11-30.
98. Gardner SE, Humphry M, Bennett MR, Clarke MC. senescent vascular smooth muscle cells drive inflammation through an interleukin-1?-dependent senescence-associated secretory phenotype. Arterioscler Thromb Vasc Biol. 2015;35:1963-1974. doi: 10. 1161/ATVBAHA. 115. 305896.
99. Wang M, Zhang J, Spinetti G, Jiang LQ, Monticone R, Zhao D, Cheng L, Krawczyk M, Talan M, Pintus G, Lakatta EG. Angiotensin II activates matrix metalloproteinase type II and mimics age-associated carotid arterial remodeling in young rats. Am J Pathol. 2005;167:1429-1442. doi: 10. 1016/S0002-9440(10)61229-1.
100. James PA, Oparil S, Carter BL, et al. 2014 evidence-based guideline for the management of high blood pressure in adults: report from the panel members appointed to the Eighth Joint National Committee (JNC 8). JAMA. 2014;311:507-520. doi: 10. 1001/jama. 2013. 284427.
101. Wang M, Jiang L, Monticone RE, Lakatta EG. Proinflammation: The key to arterial aging. Trends Endocrinol Metab. 2014;25:72-79. doi: 10. 1016/j. Tem. 2013. 10. 002.
102. Benigni A, Corna D, Zoja C, Sonzogni A, Latini R, Salio M, Conti S, Rottoli D, Longaretti L, Cassis P, Morigi M, Coffman TM, Remuzzi G. Disruption of the Ang II type 1 receptor promotes longevity in mice. J Clin Invest. 2009;119:524-530. doi: 10. 1172/JCI36703.
103. Jiang L, Zhang J, Monticone RE, Telljohann R, Wu J, Wang M, Lakatta EG. Calpain-1 regulation of matrix metalloproteinase 2 activity in vascular smooth muscle cells facilitates age-associated aortic wall calcification and fibrosis. Hypertension. 2012;60:1192-1199. doi: 10. 1161/ HYPERTENSIONAHA. 112. 196840.
104. Nabeshima Y, Washida M, Tamura M, Maeno A, Ohnishi M, Shiroishi T, Imura A, Razzaque MS, Nabeshima Y. Calpain 1 inhibitor BDA-410 ameliorates ?-klotho-deficiency phenotypes resembling human agingrelated syndromes. Sci Rep. 2014;4:5847. doi: 10. 1038/srep05847.
105. Brodeur MR, Bouvet C, Barrette M, Moreau P. Palmitic acid increases medial calcification by inducing oxidative stress. J Vasc Res. 2013;50:430-441. doi: 10. 1159/000354235.
106. Wen C, Yang X, Yan Z, Zhao M, Yue X, Cheng X, Zheng Z, Guan K, Dou J, Xu T, Zhang Y, Song T, Wei C, Zhong H. Nalp3 inflammasome is activated and required for vascular smooth muscle cell calcification. Int J Cardiol. 2013;168:2242-2247. doi: 10. 1016/j. ijcard. 2013. 01. 211.
107. Moreno PR, Fuster V. New aspects in the pathogenesis of diabetic atherothrombosis. J Am Coll Cardiol. 2004;44:2293-2300. doi: 10. 1016/j. jacc. 2004. 07. 060.
108. Adhikari N, Basi DL, Carlson M, Mariash A, Hong Z, Lehman U, Mullegama S, Weir EK, Hall JL. Increase in GLUT1 in smooth muscle alters vascular contractility and increases inflammation in response to vascular injury. Arterioscler Thromb Vasc Biol. 2011;31:86-94. doi: 10. 1161/ATVBAHA. 110. 215004.
109. Stienstra R, Joosten LA, Koenen T, et al. The inflammasome-mediated caspase-1 activation controls adipocyte differentiation and insulin sensitivity. Cell Metab. 2010;12:593-605. doi: 10. 1016/j. cmet. 2010. 11. 011.
110. Sukhova GK, Shi GP, Simon DI, Chapman HA, Libby P. Expression of the elastolytic cathepsins S and K in human atheroma and regulation of their production in smooth muscle cells. J Clin Invest. 1998;102:576-583. doi: 10. 1172/JCI181.
111. Erusalimsky JD, Kurz DJ. Endothelial cell senescence. Handb Exp Pharmacol. 2006; (176 pt 2):213-48.
112. Chen J, Xavier S, Moskowitz-Kassai E, Chen R, Lu CY, Sanduski K, Špes A, Turk B, Goligorsky MS. Cathepsin cleavage of sirtuin 1 in endothelial progenitor cells mediates stress-induced premature senescence. Am J Pathol. 2012;180:973-983. doi: 10. 1016/j. Ajpath. 2011. 11. 033.
113. Herrmann J, Edwards WD, Holmes DR Jr, Shogren KL, Lerman LO, Ciechanover A, Lerman A. Increased ubiquitin immunoreactivity in unstable atherosclerotic plaques associated with acute coronary syndromes. J Am Coll Cardiol. 2002;40:1919-1927.
114. Versari D, Herrmann J, Gössl M, Mannheim D, Sattler K, Meyer FB, Lerman LO, Lerman A. Dysregulation of the ubiquitin-proteasome system in human carotid atherosclerosis. Arterioscler Thromb Vasc Biol. 2006;26:2132-2139. doi: 10. 1161/01. ATV. 0000232501. 08576. 73.
115. Marfella R, D'Amico M, Esposito K, et al. The ubiquitin-proteasome system and inflammatory activity in diabetic atherosclerotic plaques: effects of rosiglitazone treatment. Diabetes. 2006;55:622-632.
116. Marfella R, Di Filippo C, Laieta MT, Vestini R, Barbieri M, Sangiulo P, Crescenzi B, Ferraraccio F, Rossi F, D'Amico M, Paolisso G. Effects of ubiquitin-proteasome system deregulation on the vascular senescence and atherosclerosis process in elderly patients. J Gerontol A Biol Sci Med Sci. 2008;63:200-203.
117. Wang Z, Guo D, Yang B, Wang J, Wang R, Wang X, Zhang Q. Integrated analysis of microarray data of atherosclerotic plaques: modulation of the ubiquitin-proteasome system. PLoS One. 2014;9:e110288. doi: 10. 1371/ journal. pone. 0110288.
118. Yang Z, Gagarin D, St Laurent G III, Hammell N, Toma I, Hu CA, Iwasa A, McCaffrey TA. Cardiovascular inflammation and lesion cell apoptosis: A novel connection via the interferon-inducible immunoproteasome. Arterioscler Thromb Vasc Biol. 2009;29:1213-1219. doi: 10. 1161/ ATVBAHA. 109. 189407.
119. Wang F, Lerman A, Herrmann J. Dysfunction of the ubiquitin-proteasome system in atherosclerotic cardiovascular disease. Am J Cardiovasc Dis. 2015;5:83-100.
120. Rattan SI. Synthesis, modification and turnover of proteins during aging. Adv Exp Med Biol. 2010;694:1-13.
121. Gamerdinger M, Hajieva P, Kaya AM, Wolfrum U, Hartl FU, Behl C. Protein quality control during aging involves recruitment of the macroautophagy pathway by BAG3. EMBO J. 2009;28:889-901. doi: 10. 1038/ emboj. 2009. 29.
122. Rubinsztein DC, Mariño G, Kroemer G. Autophagy and aging. Cell. 2011;146:682-695. doi: 10. 1016/j. cell. 2011. 07. 030.
123. Taneike M, Yamaguchi O, Nakai A, et al. Inhibition of autophagy in the heart induces age-related cardiomyopathy. Autophagy. 2010;6:600-606. doi: 10. 4161/auto. 6. 5. 11947.
124. Nussenzweig SC, Verma S, Finkel T. The role of autophagy in vascular biology. Circ Res. 2015;116:480-488. doi: 10. 1161/ CIRCRESAHA. 116. 303805.
125. Shan H, Guo D, Li X, Zhao X, Li W, Bai X. From autophagy to senescence and apoptosis in Angiotensin II-treated vascular endothelial cells. APMIS. 2014;122:985-992. doi: 10. 1111/apm. 12242.
126. Hirata Y, Kurobe H, Higashida M, Fukuda D, Shimabukuro M, Tanaka K, Higashikuni Y, Kitagawa T, Sata M. HMGB1 plays a critical role in vascular inflammation and lesion formation via toll-like receptor 9. Atherosclerosis. 2013;231:227-233. doi: 10. 1016/j. Atherosclerosis. 2013. 09. 010.
127. Wang W, Caldwell MC, Lin S, Furneaux H, Gorospe M. HuR regulates cyclin A and cyclin B1 mRNA stability during cell proliferation. EMBO J. 2000;19:2340-2350. doi: 10. 1093/emboj/19. 10. 2340.
128. Watanabe Y, Lee SW, Detmar M, Ajioka I, Dvorak HF. Vascular permeability factor/vascular endothelial growth factor (VPF/VEGF) delays and induces escape from senescence in human dermal microvascular endothelial cells. Oncogene. 1997;14:2025-2032. doi: 10. 1038/sj. onc. 1201033.
129. Wang W, Yang X, Cristofalo VJ, Holbrook NJ, Gorospe M. Loss of HuR is linked to reduced expression of proliferative genes during replicative senescence. Mol Cell Biol. 2001;21:5889-5898.
130. Klöss S, Rodenbach D, Bordel R, Mülsch A. Human-antigen R (HuR) expression in hypertension: downregulation of the mRNA stabilizing protein HuR in genetic hypertension. Hypertension. 2005;45:1200-1206. doi: 10. 1161/01. HYP. 0000165674. 58470. 8f.
131. Ross CR, Brennan-Laun SE, Wilson GM. Tristetraprolin: roles in cancer and senescence. Ageing Res Rev. 2012;11:473-484. doi: 10. 1016/j. Arr. 2012. 02. 005.
132. Sanduja S, Kaza V, Dixon DA. The mRNA decay factor tristetraprolin (TTP) induces senescence in human papillomavirus-transformed cervical cancer cells by targeting E6-AP ubiquitin ligase. Aging (Albany NY). 2009;1:803-817.
133. Dutta D, Calvani R, Bernabei R, Leeuwenburgh C, Marzetti E. Contribution of impaired mitochondrial autophagy to cardiac aging: mechanisms and therapeutic opportunities. Circ Res. 2012;110:1125-1138. doi: 10. 1161/CIRCRESAHA. 111. 246108.
134. Roffe C. Ageing of the heart. Br J Biomed Sci. 1998;55:136-148.
135. Oh H, Wang SC, Prahash A, Sano M, Moravec CS, Taffet GE, Michael LH, Youker KA, Entman ML, Schneider MD. Telomere attrition and Chk2 activation in human heart failure. Proc Natl Acad Sci U S A. 2003;100:5378-5383. doi: 10. 1073/pnas. 0836098100.
136. Chimenti C, Kajstura J, Torella D, Urbanek K, Heleniak H, Colussi C, Di Meglio F, Nadal-Ginard B, Frustaci A, Leri A, Maseri A, Anversa P. Senescence and death of primitive cells and myocytes lead to premature cardiac aging and heart failure. Circ Res. 2003;93:604-613. doi: 10. 1161/01. RES. 0000093985. 76901. AF.
137. Boon RA, Iekushi K, Lechner S, et al. MicroRNA-34a regulates cardiac ageing and function. Nature. 2013;495:107-110. doi: 10. 1038/ nature11919.
138. Wang M, Zhang J, Walker SJ, Dworakowski R, Lakatta EG, Shah AM. Involvement of NADPH oxidase in age-associated cardiac remodeling. J Mol Cell Cardiol. 2010;48:765-772. doi: 10. 1016/j. yjmcc. 2010. 01. 006.
139. Comstock KL, Krown KA, Page MT, Martin D, Ho P, Pedraza M, Castro EN, Nakajima N, Glembotski CC, Quintana PJ, Sabbadini RA. LPSinduced TNF-alpha release from and apoptosis in rat cardiomyocytes: obligatory role for CD14 in mediating the LPS response. J Mol Cell Cardiol. 1998;30:2761-2775. doi: 10. 1006/jmcc. 1998. 0851.
140. Yamauchi-Takihara K, Ihara Y, Ogata A, Yoshizaki K, Azuma J, Kishimoto T. Hypoxic stress induces cardiac myocyte-derived interleukin-6. Circulation. 1995;91:1520-1524.
141. Zhou J, Xu X, Liu JJ, Lin YX, Gao GD. Angiotensin II receptors subtypes mediate diverse gene expression profile in adult hypertrophic cardiomyocytes. Clin Exp Pharmacol Physiol. 2007;34:1191-1198. doi: 10. 1111/j. 1440-1681. 2007. 04694. x.
142. Nishimura Y, Inoue T, Morooka T, Node K. Mechanical stretch and angiotensin II increase interleukin-13 production and interleukin-13 receptor alpha2 expression in rat neonatal cardiomyocytes. Circ J. 2008;72:647-653.
143. Komatsu M, Isoyama S, Takishima T. Effects of aging on induction of cardiocyte growth by extracardiac factors. Am J Physiol. 1994;266:H2279-H2286.
144. Sarkar S, Vellaichamy E, Young D, Sen S. Influence of cytokines and growth factors in ANG II-mediated collagen upregulation by fibroblasts in rats: role of myocytes. Am J Physiol Heart Circ Physiol. 2004;287:H107-H117. doi: 10. 1152/ajpheart. 00763. 2003.
145. Song X, Kusakari Y, Xiao CY, Kinsella SD, Rosenberg MA, Scherrer-Crosbie M, Hara K, Rosenzweig A, Matsui T. mTOR attenuates the inflammatory response in cardiomyocytes and prevents cardiac dysfunction in pathological hypertrophy. Am J Physiol Cell Physiol. 2010;299:C1256-C1266. doi: 10. 1152/ajpcell. 00338. 2010.
146. Xu GJ, Gan TY, Tang BP, Chen ZH, Mahemuti A, Jiang T, Song JG, Guo X, Li YD, Zhou XH, Zhang Y, Li JX. Alterations in the expression of atrial calpains in electrical and structural remodeling during aging and atrial fibrillation. Mol Med Rep. 2013;8:1343-1352. doi: 10. 3892/ mmr. 2013. 1684.
147. Ausma J, Dispersyn GD, Duimel H, Thoné F, Ver Donck L, Allessie MA, Borgers M. Changes in ultrastructural calcium distribution in goat atria during atrial fibrillation. J Mol Cell Cardiol. 2000;32:355-364. doi: 10. 1006/jmcc. 1999. 1090.
148. Philipp S, Pagel I, Höhnel K, Lutz J, Buttgereit J, Langenickel T, Hamet P, Dietz R, Willenbrock R. Regulation of caspase 3 and Fas in pressure overload-induced left ventricular dysfunction. Eur J Heart Fail. 2004;6:845-851. doi: 10. 1016/j. ejheart. 2004. 01. 014.
149. Pang JJ, Xu RK, Xu XB, Cao JM, Ni C, Zhu WL, Asotra K, Chen MC, Chen C. Hexarelin protects rat cardiomyocytes from angiotensin II-induced apoptosis in vitro. Am J Physiol Heart Circ Physiol. 2004;286:H1063-H1069. doi: 10. 1152/ajpheart. 00648. 2003.
150. Mezzaroma E, Toldo S, Abbate A. Role of NLRP3 (cryopyrin) in acute myocardial infarction. Cardiovasc Res. 2013;99:225-226. doi: 10. 1093/ cvr/cvt123.
151. Bracey NA, Gershkovich B, Chun J, Vilaysane A, Meijndert HC, Wright JR Jr, Fedak PW, Beck PL, Muruve DA, Duff HJ. Mitochondrial NLRP3 protein induces reactive oxygen species to promote Smad protein signaling and fibrosis independent from the inflammasome. J Biol Chem. 2014;289:19571-19584. doi: 10. 1074/jbc. M114. 550624.
152. Hua Y, Robinson TJ, Cao Y, Shi GP, Ren J, Nair S. Cathepsin K knockout alleviates aging-induced cardiac dysfunction. Aging Cell. 2015;14:345-351. doi: 10. 1111/acel. 12276.
153. Bulteau AL, Szweda LI, Friguet B. Age-dependent declines in proteasome activity in the heart. Arch Biochem Biophys. 2002;397:298-304. doi: 10. 1006/abbi. 2001. 2663.
154. Powell SR. The ubiquitin-proteasome system in cardiac physiology and pathology. Am J Physiol Heart Circ Physiol. 2006;291:H1-H19. doi: 10. 1152/ajpheart. 00062. 2006.
155. Predmore JM, Wang P, Davis F, Bartolone S, Westfall MV, Dyke DB, Pagani F, Powell SR, Day SM. Ubiquitin proteasome dysfunction in human hypertrophic and dilated cardiomyopathies. Circulation. 2010;121:997-1004. doi: 10. 1161/CIRCULATIONAHA. 109. 904557.
156. Li J, Horak KM, Su H, Sanbe A, Robbins J, Wang X. Enhancement of proteasomal function protects against cardiac proteinopathy and ischemia/ reperfusion injury in mice. J Clin Invest. 2011;121:3689-3700. doi: 10. 1172/JCI45709.
157. Depre C, Wang Q, Yan L, Hedhli N, Peter P, Chen L, Hong C, Hittinger L, Ghaleh B, Sadoshima J, Vatner DE, Vatner SF, Madura K. Activation of the cardiac proteasome during pressure overload promotes ventricular hypertrophy. Circulation. 2006;114:1821-1828. doi: 10. 1161/ CIRCULATIONAHA. 106. 637827.
158. Tsukamoto O, Minamino T, Okada K, et al. Depression of proteasome activities during the progression of cardiac dysfunction in pressure-overloaded heart of mice. Biochem Biophys Res Commun. 2006;340:1125-1133. doi: 10. 1016/j. bbrc. 2005. 12. 120.
159. Zhang HM, Fu J, Hamilton R, Diaz V, Zhang Y. The mammalian target of rapamycin modulates the immunoproteasome system in the heart. J Mol Cell Cardiol. 2015;86:158-167. doi: 10. 1016/j. yjmcc. 2015. 07. 027.
160. Oyabu J, Yamaguchi O, Hikoso S, Takeda T, Oka T, Murakawa T, Yasui H, Ueda H, Nakayama H, Taneike M, Omiya S, Shah AM, Nishida K, Otsu K. Autophagy-mediated degradation is necessary for regression of cardiac hypertrophy during ventricular unloading. Biochem Biophys Res Commun. 2013;441:787-792. doi: 10. 1016/j. bbrc. 2013. 10. 135.
161. Nakai A, Yamaguchi O, Takeda T, Higuchi Y, Hikoso S, Taniike M, Omiya S, Mizote I, Matsumura Y, Asahi M, Nishida K, Hori M, Mizushima N, Otsu K. The role of autophagy in cardiomyocytes in the basal state and in response to hemodynamic stress. Nat Med. 2007;13:619-624. doi: 10. 1038/nm1574.
162. Pyo JO, Yoo SM, Ahn HH, Nah J, Hong SH, Kam TI, Jung S, Jung YK. Overexpression of Atg5 in mice activates autophagy and extends lifespan. Nat Commun. 2013;4:2300. doi: 10. 1038/ncomms3300.
163. Wang X, Terpstra EJ. Ubiquitin receptors and protein quality control. J Mol Cell Cardiol. 2013;55:73-84. doi: 10. 1016/j. yjmcc. 2012. 09. 012.
164. Mino T, Takeuchi O. Post-transcriptional regulation of cytokine mRNA controls the initiation and resolution of inflammation. Biotechnol Genet Eng Rev. 2013;29:49-60. doi: 10. 1080/02648725. 2013. 801236.
165. Carballo E, Blackshear PJ. Roles of tumor necrosis factor-alpha receptor subtypes in the pathogenesis of the tristetraprolin-deficiency syndrome. Blood. 2001;98:2389-2395.
166. Hikoso S, Yamaguchi O, Higuchi Y, et al. Pressure overload induces cardiac dysfunction and dilation in signal transducer and activator of transcription 6-deficient mice. Circulation. 2004;110:2631-2637. doi: 10. 1161/01. CIR. 0000146798. 70980. 9A.
167. Wang Y, Hekimi S. Mitochondrial dysfunction and longevity in animals: Untangling the knot. Science. 2015;350:1204-1207. doi: 10. 1126/science. Aac4357.
168. Loffredo FS, Steinhauser ML, Jay SM, et al. Growth differentiation factor 11 is a circulating factor that reverses age-related cardiac hypertrophy. Cell. 2013;153:828-839. doi: 10. 1016/j. cell. 2013. 04. 015.
169. Smith SC, Zhang X, Zhang X, et al. GDF11 does not rescue aging-related pathological hypertrophy. Circ Res. 2015;117:926-932. doi: 10. 1161/ CIRCRESAHA. 115. 307527.
170. Egerman MA, Cadena SM, Gilbert JA, et al. GDF11 Increases with Age and Inhibits Skeletal Muscle Regeneration. Cell Metab. 2015;22:164-174. doi: 10. 1016/j. cmet. 2015. 05. 010.
171. Vasto S, Candore G, Balistreri CR, Caruso M, Colonna-Romano G, Grimaldi MP, Listi F, Nuzzo D, Lio D, Caruso C. Inflammatory networks in ageing, age-related diseases and longevity. Mech Ageing Dev. 2007;128:83-91. doi: 10. 1016/j. mad. 2006. 11. 015.