Proteostasis and ageing: insights from long-lived mutant mice

Journal of Physiology

Volumn 595, Issue 20, 2017, Pages 6383-6390

  Sands, William A ^a   Page, Melissa M ^b   Selman, Colin ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

ageing; endoplasmin reticulum stress; immunoproteasome; longevity; proteasome; proteostasis; unfolded protein response

Indexed keywords

GROWTH HORMONE; INSULIN; MAMMALIAN TARGET OF RAPAMYCIN; PROTEOME; SOMATOMEDIN C; UBIQUITIN;

AGING; AUTOPHAGY; ENDOPLASMIC RETICULUM STRESS; GENE MUTATION; HUMAN; LIFE EXPECTANCY; LIFE EXTENSION; LONGEVITY; METABOLIC PARAMETERS; MOUSE MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN HOMEOSTASIS; PROTEOMICS; REVIEW; SIGNAL TRANSDUCTION; UBIQUITIN PROTEASOME SYSTEM; UNFOLDED PROTEIN RESPONSE; ANIMAL; METABOLISM; MOUSE; MUTANT MOUSE STRAIN;

AGING; ANIMALS; ENDOPLASMIC RETICULUM STRESS; HUMANS; LONGEVITY; MICE; MICE, MUTANT STRAINS; PROTEOSTASIS; UNFOLDED PROTEIN RESPONSE;

EID: 85026665099     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/JP274334     Document Type: Review

References (69)

1. Arif A, Terenzi F, Potdar AA, Jia J, Sacks J, China A, Halawani D, Vasu K, Li X, Brown JM, Chen J, Kozma SC, Thomas G & Fox PL (2017). EPRS is a critical mTORC1-S6K1 effector that influences adiposity in mice. Nature 542, 357–361.
2. Bennett CF, Vander Wende H, Simko M, Klum S, Barfield S, Choi H, Pineda VV & Kaeberlein M (2014). Activation of the mitochondrial unfolded protein response does not predict longevity in Caenorhabditis elegans. Nat Commun 5, 3483.
3. Bobkova NV, Evgen'ev M, Garbuz DG, Kulikov AM, Morozov A, Samokhin A, Velmeshev D, Medvinskaya N, Nesterova I, Pollock A & Nudler E (2015). Exogenous Hsp70 delays senescence and improves cognitive function in aging mice. Proc Natl Acad Sci USA 112, 16006–16011.
4. Brown-Borg HM, Borg KE, Meliska CJ & Bartke A (1996). Dwarf mice and the ageing process. Nature 384, 33.
5. Carmona-Gutierrez D, Hughes AL, Madeo F & Ruckenstuhl C (2016). The crucial impact of lysosomes in aging and longevity. Ageing Res Rev 32, 2–12.
6. Carrard G, Dieu M, Raes M, Toussaint O & Friguet B (2003). Impact of ageing on proteasome structure and function in human lymphocytes. Int J Biochem Cell Biol 35, 728–739.
7. Chondrogianni N, Georgila K, Kourtis N, Tavernarakis N & Gonos ES (2015). 20S proteasome activation promotes life span extension and resistance to proteotoxicity in Caenorhabditis elegans. FASEB J 29, 611–622.
8. Chondrogianni N, Petropoulos I, Franceschi C, Friguet B & Gonos ES (2000). Fibroblast cultures from healthy centenarians have an active proteasome. Exp Gerontol 35, 721–728.
9. Coschigano KT, Holland AN, Riders ME, List EO, Flyvbjerg A & Kopchick JJ (2003). Deletion, but not antagonism, of the mouse growth hormone receptor results in severely decreased body weights, insulin, and insulin-like growth factor I levels and increased life span. Endocrinology 144, 3799–3810.
10. Deelen J, Uh HW, Monajemi R, van Heemst D, Thijssen PE, Bohringer S, van den Akker EB, de Craen AJ, Rivadeneira F, Uitterlinden AG, Westendorp RG, Goeman JJ, Slagboom PE, Houwing-Duistermaat JJ & Beekman M (2013). Gene set analysis of GWAS data for human longevity highlights the relevance of the insulin/IGF-1 signaling and telomere maintenance pathways. Age (Dordr) 35, 235–249.
11. Ding WX, Ni HM, Gao W, Yoshimori T, Stolz DB, Ron D & Yin XM (2007). Linking of autophagy to ubiquitin-proteasome system is important for the regulation of endoplasmic reticulum stress and cell viability. Am J Pathol 171, 513–524.
12. Duran-Aniotz C, Cornejo VH, Espinoza S, Ardiles AO, Medinas DB, Salazar C, Foley A, Gajardo I, Thielen P, Iwawaki T, Scheper W, Soto C, Palacios AG, Hoozemans JJ & Hetz C (2017). IRE1 signaling exacerbates Alzheimer's disease pathogenesis. Acta Neuropathol 134, 489–506.
13. Gems D & Partridge L (2013). Genetics of longevity in model organisms: debates and paradigm shifts. Annu Rev Physiol 75, 621–644.
14. Ghazi A, Henis-Korenblit S & Kenyon C (2007). Regulation of Caenorhabditis elegans lifespan by a proteasomal E3 ligase complex. Proc Natl Acad Sci USA 104, 5947–5952.
15. Grune T, Shringarpure R, Sitte N & Davies K (2001). Age-related changes in protein oxidation and proteolysis in mammalian cells. J Gerontol A Biol Sci Med Sci 56, B459–467.
16. 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 (2009). Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 460, 392–395.
17. Henis-Korenblit S, Zhang P, Hansen M, McCormick M, Lee SJ, Cary M & Kenyon C (2010). Insulin/IGF-1 signaling mutants reprogram ER stress response regulators to promote longevity. Proc Natl Acad Sci USA 107, 9730–9735.
18. Hofmann JW, Zhao X, De Cecco M, Peterson AL, Pagliaroli L, Manivannan J, Hubbard GB, Ikeno Y, Zhang Y, Feng B, Li X, Serre T, Qi W, Van Remmen H, Miller RA, Bath KG, de Cabo R, Xu H, Neretti N & Sedivy JM (2015). Reduced expression of MYC increases longevity and enhances healthspan. Cell 160, 477–488.
19. Houtkooper RH, Mouchiroud L, Ryu D, Moullan N, Katsyuba E, Knott G, Williams RW & Auwerx J (2013). Mitonuclear protein imbalance as a conserved longevity mechanism. Nature 497, 451–457.
20. Johnston-Carey HK, Pomatto LC & Davies KJ (2015). The immunoproteasome in oxidative stress, aging, and disease. Crit Rev Biochem Mol Biol 51, 268–281.
21. Jovaisaite V & Auwerx J (2015). The mitochondrial unfolded protein response-synchronizing genomes. Curr Opin Cell Biol 33, 74–81.
22. Jung T & Grune T (2012). Structure of the proteasome. Prog Mol Biol Transl Sci 109, 1–39.
23. Kruegel U, Robison B, Dange T, Kahlert G, Delaney JR, Kotireddy S, Tsuchiya M, Tsuchiyama S, Murakami CJ, Schleit J, Sutphin G, Carr D, Tar K, Dittmar G, Kaeberlein M, Kennedy BK & Schmidt M (2011). Elevated proteasome capacity extends replicative lifespan in Saccharomyces cerevisiae. PLoS Genet 7, e1002253.
24. Labbadia J & Morimoto RI (2015). The biology of proteostasis in aging and disease. Annu Rev Biochem 84, 435–464.
25. Lamming DW, Ye L, Sabatini DM & Baur JA (2013). Rapalogs and mTOR inhibitors as anti-aging therapeutics. J Clin Invest 123, 980–989.
26. Lapierre LR, Kumsta C, Sandri M, Ballabio A & Hansen M (2015). Transcriptional and epigenetic regulation of autophagy in aging. Autophagy 11, 867–880.
27. +/− mice. J Biol Chem 283, 26217–26227.
28. Li W, Li X & Miller RA (2014). ATF4 activity: a common feature shared by many kinds of slow-aging mice. Aging Cell 13, 1012–1018.
29. Li W & Miller RA (2015). Elevated ATF4 function in fibroblasts and liver of slow-aging mutant mice. J Gerontol A Biol Sci Med Sci 70, 263–272.
30. Li Y & de Magalhaes JP (2013). Accelerated protein evolution analysis reveals genes and pathways associated with the evolution of mammalian longevity. Age (Dordr) 35, 301–314.
31. Lin YF, Schulz AM, Pellegrino MW, Lu Y, Shaham S & Haynes CM (2016). Maintenance and propagation of a deleterious mitochondrial genome by the mitochondrial unfolded protein response. Nature 533, 416–419.
32. Liu HY & Pfleger CM (2013). Mutation in E1, the ubiquitin activating enzyme, reduces Drosophila lifespan and results in motor impairment. PLoS One 8, e32835.
33. Luis NM, Wang L, Ortega M, Deng H, Katewa SD, Li PW, Karpac J, Jasper H & Kapahi P (2016). Intestinal IRE1 is required for increased triglyceride metabolism and longer lifespan under dietary restriction. Cell Reports 17, 1207–1216.
34. McKinnon C & Tabrizi SJ (2014). The ubiquitin-proteasome system in neurodegeneration. Antioxid Redox Signal 21, 2302–2321.
35. Matilainen O, Arpalahti L, Rantanen V, Hautaniemi S & Holmberg CI (2013). Insulin/IGF-1 signaling regulates proteasome activity through the deubiquitinating enzyme UBH-4. Cell Reports 3, 1980–1995.
36. Merkwirth C, Jovaisaite V, Durieux J, Matilainen O, Jordan SD, Quiros PM, Steffen KK, Williams EG, Mouchiroud L, Tronnes SU, Murillo V, Wolff SC, Shaw RJ, Auwerx J & Dillin A (2016). Two conserved histone demethylases regulate mitochondrial stress-induced longevity. Cell 165, 1209–1223.
37. Min JN, Whaley RA, Sharpless NE, Lockyer P, Portbury AL & Patterson C (2008). CHIP deficiency decreases longevity, with accelerated aging phenotypes accompanied by altered protein quality control. Mol Cell Biol 28, 4018–4025.
38. Mitchell SJ, Madrigal-Matute J, Scheibye-Knudsen M, Fang E, Aon M, Gonzalez-Reyes JA, Cortassa S, Kaushik S, Gonzalez-Freire M, Patel B, Wahl D, Ali A, Calvo-Rubio M, Buron MI, Guiterrez V, Ward TM, Palacios HH, Cai H, Frederick DW, Hine C, Broeskamp F, Habering L, Dawson J, Beasley TM, Wan J, Ikeno Y, Hubbard G, Becker KG, Zhang Y, Bohr VA, Longo DL, Navas P, Ferrucci L, Sinclair DA, Cohen P, Egan JM, Mitchell JR, Baur JA, Allison DB, Anson RM, Villalba JM, Madeo F, Cuervo AM, Pearson KJ, Ingram DK, Bernier M & de Cabo R (2016). Effects of sex, strain, and energy intake on hallmarks of aging in mice. Cell Metab 23, 1093–1112.
39. Moll L, Ben-Gedalya T, Reuveni H & Cohen E (2016). The inhibition of IGF-1 signaling promotes proteostasis by enhancing protein aggregation and deposition. FASEB J 30, 1656–1669.
40. Mulvey L, Sands WA, Salin K, Carr AE & Selman C (2016). Disentangling the effect of dietary restriction on mitochondrial function using recombinant inbred mice. Mol Cell Endocrinol 455, 41–53.
41. Naidoo N (2009). ER and aging-Protein folding and the ER stress response. Ageing Res Rev 8, 150–159.
42. Novosyadlyy R, Kurshan N, Lann D, Vijayakumar A, Yakar S & LeRoith D (2008). Insulin-like growth factor-I protects cells from ER stress-induced apoptosis via enhancement of the adaptive capacity of endoplasmic reticulum. Cell Death Differ 15, 1304–1317.
43. Nuss JE, Choksi KB, DeFord JH & Papaconstantinou J (2008). Decreased enzyme activities of chaperones PDI and BiP in aged mouse livers. Biochem Biophys Res Commun 365, 355–361.
44. O'Brien D & van Oosten-Hawle P (2016). Regulation of cell-non-autonomous proteostasis in metazoans. Essays Biochem 60, 133–142.
45. Owusu-Ansah E, Song W & Perrimon N (2013). Muscle mitohormesis promotes longevity via systemic repression of insulin signaling. Cell 155, 699–712.
46. Page MM, Sinclair A, Robb EL, Stuart JA, Withers DJ & Selman C (2014). Fibroblasts derived from long-lived insulin receptor substrate 1 null mice are not resistant to multiple forms of stress. Aging Cell 13, 962–964.
47. Passtoors WM, Beekman M, Deelen J, van der Breggen R, Maier AB, Guigas B, Derhovanessian E, van Heemst D, de Craen AJ, Gunn DA, Pawelec G & Slagboom PE (2013). Gene expression analysis of mTOR pathway: association with human longevity. Aging Cell 12, 24–31.
48. Pharaoh G, Pulliam D, Hill S, Sataranatarajan K & Van Remmen H (2016). Ablation of the mitochondrial complex IV assembly protein Surf1 leads to increased expression of the UPR(MT) and increased resistance to oxidative stress in primary cultures of fibroblasts. Redox Biol 8, 430–438.
49. Pickering AM, Lehr M & Miller RA (2015). Lifespan of mice and primates correlates with immunoproteasome expression. J Clin Invest 125, 2059–2068.
50. Pride H, Yu Z, Sunchu B, Mochnick J, Coles A, Zhang Y, Buffenstein R, Hornsby PJ, Austad SN & Perez VI (2015). Long-lived species have improved proteostasis compared to phylogenetically-related shorter-lived species. Biochem Biophys Res Commun 457, 669–675.
51. Rana A, Rera M & Walker DW (2013). Parkin overexpression during aging reduces proteotoxicity, alters mitochondrial dynamics, and extends lifespan. Proc Natl Acad Sci USA 110, 8638–8643.
52. Rauthan M, Ranji P, Abukar R & Pilon M (2015). A mutation in Caenorhabditis elegans NDUF-7 activates the mitochondrial stress response and prolongs lifespan via ROS and CED-4. G3 (Bethesda) 5, 1639–1648.
53. Raynes R, Juarez C, Pomatto LC, Sieburth D & Davies KJ (2017). Aging and SKN-1-dependent loss of 20S proteasome adaptation to oxidative stress in C. elegans. J Gerontol A Biol Sci Med Sci 72, 143–151.
54. Ristow M & Schmeisser S (2011). Extending life span by increasing oxidative stress. Free Radic Biol Med 51, 327–336.
55. Rodriguez KA, Valentine JM, Kramer DA, Gelfond JA, Kristan DM, Nevo E & Buffenstein R (2016). Determinants of rodent longevity in the chaperone-protein degradation network. Cell Stress Chaperones 21, 453–466.
56. Sadighi Akha AA, Harper JM, Salmon AB, Schroeder BA, Tyra HM, Rutkowski DT & Miller RA (2011). Heightened induction of proapoptotic signals in response to endoplasmic reticulum stress in primary fibroblasts from a mouse model of longevity. J Biol Chem 286, 30344–30351.
57. Salmon AB, Sadighi Akha AA, Buffenstein R & Miller RA (2008). Fibroblasts from naked mole-rats are resistant to multiple forms of cell injury, but sensitive to peroxide, ultraviolet light, and endoplasmic reticulum stress. J Gerontol A Biol Sci Med Sci 63, 232–241.
58. Salway KD, Gallagher EJ, Page MM & Stuart JA (2011a). Higher levels of heat shock proteins in longer-lived mammals and birds. Mech Ageing Dev 132, 287–297.
59. Salway KD, Page MM, Faure PA, Burness G & Stuart JA (2011b). Enhanced protein repair and recycling are not correlated with longevity in 15 vertebrate endotherm species. Age (Dordr) 33, 33–47.
60. Selman C (2014). Dietary restriction and the pursuit of effective mimetics. Proc Nutr Soc 73, 260–270.
61. Selman C, Lingard S, Choudhury AI, Batterham RL, Claret M, Clements M, Ramadani F, Okkenhaug K, Schuster E, Blanc E, Piper MD, Al-Qassab H, Speakman JR, Carmignac D, Robinson IC, Thornton JM, Gems D, Partridge L & Withers DJ (2008). Evidence for lifespan extension and delayed age-related biomarkers in insulin receptor substrate 1 null mice. FASEB J 22, 807–818.
62. Selman C, Tullet JM, Wieser D, Irvine E, Lingard SJ, Choudhury AI, Claret M, Al-Qassab H, Carmignac D, Ramadani F, Woods A, Robinson IC, Schuster E, Batterham RL, Kozma SC, Thomas G, Carling D, Okkenhaug K, Thornton JM, Partridge L, Gems D & Withers DJ (2009). Ribosomal protein S6 kinase 1 signaling regulates mammalian life span. Science 326, 140–144.
63. Shore DE, Carr CE & Ruvkun G (2012). Induction of cytoprotective pathways is central to the extension of lifespan conferred by multiple longevity pathways. PLoS Genet 8, e1002792.
64. Swindell WR, Masternak MM, Kopchick JJ, Conover CA, Bartke A & Miller RA (2009). Endocrine regulation of heat shock protein mRNA levels in long-lived dwarf mice. Mech Ageing Dev 130, 393–400.
65. Tawo R, Pokrzywa W, Kevei E, Akyuz ME, Balaji V, Adrian S, Hohfeld J & Hoppe T (2017). The ubiquitin ligase CHIP integrates proteostasis and aging by regulation of insulin receptor turnover. Cell 169, 470–482 e413.
66. Taylor RC & Dillin A (2013). XBP-1 is a cell-nonautonomous regulator of stress resistance and longevity. Cell 153, 1435–1447.
67. Tonoki A, Kuranaga E, Tomioka T, Hamazaki J, Murata S, Tanaka K & Miura M (2009). Genetic evidence linking age-dependent attenuation of the 26S proteasome with the aging process. Mol Cell Biol 29, 1095–1106.
68. Vilchez D, Saez I & Dillin A (2014). The role of protein clearance mechanisms in organismal ageing and age-related diseases. Nat Commun 5, 5659.
69. Zhang HM, Fu J, Hamilton R, Diaz V & Zhang Y (2015). The mammalian target of rapamycin modulates the immunoproteasome system in the heart. J Mol Cell Cardiol 86, 158–167.