Protein aggregates are associated with replicative aging without compromising protein quality control

eLife

Volumn 4, Issue NOVEMBER2015, 2015, Pages

  Saarikangas, Juha ^a   Barral, Yves ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN 104; HEAT SHOCK PROTEIN 70; PRION PROTEIN; PROTEASOME; PROTEIN AGGREGATE; UBIQUITIN; SACCHAROMYCES CEREVISIAE PROTEIN;

AGING; ARABIDOBSIS THALIANA; ARTICLE; CELL CULTURE; CELL DIVISION; CELL SURFACE DISPLAY; LIFESPAN; MICROFLUIDICS; NONHUMAN; PROTEIN HOMEOSTASIS; PROTEIN PROTEIN INTERACTION; PROTEIN QUALITY; PROTEIN REFOLDING; UBIQUITINATION; YEAST; CELL AGING; METABOLISM; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE;

CELL AGING; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN AGGREGATES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84949945857     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.06197     Document Type: Article

References (76)

1. Aguilaniu H, Gustafsson L, Rigoulet M, Nystrom T. 2003. Asymmetric inheritance of oxidatively damaged proteins during cytokinesis. Science 299:1751-1753. doi: 10.1126/science.1080418.
2. Andersson V, Hanzen S, Liu B, Molin M, Nystrom T. 2013. Enhancing protein disaggregation restores proteasome activity in aged cells. Aging 5:802-812.
3. Bennett EJ, Bence NF, Jayakumar R, Kopito RR. 2005. Global impairment of the ubiquitin-proteasome system by nuclear or cytoplasmic protein aggregates precedes inclusion body formation. Molecular Cell 17:351-365. doi: 10.1016/j.molcel.2004.12.021.
4. Bufalino MR, DeVeale B, van der Kooy D. 2013. The asymmetric segregation of damaged proteins is stem cell-type dependent. The Journal of Cell Biology 201:523-530. doi: 10.1083/jcb.201207052.
5. Caudron F, Barral Y. 2013. A super-assembly of Whi3 encodes memory of deceptive encounters by single cells during yeast courtship. Cell 155:1244-1257. doi: 10.1016/j.cell.2013.10.046.
6. Chernoff YO, Derkach IL, Inge-Vechtomov SG. 1993. Multicopy SUP35 gene induces de-novo appearance of psi-like factors in the yeast Saccharomyces cerevisiae. Current Genetics 24:268-270. doi: 10.1007/BF00351802.
7. Chong YT, Koh JL, Friesen H, Duffy SK, Cox MJ, Moses A, Moffat J, Boone C, Andrews BJ. 2015. Yeast proteome dynamics from single cell imaging and automated analysis. Cell 161:1413-1424. doi: 10.1016/j.cell.2015.04.051.
8. Clay L, Caudron F, Denoth-Lippuner A, Boettcher B, Buvelot Frei S, Snapp EL, Barral Y. 2014. A sphingolipid-dependent diffusion barrier confines ER stress to the yeast mother cell. eLife 3:e01883. doi: 10.7554/eLife.01883.
9. Coelho M, Dereli A, Haese A, Kühn S, Malinovska L, DeSantis ME, Shorter J, Alberti S, Gross T, Tolić-Nørrelykke IM. 2013. Fission yeast does not age under favorable conditions, but does so after stress. Current Biology 23:1844-1852. doi: 10.1016/j.cub.2013.07.084.
10. Coelho M, Lade SJ, Alberti S, Gross T, Tolic IM. 2014. Fusion of protein aggregates facilitates asymmetric damage segregation. PLOS Biology 12:e1001886. doi: 10.1371/journal.pbio.1001886.
11. Decker CJ, Teixeira D, Parker R. 2007. Edc3p and a glutamine/asparagine-rich domain of Lsm4p function in processing body assembly in Saccharomyces cerevisiae. The Journal of Cell Biology 179:437-449. doi: 10.1083/jcb.200704147.
12. Denoth Lippuner A, Julou T, Barral Y. 2014. Budding yeast as a model organism to study the effects of age. FEMS Microbiology Reviews 38:300-325. doi: 10.1111/1574-6976.12060.
13. Denoth-Lippuner A, Krzyzanowski MK, Stober C, Barral Y. 2014. Role of SAGA in the asymmetric segregation of DNA circles during yeast ageing. eLife 3:e03790. doi: 10.7554/eLife.03790.
14. Derdowski A, Sindi SS, Klaips CL, DiSalvo S, Serio TR. 2010. A size threshold limits prion transmission and establishes phenotypic diversity. Science 330:680-683. doi: 10.1126/science.1197785.
15. Duennwald ML, Echeverria A, Shorter J. 2012. Small heat shock proteins potentiate amyloid dissolution by protein disaggregases from yeast and humans. PLOS Biology 10:e1001346. doi: 10.1371/journal.pbio.1001346.
16. Erjavec N, Larsson L, Grantham J, Nystrom T. 2007. Accelerated aging and failure to segregate damaged proteins in Sir2 mutants can be suppressed by overproducing the protein aggregation-remodeling factor Hsp104p. Genes & Development 21:2410-2421. doi: 10.1101/gad.439307.
17. Escusa-Toret S, Vonk WI, Frydman J. 2013. Spatial sequestration of misfolded proteins by a dynamic chaperone pathway enhances cellular fitness during stress. Nature Cell Biology 15:1231-1243. doi: 10.1038/ncb2838.
18. Glover JR, Lindquist S. 1998. Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 94:73-82. doi: 10.1016/S0092-8674(00)81223-4.
19. Hartl FU, Bracher A, Hayer-Hartl M. 2011. Molecular chaperones in protein folding and proteostasis. Nature 475:324-332. doi: 10.1038/nature10317.
20. Haslberger T, Bukau B, Mogk A. 2010. Towards a unifying mechanism for ClpB/Hsp104-mediated protein disaggregation and prion propagation. Biochemistry and Cell Biology 88:63-75. doi: 10.1139/o09-118.
21. Henderson KA, Gottschling DE. 2008. A mother’s sacrifice: what is she keeping for herself? Current Opinion in Cell Biology 20:723-728. doi: 10.1016/j.ceb.2008.09.004.
22. Henderson KA, Hughes AL, Gottschling DE. 2014. Mother-daughter asymmetry of pH underlies aging and rejuvenation in yeast. eLife 3. doi: 10.7554/eLife.03504.
23. Higuchi R, Vevea JD, Swayne TC, Chojnowski R, Hill V, Boldogh IR, Pon LA. 2013. Actin dynamics affect mitochondrial quality control and aging in budding yeast. Current Biology 23:2417-2422. doi: 10.1016/j.cub.2013.10.022.
24. Higuchi-Sanabria R, Pernice WM, Vevea JD, Alessi Wolken DM, Boldogh IR, Pon LA. 2014. Role of asymmetric cell division in lifespan control in Saccharomyces cerevisiae. FEMS Yeast Research 14:1133-1146. doi: 10.1111/1567-1364.12216.
25. Hill SM, Hao X, Liu B, Nystrom T. 2014. Life-span extension by a metacaspase in the yeast Saccharomyces cerevisiae. Science 344:1389-1392. doi: 10.1126/science.1252634.
26. Hughes AL, Gottschling DE. 2012. An early age increase in vacuolar pH limits mitochondrial function and lifespan in yeast. Nature 492:261-265. doi: 10.1038/nature11654.
27. Hyman AA, Weber CA, Julicher F. 2014. Liquid-liquid phase separation in biology. Annual Review of Cell and Developmental Biology 30:39-58. doi: 10.1146/annurev-cellbio-100913-013325.
28. Kaeberlein M, McVey M, Guarente L. 1999. The SIR2/3/4 complex and SIR2 alone promote longevity in Saccharomyces cerevisiae by two different mechanisms. Genes & Development 13:2570-2580. doi: 10.1101/gad.13.19.2570.
29. Kaganovich D, Kopito R, Frydman J. 2008. Misfolded proteins partition between two distinct quality control compartments. Nature 454:1088-1095. doi: 10.1038/nature07195.
30. Katajisto P, D öhla J, Chaffer CL, Pentinmikko N, Marjanovic N, Iqbal S, Zoncu R, Chen W, Weinberg RA, Sabatini DM. 2015. Stem cells. Asymmetric apportioning of aged mitochondria between daughter cells is required for stemness. Science 348:340-343. doi: 10.1126/science.1260384.
31. Kim YE, Hipp MS, Bracher A, Hayer-Hartl M, Hartl FU. 2013. Molecular chaperone functions in protein folding and proteostasis. Annual Review of Biochemistry 82:323-355. doi: 10.1146/annurev-biochem-060208-092442.
32. Kroschwald S, Maharana S, Mateju D, Malinovska L, Nüske E, Poser I, Richter D, Alberti S. 2015. Promiscuous interactions and protein disaggregases determine the material state of stress-inducible RNP granules. eLife 4:e06807. doi: 10.7554/eLife.06807.
33. Kryndushkin DS, Shewmaker F, Wickner RB. 2008. Curing of the [URE3] prion by Btn2p, a Batten disease-related protein. The EMBO Journal 27:2725-2735. doi: 10.1038/emboj.2008.198.
34. 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 Genetics 7:e1002253. doi: 10.1371/journal.pgen.1002253.
35. Kryndushkin D, Ihrke G, Piermartiri TC, Shewmaker F. 2012. A yeast model of optineurin proteinopathy reveals a unique aggregation pattern associated with cellular toxicity. Molecular Microbiology 86:1531-1547. doi: 10.1111/mmi.12075.
36. Lee RE, Brunette S, Puente LG, Megeney LA. 2010. Metacaspase Yca1 is required for clearance of insoluble protein aggregates. Proceedings of the National Academy of Sciences of USA 107:13348-13353. doi: 10.1073/pnas.1006610107.
37. Lee SS, Avalos Vizcarra I, Huberts DH, Lee LP, Heinemann M. 2012. Whole lifespan microscopic observation of budding yeast aging through a microfluidic dissection platform. Proceedings of the National Academy of Sciences of USA 109:4916-4920. doi: 10.1073/pnas.1113505109.
38. Lindstrom DL, Gottschling DE. 2009. The mother enrichment program: a genetic system for facile replicative life span analysis in Saccharomyces cerevisiae. Genetics 183:413-422. 411SI-413SI. doi: 10.1534/genetics.109.106229.
39. Liu B, Larsson L, Caballero A, Hao X, Oling D, Grantham J, Nystr öm T. 2010. The polarisome is required for segregation and retrograde transport of protein aggregates. Cell 140:257-267. doi: 10.1016/j.cell.2009.12.031.
40. Lopez-Otin C, Blasco MA, Partridge L, Serrano M, Kroemer G. 2013. The hallmarks of aging. Cell 153:1194-1217. doi: 10.1016/j.cell.2013.05.039.
41. Malinovska L, Kroschwald S, Munder MC, Richter D, Alberti S. 2012. Molecular chaperones and stress-inducible protein-sorting factors coordinate the spatiotemporal distribution of protein aggregates. Molecular Biology of the Cell 23:3041-3056. doi: 10.1091/mbc.E12-03-0194.
42. McFaline-Figueroa JR, Vevea J, Swayne TC, Zhou C, Liu C, Leung G, Boldogh IR, Pon LA. 2011. Mitochondrial quality control during inheritance is associated with lifespan and mother-daughter age asymmetry in budding yeast. Aging Cell 10:885-895. doi: 10.1111/j.1474-9726.2011.00731.x.
43. McMurray MA, Gottschling DE. 2003. An age-induced switch to a hyper-recombinational state. Science 301:1908-1911. doi: 10.1126/science.1087706.
44. Miller SB, Ho CT, Winkler J, Khokhrina M, Neuner A, Mohamed MY, Guilbride DL, Richter K, Lisby M, Schiebel E, Mogk A, Bukau B. 2015. Compartment-specific aggregases direct distinct nuclear and cytoplasmic aggregate deposition. The EMBO Journal 34:778-797. doi: 10.15252/embj.201489524.
45. Moldavski O, Amen T, Levin-Zaidman S, Eisenstein M, Rogachev I, Brandis A, Kaganovich D, Schuldiner M. 2015. Lipid droplets are essential for efficient clearance of cytosolic inclusion bodies. Developmental Cell 33:603-610. doi: 10.1016/j.devcel.2015.04.015.
46. Neumuller RA, Knoblich JA. 2009. Dividing cellular asymmetry: asymmetric cell division and its implications for stem cells and cancer. Genes & Development 23:2675-2699. doi: 10.1101/gad.1850809.
47. Newby GA, Lindquist S. 2013. Blessings in disguise: biological benefits of prion-like mechanisms. Trends in Cell Biology 23:251-259. doi: 10.1016/j.tcb.2013.01.007.
48. Nishimura K, Fukagawa T, Takisawa H, Kakimoto T, Kanemaki M. 2009. An auxin-based degron system for the rapid depletion of proteins in nonplant cells. Nature Methods 6:917-922. doi: 10.1038/nmeth.1401.
49. Oling D, Eisele F, Kvint K, Nystrom T. 2014. Opposing roles of Ubp3-dependent deubiquitination regulate replicative life span and heat resistance. The EMBO Journal 33:747-761. doi: 10.1002/embj.201386822.
50. Osherovich LZ, Weissman JS. 2001. Multiple Gln/Asn-rich prion domains confer susceptibility to induction of the yeast [PSI(+)] prion. Cell 106:183-194. doi: 10.1016/S0092-8674(01)00440-8.
51. Park SH, Kukushkin Y, Gupta R, Chen T, Konagai A, Hipp MS, Hayer-Hartl M, Hartl FU. 2013. PolyQ proteins interfere with nuclear degradation of cytosolic proteins by sequestering the Sis1p chaperone. Cell 154:134-145. doi: 10.1016/j.cell.2013.06.003.
52. Parsell DA, Kowal AS, Singer MA, Lindquist S. 1994. Protein disaggregation mediated by heat-shock protein Hsp104. Nature 372:475-478. doi: 10.1038/372475a0.
53. Patino MM, Liu JJ, Glover JR, Lindquist S. 1996. Support for the prion hypothesis for inheritance of a phenotypic trait in yeast. Science 273:622-626. doi: 10.1126/science.273.5275.622.
54. Paushkin SV, Kushnirov VV, Smirnov VN, Ter-Avanesyan MD. 1996. Propagation of the yeast prion-like [psi+]determinant is mediated by oligomerization of the SUP35-encoded polypeptide chain release factor. The EMBO Journal 15:3127-3134.
55. Reijns MA, Alexander RD, Spiller MP, Beggs JD. 2008. A role for Q/N-rich aggregation-prone regions in P-body localization. Journal of Cell Science 121:2463-2472. doi: 10.1242/jcs.024976.
56. Rujano MA, Bosveld F, Salomons FA, Dijk F, van Waarde MA, van der Want JJ, de Vos RA, Brunt ER, Sibon OC, Kampinga HH. 2006. Polarised asymmetric inheritance of accumulated protein damage in higher eukaryotes. PLOS Biology 4:e417. doi: 10.1371/journal.pbio.0040417.
57. Saibil HR, Seybert A, Habermann A, Winkler J, Eltsov M, Perkovic M, Castano-Diez D, Scheffer MP, Haselmann U, Chlanda P, Lindquist S, Tyedmers J, Frangakis AS. 2012. Heritable yeast prions have a highly organized three- dimensional architecture with interfiber structures. Proceedings of the National Academy of Sciences of USA 109:14906-14911. doi: 10.1073/pnas.1211976109.
58. Shcheprova Z, Baldi S, Frei SB, Gonnet G, Barral Y. 2008. A mechanism for asymmetric segregation of age during yeast budding. Nature 454:728-734. doi: 10.1038/nature07212.
59. Shewmaker F, Wickner RB. 2006. Ageing in yeast does not enhance prion generation. Yeast 23:1123-1128. doi: 10.1002/yea.1425.
60. Sinclair DA, Guarente L. 1997. Extrachromosomal rDNA circles-a cause of aging in yeast. Cell 91:1033-1042. doi: 10.1016/S0092-8674(00)80493-6.
61. Song J, Yang Q, Yang J, Larsson L, Hao X, Zhu X, Malmgren-Hill S, Cvijovic M, Fernandez-Rodriguez J, Grantham J, Gustafsson CM, Liu B, Nystr öm T. 2014. Essential genetic interactors of SIR2 required for spatial sequestration and asymmetrical inheritance of protein aggregates. PLOS Genetics 10:e1004539. doi: 10.1371/journal.pgen.1004539.
62. Specht S, Miller SB, Mogk A, Bukau B. 2011. Hsp42 is required for sequestration of protein aggregates into deposition sites in Saccharomyces cerevisiae. The Journal of Cell Biology 195:617-629. doi: 10.1083/jcb.201106037.
63. Spokoini R, Moldavski O, Nahmias Y, England JL, Schuldiner M, Kaganovich D. 2012. Confinement to organelle- associated inclusion structures mediates asymmetric inheritance of aggregated protein in budding yeast. Cell Reports 2:738-747. doi: 10.1016/j.celrep.2012.08.024.
64. Ter-Avanesyan MD, Dagkesamanskaya AR, Kushnirov VV, Smirnov VN. 1994. The SUP35 omnipotent suppressor gene is involved in the maintenance of the non-Mendelian determinant [psi+] in the yeast Saccharomyces cerevisiae. Genetics 137:671-676.
65. Thayer NH, Leverich CK, Fitzgibbon MP, Nelson ZW, Henderson KA, Gafken PR, Hsu JJ, Gottschling DE. 2014. Identification of long-lived proteins retained in cells undergoing repeated asymmetric divisions. Proceedings of the National Academy of Sciences of USA 111:14019-14026. doi: 10.1073/pnas.1416079111.
66. Tyedmers J, Mogk A, Bukau B. 2010a. Cellular strategies for controlling protein aggregation. Nature Reviews Molecular Cell Biology 11:777-788. doi: 10.1038/nrm2993.
67. Tyedmers J, Treusch S, Dong J, McCaffery JM, Bevis B, Lindquist S. 2010b. Prion induction involves an ancient system for the sequestration of aggregated proteins and heritable changes in prion fragmentation. Proceedings of the National Academy of Sciences of USA 107:8633-8638. doi: 10.1073/pnas.1003895107.
68. Vilchez D, Saez I, Dillin A. 2014. The role of protein clearance mechanisms in organismal ageing and age-related diseases. Nature Communications 5:5659. doi: 10.1038/ncomms6659.
69. Wallace EW, Kear-Scott JL, Pilipenko EV, Schwartz MH, Laskowski PR, Rojek AE, Katanski CD, Riback JA, Dion MF, Franks AM, Airoldi EM, Pan T, Budnik BA, Drummond DA. 2015. Reversible, specific, active aggregates of endogenous proteins assemble upon heat stress. Cell 162:1286-1298. doi: 10.1016/j.cell.2015.08.041.
70. Webster BM, Colombi P, Jager J, Lusk CP. 2014. Surveillance of nuclear pore complex assembly by ESCRT-III/ Vps4. Cell 159:388-401. doi: 10.1016/j.cell.2014.09.012.
71. Wickner RB. 1994. [URE3] as an altered URE2 protein: evidence for a prion analog in Saccharomyces cerevisiae. Science 264:566-569. doi: 10.1126/science.7909170.
72. Winkler J, Tyedmers J, Bukau B, Mogk A. 2012. Hsp70 targets Hsp100 chaperones to substrates for protein disaggregation and prion fragmentation. The Journal of Cell Biology 198:387-404. doi: 10.1083/jcb.201201074.
73. Wolff S, Weissman JS, Dillin A. 2014. Differential scales of protein quality control. Cell 157:52-64. doi: 10.1016/j.cell.2014.03.007.
74. Xie Y, Varshavsky A. 2001. RPN4 is a ligand, substrate, and transcriptional regulator of the 26S proteasome: a negative feedback circuit. Proceedings of the National Academy of Sciences of USA 98:3056-3061. doi: 10.1073/pnas.071022298.
75. Zhou C, Slaughter BD, Unruh JR, Eldakak A, Rubinstein B, Li R. 2011. Motility and segregation of Hsp104-associated protein aggregates in budding yeast. Cell 147:1186-1196. doi: 10.1016/j.cell.2011.11.002.
76. Zhou C, Slaughter BD, Unruh JR, Guo F, Yu Z, Mickey K, Narkar A, Ross RT, McClain M, Li R. 2014. Organelle- based aggregation and retention of damaged proteins in asymmetrically dividing cells. Cell 159:530-542. doi: 10.1016/j.cell.2014.09.026.