Reversible Age-Related Phenotypes Induced during Larval Quiescence in C. Elegans

Cell Metabolism

Volumn 23, Issue 6, 2016, Pages 1113-1126

  Roux, Antoine E ^a,b   Langhans, Kelley ^a   Huynh, Walter ^a   Kenyon, Cynthia ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Calico Life Sciences LLC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DITHIOTHREITOL; KGB 1 PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN AGGREGATE; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1; CAENORHABDITIS ELEGANS PROTEIN;

AGE; AGING; ARTICLE; AUTOFLUORESCENCE; CAENORHABDITIS ELEGANS; CELL STRESS; COMPARATIVE STUDY; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; FAT CONTENT; LARVAL STAGE; LONGEVITY; MORTALITY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN HOMEOSTASIS; PROTEIN PHOSPHORYLATION; STARVATION; STRESS; UNFOLDED PROTEIN RESPONSE; WESTERN BLOTTING; ANIMAL; ENDOPLASMIC RETICULUM; FEEDING BEHAVIOR; GENETICS; LARVA; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

AGING; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; ENDOPLASMIC RETICULUM; FEEDING BEHAVIOR; LARVA; PHENOTYPE; PROTEIN AGGREGATES; STRESS, PHYSIOLOGICAL; UNFOLDED PROTEIN RESPONSE;

EID: 84975493695     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2016.05.024     Document Type: Article

References (66)

1. G. Angelo, and M.R. Van Gilst Starvation protects germline stem cells and extends reproductive longevity in C. Elegans Science 326 2009 954 958
2. J. Apfeld, and C. Kenyon Regulation of lifespan by sensory perception in Caenorhabditis elegans Nature 402 1999 804 809
3. J. Apfeld, G. O'Connor, T. McDonagh, P.S. DiStefano, and R. Curtis The AMP-activated protein kinase AAK-2 links energy levels and insulin-like signals to lifespan in C. Elegans Genes Dev. 18 2004 3004 3009
4. N.A. Baird, P.M. Douglas, M.S. Simic, A.R. Grant, J.J. Moresco, S.C. Wolff, J.R. Yates 3rd, G. Manning, and A. Dillin HSF-1-mediated cytoskeletal integrity determines thermotolerance and life span Science 346 2014 360 363
5. A.G. Barros, J. Liu, G.A. Lemieux, B.C. Mullaney, and K. Ashrafi Analyses of C. Elegans fat metabolic pathways Methods Cell Biol. 107 2012 383 407
6. L.R. Baugh To grow or not to grow: nutritional control of development during Caenorhabditis elegans L1 arrest Genetics 194 2013 539 555
7. L.R. Baugh, and P.W. Sternberg DAF-16/FOXO regulates transcription of cki-1/Cip/Kip and repression of lin-4 during C. Elegans L1 arrest Curr. Biol. 16 2006 780 785
8. A. Ben-Zvi, E.A. Miller, and R.I. Morimoto Collapse of proteostasis represents an early molecular event in Caenorhabditis elegans aging Proc. Natl. Acad. Sci. USA 106 2009 14914 14919
9. M. Calfon, H. Zeng, F. Urano, J.H. Till, S.R. Hubbard, H.P. Harding, S.G. Clark, and D. Ron IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA Nature 415 2002 92 96
10. C.-W. Cheng, G.B. Adams, L. Perin, M. Wei, X. Zhou, B.S. Lam, S. Da Sacco, M. Mirisola, D.I. Quinn, T.B. Dorff, and et al. Prolonged fasting reduces IGF-1/PKA to promote hematopoietic-stem-cell-based regeneration and reverse immunosuppression Cell Stem Cell 14 2014 810 823
11. T.H. Cheung, and T.A. Rando Molecular regulation of stem cell quiescence Nat. Rev. Mol. Cell Biol. 14 2013 329 340
12. I.M. Conboy, M.J. Conboy, G.M. Smythe, and T.A. Rando Notch-mediated restoration of regenerative potential to aged muscle Science 302 2003 1575 1577
13. I.M. Conboy, M.J. Conboy, A.J. Wagers, E.R. Girma, I.L. Weissman, and T.A. Rando Rejuvenation of aged progenitor cells by exposure to a young systemic environment Nature 433 2005 760 764
14. B.C.S. Cross, P.J. Bond, P.G. Sadowski, B.K. Jha, J. Zak, J.M. Goodman, R.H. Silverman, T.A. Neubert, I.R. Baxendale, D. Ron, and H.P. Harding The molecular basis for selective inhibition of unconventional mRNA splicing by an IRE1-binding small molecule Proc. Natl. Acad. Sci. USA 109 2012 E869 E878
15. D.C. David, N. Ollikainen, J.C. Trinidad, M.P. Cary, A.L. Burlingame, and C. Kenyon Widespread protein aggregation as an inherent part of aging in C. Elegans PLoS Biol. 8 2010 e1000450
16. J.R. Delaney, C. Murakami, A. Chou, D. Carr, J. Schleit, G.L. Sutphin, E.H. An, A.S. Castanza, M. Fletcher, S. Goswami, and et al. Dietary restriction and mitochondrial function link replicative and chronological aging in Saccharomyces cerevisiae Exp. Gerontol. 48 2013 1006 1013
17. F. Demontis, and N. Perrimon FOXO/4E-BP signaling in Drosophila muscles regulates organism-wide proteostasis during aging Cell 143 2010 813 825
18. D. Garigan, A.-L. Hsu, A.G. Fraser, R.S. Kamath, J. Ahringer, and C. Kenyon Genetic analysis of tissue aging in Caenorhabditis elegans: a role for heat-shock factor and bacterial proliferation Genetics 161 2002 1101 1112
19. P. Gerke, A. Keshet, A. Mertenskötter, and R.J. Paul The JNK-like MAPK KGB-1 of Caenorhabditis elegans promotes reproduction, lifespan, and gene expressions for protein biosynthesis and germline homeostasis but interferes with hyperosmotic stress tolerance Cell. Physiol. Biochem. 34 2014 1951 1973
20. B. Gerstbrein, G. Stamatas, N. Kollias, and M. Driscoll In vivo spectrofluorimetry reveals endogenous biomarkers that report healthspan and dietary restriction in Caenorhabditis elegans Aging Cell 4 2005 127 137
21. A. Ghazi, S. Henis-Korenblit, and C. Kenyon Regulation of Caenorhabditis elegans lifespan by a proteasomal E3 ligase complex Proc. Natl. Acad. Sci. USA 104 2007 5947 5952
22. J.-H. Hahm, S. Kim, R. DiLoreto, C. Shi, S.-J.V. Lee, C.T. Murphy, and H.G. Nam C. Elegans maximum velocity correlates with healthspan and is maintained in worms with an insulin receptor mutation Nat. Commun. 6 2015 8919
23. M. Hansen, S. Taubert, D. Crawford, N. Libina, S.-J. Lee, and C. Kenyon Lifespan extension by conditions that inhibit translation in Caenorhabditis elegans Aging Cell 6 2007 95 110
24. S. Henis-Korenblit, P. Zhang, M. Hansen, M. McCormick, S.J. Lee, M. Cary, and C. Kenyon Insulin/IGF-1 signaling mutants reprogram ER stress response regulators to promote longevity Proc. Natl. Acad. Sci. USA 107 2010 9730 9735
25. L.A. Herndon, P.J. Schmeissner, J.M. Dudaronek, P.A. Brown, K.M. Listner, Y. Sakano, M.C. Paupard, D.H. Hall, and M. Driscoll Stochastic and genetic factors influence tissue-specific decline in ageing C. Elegans Nature 419 2002 808 814
26. C. Hetz The unfolded protein response: controlling cell fate decisions under ER stress and beyond Nat. Rev. Mol. Cell Biol. 13 2012 89 102
27. A. Höhn, and T. Grune Lipofuscin: formation, effects and role of macroautophagy Redox Biol. 1 2013 140 144
28. J. Hollien, and J.S. Weissman Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response Science 313 2006 104 107
29. K. Houthoofd, B.P. Braeckman, I. Lenaerts, K. Brys, A. De Vreese, S. Van Eygen, and J.R. Vanfleteren Ageing is reversed, and metabolism is reset to young levels in recovering dauer larvae of C. Elegans Exp. Gerontol. 37 2002 1015 1021
30. A.-L. Hsu, C.T. Murphy, and C. Kenyon Regulation of aging and age-related disease by DAF-16 and heat-shock factor Science 300 2003 1142 1145
31. A.L. Hughes, and D.E. Gottschling An early age increase in vacuolar pH limits mitochondrial function and lifespan in yeast Nature 492 2012 261 265
32. M.A. Jobson, J.M. Jordan, M.A. Sandrof, J.D. Hibshman, A.L. Lennox, and L.R. Baugh Transgenerational effects of early life starvation on growth, reproduction, and stress resistance in Caenorhabditis elegans Genetics 201 2015 201 212
33. T.E. Johnson, D.H. Mitchell, S. Kline, R. Kemal, and J. Foy Arresting development arrests aging in the nematode Caenorhabditis elegans Mech. Ageing Dev. 28 1984 23 40
34. W.J. Kapulkin, B.G. Hiester, and C.D. Link Compensatory regulation among ER chaperones in C. Elegans FEBS Lett. 579 2005 3063 3068
35. C. Kenyon, J. Chang, E. Gensch, A. Rudner, and R. Tabtiang A C. Elegans mutant that lives twice as long as wild type Nature 366 1993 461 464
36. S. Kim, and Y.-K. Paik Developmental and reproductive consequences of prolonged non-aging dauer in Caenorhabditis elegans Biochem. Biophys. Res. Commun. 368 2008 588 592
37. J. Labbadia, and R.I. Morimoto Proteostasis and longevity: when does aging really begin? F1000Prime Rep. 6 2014 7
38. B.H. Lee, and K. Ashrafi A TRPV channel modulates C. Elegans neurosecretion, larval starvation survival, and adult lifespan PLoS Genet. 4 2008 e1000213
39. I. Lee, A. Hendrix, J. Kim, J. Yoshimoto, and Y.-J. You Metabolic rate regulates L1 longevity in C. Elegans PLoS ONE 7 2012 e44720
40. F.S. Loffredo, M.L. Steinhauser, S.M. Jay, J. Gannon, J.R. Pancoast, P. Yalamanchi, M. Sinha, C. Dall'Osso, D. Khong, J.L. Shadrach, and et al. Growth differentiation factor 11 is a circulating factor that reverses age-related cardiac hypertrophy Cell 153 2013 828 839
41. V.D. Longo, G.S. Shadel, M. Kaeberlein, and B. Kennedy Replicative and chronological aging in Saccharomyces cerevisiae Cell Metab. 16 2012 18 31
42. T. Mizuno, K. Fujiki, A. Sasakawa, N. Hisamoto, and K. Matsumoto Role of the Caenorhabditis elegans Shc adaptor protein in the c-Jun N-terminal kinase signaling pathway Mol. Cell. Biol. 28 2008 7041 7049
43. J.F. Morley, and R.I. Morimoto Regulation of longevity in Caenorhabditis elegans by heat shock factor and molecular chaperones Mol. Biol. Cell 15 2004 657 664
44. J.F. Morley, H.R. Brignull, J.J. Weyers, and R.I. Morimoto The threshold for polyglutamine-expansion protein aggregation and cellular toxicity is dynamic and influenced by aging in Caenorhabditis elegans Proc. Natl. Acad. Sci. USA 99 2002 10417 10422
45. M.J. Muñoz, and D.L. Riddle Positive selection of Caenorhabditis elegans mutants with increased stress resistance and longevity Genetics 163 2003 171 180
46. M. Ogata, S. Hino, A. Saito, K. Morikawa, S. Kondo, S. Kanemoto, T. Murakami, M. Taniguchi, I. Tanii, K. Yoshinaga, and et al. Autophagy is activated for cell survival after endoplasmic reticulum stress Mol. Cell. Biol. 26 2006 9220 9231
47. T.W. Peters, M.J. Rardin, G. Czerwieniec, U.S. Evani, P. Reis-Rodrigues, G.J. Lithgow, S.D. Mooney, B.W. Gibson, and R.E. Hughes Tor1 regulates protein solubility in Saccharomyces cerevisiae Mol. Biol. Cell 23 2012 4679 4688
48. E.T. Powers, R.I. Morimoto, A. Dillin, J.W. Kelly, and W.E. Balch Biological and chemical approaches to diseases of proteostasis deficiency Annu. Rev. Biochem. 78 2009 959 991
49. P. Reis-Rodrigues, G. Czerwieniec, T.W. Peters, U.S. Evani, S. Alavez, E.A. Gaman, M. Vantipalli, S.D. Mooney, B.W. Gibson, G.J. Lithgow, and R.E. Hughes Proteomic analysis of age-dependent changes in protein solubility identifies genes that modulate lifespan Aging Cell 11 2012 120 127
50. A.E. Roux, P. Chartrand, G. Ferbeyre, and L.A. Rokeach Fission yeast and other yeasts as emergent models to unravel cellular aging in eukaryotes J. Gerontol. A Biol. Sci. Med. Sci. 65 2010 1 8
51. C.Q. Scheckhuber, N. Erjavec, A. Tinazli, A. Hamann, T. Nyström, and H.D. Osiewacz Reducing mitochondrial fission results in increased life span and fitness of two fungal ageing models Nat. Cell Biol. 9 2007 99 105
52. K.J. Soprano WI-38 cell long-term quiescence model system: a valuable tool to study molecular events that regulate growth J. Cell. Biochem. 54 1994 405 414
53. P. Sousa-Victor, S. Gutarra, L. García-Prat, J. Rodriguez-Ubreva, L. Ortet, V. Ruiz-Bonilla, M. Jardí, E. Ballestar, S. González, A.L. Serrano, and et al. Geriatric muscle stem cells switch reversible quiescence into senescence Nature 506 2014 316 321
54. J.E. Sulston, and H.R. Horvitz Post-embryonic cell lineages of the nematode, Caenorhabditis elegans Dev. Biol. 56 1977 110 156
55. P. Syntichaki, K. Troulinaki, and N. Tavernarakis eIF4E function in somatic cells modulates ageing in Caenorhabditis elegans Nature 445 2007 922 926
56. M. Uno, S. Honjoh, M. Matsuda, H. Hoshikawa, S. Kishimoto, T. Yamamoto, M. Ebisuya, T. Yamamoto, K. Matsumoto, and E. Nishida A fasting-responsive signaling pathway that extends life span in C. Elegans Cell Rep. 3 2013 79 91
57. F. Urano, X. Wang, A. Bertolotti, Y. Zhang, P. Chung, H.P. Harding, and D. Ron Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1 Science 287 2000 664 666
58. J.R. Valcourt, J.M.S. Lemons, E.M. Haley, M. Kojima, O.O. Demuren, and H.A. Coller Staying alive: metabolic adaptations to quiescence Cell Cycle 11 2012 1680 1696
59. S.A. Villeda, J. Luo, K.I. Mosher, B. Zou, M. Britschgi, G. Bieri, T.M. Stan, N. Fainberg, Z. Ding, A. Eggel, and et al. The ageing systemic milieu negatively regulates neurogenesis and cognitive function Nature 477 2011 90 94
60. S.A. Villeda, K.E. Plambeck, J. Middeldorp, J.M. Castellano, K.I. Mosher, J. Luo, L.K. Smith, G. Bieri, K. Lin, D. Berdnik, and et al. Young blood reverses age-related impairments in cognitive function and synaptic plasticity in mice Nat. Med. 20 2014 659 663
61. D.M. Walther, P. Kasturi, M. Zheng, S. Pinkert, G. Vecchi, P. Ciryam, R.I. Morimoto, C.M. Dobson, M. Vendruscolo, M. Mann, and F.U. Hartl Widespread proteome remodeling and aggregation in aging C. Elegans Cell 161 2015 919 932
62. N. Watanabe, Y. Nagamatsu, K. Gengyo-Ando, S. Mitani, and Y. Ohshima Control of body size by SMA-5, a homolog of MAP kinase BMK1/ERK5, in C. Elegans Development 132 2005 3175 3184
63. G. Yao Modelling mammalian cellular quiescence Interface Focus 4 2014 20130074
64. K. Yasuda, T. Ishii, H. Suda, A. Akatsuka, P.S. Hartman, S. Goto, M. Miyazawa, and N. Ishii Age-related changes of mitochondrial structure and function in Caenorhabditis elegans Mech. Ageing Dev. 127 2006 763 770
65. S.O. Zhang, A.C. Box, N. Xu, J. Le Men, J. Yu, F. Guo, R. Trimble, and H.Y. Mak Genetic and dietary regulation of lipid droplet expansion in Caenorhabditis elegans Proc. Natl. Acad. Sci. USA 107 2010 4640 4645
66. H.Y. Zoghbi, and H.T. Orr Glutamine repeats and neurodegeneration Annu. Rev. Neurosci. 23 2000 217 247