Uncoupling lifespan and healthspan in caenorhabditis elegans longevity mutants

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 3, 2015, Pages E277-E286

  Bansal, Ankita ^a   Zhu, Lihua J ^a   Yen, Kelvin ^a,b   Tissenbaum, Heidi A ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Functional capacity; Gerospan; Healthspan; Healthy aging; Lifespan

Indexed keywords

INITIATION FACTOR; INITIATION FACTOR 4E; LIPOFUSCIN; MAMMALIAN TARGET OF RAPAMYCIN; NICOTINIC RECEPTOR; PHALLOIDIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); RIBOSOME RNA; SOMATOMEDIN C; SUCCINATE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE;

ADULT; ALLELE; ARTICLE; AUTOFLUORESCENCE; CAENORHABDITIS ELEGANS; DIET RESTRICTION; FOOD INTAKE; FUNCTIONAL STATUS; GENOTYPE; HEAT STRESS; HOMEOSTASIS; INVERTEBRATE MODEL; LIFE EXTENSION; LIFESPAN; LONGEVITY; MOUSE; MUSCLE CONTRACTION; MUSCLE FIBRIL; MUSCLE FUNCTION; NEUROMUSCULAR SYNAPSE; NONHUMAN; OXIDATIVE STRESS; PHARYNGEAL MUSCLE; PHENOTYPE; PRIORITY JOURNAL; RESPIRATORY CHAIN; RNA PROCESSING; RNA TRANSLATION; SEXUAL MATURITY; YOUNG ADULT; ANIMAL; GENETICS; MOVEMENT (PHYSIOLOGY); MUTATION; PHYSIOLOGY;

ANIMALIA; CAENORHABDITIS ELEGANS;

ANIMALS; CAENORHABDITIS ELEGANS; LONGEVITY; MOVEMENT; MUTATION;

EID: 84922385920     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1412192112     Document Type: Article

References (68)

1. World Health Organization (2014) 10 Facts on Ageing and the Life Course. Available at www.who.int/features/factfiles/ageing/en. Accessed November 28, 2014.
2. Meara E, White C, Cutler DM (2004) Trends in medical spending by age, 1963-2000.Health Aff (Millwood) 23(4):176-183.
3. Christensen K, Doblhammer G, Rau R, Vaupel JW (2009) Ageing populations: The challenges ahead. Lancet 374(9696):1196-1208.
4. Narasimhan SD, Mukhopadhyay A, Tissenbaum HA (2009) InAKTivation of insulin/IGF-1 signaling by dephosphorylation. Cell Cycle 8(23):3878-3884.
5. Smith ED, et al. (2008) Age- and calorie-independent life span extension from dietary restriction by bacterial deprivation in Caenorhabditis elegans. BMC Dev Biol 8:49.
6. Kenyon C, Chang J, Gensch E, Rudner A, Tabtiang R (1993) A C. elegans mutant that lives twice as long as wild type. Nature 366(6454):461-464.
7. Lakowski B, Hekimi S (1996) Determination of life-span in Caenorhabditis elegans by four clock genes. Science 272(5264):1010-1013.
8. Felkai S, et al. (1999) CLK-1 controls respiration, behavior and aging in the nematode Caenorhabditis elegans. EMBO J 18(7):1783-1792.
9. Syntichaki P, Troulinaki K, Tavernarakis N (2007) eIF4E function in somatic cells modulates ageing in Caenorhabditis elegans. Nature 445(7130):922-926.
10. Pan KZ, et al. (2007) Inhibition of mRNA translation extends lifespan in Caenorhabditis elegans. Aging Cell 6(1):111-119.
11. Hansen M, et al. (2007) Lifespan extension by conditions that inhibit translation in Caenorhabditis elegans. Aging Cell 6(1):95-110.
12. Braeckman BP, Houthoofd K, Vanfleteren JR (2001) Insulin-like signaling, metabolism, stress resistance and aging in Caenorhabditis elegans. Mech Ageing Dev 122(7): 673-693.
13. Murakami S, Johnson TE (1996) A genetic pathway conferring life extension and resistance to UV stress in Caenorhabditis elegans. Genetics 143(3):1207-1218.
14. Honda Y, Honda S (2002) Oxidative stress and life span determination in the nematode Caenorhabditis elegans. Ann N Y Acad Sci 959:466-474.
15. Lithgow GJ, White TM, Melov S, Johnson TE (1995) Thermotolerance and extended life-span conferred by single-gene mutations and induced by thermal stress. Proc Natl Acad Sci USA 92(16):7540-7544.
16. Lin YJ, Seroude L, Benzer S (1998) Extended life-span and stress resistance in the Drosophila mutant methuselah. Science 282(5390):943-946.
17. Kapahi P, Boulton ME, Kirkwood TB (1999) Positive correlation between mammalian life span and cellular resistance to stress. Free Radic Biol Med 26(5-6):495-500.
18. Bolanowski MA, Russell RL, Jacobson LA (1981) Quantitative measures of aging in the nematode Caenorhabditis elegans. I. Population and longitudinal studies of two behavioral parameters. Mech Ageing Dev 15(3):279-295.
19. Huang C, Xiong C, Kornfeld K (2004) Measurements of age-related changes of physiological processes that predict lifespan of Caenorhabditis elegans. Proc Natl Acad Sci USA 101(21):8084-8089.
20. Vellai T, McCulloch D, Gems D, Kovács AL (2006) Effects of sex and insulin/insulin-like growth factor-1 signaling on performance in an associative learning paradigm in Caenorhabditis elegans. Genetics 174(1):309-316.
21. Murakami H, Bessinger K, Hellmann J, Murakami S (2005) Aging-dependent and -independent modulation of associative learning behavior by insulin/insulin-like growth factor-1 signal in Caenorhabditis elegans. J Neurosci 25(47):10894-10904.
22. Burger JM, Buechel SD, Kawecki TJ (2010) Dietary restriction affects lifespan but not cognitive aging in Drosophila melanogaster. Aging Cell 9(3):327-335.
23. Burger JM, Hwangbo DS, Corby-Harris V, Promislow DE (2007) The functional costs and benefits of dietary restriction in Drosophila. Aging Cell 6(1):63-71.
24. Avanesian A, Khodayari B, Felgner JS, Jafari M (2010) Lamotrigine extends lifespan but compromises health span in Drosophila melanogaster. Biogerontology 11(1): 45-52.
25. Rockwood K, et al. (2005) A global clinical measure of fitness and frailty in elderly people. CMAJ 173(5):489-495.
26. Peña FG, et al. (2014) Comparison of alternate scoring of variables on the performance of the frailty index. BMC Geriatr 14:25.
27. Herndon LA, et al. (2002) Stochastic and genetic factors influence tissue-specific decline in ageing C. elegans. Nature 419(6909):808-814.
28. Collins JJ, Huang C, Hughes S, Kornfeld K (December 7, 2007) The measurement and analysis of age-related changes in Caenorhabditis elegans. WormBook, ed The C. elegans Research Community, 10.1895/wormbook.1.137.1. Available at www. wormbook.org. Accessed November 28, 2014.
29. Gerstbrein B, Stamatas G, Kollias N, Driscoll M (2005) In vivo spectrofluorimetry reveals endogenous biomarkers that report healthspan and dietary restriction in Caenorhabditis elegans. Aging Cell 4(3):127-137.
30. Ibáñez-Ventoso C, Driscoll M (2009) MicroRNAs in C. elegans aging: Molecular insurance for robustness? Curr Genomics 10(3):144-153.
31. Iwasa H, Yu S, Xue J, Driscoll M (2010) Novel EGF pathway regulators modulate C. elegans healthspan and lifespan via EGF receptor, PLC-gamma, and IP3R activation. Aging Cell 9(4):490-505.
32. Leiser SF, Begun A, Kaeberlein M (2011) HIF-1 modulates longevity and healthspan in a temperature-dependent manner. Aging Cell 10(2):318-326.
33. Onken B, Driscoll M (2010) Metformin induces a dietary restriction-like state and the oxidative stress response to extend C. elegans healthspan via AMPK, LKB1, and SKN-1. PLoS ONE 5(1):e8758.
34. Weindruch R, Walford RL, Fligiel S, Guthrie D (1986) The retardation of aging in mice by dietary restriction: Longevity, cancer, immunity and lifetime energy intake. J Nutr 116(4):641-654.
35. Bordone L, Guarente L (2005) Calorie restriction, SIRT1 and metabolism: Understanding longevity. Nat Rev Mol Cell Biol 6(4):298-305.
36. Partridge L, Piper MD, Mair W (2005) Dietary restriction in Drosophila. Mech Ageing Dev 126(9):938-950.
37. Greer EL, Brunet A (2009) Different dietary restriction regimens extend lifespan by both independent and overlapping genetic pathways in C. elegans. Aging Cell 8(2): 113-127.
38. McKay JP, Raizen DM, Gottschalk A, Schafer WR, Avery L (2004) eat-2 and eat-18 are required for nicotinic neurotransmission in the Caenorhabditis elegans pharynx. Genetics 166(1):161-169.
39. Liu X, et al. (2005) Evolutionary conservation of the clk-1-dependent mechanism of longevity: Loss of mclk1 increases cellular fitness and lifespan in mice. Genes Dev 19(20):2424-2434.
40. Gingras AC, Raught B, Sonenberg N (1999) eIF4 initiation factors: Effectors of mRNA recruitment to ribosomes and regulators of translation. Annu Rev Biochem 68: 913-963.
41. Harrison DE, et al. (2009) Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 460(7253):392-395.
42. Yen K, Steinsaltz D, Mobbs CV (2008) Validated analysis of mortality rates demonstrates distinct genetic mechanisms that influence lifespan. Exp Gerontol 43(12): 1044-1051.
43. Clegg A, Young J, Iliffe S, Rikkert MO, Rockwood K (2013) Frailty in elderly people. Lancet 381(9868):752-762.
44. Lithgow GJ, White TM, Hinerfeld DA, Johnson TE (1994) Thermotolerance of a longlived mutant of Caenorhabditis elegans. J Gerontol 49(6):B270-B276.
45. Metter EJ, Talbot LA, Schrager M, Conwit R (2002) Skeletal muscle strength as a predictor of all-cause mortality in healthy men. J Gerontol A Biol Sci Med Sci 57(10): B359-B365.
46. Fisher AL (2004) Of worms and women: Sarcopenia and its role in disability and mortality. J Am Geriatr Soc 52(7):1185-1190.
47. Glenn CF, et al. (2004) Behavioral deficits during early stages of aging in Caenorhabditis elegans result from locomotory deficits possibly linked to muscle frailty. J Gerontol A Biol Sci Med Sci 59(12):1251-1260.
48. Chow DK, Glenn CF, Johnston JL, Goldberg IG, Wolkow CA (2006) Sarcopenia in the Caenorhabditis elegans pharynx correlates with muscle contraction rate over lifespan. Exp Gerontol 41(3):252-260.
49. Pan CL, Peng CY, Chen CH, McIntire S (2011) Genetic analysis of age-dependent defects of the Caenorhabditis elegans touch receptor neurons. Proc Natl Acad Sci USA 108(22):9274-9279.
50. Tank EM, Rodgers KE, Kenyon C (2011) Spontaneous age-related neurite branching in Caenorhabditis elegans. J Neurosci 31(25):9279-9288.
51. Liu J, et al. (2013) Functional aging in the nervous system contributes to agedependent motor activity decline in C. elegans. Cell Metab 18(3):392-402.
52. Shaham S, ed (January 2, 2006) WormBook: Methods in cell biology. WormBook, ed The C. elegans Research Community, 10.1895/wormbook.1.49.1. Available at www. wormbook.org. Accessed November 28, 2014.
53. Avery L, Shtonda BB (2003) Food transport in the C. elegans pharynx. J Exp Biol 206(Pt 14):2441-2457.
54. Jung T, Bader N, Grune T (2007) Lipofuscin: Formation, distribution, and metabolic consequences. Ann N Y Acad Sci 1119:97-111.
55. McColl G, Jenkins NL, Walker DW, Lithgow GJ (2000) Testing evolutionary theories of aging. Ann N Y Acad Sci 908:319-320.
56. Jenkins NL, McColl G, Lithgow GJ (2004) Fitness cost of extended lifespan in Caenorhabditis elegans. Proc Biol Sci 271(1556):2523-2526.
57. Wong A, Boutis P, Hekimi S (1995) Mutations in the clk-1 gene of Caenorhabditis elegans affect developmental and behavioral timing. Genetics 139(3):1247-1259.
58. Gems D, et al. (1998) Two pleiotropic classes of daf-2 mutation affect larval arrest, adult behavior, reproduction and longevity in Caenorhabditis elegans. Genetics 150(1):129-155.
59. Crawford D, Libina N, Kenyon C (2007) Caenorhabditis elegans integrates food and reproductive signals in lifespan determination. Aging Cell 6(5):715-721.
60. Song A, et al. (2010) A C. elegans eIF4E-family member upregulates translation at elevated temperatures of mRNAs encoding MSH-5 and other meiotic crossover proteins. J Cell Sci 123(Pt 13):2228-2237.
61. Arantes-Oliveira N, Berman JR, Kenyon C (2003) Healthy animals with extreme longevity. Science 302(5645):611.
62. Chen D, et al. (2013) Germline signaling mediates the synergistically prolonged longevity produced by double mutations in daf-2 and rsks-1 in C. elegans. Cell Rep 5(6): 1600-1610.
63. Partridge L, Gems D, Withers DJ (2005) Sex and death: What is the connection? Cell 120(4):461-472.
64. Longo VD, Finch CE (2003) Evolutionary medicine: From dwarf model systems to healthy centenarians? Science 299(5611):1342-1346.
65. Stiernagle T (2006) Maintenance of C. elegans. WormBook, ed The C. elegans Research Community, 10.1895/wormbook.1.101.1. Available at www.wormbook.org. Accessed November 28, 2014.
66. Costa M, Draper BW, Priess JR (1997) The role of actin filaments in patterning the Caenorhabditis elegans cuticle. Dev Biol 184(2):373-384.
67. Yen K, et al. (2010) A comparative study of fat storage quantitation in nematode Caenorhabditis elegans using label and label-free methods. PLoS ONE 5(9):e12810.
68. Van Rompaye B, Jaffar S, Goetghebeur E (2012) Estimation with Cox models: Causespecific survival analysis with misclassified cause of failure. Epidemiology 23(2): 194-202.