Heritable Transmission of Stress Resistance by High Dietary Glucose in
Nutritional state has major effects on health and longevity, and investigations into the mechanisms of dietary restriction have taken the lion's share of recent genetic discoveries. We used Caenorhabditis elegans to investigate the role of diet on nematode physiology and report the surprising finding that exposure to high glucose at one generational time point has heritable effects in descendent progeny. Glucose promotes resistance against cellular stress and neurodegeneration in parental and descendent progeny, while reducing lifespan only in the parental generation. Furthermore, we found that glucose mediated protection is dependent on well-known metabolic and stress response genes. Numerous strategies have evolved to ensure reproductive success in the face of changing and challenging environments. It is believed that extended lifespan phenotypes observed under dietary restriction conditions maximize an organism's survival until environmental conditions improve allowing for reproduction. We discovered a novel diet-influenced reproductive advantage; animals subjected to high dietary glucose are resistant to protein damaging stress, and this resistance is transmitted to their progeny. The trade-off for stress-resistant progeny is decreased lifespan and fecundity in the parental strain suggesting that this strategy may be adaptive under nutrient rich conditions.
Vyšlo v časopise:
Heritable Transmission of Stress Resistance by High Dietary Glucose in. PLoS Genet 10(5): e32767. doi:10.1371/journal.pgen.1004346
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1004346
Souhrn
Nutritional state has major effects on health and longevity, and investigations into the mechanisms of dietary restriction have taken the lion's share of recent genetic discoveries. We used Caenorhabditis elegans to investigate the role of diet on nematode physiology and report the surprising finding that exposure to high glucose at one generational time point has heritable effects in descendent progeny. Glucose promotes resistance against cellular stress and neurodegeneration in parental and descendent progeny, while reducing lifespan only in the parental generation. Furthermore, we found that glucose mediated protection is dependent on well-known metabolic and stress response genes. Numerous strategies have evolved to ensure reproductive success in the face of changing and challenging environments. It is believed that extended lifespan phenotypes observed under dietary restriction conditions maximize an organism's survival until environmental conditions improve allowing for reproduction. We discovered a novel diet-influenced reproductive advantage; animals subjected to high dietary glucose are resistant to protein damaging stress, and this resistance is transmitted to their progeny. The trade-off for stress-resistant progeny is decreased lifespan and fecundity in the parental strain suggesting that this strategy may be adaptive under nutrient rich conditions.
Zdroje
1. FontanaL, PartridgeL, LongoVD (2010) Extending healthy life span–from yeast to humans. Science 328: 321–326 doi:10.1126/science.1172539
2. GemsD, PartridgeL (2013) Genetics of longevity in model organisms: debates and paradigm shifts. Annu Rev Physiol 75: 621–644 doi:10.1146/annurev-physiol-030212-183712
3. VennBJ, GreenTJ (2007) Glycemic index and glycemic load: measurement issues and their effect on diet-disease relationships. Eur J Clin Nutr 61(Suppl 1): S122–S131 doi:10.1038/sj.ejcn.1602942
4. KatzDJ, EdwardsTM, ReinkeV, KellyWG (2009) A C. elegans LSD1 demethylase contributes to germline immortality by reprogramming epigenetic memory. Cell 137: 308–320 Available: http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=19379696&retmode=ref&cmd=prlinks.
5. TauffenbergerA, VaccaroA, AulasA, Vande VeldeC, ParkerJA (2012) Glucose delays age-dependent proteotoxicity. Aging Cell 11: 856–866 doi:10.1111/j.1474-9726.2012.00855.x
6. LeeSJ, MurphyCT, KenyonC (2009) Glucose shortens the life span of C. elegans by downregulating DAF-16/FOXO activity and aquaporin gene expression. Cell Metab 10: 379–391 doi:10.1016/j.cmet.2009.10.003
7. MondouxMA, LoveDC, GhoshSK, FukushigeT, BondM, et al. (2011) O-GlcNAc Cycling and Insulin Signaling are Required for the Glucose Stress Response in Caenorhabditis elegans. Genetics 188: 369–82 doi:10.1534/genetics.111.126490
8. KimuraKD, TissenbaumHA, LiuY, RuvkunG (1997) daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277: 942–946.
9. LinK, DormanJB, RodanA, KenyonC (1997) daf-16: An HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science 278: 1319–1322.
10. ApfeldJ, O'ConnorG, McDonaghT, DiStefanoPS, CurtisR (2004) The AMP-activated protein kinase AAK-2 links energy levels and insulin-like signals to lifespan in C. elegans. Genes Dev 18: 3004–3009 doi:10.1101/gad.1255404
11. TissenbaumHA, GuarenteL (2001) Increased dosage of a sir-2 gene extends lifespan in Caenorhabditis elegans. Nature 410: 227–230 doi:10.1038/35065638
12. JiangH, GuoR, Powell-CoffmanJA (2001) The Caenorhabditis elegans hif-1 gene encodes a bHLH-PAS protein that is required for adaptation to hypoxia. Proc Natl Acad Sci USA 98: 7916–7921 doi:10.1073/pnas.141234698
13. VaccaroA, TauffenbergerA, AshPEA, CarlomagnoY, PetrucelliL, et al. (2012) TDP-1/TDP-43 regulates stress signaling and age-dependent proteotoxicity in Caenorhabditis elegans. PLoS Genet 8: e1002806 doi:10.1371/journal.pgen.1002806
14. HorikawaM, SakamotoK (2010) Polyunsaturated fatty acids are involved in regulatory mechanism of fatty acid homeostasis via daf-2/insulin signaling in Caenorhabditis elegans. Molecular and Cellular Endocrinology 323: 183–192 doi:10.1016/j.mce.2010.03.004
15. YangW, HekimiS (2010) A Mitochondrial Superoxide Signal Triggers Increased Longevity in Caenorhabditis elegans. PLoS Biology 8: e1000556 Available: http://dx.plos.org/10.1371/journal.pbio.1000556.t001.
16. HardingHP, ZhangY, ZengH, NovoaI, LuPD, et al. (2003) An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Molecular cell 11: 619–633.
17. NiccoliT, PartridgeL (2012) Ageing as a risk factor for disease. Current biology : CB 22: R741–R752 doi:10.1016/j.cub.2012.07.024
18. VaccaroA, TauffenbergerA, AggadD, RouleauG, DrapeauP, et al. (2012) Mutant TDP-43 and FUS cause age-dependent paralysis and neurodegeneration in C. elegans. PLoS ONE 7: e31321 doi:10.1371/journal.pone.0031321
19. VaccaroA, PattenSA, CiuraS, MaiosC, TherrienM, et al. (2012) Methylene blue protects against TDP-43 and FUS neuronal toxicity in C. elegans and D. rerio. PLoS ONE 7: e42117 doi:10.1371/journal.pone.0042117
20. VaccaroA, PattenSA, AggadD, JulienC, MaiosC, et al. (2013) Pharmacological reduction of ER stress protects against TDP-43 neuronal toxicity in vivo. Neurobiol Dis 55: 64–75 doi:10.1016/j.nbd.2013.03.015
21. TauffenbergerA, JulienC, ParkerJA (2013) Evaluation of longevity enhancing compounds against transactive response DNA-binding protein-43 neuronal toxicity. Neurobiol Aging 34: 2175–2182 doi:10.1016/j.neurobiolaging.2013.03.014
22. KabashiE, ValdmanisPN, DionP, SpiegelmanD, McConkeyBJ, et al. (2008) TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nat Genet 40: 572–4 doi:10.1038/ng.132
23. GreerEL, MauresTJ, UcarD, HauswirthAG, ManciniE, et al. (2011) Transgenerational epigenetic inheritance of longevity in Caenorhabditis elegans. Nature 479: 365–371 doi:10.1038/nature10572
24. HaagES, WangS, KimbleJ (2002) Rapid coevolution of the nematode sex-determining genes fem-3 and tra-2. Current biology: CB 12: 2035–2041.
25. KawasakiI, ShimYH, KirchnerJ, KaminkerJ, WoodWB, et al. (1998) PGL-1, a predicted RNA-binding component of germ granules, is essential for fertility in C. elegans. Cell 94: 635–645.
26. BlagosklonnyMV (2012) Answering the ultimate question “What is the Proximal Cause of Aging?.”. Aging (Albany NY) 4: 861–877.
27. RechtsteinerA, ErcanS, TakasakiT, PhippenTM, EgelhoferTA, et al. (2010) The Histone H3K36 Methyltransferase MES-4 Acts Epigenetically to Transmit the Memory of Germline Gene Expression to Progeny. PLoS Genet 6: e1001091.
28. LakowskiB, HekimiS (1998) The genetics of caloric restriction in Caenorhabditis elegans. Proc Natl Acad Sci USA 95: 13091–13096.
29. CrawfordD, LibinaN, KenyonC (2007) Caenorhabditis elegans integrates food and reproductive signals in lifespan determination. Aging Cell 6: 715–721 doi:10.1111/j.1474-9726.2007.00327.x
30. KaeberleinTL, SmithED, TsuchiyaM, WeltonKL, ThomasJH, et al. (2006) Lifespan extension in Caenorhabditis elegans by complete removal of food. Aging Cell 5: 487–494 doi:10.1111/j.1474-9726.2006.00238.x
31. LimJP, BrunetA (2013) Bridging the transgenerational gap with epigenetic memory. Trends Genet 3 doi:10.1016/j.tig.2012.12.008
32. AertsL, Van AsscheFA (2006) Animal evidence for the transgenerational development of diabetes mellitus. Int J Biochem Cell Biol 38: 894–903 doi:10.1016/j.biocel.2005.07.006
33. HoileSP, LillycropKA, ThomasNA, HansonMA, BurdgeGC (2011) Dietary protein restriction during F0 pregnancy in rats induces transgenerational changes in the hepatic transcriptome in female offspring. PLoS ONE 6: e21668 doi:10.1371/journal.pone.0021668
34. BurdgeGC, HoileSP, UllerT, ThomasNA, GluckmanPD, et al. (2011) Progressive, transgenerational changes in offspring phenotype and epigenotype following nutritional transition. PLoS ONE 6: e28282 doi:10.1371/journal.pone.0028282
35. DubosR, SchaedlerRW, CostelloR (1968) Lasting biological effects of early environmental influences. I. Conditioning of adult size by prenatal and postnatal nutrition. J Exp Med 127: 783–799.
36. NiculescuMD, LupuDS (2011) Nutritional influence on epigenetics and effects on longevity. Curr Opin Clin Nutr Metab Care 14: 35–40 doi:10.1097/MCO.0b013e328340ff7c
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2014 Číslo 5
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