Deletion of microRNA-80 Activates Dietary Restriction to Extend Healthspan and Lifespan

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Caloric/dietary restriction (CR/DR) can promote longevity and protect against age-associated disease across species. The molecular mechanisms coordinating food intake with health-promoting metabolism are thus of significant medical interest. We report that conserved Caenorhabditis elegans microRNA-80 (mir-80) is a major regulator of the DR state. mir-80 deletion confers system-wide healthy aging, including maintained cardiac-like and skeletal muscle-like function at advanced age, reduced accumulation of lipofuscin, and extended lifespan, coincident with induction of physiological features of DR. mir-80 expression is generally high under ad lib feeding and low under food limitation, with most striking food-sensitive expression changes in posterior intestine. The acetyltransferase transcription co-factor cbp-1 and interacting transcription factors daf-16/FOXO and heat shock factor-1 hsf-1 are essential for mir-80(Δ) benefits. Candidate miR-80 target sequences within the cbp-1 transcript may confer food-dependent regulation. Under food limitation, lowered miR-80 levels directly or indirectly increase CBP-1 protein levels to engage metabolic loops that promote DR.

Vyšlo v časopise: Deletion of microRNA-80 Activates Dietary Restriction to Extend Healthspan and Lifespan. PLoS Genet 9(8): e32767. doi:10.1371/journal.pgen.1003737
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003737

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Zdroje

1. KenyonCJ (2010) The genetics of ageing. Nature 464: 504–512.

2. TissenbaumHA (2012) Genetics, life span, health span, and the aging process in Caenorhabditis elegans. J Gerontol A Biol Sci Med Sci 67: 503–510.

3. FontanaL, PartridgeL, LongoVD (2010) Extending healthy life span–from yeast to humans. Science 328: 321–326.

4. GreerEL, BrunetA (2009) Different dietary restriction regimens extend lifespan by both independent and overlapping genetic pathways in C. elegans. Aging Cell 8: 113–127.

5. LeeGD, WilsonMA, ZhuM, WolkowCA, de CaboR, et al. (2006) Dietary deprivation extends lifespan in Caenorhabditis elegans. Aging Cell 5: 515–524.

6. KaeberleinTL (2006) Lifespan extension in Caenorhabditis elegans by complete removal of food. Aging Cell 5: 487–494.

7. BishopNA, GuarenteL (2007) Two neurons mediate diet-restriction-induced longevity in C. elegans. Nature 447: 545–549.

8. HouthoofdK, BraeckmanBP, JohnsonTE, VanfleterenJR (2003) Life extension via dietary restriction is independent of the Ins/IGF-1 signalling pathway in Caenorhabditis elegans. Exp Gerontol 38: 947–954.

9. GreerEL, DowlatshahiD, BankoMR, VillenJ, HoangK, et al. (2007) An AMPK-FOXO pathway mediates longevity induced by a novel method of dietary restriction in C. elegans. Curr Biol 17: 1646–1656.

10. RottiersV, NaarAM (2012) MicroRNAs in metabolism and metabolic disorders. Nat Rev Mol Cell Biol 13: 239–250.

11. PasquinelliAE (2012) MicroRNAs and their targets: recognition, regulation and an emerging reciprocal relationship. Nat Rev Genet 13: 271–282.

12. Ibanez-VentosoC, VoraM, DriscollM (2008) Sequence relationships among C. elegans, D. melanogaster and human microRNAs highlight the extensive conservation of microRNAs in biology. PLoS One 3: e2818.

13. FabianMR, SonenbergN (2012) The mechanics of miRNA-mediated gene silencing: a look under the hood of miRISC. Nat Struct Mol Biol 19: 586–593.

14. BerezikovE (2011) Evolution of microRNA diversity and regulation in animals. Nat Rev Genet 12: 846–860.

15. JohnsonSM, GrosshansH, ShingaraJ, ByromM, JarvisR, et al. (2005) RAS is regulated by the let-7 microRNA family. Cell 120: 635–647.

16. TrangP, MedinaPP, WigginsJF, RuffinoL, KelnarK, et al. (2010) Regression of murine lung tumors by the let-7 microRNA. Oncogene 29: 1580–1587.

17. MartinezNJ, OwMC, Reece-HoyesJS, BarrasaMI, AmbrosVR, et al. (2008) Genome-scale spatiotemporal analysis of Caenorhabditis elegans microRNA promoter activity. Genome Res 18: 2005–2015.

18. Alvarez-SaavedraE, HorvitzHR (2010) Many families of C. elegans microRNAs are not essential for development or viability. Curr Biol 20: 367–373.

19. GerstbreinB, StamatasG, KolliasN, DriscollM (2005) In vivo spectrofluorimetry reveals endogenous biomarkers that report healthspan and dietary restriction in Caenorhabditis elegans. Aging Cell 4: 127–137.

20. MiskaEA, Alvarez-SaavedraE, AbbottAL, LauNC, HellmanAB, et al. (2007) Most Caenorhabditis elegans microRNAs are individually not essential for development or viability. PLoS Genet 3: e215.

21. HuangC, XiongC, KornfeldK (2004) Measurements of age-related changes of physiological processes that predict lifespan of Caenorhabditis elegans. PNAS 101: 8084–8089.

22. HerndonLA, SchmeissnerPJ, DudaronekJM, BrownPA, ListnerKM, et al. (2002) Stochastic and genetic factors influence tissue-specific decline in ageing C. elegans. Nature 419: 808–814.

23. WolkowCA, KimuraKD, LeeM, RuvkunG (2000) Regulation of C. elegans life-span by insulinlike signaling in the nervous system. Science 290: 147–150.

24. ChowDK, GlennCF, JohnstonJL, GoldbergIG, WolkowCA (2006) Sarcopenia in the Caenorhabditis elegans pharynx correlates with muscle contraction rate over lifespan. Exp Gerontol 41: 252–260.

25. OnkenB, DriscollM (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: e8758.

26. HansenM, ChandraAl, MiticLL, OnkenB, DriscollM, et al. (2008) A role for autophagy genes in the extension of lifespan by dietary restriction in C. elegans. PLoS Genetics 4: e24.

27. LakowskiB, HekimiS (1998) The genetics of caloric restriction in Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America 95: 13091–13096.

28. KaeberleinTL, SmithED, TsuchiyaM, WeltonKL, ThomasJH, et al. (2006) Lifespan extension in Caenorhabditis elegans by complete removal of food. Aging Cell 5: 487–494.

29. ShibataY, FujiiT, DentJA, FujisawaH, TakagiS (2000) EAT-20, a novel transmembrane protein with EGF motifs, is required for efficient feeding in Caenorhabditis elegans. Genetics 154: 635–646.

30. HansenM, HsuAL, DillinA, KenyonC (2005) New genes tied to endocrine, metabolic, and dietary regulation of lifespan from a Caenorhabditis elegans genomic RNAi screen. PLoS Genet 1: 119–128.

31. MairW, DillinA (2008) Aging and survival: the genetics of life span extension by dietary restriction. Annu Rev Biochem 77: 727–754.

32. MairW, PanowskiSH, ShawRJ, DillinA (2009) Optimizing dietary restriction for genetic epistasis analysis and gene discovery in C. elegans. PLoS One 4: e4535.

33. AnJH, BlackwellTK (2003) SKN-1 links C. elegans mesendodermal specification to a conserved oxidative stress response. Genes Dev 17: 1882–1893.

34. de LencastreA, PincusZ, ZhouK, KatoM, LeeSS, et al. (2010) MicroRNAs both promote and antagonize longevity in C. elegans. Curr Biol 20: 2159–2168.

35. KatoM, de LencastreA, PincusZ, SlackFJ (2009) Dynamic expression of small non-coding RNAs, including novel microRNAs and piRNAs/21U-RNAs, during Caenorhabditis elegans development. Genome Biol 10: R54.

36. SteinkrausKA, SmithED, DavisC, CarrD, PendergrassWR, et al. (2008) Dietary restriction suppresses proteotoxicity and enhances longevity by an hsf-1-dependent mechanism in Caenorhabditis elegans. Aging Cell 7: 394–404.

37. ZhangM, PoplawskiM, YenK, ChengH, BlossE, et al. (2009) Role of CBP and SATB-1 in aging, dietary restriction, and insulin-like signaling. PLoS Biol 7: e1000245.

38. MastaitisJW, WurmbachE, ChengH, SealfonSC, MobbsCV (2005) Acute induction of gene expression in brain and liver by insulin-induced hypoglycemia. Diabetes 54: 952–958.

39. BadmanMK, FlierJS (2005) The gut and energy balance: visceral allies in the obesity wars. Science 307: 1909–1914.

40. NasrinN, OggS, CahillCM, BiggsW, NuiS, et al. (2000) DAF-16 recruits the CREB-binding protein coactivator complex to the insulin-like growth factor binding protein 1 promoter in HepG2 cells. Proc Natl Acad Sci U S A 97: 10412–10417.

41. HongS, KimSH, HeoMA, ChoiYH, ParkMJ, et al. (2004) Coactivator ASC-2 mediates heat shock factor 1-mediated transactivation dependent on heat shock. FEBS Lett 559: 165–170.

42. Jones-RhoadesMW, BartelDP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14: 787–799.

43. TayY, ZhangJ, ThomsonAM, LimB, RigoutsosI (2008) MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature 455: 1124–1128.

44. TayYM, TamWL, AngYS, GaughwinPM, YangH, et al. (2008) MicroRNA-134 modulates the differentiation of mouse embryonic stem cells, where it causes post-transcriptional attenuation of Nanog and LRH1. Stem Cells 26: 17–29.

45. FormanJJ, Legesse-MillerA, CollerHA (2008) A search for conserved sequences in coding regions reveals that the let-7 microRNA targets Dicer within its coding sequence. Proc Natl Acad Sci U S A 105: 14879–14884.

46. MarinRM, SulcM, VanicekJ (2013) Searching the coding region for microRNA targets. RNA 19: 467–474.

47. ShiY, MelloC (1998) A CBP/p300 homolog specifies multiple differentiation pathways in Caenorhabditis elegans. Genes Dev 12: 943–955.

48. EastburnDJ, HanM (2005) A gain-of-function allele of cbp-1, the Caenorhabditis elegans ortholog of the mammalian CBP/p300 gene, causes an increase in histone acetyltransferase activity and antagonism of activated Ras. Mol Cell Biol 25: 9427–9434.

49. XuP, GuoM, HayBA (2004) MicroRNAs and the regulation of cell death. Trends Genet 20: 617–624.

50. OhH, IrvineKD (2011) Cooperative regulation of growth by Yorkie and Mad through bantam. Dev Cell 20: 109–122.

51. ParrishJZ, XuP, KimCC, JanLY, JanYN (2009) The microRNA bantam functions in epithelial cells to regulate scaling growth of dendrite arbors in drosophila sensory neurons. Neuron 63: 788–802.

52. ThompsonBJ (2010) Developmental control of cell growth and division in Drosophila. Curr Opin Cell Biol 22: 788–794.

53. KadenerS, MenetJS, SuginoK, HorwichMD, WeissbeinU, et al. (2009) A role for microRNAs in the Drosophila circadian clock. Genes Dev 23: 2179–2191.

54. BoulanL, MartinD, MilanM (2013) bantam miRNA promotes systemic growth by connecting insulin signaling and ecdysone production. Curr Biol 23: 473–478.

55. BrennerS (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71–94.

56. Pinan-LucarreB, GabelCV, ReinaCP, HulmeSE, ShevkoplyasSS, et al. (2012) The core apoptotic executioner proteins CED-3 and CED-4 promote initiation of neuronal regeneration in Caenorhabditis elegans. PLoS Biol 10: e1001331.

57. Shaham S, editor(2006) Worm Book - Methods in Cell Biology (January 02, 2006).

58. SchneiderCA, RasbandWS, EliceiriKW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Meth 9: 671–675.

59. CalixtoA, ChelurD, TopalidouI, ChenX, ChalfieM (2010) Enhanced neuronal RNAi in C. elegans using SID-1. Nat Methods 7: 554–559.

60. RabindranSK, HarounRI, ClosJ, WisniewskiJ, WuC (1993) Regulation of heat shock factor trimer formation: role of a conserved leucine zipper. Science 259: 230–234.

61. MorleyJF, MorimotoRI (2004) Regulation of longevity in Caenorhabditis elegans by heat shock factor and molecular chaperones. Mol Biol Cell 15: 657–664.

62. MirandaKC, HuynhT, TayY, AngYS, TamWL, et al. (2006) A pattern-based method for the identification of MicroRNA binding sites and their corresponding heteroduplexes. Cell 126: 1203–1217.