Encodes the Catalytic Subunit of N Alpha-Acetyltransferase that Regulates Development, Metabolism and Adult Lifespan

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The development of a living organism is influenced by the environmental conditions such as nutrient availability. Under starvation conditions, the C. elegans larvae will enter a special developmental stage called dauer larva. An insulin-like signaling pathway controls dauer formation as well as adult lifespan by inhibiting the activity of FOXO transcription factor DAF-16 that regulates expression of stress-resistant genes. Here we isolate a new gene called daf-31; this gene encodes a protein that regulates C. elegans larval development, metabolism and adult lifespan. This protein has been found in other species to be part of an enzyme that functions to modify other proteins. We show that overexpression of our newly discovered protein stimulates the transcriptional activity of DAF-16. Interestingly, abnormal regulation of human proteins similar to DAF-31 results in tumor formation. It is known that human FOXO proteins prevent tumorigenesis. Therefore, it is possible that abnormal DAF-31 activity may lead to tumor growth by reducing DAF-16 activity. Thus, the present study may not only contribute to understanding the role of a universal enzyme in controlling development, metabolism and lifespan in other organisms besides worms but may also shed light on the mechanisms of tumorigenesis in humans.

Vyšlo v časopise: Encodes the Catalytic Subunit of N Alpha-Acetyltransferase that Regulates Development, Metabolism and Adult Lifespan. PLoS Genet 10(10): e32767. doi:10.1371/journal.pgen.1004699
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004699

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Zdroje

1. GoldenJW, RiddleDL (1984) A pheromone-induced developmental switch in Caenorhabditis elegans: Temperature-sensitive mutants reveal a wild-type temperature-dependent process. Proc Natl Acad Sci U S A 81: 819–823.

2. Riddle DL, Albert PS (1997) Genetic and environmental regulation of dauer larva development. In C elegans II (ed D L Riddle, T Blumenthal, B J Meyer and J R Priess), pp 739–768 NY: Cold Spring Harbor Laboratory Press.

3. GoldenJW, RiddleDL (1985) A gene affecting production of the Caenorhabditis elegans dauer-inducing pheromone. Mol Gen Genet 198: 534–536.

4. AlbertPS, BrownSJ, RiddleDL (1981) Sensory control of dauer larva formation in Caenorhabditis elegans. J Comp Neurol 198: 435–451.

5. BargmannCI, HorvitzHR (1991) Control of larval development by chemosensory neurons in Caenorhabditis elegans. Science 251: 1243–1246.

6. RenP, LimCS, JohnsenR, AlbertPS, PilgrimD, et al. (1996) Control of C. elegans larval development by neuronal expression of a TGF-beta homolog. Science 274: 1389–1391.

7. SchackwitzWS, InoueT, ThomasJH (1996) Chemosensory neurons function in parallel to mediate a pheromone response in C. elegans. Neuron 17: 719–728.

8. BirnbyDA, LinkEM, VowelsJJ, TianH, ColacurcioPL, et al. (2000) A transmembrane guanylyl cyclase (DAF-11) and Hsp90 (DAF-21) regulate a common set of chemosensory behaviors in Caenorhabditis elegans. Genetics 155: 85–104.

9. KimuraKD, TissenbaumHA, LiuY, RuvkunG (1997) daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277: 942–946.

10. PierceSB, CostaM, WisotzkeyR, DevadharS, HomburgerSA, et al. (2001) Regulation of DAF-2 receptor signaling by human insulin and ins-1, a member of the unusually large and diverse C. elegans insulin gene family. Genes Dev 15: 672–686.

11. AntebiA, YehWH, TaitD, HedgecockEM, RiddleDL (2000) daf-12 encodes a nuclear receptor that regulates the dauer diapause and developmental age in C. elegans. Genes Dev 14: 1512–1527.

12. AlbertPS, RiddleDL (1988) Mutants of Caenorhabditis elegans that form dauer-like larvae. Dev Biol 126: 270–293.

13. GerischB, WeitzelC, Kober-EisermannC, RottiersV, AntebiA (2001) A hormonal signaling pathway influencing C. elegans metabolism, reproductive development, and life span. Dev Cell 1: 841–851.

14. JiaK, AlbertPS, RiddleDL (2002) DAF-9, a cytochrome P450 regulating C. elegans larval development and adult longevity. Development 129: 221–231.

15. MotolaDL, CumminsCL, RottiersV, SharmaKK, LiT, et al. (2006) Identification of ligands for DAF-12 that govern dauer formation and reproduction in C. elegans. Cell 124: 1209–1223.

16. RottiersV, MotolaDL, GerischB, CumminsCL, NishiwakiK, et al. (2006) Hormonal control of C. elegans dauer formation and life span by a Rieske-like oxygenase. Dev Cell 10: 473–482.

17. Caldicott IM (1995) Non-conditional dauer and dauer-like mutants of Caenorhabditis elegans [PhD dissertation]. Columbia (Missouri): Division of Biological Sciences, University of Missouri, Columbia.

18. JiaK, ChenD, RiddleDL (2004) The TOR pathway interacts with the insulin signaling pathway to regulate C. elegans larval development, metabolism and life span. Development 131: 3897–3906.

19. YenK, LeTT, BansalA, NarasimhanSD, ChengJX, et al. (2010) A comparative study of fat storage quantitation in nematode Caenorhabditis elegans using label and label-free methods. PLoS ONE 5: e12810.

20. PolevodaB, ShermanF (2003) N-terminal acetyltransferases and sequence requirements for N-terminal acetylation of eukaryotic proteins. J Mol Biol 325: 595–622.

21. GuntherCV, GeorgiLL, RiddleDL (2000) A Caenorhabditis elegans type I TGF beta receptor can function in the absence of type II kinase to promote larval development. Development 127: 3337–3347.

22. LiJ, TewariM, VidalM, LeeSS (2007) The 14-3-3 protein FTT-2 regulates DAF-16 in Caenorhabditis elegans. Dev Biol 301: 82–91.

23. HendersonST, JohnsonTE (2001) daf-16 integrates developmental and environmental inputs to mediate aging in the nematode Caenorhabditis elegans. Curr Biol 11: 1975–1980.

24. LinK, HsinH, LibinaN, KenyonC (2001) Regulation of the Caenorhabditis elegans longevity protein DAF-16 by insulin/IGF-1 and germline signaling. Nat Genet 28: 139–145.

25. LithgowGJ, WhiteTM, MelovS, JohnsonTE (1995) Thermotolerance and extended life-span conferred by single-gene mutations and induced by thermal stress. Proc Natl Acad Sci U S A 92: 7540–7544.

26. HondaY, HondaS (1999) The daf-2 gene network for longevity regulates oxidative stress resistance and Mn-superoxide dismutase gene expression in Caenorhabditis elegans. FASEB J 13: 1385–1393.

27. KenyonC (2005) The plasticity of aging: insights from long-lived mutants. Cell 120: 449–460.

28. KenyonC, ChangJ, GenschE, RudnerA, TabtiangR (1993) A C. elegans mutant that lives twice as long as wild type. Nature 366: 461–464.

29. GemsD, SuttonAJ, SundermeyerML, AlbertPS, KingKV, et al. (1998) Two pleiotropic classes of daf-2 mutation affect larval arrest, adult behavior, reproduction and longevity in Caenorhabditis elegans. Genetics 150: 129–155.

30. MorrisJZ, TissenbaumHA, RuvkunG (1996) A phosphatidylinositol-3-OH kinase family member regulating longevity and diapause in Caenorhabditis elegans. Nature 382: 536–539.

31. ParadisS, AilionM, TokerA, ThomasJH, RuvkunG (1999) A PDK1 homolog is necessary and sufficient to transduce AGE-1 PI3 kinase signals that regulate diapause in Caenorhabditis elegans. Genes Dev 13: 1438–1452.

32. OggS, RuvkunG (1998) The C. elegans PTEN homolog, DAF-18, acts in the insulin receptor-like metabolic signaling pathway. Mol Cell 2: 887–893.

33. OggS, ParadisS, GottliebS, PattersonGI, LeeL, et al. (1997) The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 389: 994–999.

34. 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.

35. ApfeldJ, KenyonC (1998) Cell nonautonomy of C. elegans daf-2 function in the regulation of diapause and life span. Cell 95: 199–210.

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

37. LibinaN, BermanJR, KenyonC (2003) Tissue-specific activities of C. elegans DAF-16 in the regulation of lifespan. Cell 115: 489–502.

38. FujiiM, TanakaN, MikiK, HossainMN, EndohM, et al. (2005) Uncoupling of longevity and paraquat resistance in mutants of the nematode Caenorhabditis elegans. Biosci Biotechnol Biochem 69: 2015–2018.

39. TimmonsL, CourtDL, FireA (2001) Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263: 103–112.

40. WhitewayM, SzostakJW (1985) The ARD1 gene of yeast functions in the switch between the mitotic cell cycle and alternative developmental pathways. Cell 43: 483–492.

41. WangY, MijaresM, GallMD, TuranT, JavierA, et al. (2010) Drosophila variable nurse cells encodes arrest defective 1 (ARD1), the catalytic subunit of the major N-terminal acetyltransferase complex. Dev Dyn 239: 2813–2827.

42. ArnesenT, Van DammeP, PolevodaB, HelsensK, EvjenthR, et al. (2009) Proteomics analyses reveal the evolutionary conservation and divergence of N-terminal acetyltransferases from yeast and humans. Proc Natl Acad Sci U S A 106: 8157–8162.

43. LimJH, ParkJW, ChunYS (2006) Human arrest defective 1 acetylates and activates beta-catenin, promoting lung cancer cell proliferation. Cancer Res 66: 10677–10682.

44. ArnesenT, ThompsonPR, VarhaugJE, LillehaugJR (2008) The protein acetyltransferase ARD1: a novel cancer drug target? Curr Cancer Drug Targets 8: 545–553.

45. KuoHP, HungMC (2010) Arrest-defective-1 protein (ARD1): tumor suppressor or oncoprotein? Am J Transl Res 2: 56–64.

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

47. PinoEC, WebsterCM, CarrCE, SoukasAA (2013) Biochemical and high throughput microscopic assessment of fat mass in Caenorhabditis elegans. J Vis Exp 73: 50180.

48. KamathRS, Martinez-CamposM, ZipperlenP, FraserAG, AhringerJ (2001) Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol 2: RESEARCH0002.

49. FireA, XuS, MontgomeryMK, KostasSA, DriverSE, et al. (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391: 806–811.