Monoubiquitination of histone H2B lysine 123 regulates methylation of histone H3 lysine 4 (H3K4) and 79 (H3K79) and the lack of H2B ubiquitination in Saccharomyces cerevisiae coincides with metacaspase-dependent apoptosis. Here, we discovered that loss of H3K4 methylation due to depletion of the methyltransferase Set1p (or the two COMPASS subunits Spp1p and Bre2p, respectively) leads to enhanced cell death during chronological aging and increased sensitivity to apoptosis induction. In contrast, loss of H3K79 methylation due to DOT1 disruption only slightly affects yeast survival. SET1 depleted cells accumulate DNA damage and co-disruption of Dot1p, the DNA damage adaptor protein Rad9p, the endonuclease Nuc1p, and the metacaspase Yca1p, respectively, impedes their early death. Furthermore, aged and dying wild-type cells lose H3K4 methylation, whereas depletion of the H3K4 demethylase Jhd2p improves survival, indicating that loss of H3K4 methylation is an important trigger for cell death in S. cerevisiae. Given the evolutionary conservation of H3K4 methylation this likely plays a role in apoptosis regulation in a wide range of organisms.
Vyšlo v časopise: Loss of Histone H3 Methylation at Lysine 4 Triggers Apoptosis in. PLoS Genet 10(1): e32767. doi:10.1371/journal.pgen.1004095 Kategorie: Research Article prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004095
1. FadeelB, OrreniusS (2005) Apoptosis: a basic biological phenomenon with wide-ranging implications in human disease. J Intern Med 258 : 479–517.
2. Carmona-GutierrezD, EisenbergT, ButtnerS, MeisingerC, KroemerG, et al. (2010) Apoptosis in yeast: triggers, pathways, subroutines. Cell Death Differ 17 : 763–773.
3. RockenfellerP, MadeoF (2008) Apoptotic death of aging yeast. Exp Gerontol 43 : 876–881.
4. FabrizioP, LongoVD (2003) The chronological life span of Saccharomyces cerevisiae. Aging Cell 2 : 73–81.
5. KaeberleinM (2010) Lessons on longevity from budding yeast. Nature 464 : 513–519.
6. WalterD, WissingS, MadeoF, FahrenkrogB (2006) The inhibitor-of-apoptosis protein Bir1p protects against apoptosis in S. cerevisiae and is a substrate for the yeast homologue of Omi/HtrA2. J Cell Sci 119 : 1843–1851.
7. WissingS, LudovicoP, HerkerE, ButtnerS, EngelhardtSM, et al. (2004) An AIF orthologue regulates apoptosis in yeast. J Cell Biol 166 : 969–974.
8. MadeoF, HerkerE, MaldenerC, WissingS, LacheltS, et al. (2002) A caspase-related protease regulates apoptosis in yeast. Mol Cell 9 : 911–917.
9. HerkerE, JungwirthH, LehmannKA, MaldenerC, FrohlichKU, et al. (2004) Chronological aging leads to apoptosis in yeast. J Cell Biol 164 : 501–507.
10. BelangerKD, WalterD, HendersonTA, YeltonAL, O'BrienTG, et al. (2009) Nuclear localisation is crucial for the proapoptotic activity of the HtrA-like serine protease Nma111p. J Cell Sci 122 : 3931–3941.
11. KerrJF, WyllieAH, CurrieAR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26 : 239–257.
12. WyllieAH (1980) Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284 : 555–556.
13. RogakouEP, Nieves-NeiraW, BoonC, PommierY, BonnerWM (2000) Initiation of DNA fragmentation during apoptosis induces phosphorylation of H2AX histone at serine 139. J Biol Chem 275 : 9390–9395.
14. CheungWL, AjiroK, SamejimaK, KlocM, CheungP, et al. (2003) Apoptotic phosphorylation of histone H2B is mediated by mammalian sterile twenty kinase. Cell 113 : 507–517.
15. AjiroK (2000) Histone H2B phosphorylation in mammalian apoptotic cells. An association with DNA fragmentation. J Biol Chem 275 : 439–443.
16. Fernandez-CapetilloO, AllisCD, NussenzweigA (2004) Phosphorylation of histone H2B at DNA double-strand breaks. J Exp Med 199 : 1671–1677.
17. AjiroK, ScoltockAB, SmithLK, AshasimaM, CidlowskiJA (2010) Reciprocal epigenetic modification of histone H2B occurs in chromatin during apoptosis in vitro and in vivo. Cell Death Differ 17 : 984–993.
18. SukaN, SukaY, CarmenAA, WuJ, GrunsteinM (2001) Highly specific antibodies determine histone acetylation site usage in yeast heterochromatin and euchromatin. Mol Cell 8 : 473–479.
19. AhnSH, CheungWL, HsuJY, DiazRL, SmithMM, et al. (2005) Sterile 20 kinase phosphorylates histone H2B at serine 10 during hydrogen peroxide-induced apoptosis in S. cerevisiae. Cell 120 : 25–36.
20. AhnSH, DiazRL, GrunsteinM, AllisCD (2006) Histone H2B deacetylation at lysine 11 is required for yeast apoptosis induced by phosphorylation of H2B at serine 10. Mol Cell 24 : 211–220.
21. BakerSP, PhillipsJ, AndersonS, QiuQ, ShabanowitzJ, et al. (2010) Histone H3 Thr 45 phosphorylation is a replication-associated post-translational modification in S. cerevisiae. Nat Cell Biol 12 : 294–298.
22. ChandrasekharanMB, HuangF, SunZW (2010) Histone H2B ubiquitination and beyond: Regulation of nucleosome stability, chromatin dynamics and the trans-histone H3 methylation. Epigenetics 5 : 460–468.
23. WoodA, SchneiderJ, ShilatifardA (2005) Cross-talking histones: implications for the regulation of gene expression and DNA repair. Biochem Cell Biol 83 : 460–467.
24. Santos-RosaH, SchneiderR, BannisterAJ, SherriffJ, BernsteinBE, et al. (2002) Active genes are tri-methylated at K4 of histone H3. Nature 419 : 407–411.
25. BernsteinBE, HumphreyEL, ErlichRL, SchneiderR, BoumanP, et al. (2002) Methylation of histone H3 Lys 4 in coding regions of active genes. Proc Natl Acad Sci U S A 99 : 8695–8700.
26. NgHH, RobertF, YoungRA, StruhlK (2003) Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol Cell 11 : 709–719.
27. NislowC, RayE, PillusL (1997) SET1, a yeast member of the trithorax family, functions in transcriptional silencing and diverse cellular processes. Mol Biol Cell 8 : 2421–2436.
28. SingerMS, KahanaA, WolfAJ, MeisingerLL, PetersonSE, et al. (1998) Identification of high-copy disruptors of telomeric silencing in Saccharomyces cerevisiae. Genetics 150 : 613–632.
29. BriggsSD, BrykM, StrahlBD, CheungWL, DavieJK, et al. (2001) Histone H3 lysine 4 methylation is mediated by Set1 and required for cell growth and rDNA silencing in Saccharomyces cerevisiae. Genes Dev 15 : 3286–3295.
30. BrykM, BriggsSD, StrahlBD, CurcioMJ, AllisCD, et al. (2002) Evidence that Set1, a factor required for methylation of histone H3, regulates rDNA silencing in S. cerevisiae by a Sir2-independent mechanism. Curr Biol 12 : 165–170.
31. NgHH, CicconeDN, MorsheadKB, OettingerMA, StruhlK (2003) Lysine-79 of histone H3 is hypomethylated at silenced loci in yeast and mammalian cells: a potential mechanism for position-effect variegation. Proc Natl Acad Sci U S A 100 : 1820–1825.
32. WysockiR, JavaheriA, AllardS, ShaF, CoteJ, et al. (2005) Role of Dot1-dependent histone H3 methylation in G1 and S phase DNA damage checkpoint functions of Rad9. Mol Cell Biol 25 : 8430–8443.
33. GiannattasioM, LazzaroF, PlevaniP, Muzi-FalconiM (2005) The DNA damage checkpoint response requires histone H2B ubiquitination by Rad6-Bre1 and H3 methylation by Dot1. J Biol Chem 280 : 9879–9886.
34. HuyenY, ZgheibO, DitullioRAJr, GorgoulisVG, ZacharatosP, et al. (2004) Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432 : 406–411.
35. WoodA, KroganNJ, DoverJ, SchneiderJ, HeidtJ, et al. (2003) Bre1, an E3 ubiquitin ligase required for recruitment and substrate selection of Rad6 at a promoter. Mol Cell 11 : 267–274.
36. HwangWW, VenkatasubrahmanyamS, IanculescuAG, TongA, BooneC, et al. (2003) A conserved RING finger protein required for histone H2B monoubiquitination and cell size control. Mol Cell 11 : 261–266.
37. RobzykK, RechtJ, OsleyMA (2000) Rad6-dependent ubiquitination of histone H2B in yeast. Science 287 : 501–504.
38. GameJC, WilliamsonMS, SpicakovaT, BrownJM (2006) The RAD6/BRE1 histone modification pathway in Saccharomyces confers radiation resistance through a RAD51-dependent process that is independent of RAD18. Genetics 173 : 1951–1968.
39. WalterD, MatterA, FahrenkrogB (2010) Bre1p-mediated histone H2B ubiquitylation regulates apoptosis in Saccharomyces cerevisiae. J Cell Sci 123 : 1931–1939.
40. PowersRW3rd, KaeberleinM, CaldwellSD, KennedyBK, FieldsS (2006) Extension of chronological life span in yeast by decreased TOR pathway signaling. Genes Dev 20 : 174–184.
41. PerroneGG, TanSX, DawesIW (2008) Reactive oxygen species and yeast apoptosis. Biochim Biophys Acta 1783 : 1354–1368.
42. MadeoF, Carmona-GutierrezD, RingJ, ButtnerS, EisenbergT, et al. (2009) Caspase-dependent and caspase-independent cell death pathways in yeast. Biochem Biophys Res Commun 382 : 227–231.
43. GilbertCS, GreenCM, LowndesNF (2001) Budding yeast Rad9 is an ATP-dependent Rad53 activating machine. Mol Cell 8 : 129–136.
44. SchwartzMF, DuongJK, SunZ, MorrowJS, PradhanD, et al. (2002) Rad9 phosphorylation sites couple Rad53 to the Saccharomyces cerevisiae DNA damage checkpoint. Mol Cell 9 : 1055–1065.
45. WatanabeK, MorishitaJ, UmezuK, ShirahigeK, MakiH (2002) Involvement of RAD9-dependent damage checkpoint control in arrest of cell cycle, induction of cell death, and chromosome instability caused by defects in origin recognition complex in Saccharomyces cerevisiae. Eukaryot Cell 1 : 200–212.
46. WeinbergerM, FengL, PaulA, SmithDLJr, HontzRD, et al. (2007) DNA replication stress is a determinant of chronological lifespan in budding yeast. PLoS ONE 2: e748.
47. ButtnerS, EisenbergT, Carmona-GutierrezD, RuliD, KnauerH, et al. (2007) Endonuclease G regulates budding yeast life and death. Mol Cell 25 : 233–246.
48. McClintockD, GordonLB, DjabaliK (2006) Hutchinson-Gilford progeria mutant lamin A primarily targets human vascular cells as detected by an anti-Lamin A G608G antibody. Proc Natl Acad Sci U S A 103 : 2154–2159.
49. TuS, BullochEM, YangL, RenC, HuangWC, et al. (2007) Identification of histone demethylases in Saccharomyces cerevisiae. J Biol Chem 282 : 14262–14271.
50. LiangG, KloseRJ, GardnerKE, ZhangY (2007) Yeast Jhd2p is a histone H3 Lys4 trimethyl demethylase. Nat Struct Mol Biol 14 : 243–245.
51. SchneiderJ, WoodA, LeeJS, SchusterR, DuekerJ, et al. (2005) Molecular regulation of histone H3 trimethylation by COMPASS and the regulation of gene expression. Mol Cell 19 : 849–856.
52. DaiJ, HylandEM, YuanDS, HuangH, BaderJS, et al. (2008) Probing nucleosome function: a highly versatile library of synthetic histone H3 and H4 mutants. Cell 134 : 1066–1078.
53. BoerVM, AminiS, BotsteinD (2008) Influence of genotype and nutrition on survival and metabolism of starving yeast. Proceedings of the National Academy of Sciences 105 : 6930–6935.
54. FullgrabeJ, HajjiN, JosephB (2010) Cracking the death code: apoptosis-related histone modifications. Cell Death Differ 17 : 1238–1243.
55. ChandrasekharanMB, HuangF, SunZW (2009) Ubiquitination of histone H2B regulates chromatin dynamics by enhancing nucleosome stability. Proc Natl Acad Sci U S A 106 : 16686–16691.
56. FaucherD, WellingerRJ (2010) Methylated H3K4, a transcription-associated histone modification, is involved in the DNA damage response pathway. PLoS Genet 6: e1001082.
57. SunZW, AllisCD (2002) Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature 418 : 104–108.
58. BriggsSD, XiaoT, SunZW, CaldwellJA, ShabanowitzJ, et al. (2002) Gene silencing: trans-histone regulatory pathway in chromatin. Nature 418 : 498.
59. RenQ, YangH, RosinskiM, ConradMN, DresserME, et al. (2005) Mutation of the cohesin related gene PDS5 causes cell death with predominant apoptotic features in Saccharomyces cerevisiae during early meiosis. Mutat Res 570 : 163–173.
60. WeinbergerM, RamachandranL, FengL, SharmaK, SunX, et al. (2005) Apoptosis in budding yeast caused by defects in initiation of DNA replication. J Cell Sci 118 : 3543–3553.
61. HauptmannP, RielC, Kunz-SchughartLA, FrohlichKU, MadeoF, et al. (2006) Defects in N-glycosylation induce apoptosis in yeast. Mol Microbiol 59 : 765–778.
62. MazzoniC, HerkerE, PalermoV, JungwirthH, EisenbergT, et al. (2005) Yeast caspase 1 links messenger RNA stability to apoptosis in yeast. EMBO Rep 6 : 1076–1081.
63. FabrizioP, LongoVD (2008) Chronological aging-induced apoptosis in yeast. Biochim Biophys Acta 1783 : 1280–1285.
64. ButtnerS, EisenbergT, HerkerE, Carmona-GutierrezD, KroemerG, et al. (2006) Why yeast cells can undergo apoptosis: death in times of peace, love, and war. J Cell Biol 175 : 521–525.
65. RuckenstuhlC, Carmona-GutierrezD, MadeoF (2010) The sweet taste of death: glucose triggers apoptosis during yeast chronological aging. Aging (Albany NY) 2 : 643–649.
66. BerntKM, ZhuN, SinhaAU, VempatiS, FaberJ, et al. (2011) MLL-rearranged leukemia is dependent on aberrant H3K79 methylation by DOT1L. Cancer Cell 20 : 66–78.
67. GueldenerU, HeinischJ, KoehlerGJ, VossD, HegemannJH (2002) A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast. Nucleic Acids Res 30: e23.
68. FinkGa (1991) Guide to yeast genetics and molecular biology. Methods Enzymol 194 : 1–863.
69. GietzD, St JeanA, WoodsRA, SchiestlRH (1992) Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res 20 : 1425.
70. CoxJS, ChapmanRE, WalterP (1997) The unfolded protein response coordinates the production of endoplasmic reticulum protein and endoplasmic reticulum membrane. Mol Biol Cell 8 : 1805–1814.
Zvýšte si kvalifikáciu online z pohodlia domova
Nemáte účet? Registrujte sa
Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.
