Transgenerational Inheritance of Diet-Induced Genome Rearrangements in Drosophila

PLoS Genetics

Volumn 11, Issue 4, 2015, Pages

  Aldrich, John C ^a   Maggert, Keith A ^a,b  

^a TEXAS A AND M UNIVERSITY   (United States)

^b UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN; INSULIN RECEPTOR; RIBOSOME DNA; TARGET OF RAPAMYCIN KINASE; HETEROCHROMATIN;

ADULT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; COPY NUMBER VARIATION; DIET; DROSOPHILA; FEMALE; GENE EXPRESSION; GENE MUTATION; GENE REARRANGEMENT; GENETIC STABILITY; IN VITRO STUDY; INHERITANCE; MALE; NONHUMAN; NUCLEOLUS; SIGNAL TRANSDUCTION; YEAST; ANIMAL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HETEROCHROMATIN; INSECT GENOME;

ANIMALS; DIET; DNA COPY NUMBER VARIATIONS; DNA, RIBOSOMAL; DROSOPHILA; GENE EXPRESSION REGULATION; GENE REARRANGEMENT; GENOME, INSECT; HETEROCHROMATIN; INSULIN; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84930357780     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005148     Document Type: Article

References (96)

1. Anway M.D., et al., Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science, 2005. 308(5727): p. 1466–9. 15933200
2. Jirtle R.L., Skinner M.K., Environmental epigenomics and disease susceptibility. Nat Rev Genet, 2007. 8(4): p. 253–62. 17363974
3. Arico J.K., et al., Epigenetic Patterns Maintained in Early Caenorhabditis elegans Embryos Can Be Established by Gene Activity in the Parental Germ Cells. PLoS Genet, 2011. 7(6): p. e1001391. doi: 10.1371/journal.pgen.1001391 21695223
4. Feil R., Fraga M.F., Epigenetics and the environment: emerging patterns and implications. Nat Rev Genet, 2011. 13(2): p. 97–109. doi: 10.1038/nrg3142 22215131
5. Greer E.L., et al., Transgenerational epigenetic inheritance of longevity in Caenorhabditis elegans. Nature, 2011. 479(7373): p. 365–71. doi: 10.1038/nature10572 22012258
6. Seong K.H., et al., Inheritance of stress-induced, ATF-2-dependent epigenetic change. Cell, 2011. 145(7): p. 1049–61. doi: 10.1016/j.cell.2011.05.029 21703449
7. Crews D., et al., Epigenetic transgenerational inheritance of altered stress responses. Proc Natl Acad Sci U S A, 2012. 109(23): p. 9143–8. doi: 10.1073/pnas.1118514109 22615374
8. Padmanabhan N., et al., Mutation in folate metabolism causes epigenetic instability and transgenerational effects on development. Cell, 2013. 155(1): p. 81–93. doi: 10.1016/j.cell.2013.09.002 24074862
9. Ahmad K., Henikoff S., Epigenetic consequences of nucleosome dynamics. Cell, 2002. 111(3): p. 281–4. 12419239
10. Deal R.B., Henikoff J.G., Henikoff S., Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science, 2010. 328(5982): p. 1161–4. doi: 10.1126/science.1186777 20508129
11. Hathaway N.A., et al., Dynamics and memory of heterochromatin in living cells. Cell, 2012. 149(7): p. 1447–60. doi: 10.1016/j.cell.2012.03.052 22704655
12. Teves S.S., Deal R.B., Henikoff S., Measuring genome-wide nucleosome turnover using CATCH-IT. Methods Enzymol, 2012. 513: p. 169–84. doi: 10.1016/B978-0-12-391938-0.00007-0 22929769
13. Ptashne M., Epigenetics: core misconcept. Proc Natl Acad Sci U S A, 2013. 110(18): p. 7101–3. doi: 10.1073/pnas.1305399110 23584020
14. Struhl K., Is DNA methylation of tumour suppressor genes epigenetic? Elife, 2014. 3: p. e02475. doi: 10.7554/eLife.02475 24623307
15. Ahmad K., Golic K.G., Somatic reversion of chromosomal position effects in Drosophila melanogaster. Genetics, 1996. 144(2): p. 657–70. 8889528
16. Conconi A., et al., Two different chromatin structures coexist in ribosomal RNA genes throughout the cell cycle. Cell, 1989. 57(5): p. 753–61. 2720786
17. Riddle N.C., Richards E.J., Genetic variation in epigenetic inheritance of ribosomal RNA gene methylation in Arabidopsis. Plant J, 2005. 41(4): p. 524–32. 15686517
18. Eickbush D.G., et al., Epigenetic regulation of retrotransposons within the nucleolus of Drosophila. Mol Cell Biol, 2008. 28(20): p. 6452–61. doi: 10.1128/MCB.01015-08 18678644
19. Grummt I., Langst G., Epigenetic control of RNA polymerase I transcription in mammalian cells. Biochim Biophys Acta, 2013. 1829(3–4): p. 393–404.
20. Warner J.R., The economics of ribosome biosynthesis in yeast. Trends Biochem Sci, 1999. 24(11): p. 437–40. 10542411
21. Pellegrini M., Manning J., Davidson N., Sequence arrangement of the rDNA of Drosophila melanogaster. Cell, 1977. 10(2): p. 213–4. 402223
22. French S.L., et al., In exponentially growing Saccharomyces cerevisiae cells, rRNA synthesis is determined by the summed RNA polymerase I loading rate rather than by the number of active genes. Mol Cell Biol, 2003. 23(5): p. 1558–68. 12588976
23. Peng J.C., Karpen G.H., H3K9 methylation and RNA interference regulate nucleolar organization and repeated DNA stability. Nat Cell Biol, 2007. 9(1): p. 25–35. 17159999
24. Paredes S., Maggert K.A., Ribosomal DNA contributes to global chromatin regulation. Proc Natl Acad Sci U S A, 2009. 106(42): p. 17829–34. doi: 10.1073/pnas.0906811106 19822756
25. Guerrero P.A., Maggert K.A., The CCCTC-binding factor (CTCF) of Drosophila contributes to the regulation of the ribosomal DNA and nucleolar stability. PLoS One, 2011. 6(1): p. e16401. doi: 10.1371/journal.pone.0016401 21283722
26. Larson K., et al., Heterochromatin formation promotes longevity and represses ribosomal RNA synthesis. PLoS Genet, 2012. 8(1): p. e1002473. doi: 10.1371/journal.pgen.1002473 22291607
27. Saka K., et al., Cellular senescence in yeast is regulated by rDNA noncoding transcription. Curr Biol, 2013. 23(18): p. 1794–8. doi: 10.1016/j.cub.2013.07.048 23993840
28. Cohen S., Yacobi K., Segal D., Extrachromosomal circular DNA of tandemly repeated genomic sequences in Drosophila. Genome Res, 2003. 13(6A): p. 1133–45. 12799349
29. Takeuchi Y., Horiuchi T., Kobayashi T., Transcription-dependent recombination and the role of fork collision in yeast rDNA. Genes Dev, 2003. 17(12): p. 1497–506. 12783853
30. Tartof K.D., Unequal mitotic sister chromatid exchange and disproportionate replication as mechanisms regulating ribosomal RNA gene redundancy. Cold Spring Harb Symp Quant Biol, 1974. 38: p. 491–500. 4208791
31. Hawley R.S., Tartof K.D., A two-stage model for the control of rDNA magnification. Genetics, 1985. 109(4): p. 691–700. 3921426
32. Bianciardi A., et al., Ribosomal DNA organization before and after magnification in Drosophila melanogaster. Genetics, 2012. 191(3): p. 703–23. doi: 10.1534/genetics.112.140335 22505623
33. Dawid I.B., Wellauer P.K., Long E.O., Ribosomal DNA in Drosophila melanogaster. I. Isolation and characterization of cloned fragments. J Mol Biol, 1978. 126(4): p. 749–68. 106128
34. Long E.O., Dawid I.B., Repeated genes in eukaryotes. Annu Rev Biochem, 1980. 49: p. 727–64. 6996571
35. Lyckegaard E.M., Clark A.G., Ribosomal DNA and Stellate gene copy number variation on the Y chromosome of Drosophila melanogaster. Proc Natl Acad Sci U S A, 1989. 86(6): p. 1944–8. 2494656
36. Stage D.E., Eickbush T.H., Sequence variation within the rRNA gene loci of 12 Drosophila species. Genome Res, 2007. 17(12): p. 1888–97. 17989256
37. Boulon S., et al., The nucleolus under stress. Mol Cell, 2010. 40(2): p. 216–27. doi: 10.1016/j.molcel.2010.09.024 20965417
38. Ide S., et al., Abundance of ribosomal RNA gene copies maintains genome integrity. Science, 2010. 327(5966): p. 693–6. doi: 10.1126/science.1179044 20133573
39. Boyd M.T., Vlatkovic N., Rubbi C.P., The nucleolus directly regulates p53 export and degradation. J Cell Biol, 2011. 194(5): p. 689–703. doi: 10.1083/jcb.201105143 21893597
40. Kobayashi T., Regulation of ribosomal RNA gene copy number and its role in modulating genome integrity and evolutionary adaptability in yeast. Cell Mol Life Sci, 2011. 68(8): p. 1395–403. doi: 10.1007/s00018-010-0613-2 21207101
41. Paredes S., The Ribosomal DNA Genes Influence Genome-Wide Gene Expression in Drosophila melanogaster., in Biology. 2011, Texas A&M University. p. 175. doi: 10.1016/j.jphotobiol.2011.08.009 21955546
42. Tsurumi A., Li W.X., Global heterochromatin loss: a unifying theory of aging? Epigenetics, 2012. 7(7): p. 680–8. doi: 10.4161/epi.20540 22647267
43. Zhou J S.T., Martinsen L, Lemos B, Eickbush TH, Hartl DL, Y chromosome mediates ribosomal DNA silencing and modulates the chromatin state in Drosophila. Proc Natl Acad Sci U S A, 2012. doi: 10.1073/pnas.1207367109(Online).
44. Chen S., et al., Repression of RNA polymerase I upon stress is caused by inhibition of RNA-dependent deacetylation of PAF53 by SIRT7. Mol Cell, 2013. 52(3): p. 303–13. doi: 10.1016/j.molcel.2013.10.010 24207024
45. Grummt I., The nucleolus-guardian of cellular homeostasis and genome integrity. Chromosoma, 2013. 122(6): p. 487–97. 24022641
46. Gibbons J.G., et al., Ribosomal DNA copy number is coupled with gene expression variation and mitochondrial abundance in humans. Nat Commun, 2014. 5: p. 4850. doi: 10.1038/ncomms5850 25209200
47. Maggert K.A., Genetics: polymorphisms, epigenetics, and something in between. Genet Res Int, 2012. 2012: p. 867951. doi: 10.1155/2012/867951 22567405
48. Grummt I., Ladurner A.G., A metabolic throttle regulates the epigenetic state of rDNA. Cell, 2008. 133(4): p. 577–80. doi: 10.1016/j.cell.2008.04.026 18485866
49. Murayama A., et al., Epigenetic control of rDNA loci in response to intracellular energy status. Cell, 2008. 133(4): p. 627–39. doi: 10.1016/j.cell.2008.03.030 18485871
50. Smith D.L., Jr.et al., Calorie restriction effects on silencing and recombination at the yeast rDNA. Aging Cell, 2009. 8(6): p. 633–42. doi: 10.1111/j.1474-9726.2009.00516.x 19732044
51. Fontana L., Partridge L., Longo V.D., Extending healthy life span—from yeast to humans. Science, 2010. 328(5976): p. 321–6. doi: 10.1126/science.1172539 20395504
52. Grandison R.C., et al., Effect of a standardised dietary restriction protocol on multiple laboratory strains of Drosophila melanogaster. PLoS One, 2009. 4(1): p. e4067. doi: 10.1371/journal.pone.0004067 19119322
53. Zhou J., et al., Y chromosome mediates ribosomal DNA silencing and modulates the chromatin state in Drosophila. Proc Natl Acad Sci U S A, 2012. 109(25): p. 9941–6. doi: 10.1073/pnas.1207367109 22665801
54. Zhang Q., Shalaby N.A., Buszczak M., Changes in rRNA transcription influence proliferation and cell fate within a stem cell lineage. Science, 2014. 343(6168): p. 298–301. doi: 10.1126/science.1246384 24436420
55. Paredes S., Maggert K.A., Expression of I-CreI Endonuclease Generates Deletions Within the rDNA of Drosophila. Genetics, 2009. 181(4): p. 1661–71. doi: 10.1534/genetics.108.099093 19171942
56. Paredes S., et al., Ribosomal DNA deletions modulate genome-wide gene expression: "rDNA-sensitive" genes and natural variation. PLoS Genet, 2011. 7(4): p. e1001376. doi: 10.1371/journal.pgen.1001376 21533076
57. Aldrich J.C., Maggert K.A., Quantitative PCR reveals naturally occurring and mutationally-induced repetitive sequence variation on the Drosophila Y chromosome. PLoS ONE, 2014. 9: e109906. doi: 10.1371/journal.pone.0109906 25285439
58. Maggert, K.A., Reduced rDNA Copy Number Does Not Affect "Competitive" Chromosome Pairing in XYY Males of Drosophila melanogaster. G3 (Bethesda), 2014.
59. Karpen G.H., Schaefer J.E., Laird C.D., A Drosophila rRNA gene located in euchromatin is active in transcription and nucleolus formation. Genes Dev, 1988. 2(12B): p. 1745–63. 3149250
60. Peng J.C., Karpen G.H., Epigenetic regulation of heterochromatic DNA stability. Curr Opin Genet Dev, 2008. 18(2): p. 204–11. doi: 10.1016/j.gde.2008.01.021 18372168
61. Spofford J.B., Ashburner M., Novitski E., Position-effect variegation in Drosophila, in The Genetics and Biology of Drosophila, 1976, Academic Press. p. 955–1019.
62. Ashburner M., Golic K.G., Hawley R.S., Drosophila: a laboratory handbook. 2nd ed. 2005, Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory Press. xxviii, 1409 p.
63. Lemos B., Araripe L.O., Hartl D.L., Polymorphic Y chromosomes harbor cryptic variation with manifold functional consequences. Science, 2008. 319(5859): p. 91–3. doi: 10.1126/science.1148861 18174442
64. Jiang P.P., Hartl D.L., Lemos B., Y Not a Dead End: Epistatic Interactions Between Y-linked Regulatory Polymorphisms and Genetic Background Affect Global Gene Expression in Drosophila melanogaster. Genetics, 2010.
65. Kwan E.X., et al., A Natural Polymorphism in rDNA Replication Origins Links Origin Activation with Calorie Restriction and Lifespan. PLoS Genet, 2013. 9(3): p. e1003329. doi: 10.1371/journal.pgen.1003329 23505383
66. Jakubczak J.L., et al., Turnover of R1 (type I) and R2 (type II) retrotransposable elements in the ribosomal DNA of Drosophila melanogaster. Genetics, 1992. 131(1): p. 129–42. 1317313
67. Eickbush T.H., et al., Evolution of R1 and R2 in the rDNA units of the genus Drosophila. Genetica, 1997. 100(1–3): p. 49–61. 9440280
68. Grewal S.S., Evans J.R., Edgar B.A., Drosophila TIF-IA is required for ribosome synthesis and cell growth and is regulated by the TOR pathway. J Cell Biol, 2007. 179(6): p. 1105–13. 18086911
69. Grewal S.S., Insulin/TOR signaling in growth and homeostasis: a view from the fly world. Int J Biochem Cell Biol, 2009. 41(5): p. 1006–10. doi: 10.1016/j.biocel.2008.10.010 18992839
70. Rosby R., et al., Knockdown of the Drosophila GTPase nucleostemin 1 impairs large ribosomal subunit biogenesis, cell growth, and midgut precursor cell maintenance. Mol Biol Cell, 2009. 20(20): p. 4424–34. doi: 10.1091/mbc.E08-06-0592 19710426
71. Greil F., Ahmad K., Nucleolar Dominance of the Y Chromosome in Drosophila melanogaster. Genetics, 2012.
72. Bjedov I., et al., Mechanisms of life span extension by rapamycin in the fruit fly Drosophila melanogaster. Cell Metab, 2010. 11(1): p. 35–46. doi: 10.1016/j.cmet.2009.11.010 20074526
73. Ueishi S., Shimizu H., H.I Y, Male germline stem cell division and spermatocyte growth require insulin signaling in Drosophila. Cell Struct Funct, 2009. 34(1): p. 61–9. 19384053
74. Wang L., McLeod C.J., Jones D.L., Regulation of adult stem cell behavior by nutrient signaling. Cell Cycle, 2011. 10(16): p. 2628–34. 21814033
75. Endow S.A., Molecular characterization of ribosomal genes on the Ybb- chromosome of Drosophila melanogaster. Genetics, 1982. 102(1): p. 91–9. 6813192
76. Ritossa F.M., Unstable redundancy of genes for ribosomal RNA. Proc Natl Acad Sci U S A, 1968. 60(2): p. 509–16. 5248808
77. Kobayashi T., A new role of the rDNA and nucleolus in the nucleus—rDNA instability maintains genome integrity. Bioessays, 2008. 30(3): p. 267–72. doi: 10.1002/bies.20723 18293366
78. Sackton T.B., et al., Interspecific Y chromosome introgressions disrupt testis-specific gene expression and male reproductive phenotypes in Drosophila. Proc Natl Acad Sci U S A, 2011. 108(41): p. 17046–51. doi: 10.1073/pnas.1114690108 21969588
79. Tartof K.D., Regulation of ribosomal RNA gene multiplicity in Drosophila melanogaster. Genetics, 1973. 73(1): p. 57–71. 4631601
80. Endow S.A., Glover D.M., Differential replication of ribosomal gene repeats in polytene nuclei of Drosophila. Cell, 1979. 17(3): p. 597–605. 113105
81. Schneeberger R.G., Cullis C.A., Specific DNA alterations associated with the environmental induction of heritable changes in flax. Genetics, 1991. 128(3): p. 619–30. 1678726
82. Montanaro L., Trere D., Derenzini M., Nucleolus, ribosomes, and cancer. Am J Pathol, 2008. 173(2): p. 301–10. doi: 10.2353/ajpath.2008.070752 18583314
83. Derenzini M., Montanaro L., Trere D., What the nucleolus says to a tumour pathologist. Histopathology, 2009. 54(6): p. 753–62. doi: 10.1111/j.1365-2559.2008.03168.x 19178588
84. Drygin D., Rice W.G., Grummt I., The RNA polymerase I transcription machinery: an emerging target for the treatment of cancer. Annu Rev Pharmacol Toxicol, 2010. 50: p. 131–56. doi: 10.1146/annurev.pharmtox.010909.105844 20055700
85. McStay B., Grummt I., The epigenetics of rRNA genes: from molecular to chromosome biology. Annu Rev Cell Dev Biol, 2008. 24: p. 131–57. doi: 10.1146/annurev.cellbio.24.110707.175259 18616426
86. Grummt I., The nucleolus-guardian of cellular homeostasis and genome integrity. Chromosoma, 2013.
87. Wei K.H., et al., Correlated variation and population differentiation in satellite DNA abundance among lines of Drosophila melanogaster. Proc Natl Acad Sci U S A, 2014. 111(52): p. 18793–8. doi: 10.1073/pnas.1421951112 25512552
88. Maggert K.A., Golic K.G., Highly efficient sex chromosome interchanges produced by I-CreI expression in Drosophila. Genetics, 2005. 171(3): p. 1103–14. 16020774
89. Wu Q., et al., Regulation of hunger-driven behaviors by neural ribosomal S6 kinase in Drosophila. Proc Natl Acad Sci U S A, 2005. 102(37): p. 13289–94. 16150727
90. Clancy D.J., Kennington W.J., A simple method to achieve consistent larval density in bottle cultures. Drosophila Information Service, 2001. 84: p. 168–169.
91. Winkles J.A., Phillips W.H., Grainger R.M., Drosophila ribosomal RNA stability increases during slow growth conditions. J Biol Chem, 1985. 260(12): p. 7716–20. 3922989
92. Shimada H., et al., Normalization using ploidy and genomic DNA copy number allows absolute quantification of transcripts, proteins and metabolites in cells. Plant Methods, 2010. 6: p. 29. doi: 10.1186/1746-4811-6-29 21190547
93. Ramakers C., et al., Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett, 2003. 339(1): p. 62–6. 12618301
94. Pfaffl M.W., A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res, 2001. 29(9): p. e45. 11328886
95. Bogart K., Andrews J., Extraction of Total RNA from Drosophila, in CGB Technical Report 2006–10. 2006, The Center for Genomics and Bioinformatics, Indiana University, Bloomington, Indiana.
96. Krzywinski M., Altman N., Points of significance: error bars. Nat Methods, 2013. 10(10): p. 921–2. doi: 10.1038/nmeth.2659 24161969