Protein and DNA modifications: Evolutionary imprints of bacterial biochemical diversification and geochemistry on the provenance of eukaryotic epigenetics

Cold Spring Harbor Perspectives in Biology

Volumn 6, Issue 7, 2014, Pages

  Aravind, L ^a   Maxwell Burroughs, A ^a   Zhang, Dapeng ^a   Iyer, Lakshminarayan M ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; HISTONE; PROTEIN;

BIODIVERSITY; CHEMICAL STRUCTURE; CHEMISTRY; DNA METHYLATION; EPIGENETICS; EUKARYOTE; GENETICS; METABOLISM; MOLECULAR EVOLUTION; PHOSPHORYLATION; PHYLOGENY; PROTEIN PROCESSING; PROTEIN TERTIARY STRUCTURE; UBIQUITINATION;

BIODIVERSITY; DNA METHYLATION; DNA, BACTERIAL; EPIGENOMICS; EUKARYOTA; EVOLUTION, MOLECULAR; HISTONES; MODELS, MOLECULAR; PHOSPHORYLATION; PHYLOGENY; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; PROTEINS; UBIQUITINATION;

EID: 84903779475     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a016063     Document Type: Article

References (163)

1. Allis CD, Jenuwein T, Reinberg D. 2007. Epigenetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
2. Altermann W, Kazmierczak J. 2003. Archean microfossils: A reappraisal of early life on Earth. Res Microbiol 154: 611-617.
3. Ame JC, Spenlehauer C, de Murcia G. 2004. The PARP superfamily. Bioessays 26: 882-893.
4. Anne J, Ollo R, Ephrussi A, Mechler BM. 2007. Arginine methyltransferase Capsuleen is essential for methylation of spliceosomal Sm proteins and germ cell formation in Drosophila. Development 134: 137-146.
5. Aravind L, Iyer LM, Koonin EV. 2006. Comparative geno-mics and structural biology of the molecular innovations of eukaryotes. Curr Opin Struct Biol 16: 409-419.
6. Aravind L, Anantharaman V, Iyer LM. 2010. Sensory mechanisms in bacteria: Molecular aspects of signal recognition. Caister Academic, Norfolk, UK.
7. Aravind L, Abhiman S, Iyer LM. 2011. Natural history of the eukaryotic chromatin protein methylation system. Prog Mol Biol Transl Sci 101: 105-176.
8. Aravind L, Anantharaman V, Zhang D, de Souza RF, Iyer LM. 2012. Gene flow and biological conflict systems in the origin and evolution of eukaryotes. Front Cell Infect Microbiol 2: 89.
9. Avalos JL, Boeke JD, Wolberger C. 2004. Structural basis for the mechanism and regulation of Sir2 enzymes. Mol Cell 13: 639-648.
10. Babu MM. 2012. Intrinsically disordered proteins. Mol Bio-syst 8: 21.
11. Barry SM, Challis GL. 2009. Recent advances in siderophore biosynthesis. Curr Opin Chem Biol 13: 205-215.
12. Beauregard PB, Guerin R, Turcotte C, Lindquist S, Rokeach LA. 2009. A nucleolar protein allows viability in the absence of the essential ER-residing molecular chaperone calnexin. J Cell Sci 122: 1342-1351.
13. Best AA, Morrison HG, McArthur AG, Sogin ML, Olsen GJ. 2004. Evolution of eukaryotic transcription: Insights from the genome of Giardia lamblia. Genome Res 14: 1537-1547.
14. Bickle TA, Kruger DH. 1993. Biology of DNA restriction. Microbiol Rev 57: 434-450.
15. Blander G, Guarente L. 2004. The Sir2 family of protein deacetylases. Annu Rev Biochem 73: 417-435.
16. Blaskovic S, Blanc M, van der Goot FG. 2013. What does S-palmitoylation do to membrane proteins? FEBS J 280: 2766-2774.
17. Borst P, Sabatini R. 2008. Base J: Discovery, biosynthesis, and possible functions. Annu Rev Microbiol 62: 235-251.
18. Brasier M, McLoughlin N, Green O, Wacey D. 2006. A fresh look at the fossil evidence for early Archaean cellular life. Philos Trans R Soc Lond B Biol Sci 361: 887-902.
19. Brehm A, Tufteland KR, Aasland R, Becker PB. 2004. The many colours ofchromodomains. Bioessays 26: 133-140.
20. Brzeski J, Brzeska K. 2011. The maze of paramutation: A rough guide to the puzzling epigenetics of paramutation. Wiley Interdiscip Rev RNA 2: 863-874.
21. Burroughs AM, Iyer LM, Aravind L. 2011. Functional diversification of the RING finger and other binuclear treble clef domains inprokaryotes and the earlyevolutionof the ubiquitin system. Mol Biosyst 7: 2261-2277.
22. Burroughs AM, Iyer LM, Aravind L. 2012. Structure and evolution of ubiquitin and ubiquitin-related domains. Methods Mol Biol 832: 15-63.
23. Campanacci V, Mukherjee S, Roy CR, Cherfils J.2013. Structure of the Legionella effector AnkX reveals the mechanism of phosphocholine transfer by the FIC domain. EMBO J 32: 1469-1477.
24. Cavalier-Smith T. 2009. Megaphylogeny, cell body plans, adaptive zones: Causes and timing of eukaryote basal radiations. J Eukaryot Microbiol 56: 26-33.
25. Cedar H, Bergman Y. 2011. Epigenetics of haematopoietic cell development. Nat Rev Immunol 11: 478-488.
26. Chakravarty S, Zeng L, Zhou MM. 2009. Structure and site-specific recognition of histone H3 by the PHD finger of human autoimmune regulator. Structure 17: 670-679.
27. Chen Y, Yang Y, Wang F, Wan K, Yamane K, Zhang Y, Lei M. 2006. Crystal structure of human histone lysine-specific demethylase 1 (LSD1). Proc Natl Acad Sci 103: 13956-13961.
28. Citarelli M, Teotia S, Lamb RS. 2010. Evolutionary historyof the poly(ADP-ribose) polymerase gene family in eukary-otes. BMC Evol Biol 10: 308.
29. Collins RE, Northrop JP, Horton JR, Lee DY, Zhang X, Stall-cup MR, Cheng X. 2008. The ankyrin repeats of G9a and GLP histone methyltransferases are mono- and dimethyl-lysine binding modules. Nat Struct Mol Biol 15: 245-250.
30. Conaway RC, Conaway JW. 2011. Function and regulation of the Mediator complex. Curr Opin Genet Dev 21: 225-230.
31. Cook PJ, Ju BG, Telese F, Wang X, Glass CK, Rosenfeld MG. 2009. Tyrosine dephosphorylation of H2AX modulates apoptosis and survival decisions. Nature 458: 591-596.
32. Cumberworth A, Lamour G, Babu MM, Gsponer J. 2013. Promiscuity as a functional trait: Intrinsically disordered regions as central players of interactomes. Biochem J 454: 361-369.
33. Dacks JB, Doolittle WF. 2001. Reconstructing/deconstructing the earliest eukaryotes: How comparative genomics can help. Cell 107: 419-425.
34. Dann CE 3rd, Bruick RK, Deisenhofer J. 2002. Structure of factor-inhibiting hypoxia-inducible factor 1: An aspara-ginyl hydroxylase involved in the hypoxic response pathway. Proc Natl Acad Sci 99: 15351-15356.
35. Denhardt DT, Chaly N, Walden DB. 2005. The eukaryotic nucleus: A thematic issue. BioEssays 9: 43.
36. de Souza RF, Aravind L. 2012. Identification of novel components of NAD-utilizing metabolic pathways and prediction of their biochemical functions. Mol Biosyst 8: 1661-1677.
37. Dhalluin C, Carlson JE, Zeng L, He C, Aggarwal AK, Zhou MM. 1999. Structure and ligand of a histone acetyltrans-ferase bromodomain. Nature 399: 491-496.
38. Dlakic M. 2001. Chromatin silencing protein and pachytene checkpoint regulator Dot1p has a methyltransferase fold. Trends Biochem Sci 26: 405-407.
39. Duraisingh MT, Voss TS, Marty AJ, Duffy MF, Good RT, Thompson JK, Freitas-Junior LH, Scherf A, Crabb BS, Cowman AF. 2005. Heterochromatin silencing and locus repositioning linked to regulation of virulence genes in Plasmodium falciparum. Cell 121: 13-24.
40. Durant M, Pugh BF. 2006. Genome-wide relationships between TAF1 and histone acetyltransferases in Saccharo-myces cerevisiae. Mol Cell Biol 26: 2791-2802.
41. Dutnall RN. 2003. Cracking the histone code: One, two, three methyls, you're out! Mol Cell 12: 3-4.
42. Dutnall RN, Tafrov ST, Sternglanz R, Ramakrishnan V. 1998. Structure of the yeast histone acetyltransferase Hat1: Insights into substrate specificity and implications for the Gcn5-related N-acetyltransferase superfamily. Cold Spring Harb Symp Quant Biol 63: 501-507.
43. Egly JM, Coin F. 2011. A history of TFIIH: Two decades of molecular biology on a pivotal transcription/repair factor. DNA Repair (Amst) 10: 714-721.
44. Elkins JM, Hewitson KS, McNeill LA, Seibel JF, Schlem-minger I, Pugh CW, Ratcliffe PJ, Schofield CJ. 2003. Structure of factor-inhibiting hypoxia-inducible factor (HIF) reveals mechanism of oxidative modification of HIF-1a. J Biol Chem 278: 1802-1806.
45. Engel P, Goepfert A, Stanger FV, Harms A, Schmidt A, Schirmer T, Dehio C. 2012. Adenylylation control by in-tra- or intermolecular active-site obstruction in Fic proteins. Nature 482: 107-110.
46. 0-monophosphate transferase inhibits plant immune kinases. Nature 485: 114-118.
47. Flannery DT, Walter RM. 2012. Archean tufted microbial mats and the Great Oxidation Event: New insights into an ancient problem. Aust J Earth Sci 59: 1-11.
48. Forouhar F, Lee IS, Vujcic J, Vujcic S, Shen J, Vorobiev SM, Xiao R, Acton TB, Montelione GT, Porter CW, et al. 2005. Structural and functional evidence for Bacillus subtilis PaiA as a novel N1-spermidine/spermine acetyltransfer-ase. J Biol Chem 280: 40328-40336.
49. Frei R, Gaucher C, Poulton SW, Canfield DE. 2009. Fluctuations in Precambrian atmospheric oxygenation recorded by chromium isotopes. Nature 461: 250-253.
50. Fukushima N, Furuta D, Hidaka Y, Moriyama R, Tsujiuchi T. 2009. Post-translational modifications of tubulin in the nervous system. J Neurochem 109: 683-693.
51. Garcia-Alai MM, Allen MD, Joerger AC, Bycroft M. 2010. The structure of the FYR domain of transforming growth factor b regulator 1. Protein Sci 19: 1432-1438.
52. Gehring M, Huh JH, Hsieh TF, Penterman J, Choi Y, Harada JJ, Goldberg RB, Fischer RL. 2006. DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation. Cell 124: 495-506.
53. Georgiades K, Madoui MA, Le P, Robert C, Raoult D. 2011. Phylogenomic analysis of Odyssella thessalonicensis fortifies the common origin of Rickettsiales, Pelagibacter ubique and Reclimonas americana mitochondrion. PLoS ONE 6: e24857.
54. Goll MG, Bestor TH. 2005. Eukaryotic cytosine methyl-transferases. Annu Rev Biochem 74: 481-514.
55. Gommers-Ampt JH, Borst P. 1995. Hypermodified bases in DNA. FASEB J 9: 1034-1042.
56. Goto Y, Li B, Claesen J, Shi Y, Bibb MJ, van der Donk WA. 2010. Discoveryofunique lanthionine synthetases reveals new mechanistic and evolutionary insights. PLoS Biol 8: e1000339.
57. Grazini U, Zanardi F, Citterio E, Casola S, Goding CR, McBlane F. 2010. The RING domain of RAG1 ubiquity-lates histone H3: A novel activity in chromatin-mediated regulation of V(D)J joining. Mol Cell 37: 282-293.
58. Grewal SI. 2010. RNAi-dependent formation of heterochro-matin and its diverse functions. Curr Opin Genet Dev 20: 134-141.
59. Griffiths DS, Li J, Dawson MA, Trotter MW, Cheng YH, Smith AM, Mansfield W, Liu P, Kouzarides T, Nichols J, et al. 2011. LIF-independent JAK signalling to chromatin in embryonic stem cells uncovered from an adult stem cell disease. Nat Cell Biol 13: 13-21.
60. Hajkova P, Jeffries SJ, Lee C, Miller N, Jackson SP, Surani MA. 2010. Genome-wide reprogramming in the mouse germ line entails the base excision repair pathway. Science 329: 78-82.
61. Hanover JA, Krause MW, Love DC. 2012. Bittersweet memories: Linking metabolism to epigenetics through O-GlcNAcylation. Nat Rev Mol Cell Biol 13: 312-321.
62. Hauk G, Bowman GD. 2011. Structural insights into regulation and action of SWI2/SNF2 ATPases. Curr Opin Struct Biol 21: 719-727.
63. Hazen RM. 2010. Evolutionof minerals. Sci Am 302: 58-65.
64. Heun P. 2007. SUMOrganization of the nucleus. Curr Opin Cell Biol 19: 350-355.
65. Higgins JM. 2010. Haspin: A newly discovered regulator of mitotic chromosome behavior. Chromosoma 119: 137-147.
66. Hochstrasser M.2009. Origin and functionof ubiquitin-like proteins. Nature 458: 422-429.
67. Iyer LM, Abhiman S, Aravind L. 2008a. MutL homologs in restriction-modification systems and the origin of eu-karyotic MORC ATPases. Biol Direct 3: 8.
68. Iyer LM, Anantharaman V, Wolf MY, Aravind L. 2008b. Comparative genomics of transcription factors and chro-matin proteins in parasitic protists and other eukaryotes. Int J Parasitol 38: 1-31.
69. Iyer LM, Abhiman S, Maxwell Burroughs A, Aravind L. 2009. Amidoligases with ATP-grasp, glutamine synthe-tase-like and acetyltransferase-like domains: Synthesis of novel metabolites and peptide modifications of proteins. Mol Biosyst 5: 1636-1660.
70. Iyer LM, Abhiman S, de Souza RF, Aravind L. 2010. Origin and evolution of peptide-modifying dioxygenases and identification of the wybutosine hydroxylase/hydroper-oxidase. Nucleic Acids Res 38: 5261-5279.
71. Iyer LM, Abhiman S, Aravind L. 2011a. Natural history of eukaryotic DNA methylation systems. Prog Mol Biol Transl Sci 101: 25-104.
72. Iyer LM, Zhang D, Rogozin IB, Aravind L. 2011b. Evolution of the deaminase fold and multiple origins of eukaryotic editing and mutagenic nucleic acid deaminases from bacterial toxin systems. Nucleic Acids Res 39: 9473-9497.
73. Iyer LM, Zhang D, Maxwell Burroughs A, Aravind L. 2013. Computational identification of novel biochemical systems involved in oxidation, glycosylation and other complex modifications of bases in DNA. Nucleic Acids Res 41: 7635-7655.
74. Jacobs SA, Khorasanizadeh S. 2002. Structure of HP1 chro-modomain bound to a lysine 9-methylated histone H3 tail. Science 295: 2080-2083.
75. Janke C, Rogowski K, van Dijk J. 2008. Polyglutamylation: A fine-regulator of protein function? "Protein modifications: Beyond the usual suspects" review series. EMBO Rep 9: 636-641.
76. Jekely G. 2008. Origin of the nucleus and Ran-dependent transport to safeguard ribosome biogenesis in a chimeric cell. Biol Direct 3: 31.
77. Jeyaprakash AA, Basquin C, Jayachandran U, Conti E. 2011. Structural basis for the recognition of phosphorylated histone h3 by the survivin subunit of the chromosomal passenger complex. Structure 19: 1625-1634.
78. Jiang L, Mu J, Zhang Q, Ni T, Srinivasan P, Rayavara K, Yang W, Turner L, Lavstsen T, Theander TG, et al. 2013.PfSETvs methylation of histone H3K36 represses virulence genes in Plasmodium falciparum. Nature 499: 223-227.
79. Johnson SA, Hunter T. 2005. Kinomics: Methods for deciphering the kinome. Nat Methods 2: 17-25.
80. Kannan N, Taylor SS, Zhai Y, Venter JC, Manning G. 2007. Structural and functional diversity of the microbial ki-nome. PLoS Biol 5: e17.
81. Klose RJ, Kallin EM, Zhang Y. 2006. JmjC-domain-contain-ing proteins and histone demethylation. Nat Rev Genet 7: 715-727.
82. Koonin EV. 2006. The origin of introns and their role in eukaryogenesis: A compromise solution to the introns-early versus introns-late debate? Biol Direct 1: 22.
83. Kouzarides T. 2007. Chromatin modifications and their function. Cell 128: 693-705.
84. Krishnan N, Jeong DG, Jung SK, Ryu SE, Xiao A, Allis CD, Kim SJ, Tonks NK. 2009. Dephosphorylation of the C-terminal tyrosyl residue of the DNA damage-related his-tone H2A.X is mediated by the protein phosphatase eyes absent. J Biol Chem 284: 16066-16070.
85. Kroger N, Lorenz S, Brunner E, Sumper M. 2002. Self-assembly of highly phosphorylated silaffins and their function in biosilica morphogenesis. Science 298: 584-586.
86. Laing S, Unger M, Koch-Nolte F, Haag F. 2011. ADP-ribo-sylation of arginine. Amino Acids 41: 257-269.
87. Lallemand-Breitenbach V, De The H. 2010. PML nuclear bodies. Cold Spring Harb Perspect Biol 2: a000661.
88. Landry CD, Kandel ER, Rajasethupathy P. 2013. New mechanisms in memory storage: piRNAs and epigenetics. Trends Neurosci 36: 535-542.
89. Lanzuolo C, Orlando V. 2012. Memories from the polycomb group proteins. Annu Rev Genet 46: 561-589.
90. Lee YH, Stallcup MR. 2009. Minireview: Protein arginine methylation of nonhistone proteins in transcriptional regulation. Mol Endocrinol 23: 425-433.
91. Leipe DD, Landsman D. 1997. Histone deacetylases, acetoin utilization proteins and acetylpolyamine amidohydro-lases are members of an ancient protein superfamily. Nucleic Acids Res 25: 3693-3697.
92. Leonard TA, Butler PJ, Lowe J. 2004. Structural analysis of the chromosome segregation protein Spo0J from Ther-mus thermophilus. Mol Microbiol 53: 419-432.
93. Leplae R, Geeraerts D, Hallez R, Guglielmini J, Dreze P, Van Melderen L. 2011. Diversity of bacterial type II toxin-antitoxin systems: A comprehensive search and functional analysisofnovel families. Nucleic Acids Res 39: 5513-5525.
94. Linder ME, Jennings BC. 2013. Mechanism and function of DHHC S-acyltransferases. Biochem Soc Trans 41: 29-34.
95. Liu X, Wang L, Zhao K, Thompson PR, Hwang Y, Marmor-stein R, Cole PA. 2008. The structural basis of protein acetylation by the p300/CBP transcriptional coactivator. Nature 451: 846-850.
96. Lloyd J, Chapman JR, Clapperton JA, Haire LF, Hartsuiker E, Li J, Carr AM, Jackson SP, Smerdon SJ. 2009. A supra-modular FHA/BRCT-repeat architecture mediates Nbs1 adaptor function in response to DNA damage. Cell 139: 100-111.
97. Lobocka MB, Rose DJ, Plunkett G 3rd, Rusin M, Samojedny A, Lehnherr H, Yarmolinsky MB Blattner FR. 2004. Genome of bacteriophage P1. J Bacteriol 186: 7032-7068.
98. Lopez-Garcia P, Moreira D. 1999. Metabolic symbiosisat the origin of eukaryotes. Trends Biochem Sci 24: 88-93.
99. Lynch M. 2007. The origins of genome architecture. Sinauer Associates, Sunderland, MA.
100. Makarova KS, Anantharaman V, Aravind L, Koonin EV. 2012. Live virus-free or die: Coupling of antivirus immunity and programmed suicide or dormancy in prokary-otes. Biol Direct 7: 40.
101. Manning G, Plowman GD, Hunter T, Sudarsanam S. 2002. Evolution of protein kinase signaling from yeast to man. Trends Biochem Sci 27: 514-520.
102. Mans BJ, Anantharaman V, Aravind L, Koonin EV. 2004. Comparative genomics, evolution and origins of the nuclear envelope and nuclear pore complex. Cell Cycle 3: 1612-1637.
103. Manzur KL, Farooq A, Zeng L, Plotnikova O, Koch AW, Sachchidanand, Zhou MM. 2003. A dimeric viral SET domain methyltransferase specific to Lys27 of histone H3. Nat Struct Biol 10: 187-196.
104. Martinez-Campa C, Politis P, Moreau JL, Kent N, Goodall J, Mellor J, Goding CR. 2004. Precise nucleosome positioning and the TATA box dictate requirements for the histone H4 tail and the bromodomain factor Bdf1. Mol Cell 15: 69-81.
105. Maurer-Stroh S, Dickens NJ, Hughes-Davies L, Kouzarides T, Eisenhaber F, Ponting CP. 2003. The Tudor domain "Royal Family": Tudor, plant Agenet, Chromo, PWWP and MBT domains. Trends Biochem Sci 28: 69-74.
106. Maynard Smith J, Szathmáry E. 1999. The origins of life: From the birth of life to the origin of language. Oxford University Press, Oxford, New York.
107. Miranda TB, Webb KJ, Edberg DD, Reeves R, Clarke S. 2005. Protein arginine methyltransferase 6 specifically methyl-ates the nonhistone chromatin protein HMGA1a. Bio-chem Biophys Res Commun 336: 831-835.
108. Mochizuki K. 2010. DNA rearrangements directed by non-coding RNAs in ciliates. Wiley Interdiscip Rev RNA 1: 376-387.
109. Montellier E, Rousseaux S, Zhao Y, Khochbin S. 2012. His-tone crotonylation specifically marks the haploid male germ cell gene expression program: Post-meiotic male-specific gene expression. Bioessays 34: 187-193.
110. Mueller GA, Moon AF, Derose EF, Havener JM, Ramsden DA, Pedersen LC, London RE. 2008. A comparison of BRCT domains involved in nonhomologous end-joining: Introducing the solution structure of the BRCT do-mainof polymerase l. DNA Repair (Amst) 7: 1340-1351.
111. Muller J, Hart CM, Francis NJ, Vargas ML, Sengupta A, Wild B, Miller EL, O'Connor MB, Kingston RE, Simon JA. 2002. Histone methyltransferase activity of a Drosophila polycomb group repressor complex. Cell 111: 197-208.
112. Neuwald AF, Landsman D. 1997. GCN5-related histone N-acetyltransferases belong to a diverse superfamily that includes the yeast SPT10 protein. Trends Biochem Sci 22: 154-155.
113. Nicholson TB, Chen T. 2009. LSD1 demethylates histone and non-histone proteins. Epigenetics 4: 129-132.
114. Nunoura T, Takaki Y, Kakuta J, Nishi S, Sugahara J, Kazama H, Chee GJ, Hattori M, Kanai A, Atomi H, et al. 2011. Insights into the evolution of Archaea and eukaryotic protein modifier systems revealed by the genome of a novel archaeal group. Nucleic Acids Res 39: 3204-3223.
115. Oeffinger M, Wei KE, Rogers R, DeGrasse JA, Chait BT, Aitchison JD, Rout MP. 2007. Comprehensive analysis of diverse ribonucleoprotein complexes. Nat Methods 4: 951-956.
116. Ossareh-Nazari B, Bonizec M, Cohen M, Dokudovskaya S, Delalande F, Schaeffer C, Van Dorsselaer A, Dargemont C. 2010. Cdc48 and Ufd3, new partners of the ubiquitin protease Ubp3, are required for ribophagy. EMBO Rep 11: 548-554.
117. Papineau D, Purohit R, Fogel ML, Shields-Zhou GA. 2012. High phosphate availability as a possible cause for massive cyanobacterial production of oxygen in the Paleoproterozoic atmosphere. Earth Planet Sci Lett 362: 225-236.
118. Pastor WA, Aravind L, Rao A. 2013. TETonic shift: Biological roles of TET proteins in DNA demethylation and transcription. Nat Rev Mol Cell Biol 14: 341-356.
119. Peterson CL, Laniel MA. 2004. Histones and histone modifications. Curr Biol 14: R546-R551.
120. Porras-Yakushi TR, Whitelegge JP, Clarke S. 2007. Yeast ri-bosomal/cytochrome c SET domain methyltransferase subfamily: Identification of Rpl23ab methylation sites and recognition motifs. J Biol Chem 282: 12368-12376.
121. Ramirez MS, Tolmasky ME. 2010. Aminoglycoside modifying enzymes. Drug Resist Updat 13: 151-171.
122. Reinert DJ, Jank T, Aktories K, Schulz GE. 2005. Structural basis for the function of Clostridium difficile toxin B. J Mol Biol 351: 973-981.
123. Resh MD. 2006. Palmitoylation of ligands, receptors, and intracellular signaling molecules. Sci STKE 2006: re14.
124. Richards EJ, Elgin SC. 2002. Epigenetic codes for hetero-chromatin formation and silencing: Rounding up the usual suspects. Cell 108: 489-500.
125. Roberts RJ, Vincze T, Posfai J, Macelis D. 2010. REBASE-A database for DNA restriction and modification: Enzymes, genes and genomes. Nucleic Acids Res 38: D234-D236.
126. Rogozin IB, Iyer LM, Liang L, Glazko GV, Liston VG, Pavlov YI, Aravind L, Pancer Z. 2007. Evolution and diversification of lamprey antigen receptors: Evidence for involvement of an AID-APOBEC family cytosine deaminase. Nat Immunol 8: 647-656.
127. Rossetto D, Avvakumov N, Cote J. 2012. Histone phosphor-ylation: A chromatin modification involved in diverse nuclear events. Epigenetics 7: 1098-1108.
128. Sandman K, Reeve JN. 2005. Archaeal chromatin proteins: Different structures but common function? Curr Opin Microbiol 8: 656-661.
129. Sawada K, Yang Z, Horton JR, Collins RE, Zhang X, Cheng X. 2004. Structure of the conserved core of the yeast Dot1p, a nucleosomal histone H3 lysine 79 methyltrans-ferase. J Biol Chem 279: 43296-43306.
130. Schmitz-Esser S, Tischler P, Arnold R, Montanaro J, Wagner M, Rattei T, Horn M. 2010. The genome of the amoeba symbiont "Candidatus Amoebophilus asiaticus" reveals common mechanisms for host cell interaction among amoeba-associated bacteria. J Bacteriol 192: 1045-1057.
131. Scott RJ, Spielman M. 2006. Genomic imprinting in plants and mammals: How life history constrains convergence. Cytogenet Genome Res 113: 53-67.
132. Sheppard V, Poulsen N, Kroger N. 2010. Characterization of an endoplasmic reticulum-associated silaffin kinase from the diatom Thalassiosira pseudonana. J Biol Chem 285: 1166-1176.
133. Shimojo H, Sano N, Moriwaki Y, Okuda M, Horikoshi M, Nishimura Y. 2008. Novel structural and functional mode of a knot essential for RNA binding activity of the Esa1 presumed chromodomain. J Mol Biol 378: 987-1001.
134. Simpson AG, Inagaki Y, Roger AJ. 2006. Comprehensive multigene phylogenies of excavate protists reveal the evolutionary positions of "primitive" eukaryotes. Mol Biol Evol 23: 615-625.
135. Singh N, Basnet H, Wiltshire TD, Mohammad DH, Thomp-son JR, Heroux A, Botuyan MV, Yaffe MB, Couch FJ, Rosenfeld MG, et al. 2012. Dual recognition of phospho-serine and phosphotyrosine in histone variant H2A.X by DNA damage response protein MCPH1. Proc Natl Acad Sci 109: 14381-14386.
136. Spruijt CG, Gnerlich F, Smits AH, Pfaffeneder T, Jansen PW, Bauer C, Munzel M, Wagner M, Muller M, Khan F, et al. 2013. Dynamic readers for 5-(hydroxy)methylcytosine and its oxidized derivatives. Cell 152: 1146-1159.
137. Sumper M, Hett R, Lehmann G, Wenzl S. 2007. A code for lysine modifications of a silica biomineralizing silaffin protein. Angew Chem Int Ed Engl 46: 8405-8408.
138. Tagliabracci VS, Pinna LA, Dixon JE. 2013. Secreted protein kinases. Trends Biochem Sci 38: 121-130.
139. Touz MC, Ropolo AS, Rivero MR, Vranych CV, Conrad JT, Svard SG, Nash TE. 2008. Arginine deiminase has multiple regulatory roles in the biology of Giardia lamblia. J Cell Sci 121: 2930-2938.
140. Trievel RC, Shilatifard A. 2009. WDR5,acomplexed protein. Nat Struct Mol Biol 16: 678-680.
141. Trievel RC, Beach BM, Dirk LM, Houtz RL, Hurley JH. 2002. Structure and catalytic mechanism of a SET domain protein methyltransferase. Cell 111: 91-103.
142. Tsuge K, Matsui K, Itaya M. 2007. Production of the non-ribosomal peptide plipastatin in Bacillus subtilis regulated by three relevant gene blocks assembled in a single movable DNA segment. J Biotechnol 129: 592-603.
143. Tsukada Y, Fang J, Erdjument-Bromage H, Warren ME, Borchers CH, Tempst P, Zhang Y. 2006. Histone de-methylation by a family of JmjC domain-containing proteins. Nature 439: 811-816.
144. Venancio TM, Balaji S, Iyer LM, Aravind L. 2009. Reconstructing the ubiquitin network: Cross-talk with other systems and identification of novel functions. Genome Biol 10: R33.
145. Vossenaar ER, Zendman AJ, van Venrooij WJ, Pruijn GJ. 2003. PAD, a growing family of citrullinating enzymes: Genes, features and involvement in disease. Bioessays 25: 1106-1118.
146. Walsh C. 2003. Antibiotics: Actions, origins, resistance. American Society for Microbiology, Washington, DC.
147. Walsh DA, Doolittle WF. 2005. The real "domains" of life. Curr Biol 15: R237-R240.
148. Walsh CT, Garneau-Tsodikova S, Gatto GJ. 2005. Protein posttranslational modifications: The chemistry of prote-ome diversifications. Angewandte Chemie 2005: 7342-7372.
149. West AH, Stock AM. 2001. Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem Sci 26: 369-376.
150. Winkler GS, Kristjuhan A, Erdjument-Bromage H, Tempst P, Svejstrup JQ. 2002. Elongator is a histone H3 and H4 acetyltransferase important for normal histone acetyla-tion levels in vivo. Proc Natl Acad Sci 99: 3517-3522.
151. Wittschieben BO, Otero G, de Bizemont T, Fellows J, Erdju-ment-Bromage H, Ohba R, Li Y, Allis CD, Tempst P, Svejstrup JQ. 1999. A novel histone acetyltransferase is an integral subunit of elongating RNA polymerase II ho-loenzyme. Mol Cell 4: 123-128.
152. Worby CA, Mattoo S, Kruger RP, Corbeil LB, Koller A, Mendez JC, Zekarias B, Lazar C, Dixon JE. 2009. The fic domain: Regulation of cell signaling by adenylylation. Mol Cell 34: 93-103.
153. Wright DE, Wang CY, Kao CF. 2012. Histone ubiquitylation and chromatin dynamics. Front Biosci (Landmark Ed) 17: 1051-1078.
154. Xiao A, Li H, Shechter D, Ahn SH, Fabrizio LA, Erdjument-Bromage H, Ishibe-Murakami S, Wang B, Tempst P, Hof-mann K, et al. 2009. WSTF regulates the H2A.X DNA damage response via a novel tyrosine kinase activity. Nature 457: 57-62.
155. Yan Q, Dutt S, Xu R, Graves K, Juszczynski P, Manis JP, Shipp MA. 2009. BBAP monoubiquitylates histone H4 at lysine 91 and selectively modulates the DNA damage response. Mol Cell 36: 110-120.
156. Yap KL, Zhou MM. 2010. Keeping it in the family: Diverse histone recognition by conserved structural folds. Crit Rev Biochem Mol Biol 45: 488-505.
157. Yutin N, Koonin EV. 2012. Archaeal origin of tubulin. Biol Direct 7: 10.
158. Zeng L, Zhou MM. 2002. Bromodomain: An acetyl-lysine binding domain. FEBS Lett 513: 124-128.
159. Zentner GE, Henikoff S. 2013. Regulation of nucleosome dynamics by histone modifications. Nat Struct Mol Biol 20: 259-266.
160. Zhang D, Aravind L. 2012. Novel transglutaminase-like pep-tidase and C2 domains elucidate the structure, biogenesis and evolution of the ciliary compartment. Cell Cycle 11: 3861-3875.
161. Zhang D, de Souza RF, Anantharaman V, Iyer LM, Aravind L. 2012. Polymorphic toxin systems: Comprehensive characterization of trafficking modes, processing, mechanisms of action, immunity and ecology using comparative genomics. Biol Direct 7: 18.
162. Zippo A, Serafini R, Rocchigiani M, Pennacchini S, Krepe-lova A, Oliviero S. 2009. Histone crosstalk between H3S10ph and H4K16ac generates a histone code that mediates transcription elongation. Cell 138: 1122-1136.
163. Zoldos V, Novokmet M, Beceheli I, Lauc G. 2013. Genomics and epigenomics of the human glycome. Glycoconj J 30: 41-50.