A class II histone deacetylase acts on newly synthesized histones in tetrahymena

Eukaryotic Cell

Volumn 7, Issue 3, 2008, Pages 471-482

  Smith, Joshua J ^a   Torigoe, Sharon E ^a,c   Maxson, Julia ^a,d   Fish, Lisa C ^a,e   Wiley, Emily A ^a,b  

^a Claremont McKenna Scripps and Pitzer Colleges ^*  (United States)

^b KECK GRADUATE INSTITUTE   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^e Fred Hutchinson Cancer Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CILIOPHORA; TETRAHYMENA; TETRAHYMENA THERMOPHILA;

HISTONE; HISTONE DEACETYLASE;

ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; ANIMAL; ARTICLE; DNA REPLICATION; ENZYMOLOGY; GERMLINE MICRONUCLEUS; MACRONUCLEUS; METABOLISM; MOLECULAR GENETICS; NUCLEOSOME; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT; TETRAHYMENA THERMOPHILA;

ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANIMALS; DNA REPLICATION; HISTONE DEACETYLASES; HISTONES; MACRONUCLEUS; MICRONUCLEUS, GERMLINE; MOLECULAR SEQUENCE DATA; NUCLEOSOMES; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; TETRAHYMENA THERMOPHILA;

EID: 40949130395     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00409-07     Document Type: Article

References (63)

1. Ai, X., and M. R. Parthun. 2004. The nuclear Hat1p/Hat2p complex: a molecular link between type B histone acetyltransferases and chromatin assembly. Mol. Cell 14:195-205.
2. Allis, C. D., L. G. Chicoine, R. Richman, and I. G. Schulman. 1985. Deposition-related histone acetylation in micronuclei of conjugating Tetrahymena. Proc. Natl. Acad. Sci. USA 82:8048-8052.
3. Allis, C. D., C. V. Glover, and M. A. Gorovsky. 1979. Micronuclei of Tetrahymena contain two types of histone H3. Proc. Natl. Acad. Sci. USA 76:4857-4861.
4. Allis, C. D., and M. A. Gorovsky. 1981. Histone phosphorylation in macroand micronuclei of Tetrahymena thermophila. Biochemistry 20:3828-3833.
5. Allis, C. D., and J. C. Wiggins. 1984. Histone rearrangements accompany nuclear differentiation and dedifferentiation in Tetrahymena. Dev. Biol. 101:282-294.
6. Allis, C. D., and J. C. Wiggins. 1984. Proteolytic processing of micronuclear H3 and histone phosphorylation during conjugation in Tetrahymena thermophila. Exp. Cell Res. 153:287-298.
7. Annunziato, A. T., and R. L. Seale. 1983. Histone deacetylation is required for the maturation of newly replicated chromatin. J. Biol. Chem. 258:12675-12684.
8. Chicoine, L. G., I. G. Schulman, R. Richman, R. G. Cook, and C. D. Allis. 1986. Nonrandom utilization of acetylation sites in histones isolated from Tetrahymena. Evidence for functionally distinct H4 acetylation sites. J. Biol. Chem. 261:1071-1076.
9. Cole, E. S., K. R. Stuart, T. C. Marsh, K. Aufderheide, and W. Ringlien. 2002. Confocal fluorescence microscopy for Tetrahymena thermophila. Methods Cell Biol. 70:337-359.
10. Cosgrove, M. S., J. D. Boeke, and C. Wolberger. 2004. Regulated nucleosome mobility and the histone code. Nat. Struct. Mol. Biol. 11:1037-1043.
11. de Ruijter, A. J., A. H. van Gennip, H. N. Caron, S. Kemp, and A. B. van Kuilenburg. 2003. Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem. J. 370:737-749.
12. Doerder, F. P., and L. E. Debault. 1975. Cytofluorimetric analysis of nuclear DNA during meiosis, fertilization and macronuclear development in the ciliate Tetrahymena pyriformis, syngen 1. J. Cell Sci. 17:471-493.
13. Duharcourt, S., and M. C. Yao. 2002. Role of histone deacetylation in developmentally programmed DNA rearrangements in Tetrahymena thermophila. Eukaryot. Cell 1:293-303.
14. English, C. M., M. W. Adkins, J. J. Carson, M. E. Churchill, and J. K. Tyler. 2006. Structural basis for the histone chaperone activity of Asf1. Cell 127:495-508.
15. Gaertig, J., and M. A. Gorovsky. 1992. Efficient mass transformation of Tetrahymena thermophila by electroporation of conjugants. Proc. Natl. Acad. Sci. USA 89:9196-9200.
16. Gao, L., M. A. Cueto, F. Asselbergs, and P. Atadja. 2002. Cloning and functional characterization of HDAC11, a novel member of the human histone deacetylase family. J. Biol. Chem. 277:25748-25755.
17. Gorovsky, M. A., M. C. Yao, J. B. Keevert, and G. L. Pleger. 1975. Isolation of micro- and macronuclei of Tetrahymena pyriformis. Methods Cell Biol. 9:311-327.
18. Gregoretti, I. V., Y. M. Lee, and H. V. Goodson. 2004. Molecular evolution of the histone deacetylase family: functional implications of phylogenetic analysis. J. Mol. Biol. 338:17-31.
19. Hanakahi, L. A., M. Bartlet-Jones, C. Chappell, D. Pappin, and S. C. West. 2000. Binding of inositol phosphate to DNA-PK and stimulation of double-strand break repair. Cell 102:721-729.
20. Holmes, W., and G. Jogl. 2006. Crystal structure of inositol phosphate multikinase 2 and implications for substrate specificity. J. Biol. Chem. 281:38109-38116.
21. Jackson, V., A. Shires, N. Tanphaichitr, and R. Chalkley. 1976. Modifications to histones immediately after synthesis. J. Mol. Biol. 104:471-483.
22. Jaeckel-Williams, R. 1978. Nuclear divisions with reduced numbers of microtubules in Tetrahymena. J. Cell Sci. 34:303-319.
23. Kornberg, R. D., and Y. Lorch. 1999. Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 98:285-294.
24. Krajewski, W. A., and P. B. Becker. 1998. Reconstitution of hyperacetylated, DNase I-sensitive chromatin characterized by high conformational flexibility of nucleosomal DNA. Proc. Natl. Acad. Sci. USA 95:1540-1545.
25. Kuo, M. H., J. E. Brownell, R. E. Sobel, T. A. Ranalli, R. G. Cook, D. G. Edmondson, S. Y. Roth, and C. D. Allis. 1996. Transcription-linked acetylation by Gcn5p of histones H3 and H4 at specific lysines. Nature 383:269-272.
26. Leipe, D. D., and D. Landsman. 1997. Histone deacetylases, acetoin utilization proteins and acetylpolyamine amidohydrolases are members of an ancient protein superfamily. Nucleic Acids Res. 25:3693-3697.
27. Lin, R., J. W. Leone, R. G. Cook, and C. D. Allis. 1989. Antibodies specific to acetylated histones document the existence of deposition- and transcription-related histone acetylation in Tetrahymena. J. Cell Biol. 108:1577-1588.
28. Lucchini, R., R. E. Wellinger, and J. M. Sogo. 2001. Nucleosome positioning at the replication fork. EMBO J. 20:7294-7302.
29. Luger, K., A. W. Mader, R. K. Richmond, D. F. Sargent, and T. J. Richmond. 1997. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389:251-260.
30. Marsh, T. C., E. S. Cole, and D. P. Romero. 2001. The transition from conjugal development to the first vegetative cell division is dependent on RAD51 expression in the ciliate Tetrahymena thermophila. Genetics 157:1591-1598.
31. Marsh, T. C., E. S. Cole, K. R. Stuart, C. Campbell, and D. P. Romero. 2000. RAD51 is required for propagation of the germinal nucleus in Tetrahymena thermophila. Genetics 154:1587-1596.
32. Masumoto, H., D. Hawke, R. Kobayashi, and A. Verreault. 2005. A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature 436:294-298.
33. Miller, A. L., M. Suntharalingam, S. L. Johnson, A. Audhya, S. D. Emr, and S. R. Wente. 2004. Cytoplasmic inositol hexakisphosphate production is sufficient for mediating the Gle1-mRNA export pathway. J. Biol. Chem. 279:51022-51032.
34. Mitchell, E. J., S. Zimmerman, and A. M. Zimmerman. 1985. Actin and tubulin in Tetrahymena. Can. J. Biochem. Cell Biol. 63:389-396.
35. Nalaskowski, M. M., C. Deschermeier, W. Fanick, and G. W. Mayr. 2002. The human homologue of yeast ArgRIII protein is an inositol phosphate multikinase with predominantly nuclear localization. Biochem. J. 366:549-556.
36. Ohba, R., D. J. Steger, J. E. Brownell, C. A. Mizzen, R. G. Cook, J. Cote, J. L. Workman, and C. D. Allis. 1999. A novel H2A/H4 nucleosomal histone acetyltransferase in Tetrahymena thermophila. Mol. Cell. Biol. 19:2061-2068.
37. Parker, K., J. Maxson, A. Mooney, and E. A. Wiley. 2007. Class I histone deacetylase Thd1p promotes global chromatin condensation in Tetrahymena thermophila. Eukaryot. Cell 6:1913-1924.
38. Perry, C. A., and A. T. Annunziato. 1989. Influence of histone acetylation on the solubility, H1 content and DNase I sensitivity of newly assembled chromatin. Nucleic Acids Res. 17:4275-4291.
39. Perry, C. A., and A. T. Annunziato. 1991. Histone acetylation reduces H1-mediated nucleosome interactions during chromatin assembly. Exp. Cell Res. 196:337-345.
40. Richman, R., L. G. Chicoine, M. P. Collini, R. G. Cook, and C. D. Allis. 1988. Micronuclei and the cytoplasm of growing Tetrahymena contain a histone acetylase activity which is highly specific for free histone H4. J. Cell Biol. 106:1017-1026.
41. Robyr, D., Y. Suka, I. Xenarios, S. K. Kurdistani, A. Wang, N. Suka, and M. Grunstein. 2002. Microarray deacetylation maps determine genome-wide functions for yeast histone deacetylases. Cell 109:437-446.
42. Ruiz-Carrillo, A., L. J. Wangh, and V. G. Allfrey. 1975. Processing of newly synthesized histone molecules. Science 190:117-128.
43. Shen, X., H. Xiao, R. Ranallo, W. H. Wu, and C. Wu. 2003. Modulation of ATP-dependent chromatin-remodeling complexes by inositol polyphosphates. Science 299:112-114.
44. Shimamura, A., and A. Worcel. 1989. The assembly of regularly spaced nucleosomes in the Xenopus oocyte S-150 extract is accompanied by deacetylation of histone H4. J. Biol. Chem. 264:14524-14530.
45. Smith, S., and B. Stillman. 1991. Stepwise assembly of chromatin during DNA replication in vitro. EMBO J. 10:971-980.
46. Sobel, R. E., R. G. Cook, C. A. Perry, A. T. Annunziato, and C. D. Allis. 1995. Conservation of deposition-related acetylation sites in newly synthesized histones H3 and H4. Proc. Natl. Acad. Sci. USA 92:1237-1241.
47. Sogo, J. M., H. Stahl, T. Koller, and R. Knippers. 1986. Structure of replicating simian virus 40 minichromosomes. The replication fork, core histone segregation and terminal structures. J. Mol. Biol. 189:189-204.
48. Steger, D. J., E. S. Haswell, A. L. Miller, S. R. Wente, and E. K. O'Shea. 2003. Regulation of chromatin remodeling by inositol polyphosphates. Science 299:114-116.
49. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-1599.
50. Van Holde, K. E. 1989. Chromatin. Springer-Verlag, New York, NY.
51. Vavra, K. J., C. D. Allis, and M. A. Gorovsky. 1982. Regulation of histone acetylation in Tetrahymena macro- and micronuclei. J. Biol. Chem. 257:2591-2598.
52. Verreault, A., P. D. Kaufman, R. Kobayashi, and B. Stillman. 1996. Nucleosome assembly by a complex of CAF-1 and acetylated histones H3/H4. Cell 87:95-104.
53. Waterborg, J. H., S. R. Fried, and H. R. Matthews. 1983. Acetylation and methylation sites in histone H4 from Physarum polycephalum. Eur. J. Biochem. 136:245-252.
54. Wei, Y., C. A. Mizzen, R. G. Cook, M. A. Gorovsky, and C. D. Allis. 1998. Phosphorylation of histone H3 at serine 10 is correlated with chromosome condensation during mitosis and meiosis in Tetrahymena. Proc. Natl. Acad. Sci. USA 95:7480-7484.
55. Wei, Y., L. Yu, J. Bowen, M. A. Gorovsky, and C. D. Allis. 1999. Phosphorylation of histone H3 is required for proper chromosome condensation and segregation. Cell 97:99-109.
56. Wiley, E. A., T. Myers, K. Parker, T. Braun, and M. C. Yao. 2005. Class I histone deacetylase Thd1p affects nuclear integrity in Tetrahymena thermophila. Eukaryot. Cell 4:981-990.
57. Wiley, E. A., R. Ohba, M. C. Yao, and C. D. Allis. 2000. Developmentally regulated rpd3p homolog specific to the transcriptionally active macronucleus of vegetative Tetrahymena thermophila. Mol. Cell. Biol. 20:8319-8328.
58. Wu, M., C. D. Allis, and M. A. Gorovsky. 1988. Cell-cycle regulation as a mechanism for targeting proteins to specific DNA sequences in Tetrahymena thermophila. Proc. Natl. Acad. Sci. USA 85:2205-2209.
59. Yao, M. C., C. H. Yao, L. M. Halasz, P. Fuller, C. H. Rexer, S. H. Wang, R. Jain, R. S. Coyne, and D. L. Chalker. 2007. Identification of novel chromatin-associated proteins involved in programmed genome rearrangements in Tetrahymena. J. Cell Sci. 120:1978-1989.
60. Ye, J., X. Ai, E. E. Eugeni, L. Zhang, L. R. Carpenter, M. A. Jelinek, M. A. Freitas, and M. R. Parthun. 2005. Histone H4 lysine 91 acetylation: a core domain modification associated with chromatin assembly. Mol. Cell 18:123-130.
61. Yu, G. L., and E. H. Blackburn. 1990. Amplification of tandemly repeated origin control sequences confers a replication advantage on rDNA replicons in Tetrahymena thermophila. Mol. Cell. Biol. 10:2070-2080.
62. Zimmerman, A. M., S. Zimmerman, J. Thomas, and I. Ginzburg. 1983. Control of tubulin and actin gene expression in Tetrahymena pyriformis during the cell cycle. FEBS Lett. 164:318-321.
63. Zou, H., Y. Wu, M. Navre, and B. C. Sang. 2006. Characterization of the two catalytic domains in histone deacetylase 6. Biochem. Biophys. Res. Commun. 341:45-50.