A nonessential HP1-like protein affects starvation-induced assembly of condensed chromatin and gene expression in macronuclei of Tetrahymena thermophila

Molecular and Cellular Biology

Volumn 19, Issue 5, 1999, Pages 3624-3634

  Huang, Hui ^a   Smothers, James F ^b,d   Wiley, Emily A ^b,d   David Allis, C ^b,c  

^a SYRACUSE UNIVERSITY   (United States)

^b UNIVERSITY OF ROCHESTER   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

^d Fred Hutchinson Cancer Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN HHP1P; PROTOZOAL PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL SURVIVAL; CELL VIABILITY; CHROMATIN; DROSOPHILA MELANOGASTER; GENE ACTIVATION; GENE CONTROL; GENE DISRUPTION; GENE EXPRESSION; GENE EXPRESSION REGULATION; MACRONUCLEUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN PHOSPHORYLATION; STARVATION; TETRAHYMENA THERMOPHILA;

DROSOPHILA MELANOGASTER; EUKARYOTA; INVERTEBRATA; MELANOGASTER; PROTOZOA; TETRAHYMENA; TETRAHYMENA THERMOPHILA;

EID: 0032954037     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.19.5.3624     Document Type: Article

References (60)

1. Ainsztein, A. M., S. E. Kandels-Lewis, A. M. Mackay, and W. C. Earnshaw. 1998. INCENP centromere and spindle targeting: identification of essential conserved motifs and involvement of heterochromatin protein HP1. J. Cell Biol. 143:1763-1774.
2. Allshire, R. C., J.-P. Javerzat, N. J. Redhead, and G. Cranston. 1994. Position effect variegation at fission yeast centromeres. Cell 74:157-169.
3. Bannon, G. A., F. J. Calzone, J. K. Bowen, C. D. Allis, and M. A. Gorovsky. 1983. Multiple, independently regulated, polyadenylated messages for histone H3 and H4 in Tetrahymena. Nucleic Acids Res. 11:3903-3917.
4. Bruns, P. J., and T. B. Brussard. 1974. Pair formation in Tetrahymena pyriformis, an inducible developmental system. J. Exp. Zool. 188:337-344.
5. Calzone, R. J., V. A. Stathopoulos, D. Grass, M. A. Gorovsky, and R. C. Angerer. 1983. Regulation of protein synthesis in Tetrahymena: RNA sequence sets of growing and starved cells. J. Biol. Chem. 258:6899-6905.
6. Cassidy-Hanley, D., J. Bowen, H. J. Lee, E. Cole, A. L. VerPlank, J. Gaertig, M. A. Gorovsky, and P. J. Bruns. 1997. Germline and somatic transformation of mating Tetrahymena thermophila by particle bombardment. Genetics 146:135-147.
7. Coyne, R. S., and M. C. Yao. 1996. Evolutionary conservation of sequences directing chromosome breakage and rDNA palindrome formation in tetrahymenine ciliates. Genetics 144:1479-1487.
8. Csink, A. K., and S. Henikoff. 1996. Genetic modification of heterochromatin association and nuclear organization in Drosophila. Nature 381:529-531.
9. Dernburg, A. F., J. W. Sedat, and R. S. Hawley. 1996. Direct evidence of a role for heterochromatin in meiotic chromosome segregation. Cell 86:135-146.
10. Dernburg, A. F., K. W. Broman, J. C. Fung, W. F. Marshall, J. Philips, D. A. Agard, and J. W. Sedat. 1996. Perturbation of nuclear architecture by long-distance chromosome interactions. Cell 85:745-759.
11. Eissenberg, J. C., T. C. James, D. M. Foster-Hartnett, T. Hartnett, V. Ngan, and S. C. R. Elgin. 1990. Mutation in a heterochromatin-specific chromosomal protein is associated with suppression of position-effect variegation in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 87:9923-9927.
12. Eissenberg, J. C., G. D. Morris, G. Reuter, and T. Hartnett. 1992. The heterochromatin-associated protein HP-1 is an essential protein in Drosophila with dosage-dependent effects on position-effect variegation. Genetics 131:345-352.
13. Eissenberg, J. C., and T. Hartnett. 1993. A heat shock-activated cDNA rescues the recessive lethality of mutations in the heterochromatin-associated protein HP1 of Drosophila melanogaster. Mol. Gen. Genet. 240:333-338.
14. Eissenberg, J. C., Y.-W. Ge, and T. Hartnett. 1994. Increased phosphorylation of HP1, a heterochromatin-associated protein of Drosophila, is correlated with heterochromatin assembly. J. Biol. Chem. 269:21315-21321.
15. Ekwall, K., J.-P. Javerzat, A. Lorentz, H. Schmidt, G. Cranston, and R. Allshire. 1995. The chromodomain protein swi6: a key component at fission yeast centromeres. Science 269:1429-1431.
16. Elgin, S. C. R. 1996. Heterochromatin and gene regulation in Drosophila. Curr. Opin. Genet. Dev. 6:193-202.
17. Fanti, L., G. Glovinazzo, M. Berloco, and S. Pimpinelli. 1998. The heterochromatin protein 1 prevents telomere fusions in Drosophila. Mol. Cell 2:527-538.
18. Festenstein, R., M. Tolaini, P. Corbella, C. Mamalaki, J. Parrington, M. Fox, A. Miliou, M. Jones, and D. Kioussis. 1996. Locus control region function and heterochromatin-induced position effect variegation. Science 271:1123-1125.
19. 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.
20. Gaertig, J., L. Gu, B. Hai, and M. A. Gorovsky. 1994. High frequency vector-mediated transformation and gene replacement in Tetrahymena. Nucleic Acids Res. 22:5391-5398.
21. Gatti, M., and S. Pimpinelli. 1992. Functional elements in Drosophila melanogaster heterochromatin. Annu. Rev. Genet. 26:239-275.
22. Gorovsky, M. A. 1973. Macro- and micronuclei of Tetrahymena pyriformis: a model system for studying the structure and function of eukaryotic nuclei. J. Protozool. 20:19-25.
23. Gorovsky, M. A. 1980. Genome organization and reorganization in Tetrahymena. Annu. Rev. Genet. 14:203-239.
24. Gottschling, D. E., O. M. Aparicio, B. L. Billington, and V. A. Zakian. 1990. Position effect at S. cerevisiae telomeres: reversible repression of Pol II transcription. Cell 63:751-762.
25. Grunstein, M. 1998. Yeast heterochromatin: regulation of its assembly and inheritance by histones. Cell 93:325-328.
26. Hearn, M. G., A. Hedrick, T. A. Grigliatti, and B. T. Wakimoto. 1991. The effect of modifiers to position-effect variegation on the variegation of heterochromatic genes of Drosophila melanogaster. Genetics 128:785-797.
27. Hilliker, A. Y., R. Appels, and A. Schalet. 1980. The genetic analysis of D. melanogaster heterochromatin. Cell 21:607-619.
28. Holstege, F. C. P., E. G. Jennings, J. J. Wyrick, T. I. Lee, C. J. Hengartner, M. R. Green, T. R. Golub, E. S. Lander, and R. A. Young, 1998. Dissecting the regulatory circuitry of a eucaryotic genome. Cell 95:717-728.
29. Huang, D. W., L. Fanti, D. T. S. Pak, M. R. Botchan, S. Pimpinelli, and R. Kellum. 1998. Distinct cytoplasmic and nuclear fractions of Drosophila heterochromatin protein 1: their phosphorylation levels and associations with origin recognition complex proteins. J. Cell Biol. 142:307-318.
30. Huang, H., E. A. Wiley, R. C. Lending, and C. D. Allis. 1998 An HP1-like protein is missing from transcriptionally silent micronuclei but is enriched in condensed macronuclear chromatin. Proc. Natl. Acad. Sci. USA 95:13624-13629.
31. Jeter, J. R., W. A. Pavlat, and I. L. Cameron. 1975. Changes in the nuclear acidic proteins and chromatin structure in starved and refed Tetrahymena. Exp. Cell Res. 93:79-88.
32. John, B. 1988. The biology of heterochromatin, p. 1-147. In R. S. Verma (ed.), Heterochromatin: molecular and structure aspects. Cambridge University Press, New York, N.Y.
33. Karpen, G. H., M. H. Le, and H. Le. 1996. Centric heterochromatin and the efficiency of achiasmate disjunction in Drosophila female meiosis. Science 273:118-122.
34. Karrer, K. M., S. L. Peiffer, and M. E. DiTomas. 1993. Two distinct gene subfamilies within the family of cysteine protease genes. Proc. Natl. Acad. Sci. USA 90:3063-3067.
35. Kellum, R., and B. M. Alberts. 1995. Heterochromatin protein 1 is required for correct chromosome segregation in Drosophila embryos. J. Cell Sci. 108:1419-1431.
36. Kimmerly, W., A. Buchman, R. Kornberg, and J. Rine. 1988. Roles of two DNA-binding factors in replication, segregation and transcriptional repression mediated by a yeast silencer. EMBO J. 7:2241-2253.
37. Leem, S.-H., C.-H. Chung, Y. Sunwoo, and H. Araki. 1998. Meiotic role of SWI6 in Saccharomyces cerevisiae. Nucleic Acids Res. 26:3154-3158.
38. Lorentz, A., K. Osterman, O. Fleck, and H. Schmidt. 1994. Switching gene swi6, involved in the repression of silent mating-type loci in fission yeast, encodes a homologue of chromatin-associated proteins from Drosophila and mammals. Gene 143:139-143.
39. Maniatis, T., E. F. Fritsch, and J. Sambrook. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
40. Marshall, W. F., J. C. Fung, and J. W. Sedat. 1997. Deconstructing the nucleus: global architecture from local interactions. Curr. Opin. Genet. Dev. 7:259-263.
41. Martindale, D. W., and P. J. Bruns. 1983. Cloning of abundant mRNA species present during conjugation of Tetrahymena thermophila: identification of mRNA species present exclusively during meiosis. Mol. Cell. Biol. 3:1857-1865.
42. Milot, E., J. Strouboulis, T. Trimborn, M. Wijgerde, E. deBoer, A. Langeveld, K. Tan-Un, W. Vergeer, N. Yannoustsos, F. Grosveld, and P. Fraser. 1996. Heterochromatin effects on the frequency and duration of LCR-mediated gene transcription. Cell 87:105-114.
43. Nicol, L., and P. Jeppesen. 1990. Human autoimmune sera recognize a conserved 26-kD protein which associated with mammalian heterochromatin that is homologous to heterochromatin protein 1 of Drosophila. Chromosome Res. 2:245-253.
44. Pillus, L., and M. Grunstein. 1995. Chromatin structure and epigenetic regulation in yeast, p. 123-146. In S. C. R. Elgin (ed.), Chromatin structure and gene expression. IRL Press, Oxford, England.
45. Prescott, D. M. 1994. The DNA of ciliated protozoa. Microbiol. Rev. 58: 233-267.
46. Renauld, H., and S. M. Gasser. 1997. Heterochromatin: a meiotic matchmaker? Trends Cell Biol. 7:201-205.
47. Reuter, G., and P. Spierer. 1992. Position effect variegation and chromatin proteins. Bioessays 14:605-612.
48. Shen, X., L. Yu, J. W. Weir, and M. A. Gorovsky. 1995. Linker histones are not essential and affect chromatin condensation in vivo. Cell 82:47-56.
49. Shen, X., and M. A. Gorovsky. 1996. Linker histone H1 regulates specific gene expression but not global transcription in vivo. Cell 86:475-483.
50. Singh, P. B., J. R. Millwe, J. Rearce, R. Kothary, R. D. Buton, R. Paro, T. C. James, and S. J. Gaunt. 1991. A sequence motif found in a Drosophila heterochromatin protein is conserved in animals and plants. Nucleic Acids Res. 19:789-794.
51. Smothers, J. F., M. T. Madireddi, F. D. Warner, and C. D. Allis. 1997. Programmed DNA degradation and nucleolar biogenesis occur in distinct organelles during macronuclear development in Tetrahymena. J. Eukaryot. Microbiol. 44:79-88.
52. Stargell, L. A., K. M. Karrer, and M. A. Gorovsky. 1990. Transcriptional regulation of gene expression in Tetrahymena thermophila. Nucleic Acids Res. 18:6637-6639.
53. Stone, E. M., and L. Pillus. 1996. Activation of an MAP kinase cascade leads to Sir3p hyperphosphorylation and strengthens transcriptional silencing. J. Cell Biol. 135:571-583.
54. Sweet, M. T., K. Jones, and C. D. Allis. 1996. Phosphorylation of linker histone is associated with transcriptional activation in a normally silent nucleus. J. Cell Biol. 135:1219-1228.
55. Wakimoto, B. T. 1998. Beyond the nucleosome: epigenetic aspects of position-effect variegation in Drosophila. Cell 93:321-324.
56. Wakimoto, B. T., and M. G. Hearn. 1990. The effects of chromosome rearrangements on the expression of heterochromatic genes in chromosome 2L of Drosophila melanogaster. Genetics 125:141-154.
57. Wallrath, L. L. 1998. Unfolding the mysteries of heterochromatin. Curr. Opin. Genet. Dev. 8:147-153.
58. Weiler, K. S., and B. T. Wakimoto. 1995. Heterochromatin and gene expression in Drosophila. Annu. Rev. Genet. 29:577-605.
59. Ye, Q., and H. J. Worman. 1996. Interaction between an integral protein of the nuclear envelope inner membrane and human chromodomain proteins homologous to Drosophila HP1. J. Biol. Chem. 271:14653-14656.
60. Yu, L., and M. A. Gorovsky. 1997. Constitutive expression, not a particular primary sequence, is the important feature of the H3 replacement variant hv2 in Tetrahymena thermophila. Mol. Cell. Biol. 17:6303-6310.