Excision of micronuclear-specific DNA requires parental expression of Pdd2p and occurs independently from DNA replication in Tetrahymena thermophila

Genes and Development

Volumn 13, Issue 21, 1999, Pages 2852-2862

  Nikiforov, Mikhail A ^a   Smothers, James F ^a,b   Gorovsky, Martin A ^a   Allis, C David ^a,c  

^a UNIVERSITY OF ROCHESTER   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Chromosome breakage; DNA replication; Pdd2p; Programmed DNA elimination; Tetrahymena macronuclear development

Indexed keywords

DNA;

ARTICLE; CHROMOSOME BREAKAGE; DNA REPLICATION; GERM LINE; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROGENY; PROTEIN SYNTHESIS; REGULATORY MECHANISM; TETRAHYMENA THERMOPHILA;

ANIMALS; CHROMOSOME BREAKAGE; DNA DAMAGE; DNA REPLICATION; DNA, PROTOZOAN; GENE DELETION; GENES, PROTOZOAN; NUCLEAR PROTEINS; PHOSPHOPROTEINS; PROTOZOAN PROTEINS; TELOMERE; TETRAHYMENA THERMOPHILA;

CILIOPHORA; PROTOZOA; TETRAHYMENA; TETRAHYMENA THERMOPHILA;

EID: 0032750281     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.13.21.2852     Document Type: Article

References (44)

1. Abraham, J., K.A. Nasmyth, J.N. Strathern, A.J.S. Klar, and J.B. Hicks. 1984. Regulation of mating type information in yeasts. Negative control requiring sequences both 5′ and 3′ to the regulated regions. J. Mol. Biol. 176: 307-311.
2. Allis, C.D. and D.K. Dennison. 1982. Identification and purification of young macronuclear anlagen from conjugating cells of Tetrahymena thermophila. Devel. Biol. 93: 519-533.
3. Austerberry, C.F., C.D. Allis, and M.C. Yao. 1984. Specific DNA rearrangements in synchronously developing nuclei of Tetrahymena. Proc. Natl. Acad. Sci. 81: 7383-7387.
4. Bassnett, S. and D. Mataic. 1997. Chromatin degradation in differentiating fiber cells of the eye lens. J. Cell Biol. 137: 37-49.
5. Cassidy-Hanley, D., J. Bowen, J. Lee, E.S. Cole, L.A. 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.
6. Chalker, D.L. and M.C. Yao. 1996. Non-Mendelian, heritable blocks to DNA rearrangement are induced by loading the somatic nucleus of Tetrahymena thermophila with germ line-limited DNA. Mol. Cell. Biol. 16: 3658-3667.
7. Chicoine, L.G., D. Wenkert, R. Richman, J.C. Wiggins, and C.D. Allis. 1985. Modulation of linker histones during development in Tetrahymena: Selective elimination of linker histone during the differentiation of new macronuclei. Devel. Biol. 109: 1-8.
8. Coyne, R.S., D.L. Chalker, and M.C. Yao. 1996. Genome downsizing during ciliate development: Nuclear division of labor through chromosome restructuring. Annu. Rev. Genet. 30: 557-578.
9. Coyne, R.S., M.A. Nikiforov, J.F. Smothers, C.D. Allis, and M-C. Yao. 1999. Parental expression of the chromodomain protein Pdd1p is required for completion of programmed DNA elimination and nuclear differentiation. Mol. Cell (in press).
10. Duharcourt, S., A. Butler, and E. Meyer. 1995. Epigenetic self-regulation of developmental excision of an internal eliminated sequence on Paramecium tetraurelia. Genes & Dev. 9: 2065-2077
11. Duharcourt, S., A.M. Keller, and E. Meyer. 1998. Homology-dependent maternal inhibition of developmental excision of internal eliminated sequences in Paramecium tetraurelia. Mol. Cell. Biol. 18: 7075-7085
12. Engberg, J. and H. Nielsen. 1990. Complete sequence of the extrachromosomal rDNA molecule from the ciliate Tetrahymena thermophila strain B1868VII. Nucleic Acids Res. 18: 6915-6919.
13. Fuge, H. 1997. Nonrandom chromosome segregation in male meiosis of a sciarid fly: Elimination of paternal chromosomes in first division is mediated by non-kinetochore microtubules. Cell Motil. Cytoskeleton 36: 84-94.
14. 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.
15. Gellert, M. 1992. V(D)J recombination gets a break. Trends Genet. 8: 408-412.
16. Glaser, R.L. and A.C. Spradling. 1994. Unusual properties of genomic DNA molecules spanning the euchromatic-heterochromatic junction of a Drosophila minichromosome. Nucleic Acids Res. 22: 5068-5075.
17. Glaser, R.L., T.J. Leach, and S.E. Ostrowski. 1997. The structure of heterochromatic DNA is altered in polyploid cells of Drosophila melanogaster. Mol. Cell Biol. 17: 1254-1263.
18. Godiska, R. and M.C. Yao. 1990. A programmed site-specific DNA rearrangement in Tetrahymena thermophila requires flanking polypurine tracts. Cell 61: 1237-1246.
19. Gorovsky M.A. 1980. Genome organization and reorganization in Tetrahymena. Annu. Rev. Genet. 14: 203-239.
20. 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.
21. Guttman, S.D., C.V.Glover, C.D. Allis, and M.A. Gorovsky. 1980. Heat shock, deciliation and release from anoxia induce the synthesis of the same set of polypeptides in starved T. pyriformis. Cell 22: 299-307.
22. Hai, B. and M.A. Gorovsky. 1997. Germ-line knockout heterokaryons of an essential alpha-tubulin gene enable high-frequency gene replacement and a test of gene transfer from somatic to germ-line nuclei in Tetrahymena thermophila. Proc. Natl. Acad. Sci. 94: 1310-1315.
23. Ikegami, S., T. Taguchi, M. Ohashi, M. Oguro, H. Nagano, and Y. Mano. 1978. Aphidicolin prevents mitotic cell division by interfering with the activity of DNA polymerase-alpha. Nature 275: 458-460.
24. Kapler, G.M. and E.H. Blackburn. 1994. A weak germ-line excision mutation blocks developmentally controlled amplification of the rDNA minichromosome of Tetrahymena thermophila. Genes & Dev. 8: 84-95.
25. King, B.O. and M.C. Yao. 1982. Tandemly repeated hexanucleotide at Tetrahymena rDNA free end is generated from a single copy during development. Cell 31: 177-182.
26. 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.
27. Madireddi, M.T., M.C. Davis, and C.D. Allis. 1994. Identification of a novel polypeptide involved in the formation of DNA-containing vesicles during macronuclear development in Tetrahymena. Dev. Biol. 165: 418-431.
28. Madireddi, M.T., R.S. Coyne, J.F. Smothers, K.M. Mickey, M.C. Yao, and C.D. Allis. 1996. Pdd1p, a novel chromodomain-containing protein, links heterochromatin assembly and DNA elimination in Tetrahymena. Cell 87: 75-84.
29. Meyer, E. and S. Duharcourt. 1996. Epigenetic programming of developmental genome rearrangements in ciliates. Cell 87: 9-12.
30. Muller, F., V. Bernard, and H. Tobler. 1996. Chromatin diminution in nematodes. BioEssays 18: 133-138.
31. Nanney, D.L. 1986. Introduction. In Molecular biology of ciliated protozoa (ed. J.G. Gall), pp 1-21. Academic Press, Orlando, FL.
32. Orias, E. 1986. Ciliate conjunction. In Molecular biology of ciliated protozoa (ed. J.G. Gall), pp. 45-84. Academic Press, Orlando, FL.
33. Prescott, D.M. 1994. The DNA of ciliated protozoa. Microbiol. Rev. 58: 233-267.
34. Richards, E.J. 1988. Preparation and analysis of DNA. In Current Protocols in Molecular Biology (eds. Ausubel, F.M., R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, and K. Struhl), pp. 2.0.1-2.12.5. Wiley Interscience, New York, NY.
35. Robertson, B.D. and T.F. Meyer. 1992. Genetic variation in pathogenic bacteria. Trends Genet. 8: 422-427.
36. Smothers, J.F., M.T. Madireddi, F.D. Warner, and C.D. Allis. 1997a. Programmed DNA degradation and nucleolar biogenesis occur in distinct organelles during macronuclear development in Tetrahymena. J. Eukaryot. Microbiol. 44: 79-88.
37. Smothers, J.F., C.A. Mizzen, M.M. Tubbert, R.G. Cook, and C.D. Allis. 1997b. Pdd1p associates with germline-restricted chromatin and a second novel anlagen-enriched protein in developmentally programmed DNA elimination structures. Development 124: 4537-4545.
38. Van De Water, L., S.D. Guttman, M.A. Gorovsky, and J.B. Olmsted. 1982. Production of antisera and radioimmunoassays for tubulin. Methods Cell Biol. 24: 79-96.
39. Ward, J.G., P. Blomberg, N. Hoffman, and M.C. Yao. 1997. The intranuclear organization of normal, hemizygous and excision-deficient tRNA genes during developmental amplification in Tetrahymena thermophila. Chromosoma 106: 233-242.
40. Yao, M.C. 1982. Elimination of specific DNA sequences from the somatic nucleus of the ciliate Tetrahymena. J. Cell Biol. 92: 783-789.
41. Yao, M.C. and M.A. Gorovsky. 1974. Comparison of the sequences of macro- and micronuclear DNA of Tetrahymena pyriformis. Chromosoma 48: 1-18.
42. Yao, M.C., K. Zheng, and C.H. Yao. 1987. A conserved nucleotide sequence at the sites of developmentally regulated chromosomal breakage in Tetrahymena. Cell 48: 779-788.
43. Yao, M.C., C.H. Yao, and B. Monks. 1990. The controlling sequence for site-specific chromosome breakage in Tetrahymena. Cell 63: 763-772.
44. Yu, G.L. and E.H. Blackburn. 1991. Developmentally programmed healing of chromosomes by telomerase in Tetrahymena. Cell 67: 823-832.