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. 1990 Feb;87(4):1481–1485. doi: 10.1073/pnas.87.4.1481

Two versions of the gene encoding the 41-kilodalton subunit of the telomere binding protein of Oxytricha nova.

B J Hicke 1, D W Celander 1, G H MacDonald 1, C M Price 1, T R Cech 1
PMCID: PMC53499  PMID: 1689486

Abstract

Macronuclear chromosomes of the ciliated protozoan Oxytricha nova terminate with a single-stranded (T4G4)2 overhang. The (T4G4)2 telomeric overhang is tenaciously bound by a protein heterodimer. We have cloned and sequenced the gene encoding the 41-kDa subunit of this telomere binding protein. The predicted amino acid sequence comprises two distinct regions, a carboxyl-terminal two-thirds that is 23% lysine and bears similarity to histone H1 and an amino-terminal one-third containing a hydrophobic stretch of about 15 amino acids. Two macronuclear versions of the gene differ in nucleotide sequence at several positions, but the derived polypeptides differ only at a single position, Ser-110 or Ala-110. Both versions harbor a small intron. The existence of this intron demonstrates that, despite the elimination of 95% of the micronuclear genome from the developing macronucleus, at least some noncoding DNA is retained during macronuclear development of hypotrichous ciliates.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Agard D. A., Sedat J. W. Three-dimensional architecture of a polytene nucleus. Nature. 1983 Apr 21;302(5910):676–681. doi: 10.1038/302676a0. [DOI] [PubMed] [Google Scholar]
  2. Allan J., Hartman P. G., Crane-Robinson C., Aviles F. X. The structure of histone H1 and its location in chromatin. Nature. 1980 Dec 25;288(5792):675–679. doi: 10.1038/288675a0. [DOI] [PubMed] [Google Scholar]
  3. Allan J., Mitchell T., Harborne N., Bohm L., Crane-Robinson C. Roles of H1 domains in determining higher order chromatin structure and H1 location. J Mol Biol. 1986 Feb 20;187(4):591–601. doi: 10.1016/0022-2836(86)90337-2. [DOI] [PubMed] [Google Scholar]
  4. Altschul S. F., Erickson B. W. Optimal sequence alignment using affine gap costs. Bull Math Biol. 1986;48(5-6):603–616. doi: 10.1007/BF02462326. [DOI] [PubMed] [Google Scholar]
  5. Berman J., Tachibana C. Y., Tye B. K. Identification of a telomere-binding activity from yeast. Proc Natl Acad Sci U S A. 1986 Jun;83(11):3713–3717. doi: 10.1073/pnas.83.11.3713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Blackburn E. H., Chiou S. S. Non-nucleosomal packaging of a tandemly repeated DNA sequence at termini of extrachromosomal DNA coding for rRNA in Tetrahymena. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2263–2267. doi: 10.1073/pnas.78.4.2263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Blackburn E. H. The molecular structure of centromeres and telomeres. Annu Rev Biochem. 1984;53:163–194. doi: 10.1146/annurev.bi.53.070184.001115. [DOI] [PubMed] [Google Scholar]
  8. Dancis B. M., Holmquist G. P. Telomere replication and fusion in eukaryotes. J Theor Biol. 1979 May 21;78(2):211–224. doi: 10.1016/0022-5193(79)90265-0. [DOI] [PubMed] [Google Scholar]
  9. Dibb N. J., Newman A. J. Evidence that introns arose at proto-splice sites. EMBO J. 1989 Jul;8(7):2015–2021. doi: 10.1002/j.1460-2075.1989.tb03609.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gilbert W. Why genes in pieces? Nature. 1978 Feb 9;271(5645):501–501. doi: 10.1038/271501a0. [DOI] [PubMed] [Google Scholar]
  11. Gottschling D. E., Cech T. R. Chromatin structure of the molecular ends of Oxytricha macronuclear DNA: phased nucleosomes and a telomeric complex. Cell. 1984 Sep;38(2):501–510. doi: 10.1016/0092-8674(84)90505-1. [DOI] [PubMed] [Google Scholar]
  12. Gottschling D. E., Zakian V. A. Telomere proteins: specific recognition and protection of the natural termini of Oxytricha macronuclear DNA. Cell. 1986 Oct 24;47(2):195–205. doi: 10.1016/0092-8674(86)90442-3. [DOI] [PubMed] [Google Scholar]
  13. Greslin A. F., Loukin S. H., Oka Y., Prescott D. M. An analysis of the macronuclear actin genes of Oxytricha. DNA. 1988 Oct;7(8):529–536. doi: 10.1089/dna.1.1988.7.529. [DOI] [PubMed] [Google Scholar]
  14. Hartman P. G., Chapman G. E., Moss T., Bradbury E. M. Studies on the role and mode of operation of the very-lysine-rich histone H1 in eukaryote chromatin. The three structural regions of the histone H1 molecule. Eur J Biochem. 1977 Jul 1;77(1):45–51. doi: 10.1111/j.1432-1033.1977.tb11639.x. [DOI] [PubMed] [Google Scholar]
  15. Herrick G., Hunter D., Williams K., Kotter K. Alternative processing during development of a macronuclear chromosome family in Oxytricha fallax. Genes Dev. 1987 Dec;1(10):1047–1058. doi: 10.1101/gad.1.10.1047. [DOI] [PubMed] [Google Scholar]
  16. Hopp T. P., Woods K. R. A computer program for predicting protein antigenic determinants. Mol Immunol. 1983 Apr;20(4):483–489. doi: 10.1016/0161-5890(83)90029-9. [DOI] [PubMed] [Google Scholar]
  17. Hunter D. J., Williams K., Cartinhour S., Herrick G. Precise excision of telomere-bearing transposons during Oxytricha fallax macronuclear development. Genes Dev. 1989 Dec;3(12B):2101–2112. doi: 10.1101/gad.3.12b.2101. [DOI] [PubMed] [Google Scholar]
  18. Keller E. B., Noon W. A. Intron splicing: a conserved internal signal in introns of animal pre-mRNAs. Proc Natl Acad Sci U S A. 1984 Dec;81(23):7417–7420. doi: 10.1073/pnas.81.23.7417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Knowles J. A., Childs G. J. Comparison of the late H1 histone genes of the sea urchins Lytechinus pictus and Strongelocentrotus purpuratus. Nucleic Acids Res. 1986 Oct 24;14(20):8121–8133. doi: 10.1093/nar/14.20.8121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lipman D. J., Pearson W. R. Rapid and sensitive protein similarity searches. Science. 1985 Mar 22;227(4693):1435–1441. doi: 10.1126/science.2983426. [DOI] [PubMed] [Google Scholar]
  21. Lipps H. J., Gruissem W., Prescott D. M. Higher order DNA structure in macronuclear chromatin of the hypotrichous ciliate Oxytricha nova. Proc Natl Acad Sci U S A. 1982 Apr;79(8):2495–2499. doi: 10.1073/pnas.79.8.2495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Martindale D. W. Codon usage in Tetrahymena and other ciliates. J Protozool. 1989 Jan-Feb;36(1):29–34. doi: 10.1111/j.1550-7408.1989.tb02679.x. [DOI] [PubMed] [Google Scholar]
  23. McClintock B. The Fusion of Broken Ends of Chromosomes Following Nuclear Fusion. Proc Natl Acad Sci U S A. 1942 Nov;28(11):458–463. doi: 10.1073/pnas.28.11.458. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mount S. M. A catalogue of splice junction sequences. Nucleic Acids Res. 1982 Jan 22;10(2):459–472. doi: 10.1093/nar/10.2.459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nielsen H., Andreasen P. H., Dreisig H., Kristiansen K., Engberg J. An intron in a ribosomal protein gene from Tetrahymena. EMBO J. 1986 Oct;5(10):2711–2717. doi: 10.1002/j.1460-2075.1986.tb04555.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Price C. M., Cech T. R. Properties of the telomeric DNA-binding protein from Oxytricha nova. Biochemistry. 1989 Jan 24;28(2):769–774. doi: 10.1021/bi00428a053. [DOI] [PubMed] [Google Scholar]
  27. Price C. M., Cech T. R. Telomeric DNA-protein interactions of Oxytricha macronuclear DNA. Genes Dev. 1987 Oct;1(8):783–793. doi: 10.1101/gad.1.8.783. [DOI] [PubMed] [Google Scholar]
  28. Raghuraman M. K., Cech T. R. Assembly and self-association of oxytricha telomeric nucleoprotein complexes. Cell. 1989 Nov 17;59(4):719–728. doi: 10.1016/0092-8674(89)90018-4. [DOI] [PubMed] [Google Scholar]
  29. Raghuraman M. K., Dunn C. J., Hicke B. J., Cech T. R. Oxytricha telomeric nucleoprotein complexes reconstituted with synthetic DNA. Nucleic Acids Res. 1989 Jun 12;17(11):4235–4253. doi: 10.1093/nar/17.11.4235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Ruskin B., Krainer A. R., Maniatis T., Green M. R. Excision of an intact intron as a novel lariat structure during pre-mRNA splicing in vitro. Cell. 1984 Aug;38(1):317–331. doi: 10.1016/0092-8674(84)90553-1. [DOI] [PubMed] [Google Scholar]
  31. Sarkar G., Sommer S. S. Access to a messenger RNA sequence or its protein product is not limited by tissue or species specificity. Science. 1989 Apr 21;244(4902):331–334. doi: 10.1126/science.2565599. [DOI] [PubMed] [Google Scholar]
  32. Swanton M. T., Greslin A. F., Prescott D. M. Arrangement of coding and non-coding sequences in the DNA molecules coding for rRNAs in Oxytricha sp. DNA of ciliated protozoa. VII. Chromosoma. 1980;77(2):203–215. doi: 10.1007/BF00329545. [DOI] [PubMed] [Google Scholar]
  33. Weintraub H., Groudine M. Chromosomal subunits in active genes have an altered conformation. Science. 1976 Sep 3;193(4256):848–856. doi: 10.1126/science.948749. [DOI] [PubMed] [Google Scholar]
  34. Wu M., Allis C. D., Richman R., Cook R. G., Gorovsky M. A. An intervening sequence in an unusual histone H1 gene of Tetrahymena thermophila. Proc Natl Acad Sci U S A. 1986 Nov;83(22):8674–8678. doi: 10.1073/pnas.83.22.8674. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Yudkin J. Sugar and disease. Nature. 1972 Sep 22;239(5369):197–199. doi: 10.1038/239197a0. [DOI] [PubMed] [Google Scholar]

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