Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-06T00:21:14.140Z Has data issue: false hasContentIssue false
  • English
  • Français

Sequence differences between histones of procyclic Trypanosoma brucei brucei and higher eukaryotes

Published online by Cambridge University Press:  06 April 2009

K. Bender ,
B. Betschart ,
J. Schaller ,
U. Kämpfer  and
H. Hecker
K. Bender
Affiliation:
Swiss Tropical Institute, Basel, Switzerland
B. Betschart
Affiliation:
Swiss Tropical Institute, Basel, Switzerland
J. Schaller
Affiliation:
Institute of Biochemistry, Bern, Switzerland
U. Kämpfer
Affiliation:
Institute of Biochemistry, Bern, Switzerland
H. Hecker
Affiliation:
Swiss Tropical Institute, Basel, Switzerland
Get access Rights & Permissions [Opens in a new window]

Extract

Four histones, a, b, c, d from procyclic Trypanosoma brucei brucei, which show similarities with the amino acid composition of the core histones H3, H2A, H2B and H4, were isolated and cleaved with Endoproteinase Glu-C. The fragments were separated by FPLC reversed phase chromatography and a subset of the fragments (a5, a9, b6, c8, d3, d9, d11) was subjected to sequence analysis. A 54–71% identity was found in the sequences of the fragment c8 and the C-terminal half of H2B and of three fragments of protein d covering the N-terminal half as well as the C-terminal region of H4. The amino acid sequence of the fragment a9 showed a 57 and 54% identity with H3 sequences of Saccharomyces cerevisiae and Xenopus laevis. Neither the a5 nor the b6 sequence could be aligned with histone sequences of other eukaryotes. The significant differences of 21–48% between the T. b. brucei, histone sequences and those of calf thymus histones, which are more pronounced than the differences of Tetrahymena pyriformis and the higher eukaryote, resulted partially from replacements of amino acids with different properties and indicate specific patterns of histone–histone and/or histone–DNA contact sites in the nucleosome of T. b. brucei. These differences, together with the lack of a functional histone H1, may be sufficient to explain the lack of a salt-dependent formation of the nucleosome filament into the 30 nm fibre, which reflects alternative methods of organizing and processing the genetic information in the nucleus of the protozoan parasite and which may be of chemotherapeutic significance.

Keywords

Trypanosoma brucei bruceihistoneamino acid sequencehistone variationhistone phylogeny.
Type
Research Article
Information
Parasitology , Volume 105 , Issue 1 , August 1992 , pp. 97 - 104
Copyright
Copyright © Cambridge University Press 1992

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Ajiro, K. & Nishimoto, T. (1985). Specific site of histone H3 phosphorylation related to the maintenance of premature chromosome condensation. Journal of Biological Chemistry 260, 15379–81.CrossRefGoogle Scholar
Allan, J., Harborne, N., Rau, D. C. & Gould, H. (1982). Participation of core histone tails in the stabilization of the chromatin solenoid. Journal of Cell Biology 93, 285–97.CrossRefGoogle ScholarPubMed
Bender, K., Betschart, B., Schaller, J., Kämpfer, U. & Hecker, H. (1991). Biochemical properties of histone-like proteins of procyclic Trypanosoma brucei brucei. Acta Tropica 50, 169–84.CrossRefGoogle ScholarPubMed
Böm, L., Hayashi, H., Cary, P. D., Moss, T., Cranerobinson, C. & Bradbury, F. M. (1977). Sites of histone/histone interaction in the H3-H4 complex. European Journal of Biochemistry 77, 487–93.CrossRefGoogle Scholar
Brandt, W. F. & Von Holt, C. (1982). The primary structure of yeast histone H3. European Journal of Biochemistry 121, 501–10.CrossRefGoogle ScholarPubMed
Brun, R. & Schoenenberger, M. (1979). Cultivation and in vitro cloning of procyclic forms of Trypanosoma brucei in semi-defined medium. Acta Tropica 36, 289–92.Google ScholarPubMed
Burton, D. R., Butler, M. J., Hyde, J. E., Phillips, D., Skidmore, C. J. & Walker, J. O. (1978). The interaction of core histones with DNA: equilibrium binding studies. Nucleic Acids Research 5, 3643–63.CrossRefGoogle ScholarPubMed
Clement, B. (1989). Verbindungen zur Behandlung von Trypanosomeninfektionen. Pharmazie in unserer Zeit 4, 97–111.CrossRefGoogle Scholar
Dayhoff, M. O. (1972). Atlas of Protein Sequence and Structure. National Biomedical Research Foundation, Washington D.C.Google Scholar
Delange, R. J., Fambrough, D. M., Smith, E. L. & Bonner, J. (1969 a). Calf and pea histone IV. Journal of Biological Chemistry 244, 5669–79.CrossRefGoogle ScholarPubMed
Delange, R. J., Fambrough, D. M., Smith, E. L. & Bonner, J. (1969 b). Calf and pea histone IV. Journal of Biological Chemistry 244, 319–34.CrossRefGoogle ScholarPubMed
Delange, R. J. & Smith, E. L. (1971). Histones: structure and function. Annual Review of Biochemistry 40, 279–314.CrossRefGoogle ScholarPubMed
Delange, R. J., Hooper, J. A. & Smith, E. (1973). Histone III. Journal of Biological Chemistry 248, 3261–74.CrossRefGoogle Scholar
Doenecke, D. & Gallwitz, D. (1982). Acetylation of histones in nucleosomes. Molecular and Cellular Biochemistry 44, 113–28.CrossRefGoogle ScholarPubMed
Doenecke, D., Tonjes, R. (1986). Differential distribution of lysine and arginine residues in the closely related histones H1 and H5. Journal of Molecular Biology 187, 461–4.CrossRefGoogle ScholarPubMed
Doyle, J. J., Moloo, S. K. & Borowy, N. K. (1984). Development of improved control methods of animal trypanosomiasis: a review. Preventive Veterinary Medicine 2, 43.CrossRefGoogle Scholar
Drapeau, G. R. (1977). Cleavage at glutamic acid with staphylococcal protease. Methods in Enzymology 47, 189–91.CrossRefGoogle ScholarPubMed
Fusauchi, Y. & Iwai, K. (1983). Tetrahymena histone H2A. Isolation and two variant sequences. Journal of Biochemistry 93, 1487–97.CrossRefGoogle ScholarPubMed
Fusauchi, Y. & Iwai, K. (1984). Tetrahymena histone H2A. Acetylation in the N-terminal sequence and phosphorylation in the C-terminal sequence. Journal of Biochemistry 95, 147–54.CrossRefGoogle ScholarPubMed
Hayashi, O. & Ueda, K. (1977). Poly (ADP-Ribose) and ADP-ribosylation of proteins. Annual Review of Biochemistry 46, 95–116.CrossRefGoogle Scholar
Hayashi, T., Hayashi, H., Fusauchi, Y. & Iwai, K. (1984 a). Tetrahymena histone H3. Purification and two variant sequences. Journal of Biochemistry 95, 1741–9.CrossRefGoogle ScholarPubMed
Hayashi, H., Nomoto, M. & Iwai, K. (1984 b). Tetrahymena histone H4. Complete amino acid sequences of two variants. Journal of Biochemistry 96, 1449–56.Google ScholarPubMed
Hecker, H. & Gander, E. S. (1985). The compaction pattern of the chromatin of trypanosomes. Biology of the Cell 53, 199–208.CrossRefGoogle ScholarPubMed
Hecker, H., Bender, K., Betschart, B. & Modespatcher, U. P. (1989). Instability of the nuclear chromatin of procyclic Trypanosoma brucei brucei. Molecular and Biochemical Parasitology 37, 225–34.CrossRefGoogle ScholarPubMed
Isenberg, J. (1979). Histones. Annual Review of Biochemistry 48, 159–91.CrossRefGoogle ScholarPubMed
Iwai, K., Hayashi, H. & Ishikawa, K. (1972). Calf thymus lysine-and serine-rich histone. Journal of Biochemistry 72, 357–67.CrossRefGoogle ScholarPubMed
Jackson, V., Shires, A., Tanphaichitr, N. & Chalkley, R. (1976). Modifications to histones immediately after synthesis. Journal of Molecular Biology 104, 471–83.CrossRefGoogle ScholarPubMed
Kasai, K., Hayashi, H. & Iwai, K. (1986). Nucleosome core particles of calf thymus, Tetrahymena, and the reconstituted hybrid. Their structure reflects the nature of the histone octamer. Journal of Biochemistry 99, 91–8.CrossRefGoogle ScholarPubMed
Krieg, P. A., Robins, A. J., D'andrea, R. & Wells, J. R. E. (1983). The chicken H5 gene is unlinked to core and H1 histone gens. Nucleic Acids Research 11, 619–27.CrossRefGoogle Scholar
Kurochkina, L. P. & Kolomijtseva, G. YA. (1989). Isolation of modified histone H3 from ultraviolet-irradiated deoxyribonucleoprotein by reversed-phase high-performance liquid chromatography. Analytical Biochemistry 178, 88–92.CrossRefGoogle ScholarPubMed
Lipman, D. J. & Pearson, D. R. (1985). Rapid and sensitive protein similarity searches. Science 227, 1435–41.CrossRefGoogle ScholarPubMed
Macleod, A. R., Wong, N. C. W. & Dixon, G. H. (1977). The amino-acid sequence of trout-testis histone H1. Journal of Biochemistry 78, 281–91.Google ScholarPubMed
Martinson, H. G. & True, R. J. (1979). Amino acid contacts between histones are the same for plants and mammals. Binding-site studies using ultraviolet light and tetranitromethane. Biochemistry 18, 1947–51.CrossRefGoogle ScholarPubMed
Martinson, H. G., True, R., Lau, C. K. & Mehrabian, M. (1979). Histone-histone interactions within chromatin. Preliminary location of multiple contact sites between histones 2A, 2B and 4. Biochemistry 18, 1075–82.CrossRefGoogle ScholarPubMed
McGhee, J. D. & Felsenfeld, C. (1980). Nucleosome structure. Annual Review of Biochemistry 49, 1115–56.CrossRefGoogle ScholarPubMed
Mehlhorn, H. (1988). Parasitology in Focus. New York: Springer Verlag.CrossRefGoogle Scholar
Mezquita, J., Connor, W., Winkfein, R. J. & Dixon, G. H. (1985). An H1 histone gene from rainbow trout (Salmo gairdnerii). Journal of Molecular Evolution 21, 209–19.CrossRefGoogle Scholar
Moorman, A. F. M., De Boer, P. A. J., De Laaf, R. T. M., Van Dongen, W. M. A. M. & Destree, O. H. J. (1981). Primary Structure of the histone H3 and H4 genes and their flanking sequences in a minor histone gene cluster of Xenopus laevis. FEBS Letters 136, 45–52.CrossRefGoogle Scholar
Moss, T., Cary, P. D., Abercrombie, B. D., Crane-Robinson, C. & Bradbury, E. M. (1976). A pH-dependent interaction between histones H2A and H2B involving secondary and tertiary folding. European Journal of Biochemistry 71, 337–50.CrossRefGoogle ScholarPubMed
Nomoto, M., Hayashi, H. & Iwai, K. (1982). Tetrahymena histone H2B. Complete amino acid sequence. Journal of Biochemistry 91, 897–904.CrossRefGoogle ScholarPubMed
Ohe, Y., Hayashi, H. & Iwai, K. (1989). Human spleen histone H1. Isolation and amino acid sequences of three minor variants, H1a, H1c, and H1d. Journal of Biochemistry 106, 844–57.CrossRefGoogle ScholarPubMed
Sanicola, M., Ward, S., Childs, C. & Emmons, S. W. (1990). Identification of a Caenorhabditis elegans histone H1 gene family. Journal of Molecular Biology 212, 259–68.CrossRefGoogle ScholarPubMed
Schaller, J., Akiyama, K., Kimura, H., Hess, D., Affolter, M. & Rickli, E. E. (1991). Primary structure of a new actin-binding protein from human seminal plasma. European Journal of Biochemistry 196, 743–50.CrossRefGoogle ScholarPubMed
Schulz, G. E. & Schirmer, R. H. (1984). Principles of protein structure. In Springer Advanced Texts in Chemistry (ed. Cantor, C. R.) pp. 1–16. New York: Springer-Verlag.Google Scholar
Shapiro, S. Z. & Doxsey, S. J. (1982). Purification of nuclei from a flagellate protozoan, Trypanosoma brucei. Analytical Biochemistry 127, 112–15.CrossRefGoogle ScholarPubMed
Thoma, F., Koller, T. & Klug, A. (1979). Involvement of histone H1 in the organization of the nucleosome and the salt dependent superstructures of chromatin. Journal of Cell Biology 83, 403–27.CrossRefGoogle ScholarPubMed
Vanfleteren, J. R., Van Bun, S. M. & Van Beeumen, J. J. (1988). The primary structure of the major isoform (H1.1) of histone H1 from the nematode Caenorhabditis elegans. The Biochemical Journal 255, 647–52.Google ScholarPubMed
Van Holde, K. E., Shaw, B. R., Lohr, D., Herman, T. M. & Kovacic, R. T. (1975). Subunit structure of chromatins. In Proceedings of the Tenth FEBS Meeting (ed. Bernadi, G. & Gros, F.) vol. 38, pp. 57–72. Amsterdam: North Holland/American Elsevier.Google Scholar
Van Holde, K. E. (1989). Chromatin. In Springer Series in Molecular Biology (ed. Rich, A.), New York: Springer Verlag.Google Scholar
Yaguchi, M., Roy, C. & Seligy, V. L. (1979). Complete amino acid sequence of goose erythrocyte H5 histone and the homology between H1 and H5 histones. Biochemical and Biophysical Research Communications 90, 1400–6.CrossRefGoogle ScholarPubMed