Skip to main content
Biochemical Journal logoLink to Biochemical Journal
. 1996 Sep 15;318(Pt 3):813–819. doi: 10.1042/bj3180813

Organization, transcription and regulation of the Leishmania infantum histone H3 genes.

M Soto 1, J M Requena 1, L Quijada 1, C Alonso 1
PMCID: PMC1217691  PMID: 8836124

Abstract

The genomic organization and transcription of the genes encoding the histone H3 of the protozoan parasite Leishmania infantum have been studied. It was found that there are multiple copies of the histone H3 genes distributed in chromosomal bands XIX and XIV. The nucleotide sequence of two of the L. infantum H3 genes, each one located in a different chromosome, is reported. Although the nucleotide sequence of the coding region of both genes is identical, the sequence of the 3' untranslated region is highly divergent. It was found also that there exist two different size classes of histone H3 transcripts, each one derived from a different gene, and that they are polyadenylated. The steady-state level of the transcripts dramatically decreases when the parasites enter the stationary phase of growth, suggesting a mode of regulation which is linked to the proliferation status of the cell. Unlike the replication-dependent histones, the L. infantum H3 mRNA levels do not decrease after treatment with DNA synthesis inhibitors. A comparative analysis of the sensitivity of the histone mRNA levels to DNA inhibition in the parasites L. infantum and Trypanosoma cruzi revealed the existence of different control mechanisms in histone expression in these two phylogenetically related protozoan parasites.

Full Text

The Full Text of this article is available as a PDF (563.8 KB).

Selected References

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

  1. Agabian N. Trans splicing of nuclear pre-mRNAs. Cell. 1990 Jun 29;61(7):1157–1160. doi: 10.1016/0092-8674(90)90674-4. [DOI] [PubMed] [Google Scholar]
  2. Aslund L., Carlsson L., Henriksson J., Rydåker M., Toro G. C., Galanti N., Pettersson U. A gene family encoding heterogeneous histone H1 proteins in Trypanosoma cruzi. Mol Biochem Parasitol. 1994 Jun;65(2):317–330. doi: 10.1016/0166-6851(94)90082-5. [DOI] [PubMed] [Google Scholar]
  3. Bender K., Betschart B., Hecker H. Histone-DNA interactions in the chromatin of procyclic Trypanosoma brucei brucei. Parasitol Res. 1992;78(6):495–500. doi: 10.1007/BF00931570. [DOI] [PubMed] [Google Scholar]
  4. Bender K., Betschart B., Schaller J., Kämpfer U., Hecker H. Biochemical properties of histone-like proteins of procyclic Trypanosoma brucei brucei. Acta Trop. 1991 Dec;50(2):169–183. doi: 10.1016/0001-706x(91)90010-h. [DOI] [PubMed] [Google Scholar]
  5. Bontempi E. J., Porcel B. M., Henriksson J., Carlsson L., Rydåker M., Segura E. L., Ruiz A. M., Pettersson U. Genes for histone H3 in Trypanosoma cruzi. Mol Biochem Parasitol. 1994 Jul;66(1):147–151. doi: 10.1016/0166-6851(94)90046-9. [DOI] [PubMed] [Google Scholar]
  6. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  7. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fasel N. J., Robyr D. C., Mauel J., Glaser T. A. Identification of a histone H1-like gene expressed in Leishmania major. Mol Biochem Parasitol. 1993 Dec;62(2):321–323. doi: 10.1016/0166-6851(93)90123-f. [DOI] [PubMed] [Google Scholar]
  9. Flinn H. M., Smith D. F. Genomic organisation and expression of a differentially-regulated gene family from Leishmania major. Nucleic Acids Res. 1992 Feb 25;20(4):755–762. doi: 10.1093/nar/20.4.755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Galanti N., Dvorak J. A., Grenet J., McDaniel J. P. Hydroxyurea-induced synchrony of DNA replication in the Kinetoplastida. Exp Cell Res. 1994 Sep;214(1):225–230. doi: 10.1006/excr.1994.1252. [DOI] [PubMed] [Google Scholar]
  11. García-Salcedo J. A., Oliver J. L., Stock R. P., González A. Molecular characterization and transcription of the histone H2B gene from the protozoan parasite Trypanosoma cruzi. Mol Microbiol. 1994 Sep;13(6):1033–1043. doi: 10.1111/j.1365-2958.1994.tb00494.x. [DOI] [PubMed] [Google Scholar]
  12. Genske J. E., Cairns B. R., Stack S. P., Landfear S. M. Structure and regulation of histone H2B mRNAs from Leishmania enriettii. Mol Cell Biol. 1991 Jan;11(1):240–249. doi: 10.1128/mcb.11.1.240. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hecker H., Betschart B., Bender K., Burri M., Schlimme W. The chromatin of trypanosomes. Int J Parasitol. 1994 Sep;24(6):809–819. doi: 10.1016/0020-7519(94)90007-8. [DOI] [PubMed] [Google Scholar]
  14. Hentschel C. C., Birnstiel M. L. The organization and expression of histone gene families. Cell. 1981 Aug;25(2):301–313. doi: 10.1016/0092-8674(81)90048-9. [DOI] [PubMed] [Google Scholar]
  15. Johnson P. J., Kooter J. M., Borst P. Inactivation of transcription by UV irradiation of T. brucei provides evidence for a multicistronic transcription unit including a VSG gene. Cell. 1987 Oct 23;51(2):273–281. doi: 10.1016/0092-8674(87)90154-1. [DOI] [PubMed] [Google Scholar]
  16. Lehrach H., Diamond D., Wozney J. M., Boedtker H. RNA molecular weight determinations by gel electrophoresis under denaturing conditions, a critical reexamination. Biochemistry. 1977 Oct 18;16(21):4743–4751. doi: 10.1021/bi00640a033. [DOI] [PubMed] [Google Scholar]
  17. Lycan D. E., Osley M. A., Hereford L. M. Role of transcriptional and posttranscriptional regulation in expression of histone genes in Saccharomyces cerevisiae. Mol Cell Biol. 1987 Feb;7(2):614–621. doi: 10.1128/mcb.7.2.614. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Muhich M. L., Boothroyd J. C. Polycistronic transcripts in trypanosomes and their accumulation during heat shock: evidence for a precursor role in mRNA synthesis. Mol Cell Biol. 1988 Sep;8(9):3837–3846. doi: 10.1128/mcb.8.9.3837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Osley M. A. The regulation of histone synthesis in the cell cycle. Annu Rev Biochem. 1991;60:827–861. doi: 10.1146/annurev.bi.60.070191.004143. [DOI] [PubMed] [Google Scholar]
  20. Puerta C., Martin J., Alonso C., López M. C. Isolation and characterization of the gene encoding histone H2A from Trypanosoma cruzi. Mol Biochem Parasitol. 1994 Mar;64(1):1–10. doi: 10.1016/0166-6851(94)90129-5. [DOI] [PubMed] [Google Scholar]
  21. Requena J. M., López M. C., Jimenez-Ruiz A., de la Torre J. C., Alonso C. A head-to-tail tandem organization of hsp70 genes in Trypanosoma cruzi. Nucleic Acids Res. 1988 Feb 25;16(4):1393–1406. doi: 10.1093/nar/16.4.1393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Simpson L., Shaw J. RNA editing and the mitochondrial cryptogenes of kinetoplastid protozoa. Cell. 1989 May 5;57(3):355–366. doi: 10.1016/0092-8674(89)90911-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Sittman D. B., Graves R. A., Marzluff W. F. Histone mRNA concentrations are regulated at the level of transcription and mRNA degradation. Proc Natl Acad Sci U S A. 1983 Apr;80(7):1849–1853. doi: 10.1073/pnas.80.7.1849. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Soares C. M., de Carvalho E. F., Urményi T. P., Carvalho J. F., de Castro F. T., Rondinelli E. Alpha- and beta-tubulin mRNAs of Trypanosoma cruzi originate from a single multicistronic transcript. FEBS Lett. 1989 Jul 3;250(2):497–502. doi: 10.1016/0014-5793(89)80784-7. [DOI] [PubMed] [Google Scholar]
  26. Sogin M. L., Elwood H. J., Gunderson J. H. Evolutionary diversity of eukaryotic small-subunit rRNA genes. Proc Natl Acad Sci U S A. 1986 Mar;83(5):1383–1387. doi: 10.1073/pnas.83.5.1383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Soto M., Requena J. M., Garcia M., Gómez L. C., Navarrete I., Alonso C. Genomic organization and expression of two independent gene arrays coding for two antigenic acidic ribosomal proteins of Leishmania. J Biol Chem. 1993 Oct 15;268(29):21835–21843. [PubMed] [Google Scholar]
  28. Soto M., Requena J. M., Gomez L. C., Navarrete I., Alonso C. Molecular characterization of a Leishmania donovani infantum antigen identified as histone H2A. Eur J Biochem. 1992 Apr 1;205(1):211–216. doi: 10.1111/j.1432-1033.1992.tb16770.x. [DOI] [PubMed] [Google Scholar]
  29. Soto M., Requena J. M., Jimenez-Ruiz A., Alonso C. The mRNA coding for the nucleosomal protein H2A of Leishmania is polyadenylated and has stem-loops at the 3' end. Nucleic Acids Res. 1991 Aug 25;19(16):4554–4554. doi: 10.1093/nar/19.16.4554. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Soto M., Requena J. M., Morales G., Alonso C. The Leishmania infantum histone H3 possesses an extremely divergent N-terminal domain. Biochim Biophys Acta. 1994 Oct 18;1219(2):533–535. doi: 10.1016/0167-4781(94)90082-5. [DOI] [PubMed] [Google Scholar]
  31. Soto M., Requena J. M., Moreira D., Alonso C. Assignment of genes to Leishmania infantum chromosomes: karyotype and ploidy. FEMS Microbiol Lett. 1995 Jun 1;129(1):27–32. doi: 10.1016/0378-1097(95)00129-S. [DOI] [PubMed] [Google Scholar]
  32. Stein G. S., Stein J. L., van Wijnen A. J., Lian J. B. Histone gene transcription: a model for responsiveness to an integrated series of regulatory signals mediating cell cycle control and proliferation/differentiation interrelationships. J Cell Biochem. 1994 Apr;54(4):393–404. doi: 10.1002/jcb.240540406. [DOI] [PubMed] [Google Scholar]
  33. Toro G. C., Galanti N. Trypanosoma cruzi histones. Further characterization and comparison with higher eukaryotes. Biochem Int. 1990;21(3):481–490. [PubMed] [Google Scholar]
  34. Vanhamme L., Pays E. Control of gene expression in trypanosomes. Microbiol Rev. 1995 Jun;59(2):223–240. doi: 10.1128/mr.59.2.223-240.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Wells D. E. Compilation analysis of histones and histone genes. Nucleic Acids Res. 1986;14 (Suppl):r119–r149. doi: 10.1093/nar/14.suppl.r119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Wells D., McBride C. A comprehensive compilation and alignment of histones and histone genes. Nucleic Acids Res. 1989;17 (Suppl):r311–r346. doi: 10.1093/nar/17.suppl.r311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wu R. S., Tsai S., Bonner W. M. Patterns of histone variant synthesis can distinguish G0 from G1 cells. Cell. 1982 Dec;31(2 Pt 1):367–374. doi: 10.1016/0092-8674(82)90130-1. [DOI] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES