Chromatin remodelling during the life cycle of trypanosomatids

International Journal for Parasitology

Volumn 30, Issue 6, 2000, Pages 679-687

  Belli, S I ^a  

^a UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

Author keywords

Chromatin; Epigenetic; Gene regulation; Leishmania; Trypanosomes

Indexed keywords

DNA DIRECTED RNA POLYMERASE; HISTONE; HISTONE H1; MESSENGER RNA; RNA POLYMERASE II; VARIANT SURFACE GLYCOPROTEIN;

CHROMATIN STRUCTURE; CISTRON; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE SILENCING; GENOTYPE; KARYOTYPE; LEISHMANIA; LIFE CYCLE; NONHUMAN; POLYADENYLATION; PROMOTER REGION; REVIEW; TRANS SPLICING; TRANSCRIPTION INITIATION; TRYPANOSOMA;

ANIMALS; CHROMATIN; GENE EXPRESSION REGULATION; GENOTYPE; HISTONES; KARYOTYPING; LIFE CYCLE STAGES; TRYPANOSOMA;

EUKARYOTA; PROTOZOA; TRYPANOSOMA; TRYPANOSOMATIDAE;

EID: 0034193649     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0020-7519(00)00052-7     Document Type: Review

References (87)

1. Schmidt G.D., Roberts L.S. Order Kinetoplastida: trypanosomes and their kin. Bowen E.L. Foundations of Parasitology. 1985;56-83 Times Mirror/Mosby College Publishing, Toronto.
2. Chimelli L., Scaravilli F. Trypanosomiasis. Brain Pathol. 7:1997;599-611.
3. Herwaldt B.L. Leishmaniasis. Lancet. 354:1999;1191-1199.
4. Wolffe A.P., Hayes J.J. Chromatin disruption and modification. Nucleic Acids Res. 27:1999;711-720.
5. Latham K.E. Mechanisms and control of embryonic genome activation in mammalian embryos. Int Rev Cytol. 193:1999;71-124.
6. Olovnikov A.M. Towards the quantitative traits regulation: fountain theory implications in comparative and developmental biology. Int J Dev Biol. 41:1997;923-931.
7. Monier R., Trott K.R. The various models of carcinogenesis. Susceptibility genes, mutations, epigenetic processes. C R Acad Sci Iii. 322:1999;177-180.
8. Dhalluin S., Elias Z., Poirot O., et al. Apoptosis inhibition and ornithine decarboxylase superinduction as early epigenetic events in morphological transformation of Syrian hamster embryo cells exposed to 2-methoxyacetaldehyde, a metabolite of 2-methoxyethanol. Toxicol Lett. 105:1999;163-175.
9. Iwamoto K.S., Mizuno T., Seyama T., et al. Mutant p53: epigenetic mutator of the T-cell receptor via induction of methylation. Mol Carcinog. 25:1999;113-121.
10. Agarwal S., Viola J.P., Rao A. Chromatin-based regulatory mechanisms governing cytokine gene transcription. J Allergy Clin Immunol. 103:1999;990-999.
11. Ensoli F., Fiorelli V., Muratori D.S., et al. Immune-derived cytokines in the nervous system: epigenetic instructive signals or neuropathogenic mediators? Crit Rev Immunol. 19:1999;97-116.
12. Matzke A.J., Matzke M.A. Position effects and epigenetic silencing of plant transgenes. Curr Opin Plant Biol. 1:1998;142-148.
13. Ersfeld K., Melville S.E., Gull K. Nuclear and genome organization of Trypanosoma brucei. Parasitol Today. 15:1999;58-63.
14. Graham S.V. Mechanisms of stage-regulated gene expression in kinetoplastida. Parasitology Today. 1:1995;217-224.
15. Ullu E., Tschudi C., Gunzl A. Trans-splicing in trypanosomatid protozoa. Smith D.F., Parsons M. Molecular Biology of Parasitic Protozoa. 1996;115-133 IRL Press, New York.
16. Hug M., Hotz H.R., Hartmann C., et al. Hierarchies of RNA-processing signals in a trypanosome surface antigen mRNA precursor. Mol Cell Biol. 14:1994;7428-7435.
17. Laufer G., Schaaf G., Bollgonn S., et al. In vitro analysis of alpha-amanitin-resistant transcription from the rRNA, procyclic acidic repetitive protein, and variant surface glycoprotein gene promoters in Trypanosoma brucei. Mol Cell Biol. 19:1999;5466-5473.
18. Pays E, Vanhamme L. Developmental regulation of gene expression in African trypanosomes. Smith D.F., Parsons M. Molecular Biology of Parasitic Protozoa. 1996;88-114 IRL Press, New York.
19. Huang J., Van der Ploeg L.H. Requirement of a polypyrimidine tract for trans-splicing in trypanosomes: discriminating the PARP promoter from the immediately adjacent 3′ splice acceptor site. EMBO J. 10:1991;3877-3885.
20. Huang J., Van der Ploeg L.H. Maturation of polycistronic pre-mRNA in Trypanosoma brucei: analysis of trans splicing and poly(A) addition at nascent RNA transcripts from the hsp70 locus. Mol Cell Biol. 11:1991;3180-3190.
21. Kapotas N., Bellofatto V. Differential response to RNA trans-splicing signals within the phosphoglycerate kinase gene cluster in Trypanosoma brucei. Nucleic Acids Res. 21:1993;4067-4072.
22. Lee M.G. The 3′ untranslated region of the hsp 70 genes maintains the level of steady state mRNA in Trypanosoma brucei upon heat shock. Nucleic Acids Res. 26:1998;4025-4033.
23. Wagner E.G., Simons R.W. Antisense RNA control in bacteria, phages, and plasmids. Annu Rev Microbiol. 48:1994;713-742.
24. Vanhee-Brossollet C., Vaquero C. Do natural antisense transcripts make sense in eukaryotes? Gene. 211:1998;1-9.
25. Wolffe A.P., Matzke M.A. Epigenetics: regulation through repression. Science. 286:1999;481-486.
26. Kapler G.M., Beverley S.M. Transcriptional mapping of the amplified region encoding the dihydrofolate reductase-thymidylate synthase of Leishmania major reveals a high density of transcripts, including overlapping and antisense RNAs. Mol Cell Biol. 9:1989;3959-3972.
27. Hughes D.E., Shonekan O.A., Simpson L. Structure, genomic organization and transcription of the bifunctional dihydrofolate reductase-thymidylate synthase gene from Crithidia fasciculata. Mol Biochem Parasitol. 34:1989;155-166.
28. Chen D.Q., Kolli B.K., Yadava N., et al. Episomal expression of specific sense and antisense mRNAs in Leishmania amazonensis: modulation of gp63 level in promastigotes and their infection of macrophages in vitro. Infect Immun. 68:2000;80-86.
29. Johnston D.A., Blaxter M.L., Degrave W.M., et al. Genomics and the biology of parasites. Bioessays. 21:1999;131-147.
30. Myler P.J., Audleman L., de Vos T., et al. Leishmania major Friedlin chromosome 1 has an unusual distribution of protein-coding genes. Proc Natl Acad Sci USA. 96:1999;2902-2906.
31. Nakaar V., Dare A.O., Hong D., et al. Upstream tRNA genes are essential for expression of small nuclear and cytoplasmic RNA genes in trypanosomes. Mol Cell Biol. 14:1994;6736-6742.
32. Widom J. Structure, dynamics, and function of chromatin in vitro. Annu Rev Biophys Biomol Struct. 27:1998;285-327.
33. Hecker H., Gander E.S. The compaction pattern of the chromatin of trypanosomes. Biol Cell. 53:1985;199-208.
34. Vickerman K., Tetley L. Recent ultrastructural studies on trypanosomes. Ann Soc Belg Med Trop. 57:1977;441-457.
35. Wincker P., Ravel C., Blaineau C., et al. The Leishmania genome comprises 36 chromosomes conserved across widely divergent human pathogenic species. Nucleic Acids Res. 24:1996;1688-1694.
36. Melville S.E. Parasite genome analysis. Genome research in Trypanosoma brucei: chromosome size polymorphism and its relevance to genome mapping and analysis. Trans R Soc Trop Med Hyg. 91:1997;116-120.
37. Borst P., Hoeijmakers J.H. Kinetoplast DNA. Plasmid. 2:1979;20-40.
38. Astolfi Filho S., Martins de Sa C., Gander E.S. On the chromatin structure of Trypanosoma cruzi. Mol Biochem Parasitol. 1:1980;45-53.
39. Pays E., Lheureux M., Steinert M. The expression-linked copy of a surface antigen gene in Trypanosoma is probably the one transcribed. Nature. 292:1981;265-267.
40. Hecker H., Bender K., Betschart B., et al. Instability of the nuclear chromatin of procyclic Trypanosoma brucei brucei. Mol Biochem Parasitol. 37:1989;225-234.
41. Hecker H., Betschart B., Bender K., et al. The chromatin of trypanosomes. Int J Parasitol. 24:1994;809-819.
42. Bender K., Betschart B., Schaller J., et al. Biochemical properties of histone-like proteins of procyclic Trypanosoma brucei brucei. Acta Trop. 50:1991;169-183.
43. Souto-Padron T., De Souza W. Ultrastructural localization of basic proteins in Trypanosoma cruzi. J Histochem Cytochem. 26:1978;349-358.
44. Rubio J., Rosado Y., Castaneda M. Subunit structure of Trypanosoma cruzi chromatin. Can J Biochem. 58:1980;1247-1251.
45. Bender K., Betschart B., Schaller J., et al. Sequence differences between histones of procyclic Trypanosoma brucei brucei and higher eukaryotes. Parasitology. 105:1992;97-104.
46. Soto M., Requena J.M., Gomez L.C., et al. Molecular characterization of a Leishmania donovani infantum antigen identified as histone H2A. Eur J Biochem. 205:1992;211-216.
47. Fasel N.J., Robyr D.C., Mauel J., et al. Identification of a histone H1-like gene expressed in Leishmania major. Mol Biochem Parasitol. 62:1994;321-323.
48. Soto M., Requena J.M., Jimenez R.A., et al. The mRNA coding for the nucleosomal protein H2A of Leishmania is polyadenylated and has stem-loops at the 3′ end. Nucleic Acids Res. 19:1991;4554.
49. Genske J.E., Cairns B.R., Stack S.P., et al. Structure and regulation of histone H2B mRNAs from Leishmania enriettii. Mol Cell Biol. 11:1991;240-249.
50. Soto M, Requena JM, Quijada L, et al. Organization, transcription and regulation of the Leishmania infantum histone H3 genes. Biochem J. 318:1996;813-819.
51. Soto M., Quijada L., Alonso C., et al. Molecular cloning and analysis of expression of the Leishmania infantum histone H4 genes. Mol Biochem Parasitol. 90:1997;439-447.
52. Espinoza I., Toro G.C., Hellman U., et al. Histone H1 and core histones in Leishmania and Crithidia: comparison with Trypanosoma. Exp Cell Res. 224:1996;1-7.
53. Widom J. Chromatin structure: linking structure to function with histone H1. Curr Biol. 8:1998;R788-R791.
54. Bender K., Betschart B., Marion C., et al. Structural differences between the chromatin of procyclic Trypanosoma brucei brucei and of higher eukaryotes as probed by immobilized trypsin. Acta Trop. 52:1992;69-78.
55. Bender K., Betschart B., Hecker H. Histone-DNA interactions in the chromatin of procyclic Trypanosoma brucei brucei. Parasitol Res. 78:1992;495-500.
56. Schlimme W., Burri M., Bender K., et al. Trypanosoma brucei brucei: differences in the nuclear chromatin of bloodstream forms and procyclic culture forms. Parasitology. 107:1993;237-247.
57. Toro G.C., Galanti N. H1 histone and histone variants in Trypanosoma cruzi. Exp Cell Res. 174:1988;16-24.
58. Burri M., Schlimme W., Betschart B., et al. Biochemical and functional characterization of histone H1-like proteins in procyclic Trypanosoma brucei brucei. Parasitol Res. 79:1993;649-659.
59. Belli S., Formenton A., Noll T., et al. Leishmania major: histone H1 gene expression from the sw3 locus. Exp Parasitol. 91:1999;151-160.
60. Doenecke D., Tonjes R., Kress H. The H1 and core histone subtypes: differential gene expression and varied primary structures. Adv Enzyme Regul. 27:1988;107-120.
61. Khochbin S., Wolffe A.P. Developmentally regulated expression of linker-histone variants in vertebrates. Eur J Biochem. 225:1994;501-510.
62. Khochbin S., Lawrence J.J. Molecular basis of the activation of basal histone H1(0) gene expression. Nucleic Acids Res. 22:1994;2887-2893.
63. Burri M., Schlimme W., Betschart B., et al. Partial amino acid sequence and functional aspects of histone H1 proteins in Trypanosoma brucei brucei. Biol Cell. 83:1995;23-31.
64. Schlimme W., Burri M., Betschart B., et al. Properties of the histones and functional aspects of the soluble chromatin of epimastigote Trypanosoma cruzi. Acta Trop. 60:1995;141-154.
65. Noll T.M., Desponds C., Belli S.I., et al. Histone H1 expression varies during the Leishmania major life cycle. Mol Biochem Parasitol. 84:1997;215-227.
66. Shen X., Yu L., Weir J.W., et al. Linker histones are not essential and affect chromatin condensation in vivo. Cell. 82:1995;47-56.
67. Shen X., Gorovsky M.A. Linker histone H1 regulates specific gene expression but not global transcription in vivo. Cell. 86:1996;475-483.
68. Steinbach O.C., Wolffe A.P., Rupp R.A. Somatic linker histones cause loss of mesodermal competence in Xenopus. Nature. 389:1997;395-399.
69. Miloshev G., Venkov P., van Holde K., et al. Low levels of exogenous histone H1 in yeast cause cell death. Proc Natl Acad Sci USA. 91:1994;11567-11570.
70. Landsman D. Histone H1 in Saccharomyces cerevisiae: a double mystery solved? [see comments]. Trends Biochem Sci. 21:1996;287-288.
71. Navarro M., Cross G.A., Wirtz E. Trypanosoma brucei variant surface glycoprotein regulation involves coupled activation/inactivation and chromatin remodeling of expression sites. EMBO J. 18:1999;2265-2272.
72. Darkin-Rattray S.J., Gurnett A.M., Myers R.W., et al. Apicidin: a novel antiprotozoal agent that inhibits parasite histone deacetylase. Proc Natl Acad Sci USA. 93:1996;13143-13147.
73. Soete M, Hettman C, Soldati D. The importance of reverse genetics in determining gene function in apicomplexan parasites. Parasitology 1999:S53-S61.
74. Scherf A., Hernandez R.R., Buffet P., et al. Antigenic variation in malaria: in situ switching, relaxed and mutually exclusive transcription of var genes during intra-erythrocytic development in Plasmodium falciparum. EMBO J. 17:1998;5418-5426.
75. Burri M., Schlimme W., Betschart B., et al. Characterization of the histones of Trypanosoma brucei brucei bloodstream forms. Acta Trop. 58:1994;291-305.
76. Sabaj V., Diaz J., Toro G.C., et al. Histone synthesis in Trypanosoma cruzi. Exp Cell Res. 236:1997;446-452.
77. Gommers-Ampt J., Borst P. Hypermodified bases in DNA. Faseb J. 9:1995;1034-1042.
78. Selker E.U. DNA methylation and chromatin structure: a view from below. Trends Biochem Sci. 15:1990;103-107.
79. Ashraf S.I., Ip Y.T. Transcriptional control: repression by local chromatin modification. Curr Biol. 8:1998;R683-R686.
80. Razin A., Shemer R. Epigenetic control of gene expression. Results Probl Cell Differ. 25:1999;189-204.
81. Borst P., Rudenko G., Blundell P.A., et al. Mechanisms of antigenic variation in African trypanosomes. Behring Inst Mitt. 99:1997;1-15.
82. Simpson L. A base called J [comment]. Proc Natl Acad Sci USA. 95:1998;2037-2038.
83. van Leeuwen F., Kieft R., Cross M., et al. Biosynthesis and function of the modified DNA base beta-D-glucosyl-hydroxymethyluracil in Trypanosoma brucei. Mol Cell Biol. 18:1998;5643-5651.
84. Gommers-Ampt J., Lutgerink J., Borst P. A novel DNA nucleotide in Trypanosoma brucei only present in the mammalian phase of the life-cycle. Nucleic Acids Res. 19:1991;1745-1751.
85. van Leeuwen F., Taylor M.C., Mondragon A., et al. beta-D-glucosyl-hydroxymethyluracil is a conserved DNA modification in kinetoplastid protozoans and is abundant in their telomeres [see comments]. Proc Natl Acad Sci USA. 95:1998;2366-2371.
86. Cross M., Kieft R., Sabatini R., et al. The modified base J is the target for a novel DNA-binding protein in kinetoplastid protozoans. EMBO J. 18:1999;6573-6581.
87. Akopyants N.S., Beverley S.M. A survey of the Leishmania major Friedlin strain VI genome by shotgun sequencing. 1999;Washington University Sequencing Center.