Animals; Antimetabolites/pharmacology; Bromodeoxyuridine/pharmacology; Cell Division; Cell Nucleus/metabolism/ultrastructure; Chromosomes; Electrophoresis, Gel, Pulsed-Field; Flow Cytometry; G2 Phase; Immunohistochemistry; In Situ Hybridization; In Situ Hybridization, Fluorescence; Microscopy, Electron; Microscopy, Fluorescence; Mitosis; S Phase; Time Factors; Trypanosoma cruzi/genetics/ultrastructure
Abstract :
[en] Chromosome localization in the interphase nuclei of eukaryotes depends on gene replication and transcription. Little is known about chromosome localization in protozoan parasites such as trypanosomes, which have unique mechanisms for the control of gene expression, with most genes being posttranscriptionally regulated. In the present study, we examined where the chromosomes are replicated in Trypanosoma cruzi, the agent of Chagas' disease. The replication sites, identified by the incorporation of 5-bromodeoxyuridine, are located at the nuclear periphery in proliferating epimastigote forms in the early S phase of the cell cycle. When the S phase ends and cells progress through the cell cycle, 5-bromodeoxyuridine labeling is observed in the nuclear interior, suggesting that chromosomes move. We next monitored chromosome locations in different stages of the cell cycle by using a satellite DNA sequence as a probe in a fluorescence in situ hybridization assay. We found two distinct labeling patterns according to the cell cycle stage. The first one is seen in the G(1) phase, in hydroxyurea-arrested epimastigotes or in trypomastigotes, which are differentiated nondividing forms. In all of these forms the satellite DNA is found in dots randomly dispersed in the nucleus. The other pattern is found in cells from the S phase to the G(2) phase. In these cells, the satellite DNA is found preferentially at the nuclear periphery. The labeling at the nuclear periphery disappears only after mitosis. Also, DNA detected with terminal deoxynucleotidyl transferase is found distributed throughout the nuclear space in the G(1) phase but concentrated at the nuclear periphery in the S phase to the G(2) phase. These results strongly suggest that T. cruzi chromosomes move and, after entering the S phase, become constrained at the nuclear periphery, where replication occurs.
scite shows how a scientific paper has been cited by providing the context of the citation, a classification describing whether it supports, mentions, or contrasts the cited claim, and a label indicating in which section the citation was made.
Bibliography
Abuin, G., L. H. G. Freitas-Junior, W. Colli, M. J. Alves, and S. Schenkman. 1999. Expression of trans-sialidase and 85 kDa glycoprotein genes in Trypanosoma cruzi is differentially regulated at the post-transcriptional level by labile protein factors. J. Biol. Chem. 274:13041-13047.
Bannister, A. J., P. Zegerman, J. F. Partridge, E. A. Miska, J. O. Thomas, R. C. Allshire, and T. Kouzarides. 2001. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410:120-124.
Camargo, E. P. 1964. Growth and differentiation in Trypanosoma cruzi: origin of metacyclic trypomastigotes in liquid media. Rev. Inst. Med. Trop. Sao Paulo 6:93-100.
Cano, M. I., A. Gruber, M. Vazquez, A. Cortés, M. J. Levin, A. Gonzalez, W. Degrave, E. Rondinelli, B. Zingales, J. L. Ramirez, C. Alonso, J. M. Requena, and J. F. Da Silveira. 1995. Molecular karyotype of clone CL Brener chosen for the Trypanosoma cruzi genome project. Mol. Biochem. Parasitol. 71:273-278.
Cavalli, G., and R. Paro. 1998. Chromo-domain proteins: linking chromatin structure to epigenetic regulation. Curr. Opin. Cell Biol. 10:354-360.
Cremer, T., G. Kreth, H. Koester, R. H. Fink, R. Heintzmann, M. Cremer, I. Solovei, D. Zink, and C. Cremer. 2000. Chromosome territories, interchromatin domain compartment, and nuclear matrix: an integrated view of the functional nuclear architecture. Crit. Rev. Eukaryot. Gene Expr. 10:179-212.
DePamphilis, M. L. 2000. Review: nuclear structure and DNA replication. J. Struct. Biol. 129:186-197.
Dundr, M., and T. Misteli. 2001. Functional architecture in the cell nucleus. Biochem. J. 356:297-310.
Elias, M. C., R. Marques-Porto, E. Freymuller, and S. Schenkman. 2001. Transcription rate modulation through the Trypanosoma cruzi life cycle occurs in parallel with changes in nuclear organisation. Mol. Biochem. Parasitol. 112:79-90.
Ferguson, M., and D. C. Ward. 1992. Cell cycle dependent chromosomal movement in pre-mitotic human T-lymphocyte nuclei. Chromosoma 101:557-565.
Ferreira, J., G. Paolella, C. Ramos, and A. I. Lamond. 1997. Spatial organization of large-scale chromatin domains in the nucleus: a magnified view of single chromosome territories. J. Cell Biol. 139:1597-1610.
Filho, S. A., E. R. Pereira de Almeida, and E. S. Gander. 1978. The influence of hydroxyurea and colchicine on growth and morphology of Trypanosoma cruzi. Acta Trop. 35:229-237.
Freitas-Junior, L. H., R. M. Porto, L. A. Pirrit, S. Schenkman, and A. Scherf. 1999. Identification of the telomere in Trypanosoma cruzi reveals highly heterogeneous telomere lengths in different parasite strains. Nucleic Acids Res. 27:2451-2456.
Galanti, N., J. A. Dvorak, J. Grenet, and J. P. McDaniel. 1994. Hydroxyurea-induced synchrony of DNA replication in the Kinetoplastida. Exp. Cell Res. 214:225-230.
Gonzalez, A., E. Prediger, M. E. Huecas, N. Nogueira, and P. M. Lizardi. 1984. Minichromosomal repetitive DNA in Trypanosoma cruzi: its use in a high-sensitivity parasite detection assay. Proc. Natl. Acad. Sci. USA 81:3356-3360.
Gunawardena, S., and M. C. Rykowski. 2000. Direct evidence for interphase chromosome movement during the mid-blastula transition in Drosophila. Curr. Biol. 10:285-288.
Hediger, F., and S. M. Gasser. 2002. Nuclear organization and silencing: putting things in their place. Nat. Cell Biol. 4:E53-E55.
Heun, P., T. Laroche, K. Shimada, P. Furrer, and S. M. Gasser. 2001. Chromosome dynamics in the yeast interphase nucleus. Science 294:2181-2186.
Heun, P., A. Taddei, and S. M. Gasser. 2001. From snapshots to moving pictures: new perspectives on nuclear organization. Trends Cell Biol. 11:519-525.
Hofer, A., J. T. Ekanem, and L. Thelander. 1998. Allosteric regulation of Trypanosoma brucei ribonucleotide reductase studied in vitro and in vivo. J. Biol. Chem. 273:34098-34104.
Hotz, H. R., S. Biebinger, J. Flaspohler, and C. Clayton. 1998. PARP gene expression: control at many levels. Mol. Biochem. Parasitol. 91:131-143.
Hozak, P., A. B. Hassan, D. A. Jackson, and P. R. Cook. 1993. Visualization of replication factories attached to nucleoskeleton. Cell 73:361-373.
Lachner, M., D. O'Carroll, S. Rea, K. Mechtler, and T. Jenuwein. 2001. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410:116-120.
Lamond, A. I., and W. C. Earnshaw. 1998. Structure and function in the nucleus. Science 280:547-553.
Leonhardt, H., H. P. Rahn, P. Weinzierl, A. Sporbert, T. Cremer, D. Zink, and M. C. Cardoso. 2000. Dynamics of DNA replication factories in living cells. J. Cell Biol. 149:271-280.
Li, G., G. Sudlow, and A. S. Belmont. 1998. Interphase cell cycle dynamics of a late-replicating, heterochromatic homogeneously staining region: precise choreography of condensation/decondensation and nuclear positioning. J. Cell Biol. 140:975-989.
Ma, H., J. Samarabandu, R. S. Devdhar, R. Acharya, P. C. Cheng, C. Meng, and R. Berezney. 1998. Spatial and temporal dynamics of DNA replication sites in mammalian cells. J. Cell Biol. 143:1415-1425.
Ma, H., A. J. Siegel, and R. Berezney. 1999. Association of chromosome territories with the nuclear matrix. Disruption of human chromosome territories correlates with the release of a subset of nuclear matrix proteins. J. Cell Biol. 146:531-542.
Moir, R. D., T. P. Spann, H. Herrmann, and R. D. Goldman. 2000. Disruption of nuclear lamin organization blocks the elongation phase of DNA replication. J. Cell Biol. 149:1179-1192.
Morgan, G. A., E. A. Hamilton, and S. J. Black. 1996. The requirements for G1 checkpoint progression of Trypanosoma brucei S 427 clone 1. Mol. Biochem. Parasitol. 78:195-207.
Nakamura, H., T. Morita, and C. Sato. 1986. Structural organizations of replicon domains during DNA synthetic phase in the mammalian nucleus. Exp. Cell Res. 165:291-297.
Sadoni, N., S. Langer, C. Fauth, G. Bernardi, T. Cremer, B. M. Turner, and D. Zink. 1999. Nuclear organization of mammalian genomes. Polar chromosome territories build up functionally distinct higher order compartments. J. Cell Biol. 146:1211-1226.
Santos, M. R., H. Lorenzi, P. Porcile, M. S. Carmo, A. Schijman, A. Brandao, J. E. Araya, H. B. Gomes, M. A. Chiurillo, J. L. Ramirez, W. M. Degrave, M. J. Levin, and J. F. Da Silveira. 1999. Physical mapping of a 670-kb region of chromosomes XVI and XVII from the human protozoan parasite Trypanosoma cruzi encompassing the genes for two immunodominant antigens. Genome Res. 9:1268-1276.
Shelby, R. D., K. M. Hahn, and K. F. Sullivan. 1996. Dynamic elastic behavior of alpha-satellite DNA domains visualized in situ in living human cells. J. Cell Biol. 135:545-557.
Simpson, A. M., and L. Simpson. 1974. Labeling of Crithidia fasciculata DNA with (3H)thymidine. J. Protozool. 21:379-382.
Spector, D. L. 1993. Macromolecular domains within the cell nucleus. Annu. Rev. Cell Biol. 9:265-315.
Taddei, A., C. Maison, D. Roche, and G. Almouzni. 2001. Reversible disruption of pericentric heterochromatin and centromere function by inhibiting deacetylases. Nat. Cell Biol. 3:114-120.
Teixeira, S. M. 1998. Control of gene expression in Trypanosomatidae. Braz. J. Med. Biol. Res. 31:1503-1516.
Thiry, M. 1992. Highly sensitive immunodetection of DNA on sections with exogenous terminal deoxynucleotidyl transferase and non-isotopic nucleotide analogues. J. Histochem. Cytochem. 40:411-419.
Woodward, R., and K. Gull. 1990. Timing of nuclear and kinetoplast DNA replication and early morphological events in the cell cycle of Trypanosoma brucei. J. Cell Sci. 95:49-57.
Ye, Q., I. Callebaut, A. Pezhman, J. C. Courvalin, and H. J. Worman. 1997. Domain-specific interactions of human HP1-type chromodomain proteins and inner nuclear membrane protein LBR. J. Biol. Chem. 272:14983-14989.
Young, C. W., G. Schochetman, S. Hodas, and M. E. Balis. 1967. Inhibition of DNA synthesis by hydroxyurea: structure-activity relationships. Cancer Res. 27:535-540.
Zink, D., H. Bornfleth, A. Visser, C. Cremer, and T. Cremer. 1999. Organization of early and late replicating DNA in human chromosome territories. Exp. Cell Res. 247:176-188.
Similar publications
Sorry the service is unavailable at the moment. Please try again later.
This website uses cookies to improve user experience. Read more
Save & Close
Accept all
Decline all
Show detailsHide details
Cookie declaration
About cookies
Strictly necessary
Performance
Strictly necessary cookies allow core website functionality such as user login and account management. The website cannot be used properly without strictly necessary cookies.
This cookie is used by Cookie-Script.com service to remember visitor cookie consent preferences. It is necessary for Cookie-Script.com cookie banner to work properly.
Performance cookies are used to see how visitors use the website, eg. analytics cookies. Those cookies cannot be used to directly identify a certain visitor.
Used to store the attribution information, the referrer initially used to visit the website
Cookies are small text files that are placed on your computer by websites that you visit. Websites use cookies to help users navigate efficiently and perform certain functions. Cookies that are required for the website to operate properly are allowed to be set without your permission. All other cookies need to be approved before they can be set in the browser.
You can change your consent to cookie usage at any time on our Privacy Policy page.