Artículo

Da Cunha, J.P.C.; Nakayasu, E.S.; Elias, M.C.; Pimenta, D.C.; Tellez-Inon, M.T.; Rojas, F.; Manuel, M.; Almeida, I.C.; Schenkman, S. "Trypanosoma cruzi histone H1 is phosphorylated in a typical cyclin dependent kinase site accordingly to the cell cycle" (2005) Molecular and Biochemical Parasitology. 140(1):75-86
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Abstract:

Histone H1 of most eukaryotes is phosphorylated during the cell cycle progression and seems to play a role in the regulation of chromatin structure, affecting replication and chromosome condensation. In trypanosomatids, histone H1 lacks the globular domain and is shorter when compared with the histone of other eukaryotes. We have previously shown that in Trypanosoma cruzi, the agent of Chagas' disease, histone H1 is phosphorylated and this increases its dissociation from chromatin. Here, we demonstrate using mass spectrometry analysis that T. cruzi histone H1 is only phosphorylated at the serine 12 in the sequence SPKK, a typical cyclin-dependent kinase site. We also found a correlation between the phosphorylation state of histone H1 and the cell cycle. Hydroxyurea and lactacystin, which, respectively, arrest parasites at the G1/S and G2/M stages of the cell cycle, increased the level of histone H1 phosphorylation. Cyclin-dependent kinase-related enzymes TzCRK3, and less intensely the TzCRK1 were able to phosphorylate histone H1 in vitro. Histone H1 dephosphorylation was prevented by treating the parasites with okadaic acid but not with calyculin A. These findings suggest that T. cruzi histone H1 phosphorylation is promoted by cyclin dependent kinases, present during S through G2 phase of the cell cycle, and its dephosphorylation is promoted by specific phosphatases. © 2004 Elsevier B.V. All rights reserved.

Registro:

Documento: Artículo
Título:Trypanosoma cruzi histone H1 is phosphorylated in a typical cyclin dependent kinase site accordingly to the cell cycle
Autor:Da Cunha, J.P.C.; Nakayasu, E.S.; Elias, M.C.; Pimenta, D.C.; Tellez-Inon, M.T.; Rojas, F.; Manuel, M.; Almeida, I.C.; Schenkman, S.
Filiación:Depto. Microbiol., Imunologia P., EPM-UNIFESP, R. Botucatu 862-8a, São Paulo, SP 04023-062, Brazil
Departamento de Parasitologia, ICB, USP, São Paulo, Brazil
Centro de Toxinologia Aplicada, CAT/CEPID, Instituto Butantan, São Paulo, SP, Brazil
Inst. Invest. Ing. Genet. Biol. M., Vta de Obligado 2490, 1428 Buenos Aires, Argentina
Department of Biological Sciences, University of Texas at El Paso, 500 W. University Ave., El Paso, TX 79968-0519, United States
Laboratorio de Parasitologia, Instituto Butantan, São Paulo, SP, 05503-900, Brazil
Palabras clave:CDK; Cell cycle; Histone H1; Phosphatase; Phosphorylation; Trypanosoma cruzi; amino acid; calyculin A; cyclin dependent kinase; enzyme; histone H1; hydroxyurea; lactacystin; okadaic acid; serine; serylprolyllysyllysine; unclassified drug; amino acid sequence; article; cell cycle G1 phase; cell cycle G2 phase; cell cycle S phase; cell proliferation; enzyme binding; mass spectrometry; nonhuman; nucleotide sequence; priority journal; protein dephosphorylation; protein localization; protein phosphorylation; Trypanosoma cruzi; Eukaryota; Trypanosoma; Trypanosoma cruzi; Trypanosoma cruzi
Año:2005
Volumen:140
Número:1
Página de inicio:75
Página de fin:86
DOI: http://dx.doi.org/10.1016/j.molbiopara.2004.12.007
Título revista:Molecular and Biochemical Parasitology
Título revista abreviado:Mol. Biochem. Parasitol.
ISSN:01666851
CODEN:MBIPD
CAS:amino acid, 65072-01-7; calyculin A, 101932-71-2; cyclin dependent kinase, 150428-23-2; hydroxyurea, 127-07-1; lactacystin, 133343-34-7, 133398-98-8, 154333-21-8; okadaic acid, 78111-17-8; serine, 56-45-1, 6898-95-9
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_01666851_v140_n1_p75_DaCunha

Referencias:

  • Kasinsky, H.E., Lewis, J.D., Dacks, J.B., Ausio, J., Origin of H1 linker histones (2001) FASEB J, 15, pp. 34-42
  • Thoma, F., Koller, T., Klug, A., Involvement of histone H1 in the organization of the nucleosome and of the salt-dependent superstructures of chromatin (1979) J Cell Biol, 83, pp. 403-427
  • Carruthers, L.M., Bednar, J., Woodcock, C.L., Hansen, J.C., Linker histones stabilize the intrinsic salt-dependent folding of nucleosomal arrays: Mechanistic ramifications for higher-order chromatin folding (1998) Biochemistry, 37, pp. 14776-14787
  • Meersseman, G., Pennings, S., Bradbury, E.M., Chromatosome positioning on assembled long chromatin. Linker histones affect nucleosome placement on 5 S rDNA (1991) J Mol Biol, 220, pp. 89-100
  • Blank, T.A., Becker, P.B., Electrostatic mechanism of nucleosome spacing (1995) J Mol Biol, 252, pp. 305-313
  • Halmer, L., Gruss, C., Effects of cell cycle dependent histone H1 phosphorylation on chromatin structure and chromatin replication (1996) Nucleic Acids Res, 24, pp. 1420-1427
  • Hill, D.A., Influence of linker histone H1 on chromatin remodeling (2001) Biochem Cell Biol, 79, pp. 317-324
  • De La Barre, A.E., Gerson, V., Gout, S., Creaven, M., Allis, C.D., Dimitrov, S., Core histone N-termini play an essential role in mitotic chromosome condensation (2000) EMBO J, 19, pp. 379-391
  • Brown, D.T., Histone, H1 and the dynamic regulation of chromatin function (2003) Biochem Cell Biol, 81, pp. 221-227
  • Konishi, A., Shimizu, S., Hirota, J., Involvement of histone H1.2 in apoptosis induced by DNA double-strand breaks (2003) Cell, 114, pp. 673-688
  • Belikov, S., Karpov, V., Linker histones: Paradigm lost but questions remain (1998) FEBS Lett, 441, pp. 161-164
  • Thomas, J.O., Histone H1: Location and role (1999) Curr Opin Cell Biol, 11, pp. 312-317
  • Wolffe, A.P., Histone H1 (1997) Int J Biochem Cell Biol, 29, pp. 1463-1466
  • Nurse, P., Universal control mechanism regulating onset of M phase (1990) Nature, 344, pp. 503-508
  • Gurley, L.R., Valdez, J.G., Buchanan, J.S., Characterization of the mitotic specific phosphorylation site of histone H1. Absence of a consensus sequence for the p34cdc2/cyclin B kinase (1995) J Biol Chem, 270, pp. 27653-27660
  • Langan, T.A., Gautier, J., Lohka, M., Mammalian growth-associated H-1 histone kinase-A homolog of Cdc2+/Cdc28 protein-kinases controlling mitotic entry in yeast and frog cells (1989) Mol Cell Biol, 9, pp. 3860-3868
  • Swank, R.A., Th'Ng, J.P., Guo, X.W., Valdez, J., Bradbury, E.M., Gurley, L.R., Four distinct cyclin-dependent kinases phosphorylate histone H1 at all of its growth-related phosphorylation sites (1997) Biochemistry, 36, pp. 13761-13768
  • Contreras, A., Hale, T.K., Stenoien, D.L., Rosen, J.M., Mancini, M.A., Herrera, R.E., The dynamic mobility of histone H1 is regulated by cyclin/CDK phosphorylation (2003) Mol Cell Biol, 23, pp. 8626-8636
  • Hohmann, P., Phosphorylation of H1 histones (1983) Mol Cell Biochem, 57, pp. 81-92
  • Bharath, M.M., Chandra, N.R., Rao, M.R., Molecular modeling of the chromatosome particle (2003) Nucleic Acids Res, 31, pp. 4264-4274
  • Boggs, B.A., Allis, C.D., Chinault, A.C., Immunofluorescent studies of human chromosomes with antibodies against phosphorylated H1 histone (2000) Chromosoma, 108, pp. 485-490
  • Roth, S.Y., Allis, C.D., Chromatin condensation. Does H1 dephosphorylation play a role? (1992) Trends Biochem Sci, 17, pp. 93-98
  • Aslund, L., Carlsson, L., Henriksson, J., A gene family encoding heterogeneous histone H1 proteins in Trypanosoma cruzi (1994) Mol Biochem Parasitol, 65, pp. 317-330
  • Burri, M., Schlimme, W., Betschart, B., Kampfer, U., Schaller, J., Hecker, H., Biochemical and functional characterization of histone H1-like proteins in procyclic Trypanosoma brucei brucei (1993) Mol Biochem Parasitol, 79, pp. 649-659
  • Burri, M., Schlimme, W., Betschart, B., Partial amino acid sequence and functional aspects of histone H1 proteins in Trypanosoma brucei brucei (1995) Biol Cell, 83, pp. 23-31
  • Espinoza, I., Toro, G.C., Hellman, U., Galanti, N., Histone H1 and core histones in Leishmania and Crithidia: Comparison with Trypanosoma (1996) Exp Cell Res, 224, pp. 1-7
  • Schlimme, W., Burri, M., Betschart, B., Hecker, H., Properties of the histones and functional aspects of the soluble chromatin of epimastigote Trypanosoma cruzi (1995) Acta Trop, 60, pp. 141-154
  • Syed, S., Rajpurohit, R., Kim, S., Paik, W.K., In vivo and in vitro methylation of lysine residues of Euglena gracilis histone H1 (1992) J Protein Chem, 11, pp. 239-246
  • Toro, G.C., Galanti, N., H1 histone and histone variants in Trypanosoma cruzi (1988) Exp Cell Res, 174, pp. 16-24
  • Toro, G.C., Galanti, N., Trypanosoma cruzi histones. Further characterization and comparison with higher eukaryotes (1990) Biochem Int, 21, pp. 481-490
  • Toro, G.C., Galanti, N., Hellman, U., Wernstedt, C., Unambiguous identification of histone H1 in Trypanosoma cruzi (1993) J Cell Biochem, 52, pp. 431-439
  • Sabaj, V., Diaz, J., Toro, G.C., Galanti, N., Histone synthesis in Trypanosoma cruzi (1997) Exp Cell Res, 236, pp. 446-452
  • Noll, T.M., Desponds, C., Belli, S.I., Glaser, T.A., Fasel, N.J., Histone H1 expression varies during the Leishmania major life cycle (1997) Mol Biochem Parasitol, 84, pp. 215-227
  • Sabaj, V., Aslund, L., Pettersson, U., Galanti, N., Histone genes expression during the cell cycle in Trypanosoma cruzi (2001) J Cell Biochem, 80, pp. 617-624
  • Marques Porto, R., Amino, R., Elias, M.C., Faria, M., Schenkman, S., Histone H1 is phosphorylated in non-replicating and infective forms of Trypanosoma cruzi (2002) Mol Biochem Parasitol, 119, pp. 265-271
  • Teixeira, S.M., Control of gene expression in Trypanosomatidae (1998) Braz J Med Biol Res, 31, pp. 1503-1516
  • Grant, K.M., Hassan, P., Anderson, J.S., Mottram, J.C., The crk3 gene of Leishmania mexicana encodes a stage-regulated cdc2-related histone H1 kinase that associates with p12 (1998) J Biol Chem, 273, pp. 10153-10159
  • Hassan, P., Fergusson, D., Grant, K.M., Mottram, J.C., The CRK3 protein kinase is essential for cell cycle progression of Leishmania mexicana (2001) Mol Biochem Parasitol, 113, pp. 189-198
  • Santori, M.I., Laria, S., Gomez, E.B., Espinosa, I., Galanti, N., Tellez-Inon, M.T., Evidence for CRK3 participation in the cell division cycle of Trypanosoma cruzi (2002) Mol Biochem Parasitol, 121, pp. 225-232
  • Hammarton, T.C., Clark, J., Douglas, F., Boshart, M., Mottram, J.C., Stage-specific differences in cell cycle control in Trypanosoma brucei revealed by RNA interference of a mitotic cyclin (2003) J Biol Chem, 278, pp. 22877-22886
  • Camargo, E.P., Growth and differentiation in Trypanosoma cruzi: Origin of metacyclic trypomastigotes in liquid media (1964) Rev Inst Med Trop São Paulo, 6, pp. 93-100
  • Schenkman, S., Chaves, L.B., Pontes De Carvalho, L., Eichinger, D., A proteolytic fragment of Trypanosoma cruzi trans-sialidase lacking the carboxy-terminal domain is active, monomeric and generates antibodies that inhibit enzymatic activity (1994) J Biol Chem, 269, pp. 7970-7975
  • Elias, M.C., Faria, M., Mortara, R.A., Chromosome localization changes in the Trypanosoma cruzi nucleus (2002) Eukaryotic Cell, 1, pp. 944-953
  • Gomez, E.B., Santori, M.I., Laria, S., Characterization of the Trypanosoma cruzi Cdc2p-related protein kinase 1 and identification of three novel associating cyclins (2001) Mol Biochem Parasitol, 113, pp. 97-108
  • Vanfleteren, J.R., Van Bun, S.M., Van Beeumen, J.J., The primary structure of the major isoform (H1.1) of histone H1 from the nematode Caenorhabditis elegans (1988) Biochem J, 255, pp. 647-652
  • Mutomba, M.C., To, W.Y., Hyun, W.C., Wang, C.C., Inhibition of proteasome activity blocks cell cycle progression at specific phase boundaries in African trypanosomes (1997) Mol Biochem Parasitol, 90, pp. 491-504
  • Gomez, E.B., Kornblihtt, A.R., Tellez-Inon, M.T., Cloning of a cdc2-related protein kinase from Trypanosoma cruzi that interacts with mammalian cyclins (1998) Mol Biochem Parasitol, 91, pp. 337-351
  • Gonzalez, J., Cornejo, A., Santos, M.R., A novel protein phosphatase 2A (PP2A) is involved in the transformation of human protozoan parasite Trypanosoma cruzi (2003) Biochem J, 374, pp. 647-656
  • Orr, G.A., Werner, C., Xu, J., Identification of novel serine/threonine protein phosphatases in Trypanosoma cruzi: A potential role in control of cytokinesis and morphology (2000) Infect Immunol, 68, pp. 1350-1358
  • Jerzmanowski, A., Moraczewska, J., Distribution of postsynthetic methylation sites in Physarum histone H1 (1988) Mol Biol Rep, 13, pp. 97-101
  • Gruter, E., Betschart, B., Isolation, characterisation and organisation of histone H1 genes in African trypanosomes (2001) Parasitol Res, 87, pp. 977-984
  • Mottram, J.C., Smith, G., A family of trypanosome cdc2-related protein kinases (1995) Gene, 162, pp. 147-152
  • Grellier, P., Blum, J., Santana, J., Involvement of calyculin A-sensitive phosphatase(s) in the differentiation of Trypanosoma cruzi trypomastigotes to amastigotes (1999) Mol Biochem Parasitol, 98, pp. 239-252

Citas:

---------- APA ----------
Da Cunha, J.P.C., Nakayasu, E.S., Elias, M.C., Pimenta, D.C., Tellez-Inon, M.T., Rojas, F., Manuel, M.,..., Schenkman, S. (2005) . Trypanosoma cruzi histone H1 is phosphorylated in a typical cyclin dependent kinase site accordingly to the cell cycle. Molecular and Biochemical Parasitology, 140(1), 75-86.
http://dx.doi.org/10.1016/j.molbiopara.2004.12.007
---------- CHICAGO ----------
Da Cunha, J.P.C., Nakayasu, E.S., Elias, M.C., Pimenta, D.C., Tellez-Inon, M.T., Rojas, F., et al. "Trypanosoma cruzi histone H1 is phosphorylated in a typical cyclin dependent kinase site accordingly to the cell cycle" . Molecular and Biochemical Parasitology 140, no. 1 (2005) : 75-86.
http://dx.doi.org/10.1016/j.molbiopara.2004.12.007
---------- MLA ----------
Da Cunha, J.P.C., Nakayasu, E.S., Elias, M.C., Pimenta, D.C., Tellez-Inon, M.T., Rojas, F., et al. "Trypanosoma cruzi histone H1 is phosphorylated in a typical cyclin dependent kinase site accordingly to the cell cycle" . Molecular and Biochemical Parasitology, vol. 140, no. 1, 2005, pp. 75-86.
http://dx.doi.org/10.1016/j.molbiopara.2004.12.007
---------- VANCOUVER ----------
Da Cunha, J.P.C., Nakayasu, E.S., Elias, M.C., Pimenta, D.C., Tellez-Inon, M.T., Rojas, F., et al. Trypanosoma cruzi histone H1 is phosphorylated in a typical cyclin dependent kinase site accordingly to the cell cycle. Mol. Biochem. Parasitol. 2005;140(1):75-86.
http://dx.doi.org/10.1016/j.molbiopara.2004.12.007