Leishmania histone H1 overexpression delays parasite cell-cycle progression, parasite differentiation and reduces Leishmania infectivity in vivo

Molecular Microbiology

Volumn 60, Issue 6, 2006, Pages 1457-1473

  Smirlis, Despina ^a   Bisti, Sylvia N ^a   Xingi, Evangelia ^a   Konidou, Georgia ^a   Thiakaki, Maria ^a   Soteriadou, Ketty P ^a  

^a HELLENIC PASTEUR INSTITUTE   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H1;

AMASTIGOTE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL CYCLE; CELL CYCLE REGULATION; CONTROLLED STUDY; EPISOME; FEMALE; GENETIC TRANSFECTION; IN VITRO STUDY; IN VIVO STUDY; LEISHMANIA; LEISHMANIA MAJOR; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE DEVELOPMENT; PARASITE VIRULENCE; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEQUENCE HOMOLOGY;

ANIMALS; CELL CYCLE; CELL DIFFERENTIATION; CERCOPITHECUS AETHIOPS; COS CELLS; HISTONES; LEISHMANIA DONOVANI; LEISHMANIA MAJOR; MICE; MICE, INBRED BALB C; NIH 3T3 CELLS; NOCODAZOLE; PROTOZOAN PROTEINS; TRANS-ACTIVATION (GENETICS); VIRULENCE;

ANIMALIA; LEISHMANIA MAJOR; MAMMALIA; METAZOA;

EID: 33744499197     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2006.05205.x     Document Type: Article

References (67)

1. Afonso L.C. Scott P. 1993 Immune responses associated with susceptibility of C57BL/10 mice to Leishmania amazonensis. Infect Immun 61: 2952 2959.
2. Almeida R. Gilmartin B.J. McCann S.H. Norrish A. Ivens A.C. Lawson D., et al. 2004 Expression profiling of the Leishmania life cycle: cDNA arrays identify developmentally regulated genes present but not annotated in the genome. Mol Biochem Parasitol 136: 87 100.
3. Alsford S. Horn D. 2004 Trypanosomatid histones. Mol Microbiol 53: 365 372.
4. Barak E. Amin-Spector S. Gerliak E. Goyard S. Holland N. Zilberstein D. 2005 Differentiation of Leishmania donovani in host-free system: analysis of signal perception and response. Mol Biochem Parasitol 141: 99 108.
5. Bard E. 1989 Molecular biology of Leishmania. Biochem Cell Biol 67: 516 524.
6. Bergman M.G. Wawra E. Winge M. 1988 Chicken histone H5 inhibits transcription and replication when introduced into proliferating cells by microinjection. J Cell Sci 91: 201 209.
7. Beverley S.M. Clayton C.E. 1993 Transfection of Leishmania and Trypanosoma brucei by electroporation. Methods Mol Biol 21: 333 348.
8. Bisti S. Konidou G. Papageorgiou F. Milon G. Boelaert J.R. Soteriadou K. 2000 The outcome of Leishmania major experimental infection in BALB/c mice can be modulated by exogenously delivered iron. Eur J Immunol 30: 3732 3740.
9. Bouvet P. Dimitrov S. Wolffe A.P. 1994 Specific regulation of Xenopus chromosomal 5S rRNA gene transcription in vivo by histone H1. Genes Dev 8: 1147 1159.
10. Bradbury E.M. 1992 Reversible histone modifications and the chromosome cell cycle. Bioessays 14: 9 16.
11. Brown D.T. Alexander B.T. Sittman D.B. 1996 Differential effect of H1 variant overexpression on cell cycle progression and gene expression. Nucleic Acids Res 24: 486 493.
12. Chang K.P. 1983 Cellular and molecular mechanisms of intracellular symbiosis in leishmaniasis. Int Rev Cytol Suppl 14: 267 305.
13. Contreras A. Hale T.K. Stenoien D.L. Rosen J.M. Mancini M.A. Herrera R.E. 2003 The dynamic mobility of histone H1 is regulated by cyclin/CDK phosphorylation. Mol Cell Biol 23: 8626 8636.
14. da Cunha J.P. Nakayasu E.S. Elias M.C. Pimenta D.C. Tellez-Inon M.T. Rojas F., et al. 2005 Trypanosoma cruzi histone H1 is phosphorylated in a typical cyclin dependent kinase site accordingly to the cell cycle. Mol Biochem Parasitol 140: 75 86.
15. De S. Brown D.T. Lu Z.H. Leno G.H. Wellman S.E. Sittman D.B. 2002 Histone H1 variants differentially inhibit DNA replication through an affinity for chromatin mediated by their carboxyl-terminal domains. Gene 292: 173 181.
16. Debrabant A. Joshi M.B. Pimenta P.F. Dwyer D.M. 2004 Generation of Leishmania donovani axenic amastigotes: their growth and biological characteristics. Int J Parasitol 34: 205 217.
17. Diffley J.F. 2004 Regulation of early events in chromosome replication. Curr Biol 14: R778 R786.
18. Dou Y. Mizzen C.A. Abrams M. Allis C.D. Gorovsky M.A. 1999 Phosphorylation of linker histone H1 regulates gene expression in vivo by mimicking H1 removal. Mol Cell 4: 641 647.
19. Dou Y. Song X. Liu Y. Gorovsky M.A. 2005 The H1 phosphorylation state regulates expression of CDC2 and other genes in response to starvation in Tetrahymena thermophila. Mol Cell Biol 25: 3914 3922.
20. Downs J.A. Kosmidou E. Morgan A. Jackson S.P. 2003 Suppression of homologous recombination by the Saccharomyces cerevisiae linker histone. Mol Cell 11: 1685 1692.
21. Doyle P.S. Engel J.C. Pimenta P.F. da Silva P.P. Dwyer D.M. 1991 Leishmania donovani: long-term culture of axenic amastigotes at 37 degrees C. Exp Parasitol 73: 326 334.
22. Dyson N. 1998 The regulation of E2F by pRB-family proteins. Genes Dev 12: 2245 2262.
23. Fairley E.A. Kendrick-Jones J. Ellis J.A. 1999 The Emery-Dreifuss muscular dystrophy phenotype arises from aberrant targeting and binding of emerin at the inner nuclear membrane. J Cell Sci 112: 2571 2582.
24. Fan Y. Nikitina T. Morin-Kensicki E.M. Zhao J. Magnuson T.R. Woodcock C.L., et al. 2003 H1 linker histones are essential for mouse development and affect nucleosome spacing in vivo. Mol Cell Biol 23: 4559 4572.
25. Fasel N.J. Robyr D.C. Mauel J. Glaser T.A. 1993 Identification of a histone H1-like gene expressed in Leishmania major. Mol Biochem Parasitol 62: 321 323.
26. Frolov M.V. Dyson N.J. 2004 Molecular mechanisms of E2F-dependent activation and pRB-mediated repression. J Cell Sci 117: 2173 2181.
27. Galanti N. Galindo M. Sabaj V. Espinoza I. Toro G.C. 1998 Histone genes in trypanosomatids. Parasitol Today 14: 64 70.
28. Gupta N. Goyal N. Rastogi A.K. 2001 In vitro cultivation and characterization of axenic amastigotes of Leishmania. Trends Parasitol 17: 150 153.
29. Hammarton T.C. Mottram J.C. Doerig C. 2003 The cell cycle of parasitic protozoa: potential for chemotherapeutic exploitation. Prog Cell Cycle Res 5: 91 101.
30. Holzer T.R. McMaster W.R. Forney J.D. 2006 Expression profiling by whole-genome interspecies microarray hybridization reveals differential gene expression in procyclic promastigotes, lesion-derived amastigotes, and axenic amastigotes in Leishmania mexicana. Mol Biochem Parasitol 146: 198 218.
31. Ishiura M. Ohashi H. Hazumi N. Uchida T. Okada Y. 1989 Simplified cosmid vectors for gene transfer to cultured mammalian cells: isolation of the gene for elongation factor 2 from the mouse. Gene 85: 427 433.
32. Kamhawi S. Modi G.B. Pimenta P.F. Rowton E. Sacks D.L. 2000 The vectorial competence of Phlebotomus sergenti is specific for Leishmania tropica and is controlled by species-specific, lipophosphoglycan-mediated midgut attachment. Parasitology 121: 25 33.
33. Khan S.H. Wahl G.M. 1998 p53 and pRb prevent rereplication in response to microtubule inhibitors by mediating a reversible G1 arrest. Cancer Res 58: 396 401.
34. Khochbin S. 2001 Histone H1 diversity: bridging regulatory signals to linker histone function. Gene 271: 1 12.
35. Knoll A.H. 1992 The early evolution of eukaryotes: a geological perspective. Science 256: 622 627.
36. Konishi A. Shimizu S. Hirota J. Takao T. Fan Y. Matsuoka Y., et al. 2003 Involvement of histone H1.2 in apoptosis induced by DNA double-strand breaks. Cell 114: 673 688.
37. Laemmli U.K. 1970 Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680 685.
38. Lee H. Habas R. Abate-Shen C. 2004 MSX1 cooperates with histone H1b for inhibition of transcription and myogenesis. Science 304: 1675 1678.
39. Lohez O.D. Reynaud C. Borel F. Andreassen P.R. Margolis R.L. 2003 Arrest of mammalian fibroblasts in G1 in response to actin inhibition is dependent on retinoblastoma pocket proteins but not on p53. J Cell Biol 161: 67 77.
40. Lu Z.H. Sittman D.B. Brown D.T. Munshi R. Leno G.H. 1997 Histone H1 modulates DNA replication through multiple pathways in Xenopus egg extract. J Cell Sci 110: 2745 2758.
41. Lu Z.H. Sittman D.B. Romanowski P. Leno G.H. 1998 Histone H1 reduces the frequency of initiation in Xenopus egg extract by limiting the assembly of prereplication complexes on sperm chromatin. Mol Biol Cell 9: 1163 1176.
42. Lyons A.B. 2000 Analysing cell division in vivo and in vitro using flow cytometric measurement of CFSE dye dilution. J Immunol Methods 243: 147 154.
43. Margolis R.L. Lohez O.D. Andreassen P.R. 2003 G1 tetraploidy checkpoint and the suppression of tumorigenesis. J Cell Biochem 88: 673 683.
44. Martinez E. Thomas M.C. Alonso V. Carmelo E. Gonzalez A.C. Del Castillo A., et al. 2002 Cloning and molecular characterization of the cDNA encoding histone H1 from Leishmania braziliensis. J Parasitol 88: 199 203.
45. Martinsson H.S. Starborg M. Erlandsson F. Zetterberg A. 2005 Single cell analysis of G1 check points - the relationship between the restriction point and phosphorylation of pRb. Exp Cell Res 305: 383 391.
46. Masina S.M.M.G. Demotz S.O. Fasel N.J. 2003 Protection against cutaneous leishmaniasis in outbred vervet monkeys using a recombinant histone H1 antigen. J Infect Dis 188: 1250 1257.
47. Matera G. Lupi M. Ubezio P. 2004 Heterogeneous cell response to topotecan in a CFSE-based proliferation test. Cytometry A 62: 118 128.
48. Noll T.M. Desponds C. Belli S.I. Glaser T.A. Fasel N.J. 1997 Histone H1 expression varies during the Leishmania major life cycle. Mol Biochem Parasitol 84: 215 227.
49. Papageorgiou F.T. Soteriadou K.P. 2002 Expression of a novel Leishmania gene encoding a histone H1-like protein in Leishmania major modulates parasite infectivity in vitro. Infect Immun 70: 6976 6986.
50. Rainey P.M. Spithill T.W. McMahon-Pratt D. Pan A.A. 1991 Biochemical and molecular characterization of Leishmania pifanoi amastigotes in continuous axenic culture. Mol Biochem Parasitol 49: 111 118.
51. Saar Y. Ransford A. Waldman E. Mazareb S. Amin-Spector S. Plumblee J., et al. 1998 Characterization of developmentally-regulated activities in axenic amastigotes of Leishmania donovani. Mol Biochem Parasitol 95: 9 20.
52. Sacks D. Kamhawi S. 2001 Molecular aspects of parasite-vector and vector-host interactions in leishmaniasis. Annu Rev Microbiol 55: 453 483.
53. Sacks D.L. Hieny S. Sher A. 1985 Identification of cell surface carbohydrate and antigenic changes between noninfective and infective developmental stages of Leishmania major promastigotes. J Immunol 135: 564 569.
54. Solioz N. Blum-Tirouvanziam U. Jacquet R. Rafati S. Corradin G. Mauel J., et al. 1999 The protective capacities of histone H1 against experimental murine cutaneous leishmaniasis. Vaccine 18: 850 859.
55. Soto M. Requena J.M. Jimenez-Ruiz A. Alonso C. 1991 The mRNA coding for the nucleosomal protein H2A of Leishmania is polyadenylated and has stem-loops at the 3′ end. Nucleic Acids Res 19: 4554.
56. Soto M. Requena J.M. Gomez L.C. Navarrete I. Alonso C. 1992 Molecular characterization of a Leishmania donovani infantum antigen identified as histone H2A. Eur J Biochem 205: 211 216.
57. Soto M. Quijada L. Alonso C. Requena J.M. 1997 Molecular cloning and analysis of expression of the Leishmania infantum histone H4 genes. Mol Biochem Parasitol 90: 439 447.
58. Stein G.S. Stein J.L. Van Wijnen A.J. Lian J.B. 1996 Transcriptional control of cell cycle progression: the histone gene is a paradigm for the G1/S phase and proliferation/differentiation transitions. Cell Biol Int 20: 41 49.
59. Steinbach O.C. Wolffe A.P. Rupp R.A. 1997 Somatic linker histones cause loss of mesodermal competence in Xenopus. Nature 389: 395 399.
60. Stiles J.K. Hicock P.I. Shah P.H. Meade J.C. 1999 Genomic organization, transcription, splicing and gene regulation in Leishmania. Ann Trop Med Parasitol 93: 781 807.
61. Sullivan C.S. Pipas J.M. 2002 T antigens of simian virus 40: molecular chaperones for viral replication and tumorigenesis. Microbiol Mol Biol Rev 66: 179 202.
62. Sun J.M. Wiaderkiewicz R. Ruiz-Carrillo A. 1989 Histone H5 in the control of DNA synthesis and cell proliferation. Science 245: 68 71.
63. Titus R.G. Marchand M. Boon T. Louis J.A. 1985 A limiting dilution assay for quantifying Leishmania major in tissues of infected mice. Parasite Immunol 7: 545 555.
64. Voyiatzaki C.S. Soteriadou K.P. 1992 Identification and isolation of the Leishmania transferrin receptor. J Biol Chem 267: 9112 9117.
65. Widlak P. Kalinowska M. Parseghian M.H. Lu X. Hansen J.C. Garrard W.T. 2005 The histone H1 C-terminal domain binds to the apoptotic nuclease, DNA fragmentation factor (DFF40/CAD) and stimulates DNA cleavage. Biochemistry 44: 7871 7878.
66. Wolffe A. 1998 Chromatin: Structure and Function. London: Academic Press.
67. Zhang W.W. Matlashewski G. 1997 Loss of virulence in Leishmania donovani deficient in an amastigote-specific protein, A2. Proc Natl Acad Sci USA 94: 8807 8811.