Trypanosoma brucei DMC1 does not act in DNA recombination, repair or antigenic variation in bloodstream stage cells

Molecular and Biochemical Parasitology

Volumn 145, Issue 2, 2006, Pages 245-253

  Proudfoot, Chris ^a   McCulloch, Richard ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Antigenic variation; Dmc1; Meiosis; Rad51; Recombination; Trypanosome

Indexed keywords

GLYCOPROTEIN; PROTEIN DMC1; PROTOZOAL PROTEIN; RAD51 PROTEIN; UNCLASSIFIED DRUG;

AFRICA; AFRICAN TRYPANOSOMIASIS; ANTIGENIC VARIATION; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DNA RECOMBINATION; DNA REPAIR; EUKARYOTE; GENE DISRUPTION; HOMOLOGOUS RECOMBINATION; LEISHMANIA MAJOR; LIFE CYCLE; MEIOSIS; NONHUMAN; PRIORITY JOURNAL; REVERTANT; TRYPANOSOMA BRUCEI; TRYPANOSOMA CRUZI;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENIC VARIATION; DNA REPAIR; GENE EXPRESSION; LEISHMANIA MAJOR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; MUTATION; PROTOZOAN PROTEINS; RAD51 RECOMBINASE; RECOMBINATION, GENETIC; SEQUENCE HOMOLOGY, AMINO ACID; TRYPANOSOMA BRUCEI BRUCEI; TRYPANOSOMA CRUZI;

EUKARYOTA; LEISHMANIA MAJOR; TRYPANOSOMA BRUCEI; TRYPANOSOMA CRUZI;

EID: 30544454048     PISSN: 01666851     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molbiopara.2005.10.007     Document Type: Article

References (87)

1. J.A. Eisen, and P.C. Hanawalt A phylogenomic study of DNA repair genes, proteins, and processes Mutat Res 435 1999 171 213
2. S.C. West Molecular views of recombination proteins and their control Nat Rev Mol Cell Biol 4 2003 435 445
3. B. Michel, G. Grompone, M.J. Flores, and V. Bidnenko Multiple pathways process stalled replication forks Proc Natl Acad Sci USA 101 2004 12783 12788
4. R.S. Maser, and R.A. DePinho Telomeres and the DNA damage response: why the fox is guarding the henhouse DNA Repair (Amst) 3 2004 979 988
5. S.L. Page, and R.S. Hawley Chromosome choreography: the meiotic ballet Science 301 2003 785 789
6. C. Richardson, N. Horikoshi, and T.K. Pandita The role of the DNA double-strand break response network in meiosis DNA Repair (Amst) 3 2004 1149 1164
7. K.W. Deitsch, E.R. Moxon, and T.E. Wellems Shared themes of antigenic variation and virulence in bacterial, protozoal, and fungal infections Microbiol Mol Biol Rev 61 1997 281 293
8. J.D. Barry, and R. McCulloch Antigenic variation in trypanosomes: enhanced phenotypic variation in a eukaryotic parasite Adv Parasitol 49 2001 1 70
9. R. McCulloch Antigenic variation in African trypanosomes: monitoring progress Trends Parasitol 20 2004 117 121
10. D. Horn The molecular control of antigenic variation in Trypanosoma brucei Curr Mol Med 4 2004 563 576
11. M. Becker, N. Aitcheson, E. Byles, B. Wickstead, E. Louis, and G. Rudenko Isolation of the repertoire of VSG expression site containing telomeres of Trypanosoma brucei 427 using transformation-associated recombination in yeast Genome Res 14 2004 2319 2329
12. L. Vanhamme, L. Lecordier, and E. Pays Control and function of the bloodstream variant surface glycoprotein expression sites in Trypanosoma brucei Int J Parasitol 31 2001 523 531
13. P. Borst Antigenic variation and allelic exclusion Cell 109 2002 5 8
14. C. Conway, C. Proudfoot, P. Burton, J.D. Barry, and R. McCulloch Two pathways of homologous recombination in Trypanosoma brucei Mol Microbiol 45 2002 1687 1700
15. R. McCulloch, and J.D. Barry A role for RAD51 and homologous recombination in Trypanosoma brucei antigenic variation Genes Dev 13 1999 2875 2888
16. P.G. McKean, J.K. Keen, D.F. Smith, and F.E. Benson Identification and characterisation of a RAD51 gene from Leishmania major Mol Biochem Parasitol 115 2001 209 216
17. M.K. Bhattacharyya, and N. Kumar Identification and molecular characterisation of DNA damaging agent induced expression of Plasmodium falciparum recombination protein PfRad51 Int J Parasitol 33 2003 1385 1392
18. J. Thacker The RAD51 gene family, genetic instability and cancer Cancer Lett 219 2005 125 135
19. J.Y. Bleuyard, M.E. Gallego, F. Savigny, and C.I. White Differing requirements for the Arabidopsis Rad51 paralogs in meiosis and DNA repair Plant J 41 2005 533 545
20. E. Staeva-Vieira, S. Yoo, and R. Lehmann An essential role of DmRad51/SpnA in DNA repair and meiotic checkpoint control EMBO J 22 2003 5863 5874
21. B.O. Krogh, and L.S. Symington Recombination proteins in yeast Annu Rev Genet 2004
22. P. Sung, L. Krejci, S. VanKomen, and M.G. Sehorn Rad51 recombinase and recombination mediators J Biol Chem 278 2003 42729 42732
23. J.Y. Masson, and S.C. West TheRad51 andDmc1 recombinases: a non-identical twin relationship Trends Biochem Sci 26 2001 131 136
24. D.K. Bishop, D. Park, L. Xu, and N. Kleckner DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression Cell 69 1992 439 456
25. B. Rockmill, M. Sym, H. Scherthan, and G.S. Roeder Roles for two RecA homologs in promoting meiotic chromosome synapsis Genes Dev 9 1995 2684 2695
26. D.K. Bishop RecA homologs Dmc1 and Rad51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis Cell 79 1994 1081 1092
27. O. Bezzubova, A. Shinohara, R.G. Mueller, H. Ogawa, and J.M. Buerstedde A chicken RAD51 homologue is expressed at high levels in lymphoid and reproductive organs Nucleic Acids Res 21 1993 1577 1580
28. T. Habu, T. Taki, A. West, Y. Nishimune, and T. Morita The mouse and human homologs of DMC1, the yeast meiosis-specific homologous recombination gene, have a common unique form of exon-skipped transcript in meiosis Nucleic Acids Res 24 1996 470 477
29. D.L. Pittman, J. Cobb, and K.J. Schimenti Meiotic prophase arrest with failure of chromosome synapsis in mice deficient for Dmc1, a germline-specific RecA homolog Mol Cell 1 1998 697 705
30. K. Yoshida, G. Kondoh, Y. Matsuda, T. Habu, Y. Nishimune, and T. Morita The mouse RecA-like gene Dmc1 is required for homologous chromosome synapsis during meiosis Mol Cell 1 1998 707 718
31. M. Tarsounas, T. Morita, R.E. Pearlman, and P.B. Moens RAD51 and DMC1 form mixed complexes associated with mouse meiotic chromosome cores and synaptonemal complexes J Cell Biol 147 1999 207 220
32. V.I. Klimyuk, and J.D. Jones AtDMC1, the Arabidopsis homologue of the yeast DMC1 gene: characterization, transposon-induced allelic variation and meiosis-associated expression Plant J 11 1997 1 14
33. L.K. Anderson, H.H. Offenberg, W.M. Verkuijlen, and C. Heyting RecA-like proteins are components of early meiotic nodules in lily Proc Natl Acad Sci USA 94 1997 6868 6873
34. M. Terasawa, A. Shinohara, Y. Hotta, H. Ogawa, and T. Ogawa Localization of RecA-like recombination proteins on chromosomes of the lily at various meiotic stages Genes Dev 9 1995 925 934
35. F. Couteau, F. Belzile, C. Horlow, O. Grandjean, D. Vezon, and M.P. Doutriaux Random chromosome segregation without meiotic arrest in both male and female meiocytes of a dmc1 mutant of Arabidopsis Plant Cell 11 1999 1623 1634
36. M.P. Doutriaux, F. Couteau, C. Bergounioux, and C. White Isolation and characterisation of the RAD51 and DMC1 homologs from Arabidopsis thaliana Mol Gen Genet 257 1998 283 291
37. A. Kathiresan, G.S. Khush, and J. Bennett Two rice DMC1 genes are differentially expressed during meiosis and during haploid and diploid mitosis Sex Plant Reprod 14 2002 257 267
38. M.G. Sehorn, S. Sigurdsson, W. Bussen, V.M. Unger, and P. Sung Human meiotic recombinase Dmc1 promotes ATP-dependent homologous DNA strand exchange Nature 429 2004 433 437
39. S.I. Passy, X. Yu, and Z. Li Human Dmc1 protein binds DNA as an octameric ring Proc Natl Acad Sci USA 96 1999 10684 10688
40. T. Kinebuchi, W. Kagawa, and R. Enomoto Structural basis for octameric ring formation and DNA interaction of the human homologous-pairing protein Dmc1 Mol Cell 14 2004 363 374
41. J.Y. Masson, A.A. Davies, and N. Hajibagheri The meiosis-specific recombinase hDmc1 forms ring structures and interacts with hRad51 EMBO J 18 1999 6552 6560
42. R. McCulloch, G. Rudenko, and P. Borst Gene conversions mediating antigenic variation in Trypanosoma brucei can occur in variant surface glycoprotein expression sites lacking 70-base-pair repeat sequences Mol Cell Biol 17 1997 833 843
43. H. Hirumi, and K. Hirumi Continuous cultivation of Trypanosoma brucei blood stream forms in a medium containing a low concentration of serum protein without feeder cell layers J Parasitol 75 1989 985 989
44. J.S. Bell, and R. McCulloch Mismatch repair regulates homologous recombination, but has little influence on antigenic variation, in Trypanosoma brucei J Biol Chem 278 2003 45182 45188
45. A. Gaud, M. Carrington, J. Deshusses, and D.R. Schaller Polymerase chain reaction-based gene disruption in Trypanosoma brucei Mol Biochem Parasitol 87 1997 113 115
46. S. Shen, G.K. Arhin, E. Ullu, and C. Tschudi In vivo epitope tagging of Trypanosoma brucei genes using a one step PCR-based strategy Mol Biochem Parasitol 113 2001 171 173
47. G. Rudenko, R. McCulloch, A. Dirks-Mulder, and P. Borst Telomere exchange can be an important mechanism of variant surface glycoprotein gene switching in Trypanosoma brucei Mol Biochem Parasitol 80 1996 65 75
48. C. Conway, R. McCulloch, M.L. Ginger, N.P. Robinson, A. Browitt, and J.D. Barry Ku is important for telomere maintenance, but not for differential expression of telomeric VSG genes, in African trypanosomes J Biol Chem 277 2002 21269 21277
49. N.P. Robinson, R. McCulloch, C. Conway, A. Browitt, and J.D. Barry Inactivation of Mre11 Does Not Affect VSG Gene Duplication Mediated by Homologous Recombination in Trypanosoma brucei J Biol Chem 277 2002 26185 26193
50. M. Berriman, E. Ghedin, and C. Hertz-Fowler The genome of the African trypanosome Trypanosoma brucei Science 309 2005 416 422
51. N.M. El Sayed, P.J. Myler, and G. Blandin Comparative genomics of trypanosomatid parasitic protozoa Science 309 2005 404 409
52. X. Shao, and N.V. Grishin Common fold in helix-hairpin-helix proteins Nucleic Acids Res 28 2000 2643 2650
53. D.S. Shin, L. Pellegrini, and D.S. Daniels Full-length archaeal Rad51 structure and mutants: mechanisms for RAD51 assembly and control by BRCA2 EMBO J 22 2003 4566 4576
54. L. Pellegrini, D.S. Yu, and T. Lo Insights into DNA recombination from the structure of a RAD51-BRCA2 complex Nature 420 2002 287 293
55. R.M. Story, D.K. Bishop, N. Kleckner, and T.A. Steitz Structural relationship of bacterial RecA proteins to recombination proteins from bacteriophage T4 and yeast Science 259 1993 1892 1896
56. W.E. Glaab, J.I. Risinger, A. Umar, J.C. Barrett, T.A. Kunkel, and K.R. Tindall Cellular resistance and hypermutability in mismatch repair-deficient human cancer cell lines following treatment with methyl methanesulfonate Mutat Res 398 1998 197 207
57. E. Kafer MMS sensitivity of all amino acid-requiring mutants in aspergillus and its suppression by mutations in a single gene Genetics 115 1987 671 676
58. M.L. Kuo, Y.W. Chou, Y.P. Chau, and T.S. Huang Resistance to apoptosis induced by alkylating agents in v-Ha-ras-transformed cells due to defect in p53 function Mol Carcinog 18 1997 221 231
59. M. Cross, R. Kieft, R. Sabatini, A. Dirks-Mulder, I. Chaves, and P. Borst J-binding protein increases the level and retention of the unusual base J in trypanosome DNA Mol Microbiol 46 2002 37 47
60. R. McCulloch, E. Vassella, P. Burton, M. Boshart, and J.D. Barry Transformation of Monomorphic and Pleomorphic Trypanosoma brucei Methods Mol Biol 2004 53 86
61. F. Njiokou, S.W. Nkinin, and P. Grebaut An isoenzyme survey of Trypanosoma brucei s.l. from the Central African subregion: population structure, taxonomic and epidemiological considerations Parasitology 128 2004 645 653
62. M. Tibayrenc, and F.J. Ayala Evolutionary genetics of Trypanosoma and Leishmania Microbes Infect 1 1999 465 472
63. M. Tibayrenc Population genetics of parasitic protozoa and other microorganisms Adv Parasitol 36 1995 47 115
64. A. MacLeod, A. Tweedie, S.C. Welburn, I. Maudlin, C.M. Turner, and A. Tait Minisatellite marker analysis of Trypanosoma brucei: reconciliation of clonal, panmictic, and epidemic population genetic structures Proc Natl Acad Sci USA 97 2000 13442 13447
65. A. MacLeod, A. Tait, and C.M. Turner The population genetics of Trypanosoma brucei and the origin of human infectivity Philos Trans R Soc Lond B Biol Sci 356 2001 1035 1044
66. A. MacLeod, C.M. Turner, and A. Tait A high level of mixed Trypanosoma brucei infections in tsetse flies detected by three hypervariable minisatellites Mol Biochem Parasitol 102 1999 237 248
67. W. Gibson Sex and evolution in trypanosomes Int J Parasitol 31 2001 643 647
68. W. Gibson, and J. Stevens Genetic exchange in the trypanosomatidae Adv Parasitol 43 1999 1 46
69. L. Jenni, S. Marti, and J. Schweizer Hybrid formation between African trypanosomes during cyclical transmission Nature 322 1986 173 175
70. W.C. Gibson Analysis of a genetic cross between Trypanosoma brucei rhodesiense and T. b. brucei Parasitology 99 Pt 3 1989 391 402
71. J. Sternberg, A. Tait, and S. Haley Gene exchange in African trypanosomes: characterisation of a new hybrid genotype Mol Biochem Parasitol 27 1988 191 200
72. J. Sternberg, C.M. Turner, J.M. Weils, L.C. Ranford-Cartwright, R.W. Le Page, and A. Tait Gene exchange in African trypanosomes: frequency and allelic segregation Mol Biochem Parasitol 34 1989 269 279
73. P. Paindavoine, F. Zampetti-Bosseler, and E. Pays Trypanosome hybrids generated in tsetse flies by nuclear fusion EMBO J 5 1986 3631 3636
74. J.M. Weils, T.D. Prospero, L. Jenni, and R.W. Le Page DNA contents and molecular karyotypes of hybrid Trypanosoma brucei Mol Biochem Parasitol 24 1987 103 116
75. M. Hope, A. MacLeod, and V. Leech Analysis of ploidy (in megabase chromosomes) in Trypanosoma brucei after genetic exchange Mol Biochem Parasitol 104 1999 1 9
76. A. MacLeod, A. Tweedie, and S. McLellan Allelic segregation and independent assortment in T. brucei crosses: proof that the genetic system is Mendelian and involves meiosis Mol Biochem Parasitol 2005
77. A. Tait, D. Masiga, and J. Ouma Genetic analysis of phenotype in Trypanosoma brucei: a classical approach to potentially complex traits Philos Trans R Soc Lond B Biol Sci 357 2002 89 99
78. C.M. Turner, J. Sternberg, N. Buchanan, E. Smith, G. Hide, and A. Tait Evidence that the mechanism of gene exchange in Trypanosoma brucei involves meiosis and syngamy Parasitology 101 Pt 3 1990 377 386
79. W. Gibson, and H. Whittington Genetic exchange in Trypanosoma brucei: selection of hybrid trypanosomes by introduction of genes conferring drug resistance Mol Biochem Parasitol 60 1993 19 26
80. N.M. El Sayed, E. Ghedin, and J. Song The sequence and analysis of Trypanosoma brucei chromosome II Nucleic Acids Res 31 2003 4856 4863
81. A. Tait, C.M. Turner, R.W. Le Page, and J.M. Weils Genetic evidence that metacyclic forms of Trypanosoma brucei are diploid Mol Biochem Parasitol 37 1989 247 255
82. S. Sato, T. Kobayashi, Y. Hotta, and S. Tabata Characterization of a mouse recA-like gene specifically expressed in testis DNA Res 2 1995 147 150
83. M.A. Ramesh, S.B. Malik, and J.M. Logsdon Jr. A phylogenomic inventory of meiotic genes; evidence for sex in Giardia and an early eukaryotic origin of meiosis Curr Biol 15 2005 185 191
84. N.M. El Sayed, P.J. Myler, and D.C. Bartholomeu The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease Science 309 2005 409 415
85. M.W. Gaunt, M. Yeo, and I.A. Frame Mechanism of genetic exchange in American trypanosomes Nature 421 2003 936 939
86. A.A. Belli, M.A. Miles, and J.M. Kelly A putative Leishmania panamensis/Leishmania braziliensis hybrid is a causative agent of human cutaneous leishmaniasis in Nicaragua Parasitology 109 Pt 4 1994 435 442
87. J.C. Dujardin, A.L. Banuls, and A. Llanos-Cuentas Putative Leishmania hybrids in the Eastern Andean valley of Huanuco, Peru Acta Trop 59 1995 293 307