Capturing the variant surface glycoprotein repertoire (the VSGnome) of Trypanosoma brucei Lister 427

Molecular and Biochemical Parasitology

Volumn 195, Issue 1, 2014, Pages 59-73

  Cross, George A M ^a   Kim, Hee Sook ^a   Wickstead, Bill ^b  

^a ROCKEFELLER UNIVERSITY   (United States)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Antigenic variation; Codon usage bias; Expression site; Metacyclic expression site; Minichromosome; Variant surface glycoprotein

Indexed keywords

VARIANT SURFACE GLYCOPROTEIN;

AFRICAN TRYPANOSOMIASIS; CHEMISTRY; CLASSIFICATION; GENETIC VARIABILITY; GENETICS; GENOME; HUMAN; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PARASITOLOGY; PHYLOGENY; TRYPANOSOMA BRUCEI BRUCEI;

BASE SEQUENCE; GENETIC VARIATION; GENOME, PROTOZOAN; HUMANS; MOLECULAR SEQUENCE DATA; PHYLOGENY; TRYPANOSOMA BRUCEI BRUCEI; TRYPANOSOMIASIS, AFRICAN; VARIANT SURFACE GLYCOPROTEINS, TRYPANOSOMA;

EID: 84905324241     PISSN: 01666851     EISSN: 18729428     Source Type: Journal    
DOI: 10.1016/j.molbiopara.2014.06.004     Document Type: Article

References (93)

1. E. Franke Ueber trypanosomentherapie Muenchener Medizinische Wochenschrift 42 1905 2059 2060
2. L.J. Morrison, L. Marcello, and R. Mcculloch Antigenic variation in the African trypanosome: molecular mechanisms and phenotypic complexity Cell Microbiol 11 2009 1724 1734
3. D. Horn, and R. Mcculloch Molecular mechanisms underlying the control of antigenic variation in African trypanosomes Curr Opin Microbiol 13 2010 700 705
4. J.D. Barry, J.P.J. Hall, and L. Plenderleith Genome hyperevolution and the success of a parasite Ann N Y Acad Sci 1267 2012 11 17
5. L.H.T. Van Der Ploeg, D. Valerio, T. De Lange, A. Bernards, P. Borst, and F.G. Grosveld An analysis of cosmid clones of nuclear DNA from Trypanosoma brucei shows that the genes for variant surface glycoproteins are clustered in the genome Nucl Acids Res 10 1982 5905 5923
6. S.E. Melville, V. Leech, C.S. Gerrard, A. Tait, and J.M. Blackwell The molecular karyotype of the megabase chromosomes of Trypanosoma brucei and the assignment of chromosome markers Mol Biochem Parasitol 94 1998 155 173 (Pubitemid 28377283)
7. S.E. Melville, V. Leech, M. Navarro, and G.A.M. Cross The molecular karyotype of the megabase chromosomes of Trypanosoma brucei stock 427 Mol Biochem Parasitol 111 2000 261 273 (Pubitemid 32121670)
8. S. Callejas, V. Leech, C. Reitter, and S. Melville Hemizygous subtelomeres of an African trypanosome chromosome may account for over 75% of chromosome length Genome Res 16 2006 1109 1118 (Pubitemid 44320398)
9. J.P.J. Hall, H. Wang, and J.D. Barry Mosaic VSGs and the scale of Trypanosoma brucei antigenic variation PLoS Pathogens 9 2013 e1003502
10. M. Berriman, E. Ghedin, C. Hertz-Fowler, G. Blandin, H. Renauld, and D.C. Bartholomeu et al. The genome of the African trypanosome Trypanosoma brucei Science 309 2005 416 422 (Pubitemid 40994676)
11. L.H.T. Van Der Ploeg, D.C. Schwartz, C.R. Cantor, and P. Borst Antigenic variation in Trypanosoma brucei analysed by electrophoretic separation of chromosome-sized DNA molecules Cell 37 1984 77 84 (Pubitemid 14079838)
12. L. Marcello, and J.D. Barry Analysis of the VSG gene silent archive in Trypanosoma brucei reveals that mosaic gene expression is prominent in antigenic variation and is favored by archive substructure Genome Res 17 2007 1344 1352 (Pubitemid 47360909)
13. N.G. Kolev, K. Ramey-Butler, G.A.M. Cross, E. Ullu, and C. Tschudi Developmental progression to infectivity in Trypanosoma brucei triggered by an RNA-binding protein Science 338 2012 1352 1353
14. H. Hirumi, and K. Hirumi Continuous cultivation of Trypanosoma brucei bloodstream forms in a medium containing a low concentration of serum protein without feeder cell layers J Parasitol 75 1989 985 989 (Pubitemid 20099178)
15. R. Brun, and M. Schonenberger Cultivation and in vitro cloning of procyclic culture forms of Trypanosoma brucei in a semi-defined medium Acta Trop 36 1979 289 292 (Pubitemid 10181444)
16. L. Peacock, V. Ferris, M. Bailey, and W. Gibson Fly transmission and mating of Trypanosoma brucei brucei strain 427 Mol Biochem Parasitol 160 2008 100 106
17. P. Serwer Gel electrophoresis with discontinuous rotation of the gel: an alternative to gel electrophoresis with changing direction of the electrical field Electrophoresis 8 1987 301 304
18. A.L. Delcher, D. Harmon, S. Kasif, O. White, and S.L. Salzberg Improved microbial gene identification with GLIMMER Nucl Acids Res 27 1999 4636 4641
19. A. Lukashin, and M. Borodovsky GeneMark.hmm: new solutions for gene finding Nucl Acids Res 26 1998 1107 1115 (Pubitemid 28291669)
20. X.J. Min, G. Butler, R. Storms, A. Tsang, and OrfPredictor: predicting protein-coding regions in EST-derived sequences Nucl Acids Res 33 2005 W677 W680
21. H. Nielsen, J. Engelbrecht, S. Brunak, and G. Von Heijne Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites Protein Eng 10 1997 1 6
22. H. Nielsen, and A. Krogh Prediction of signal peptides and signal anchors by a hidden Markov model Proc Int Conf Intell Syst Mol Biol 6 1998 122 130
23. O.R. Bininda-Emonds transAlign: using amino acids to facilitate the multiple alignment of protein-coding DNA sequences BMC Bioinformatics 6 2005 156
24. Z. Zhang, J. Li, X.Q. Zhao, J. Wang, G.K. Wong, and J. Yu KaKs-Calculator: calculating Ka and Ks through model selection and model averaging Genomics Proteomics Bioinformatics 4 2006 259 263
25. B. Langmead, C. Trapnell, M. Pop, and S.L. Salzberg Ultrafast and memory-efficient alignment of short DNA sequences to the human genome Genome Biol 10 2009 R25
26. C. Camacho, G. Coulouris, V. Avagyan, N. Ma, J. Papadopoulos, and J. Bealer et al. BLAST+: architecture and applications BMC Bioinformatics 10 2009 421
27. P. Borst, L.H.T. Van Der Ploeg, J.F.M. Van Hoek, J. Tas, and J. James On the DNA content and ploidy of trypanosomes Mol Biochem Parasitol 6 1982 13 23 (Pubitemid 12061370)
28. S.F. Altschul, T.L. Madden, A.A. Schaffer, J. Zhang, Z. Zhang, and W. Miller et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucl Acids Res 25 1997 3389 3402 (Pubitemid 27359211)
29. F. Bringaud, N. Biteau, S.E. Melville, S. Hez, N.M. El-Sayed, and V. Leech et al. A new, expressed multigene family containing a hot spot for insertion of retroelements is associated with polymorphic subtelomeric regions of Trypanosoma brucei Euk Cell 1 2002 137 151 (Pubitemid 36562357)
30. F. Bringaud, N. Biteau, E. Zuiderwijk, M. Berriman, N.M. El-Sayed, and E. Ghedin et al. The ingi and RIME non-LTR retrotransposons are not randomly distributed in the genome of Trypanosoma brucei Mol Biol Evol 21 2004 520 528 (Pubitemid 38339668)
31. J.H.J. Hoeijmakers, A.C.C. Frasch, A. Bernards, P. Borst, and G.A.M. Cross Novel expression-linked copies of the genes for variant surface antigens in trypanosomes Nature 284 1980 78 80 (Pubitemid 10098775)
32. T.P. Beals, and J.C. Boothroyd Genomic organization and context of a trypanosome variant surface glycoprotein gene family J Mol Biol 225 1992 961 971
33. T.P. Beals, and J.C. Boothroyd Sequence divergence among members of a trypanosome variant surface glycoprotein gene family J Mol Biol 225 1992 973 983
34. M.C. Field, and J.C. Boothroyd Sequence divergence in a family of variant surface glycoprotein genes from trypanosomes: coding region hypervariability and downstream recombinogenic repeats J Mol Evol 42 1996 500 511 (Pubitemid 26197140)
35. E. Wirtz, S. Leal, C. Ochatt, and G.A.M. Cross A tightly regulated inducible expression system for dominant negative approaches in Trypanosoma brucei Mol Biochem Parasitol 99 1999 89 101 (Pubitemid 29127189)
36. J.J. Doyle, H. Hirumi, K. Hirumi, E.N. Lupton, and G.A.M. Cross Antigenic variation in clones of animal-infective Trypanosoma brucei derived and maintained in vitro Parasitology 80 1980 359 369 (Pubitemid 10019837)
37. R.F. Aline Jr., G. Macdonald, E. Brown, J. Allison, P. Myler, and V. Rothwell et al. (TAA)n within sequences flanking several intrachromosomal variant surface glycoprotein genes in Trypanosoma brucei Nucl Acids Res 13 1985 3161 3177
38. H.K. Majumder, J.C. Boothroyd, and H. Weber Homologous 3′-terminal regions of mRNAs for surface antigens of different antigenic variants of Trypanosoma brucei Nucl Acids Res 9 1981 4745 4753 (Pubitemid 12237224)
39. M. Carrington, N. Miller, M. Blum, I. Roditi, D. Wiley, and M.J. Turner Variant specific glycoprotein of Trypanosoma brucei consists of two domains each having an independently conserved pattern of cysteine residues J Mol Biol 221 1991 823 835 (Pubitemid 121003422)
40. L. Marcello, S. Menon, P. Ward, J.M. Wilkes, N.G. Jones, and M. Carrington et al. VSGdb: a database for trypanosome variant surface glycoproteins, a large and diverse family of coiled coil proteins BMC Bioinformatics 8 2007 143
41. G.A.M. Cross, and Identification purification and properties of clone-specific glycoprotein antigens constituting the surface coat of Trypanosoma brucei Parasitology 71 1975 393 417
42. D. Horn Codon usage suggests that translational selection has a major impact on protein expression in trypanosomatids BMC Genomics 9 2008 2
43. B. Wickstead, and K. Gull Dyneins across eukaryotes: a comparative genomic analysis Traffic 8 2007 1708 1721 (Pubitemid 350066684)
44. A.P. Jackson, A. Berry, M. Aslett, H.C. Allison, P. Burton, and J. Vavrova-Anderson et al. Antigenic diversity is generated by distinct evolutionary mechanisms in African trypanosome species Proc Natl Acad Sci USA 109 2012 3416 3421
45. J.L. Weirather, M.E. Wilson, and J.E. Donelson Mapping of VSG similarities in Trypanosoma brucei Mol Biochem Parasitol 181 2012 141 152
46. C. Hertz-Fowler, L.M. Figueiredo, M.A. Quail, M. Becker, A. Jackson, and N. Bason et al. Telomeric expression sites are highly conserved in Trypanosoma brucei PLoS ONE 3 2008 e3527
47. M.J. Lenardo, A.C. Rice-Ficht, G. Kelly, K.M. Esser, and J.E. Donelson Characterization of the genes specifying two metacyclic variable antigen types in Trypanosoma brucei rhodesiense Proc Natl Acad Sci USA 81 1984 6642 6646 (Pubitemid 15220975)
48. K.R. Matthews, P.G. Shiels, S.V. Graham, C. Cowan, and J.D. Barry Duplicative activation mechanisms of two trypanosome telomeric VSG genes with structurally simple 5′ flanks Nucl Acids Res 18 1990 7219 7227 (Pubitemid 120006021)
49. J.D. Barry, S.V. Graham, M. Fotheringham, V.S. Graham, K. Kobryn, and B. Wymer VSG gene control and infectivity strategy of metacyclic stage Trypanosoma brucei Mol Biochem Parasitol 91 1998 93 105 (Pubitemid 28242509)
50. M. Pedram, and J.E. Donelson The anatomy and transcription of a monocistronic expression site for a metacyclic variant surface glycoprotein gene in Trypanosoma brucei J Biol Chem 274 1999 16876 16883
51. M. Mcandrew, S. Graham, C. Hartmann, and C. Clayton Testing promoter activity in the trypanosome genome: isolation of a metacyclic-type VSG promoter and unexpected insights into RNA polymerase II transcription Exp Parasitol 90 1998 65 76 (Pubitemid 28406688)
52. F. Bringaud, N. Biteau, J.E. Donelson, and T. Baltz Conservation of metacyclic variant surface glycoprotein expression sites among different trypanosome isolates Mol Biochem Parasitol 113 2001 67 78 (Pubitemid 32209283)
53. O. Dreesen, B. Li, and G.A.M. Cross Telomere structure and function in trypanosomes: a proposal Nat Rev Microbiol 5 2007 70 75 (Pubitemid 44942305)
54. G.A. Hovel-Miner, C.E. Boothroyd, M. Mugnier, O. Dreesen, G.A.M. Cross, and F.N. Papavasiliou Telomere length affects the frequency and mechanism of antigenic variation in Trypanosoma brucei PLoS Pathogens 8 2012 e1002900
55. O. Dreesen, and G.A.M. Cross Telomerase-independent stabilization of short telomeres in Trypanosoma brucei Mol Cell Biol 26 2006 4911 4919 (Pubitemid 43955808)
56. B. Wickstead, K. Ersfeld, and K. Gull The small chromosomes of Trypanosoma brucei involved in antigenic variation are constructed around repetitive palindromes Genome Res 14 2004 1014 1024 (Pubitemid 38811537)
57. W.C. Gibson, and P. Borst Size-fractionation of the small chromosomes of Trypanozoon and Nannomonas trypanosomes by pulsed field gradient gel electrophoresis Mol Biochem Parasitol 18 1986 127 141
58. B. Dero, F. Zampetti-Bosseler, E. Pays, and M. Steinert The genome and the antigen gene repertoire of Trypanosoma brucei gambiense are smaller than those of T. b. brucei Mol Biochem Parasitol 26 1987 247 256
59. G.D. Kanmogne, M. Bailey, and W.C. Gibson Wide variation in DNA content among isolates of Trypanosoma brucei ssp Acta Trop 63 1997 75 87 (Pubitemid 27148038)
60. O. Dreesen, and G.A.M. Cross Consequences of telomere shortening of an active VSG expression site in telomerase-deficient Trypanosoma brucei Eukaryot Cell 5 2006 2114 2119 (Pubitemid 44956822)
61. J.C.B.M. Zomerdijk, R. Kieft, and P. Borst A ribosomal RNA gene promoter at the telomere of a mini-chromosome in Trypanosoma brucei Nucleic Acids Res 20 1992 2725 2734
62. J.T. Robinson, H. Thorvaldsdottir, W. Winckler, M. Guttman, E.S. Lander, and G. Getz et al. Integrative genomics viewer Nat Biotechnol 29 2011 24 26
63. H. Thorvaldsdóttir, J.T. Robinson, and J.P. Mesirov Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration Brief Bioinform 2012 10.1093/bib/bbs017
64. B. Wickstead, K. Ersfeld, and K. Gull The mitotic stability of the minichromosomes of Trypanosoma brucei Mol Biochem Parasitol 132 2003 97 100 (Pubitemid 37352906)
65. M.M. Klingbeil, S.A. Motyka, and P.T. Englund Multiple mitochondrial DNA polymerases in Trypanosoma brucei Mol Cell 10 2002 175 186 (Pubitemid 34876571)
66. L. Glover, S. Alsford, and D. Horn DNA break site at fragile subtelomeres determines probability and mechanism of antigenic variation in African trypanosomes PLoS Pathogens 9 2013 e1003260
67. M. Zhou, J. Guo, J. Cha, M. Chae, S. Chen, and J.M. Barral et al. Non-optimal codon usage affects expression, structure and function of clock protein FRQ Nature 495 2013 111 115
68. D.B. Goodman, G.M. Church, and S. Kosuri Causes and effects of N-terminal codon bias in bacterial genes Science 342 2013 475 479
69. A.Y.C. Liu, L.H.T. Van Der Ploeg, F.A.M. Rijsewijk, and P. Borst The transposition unit of VSG gene 118 of Trypanosoma brucei: presence of repeated elements at its border and absence of promoter associated sequences J Mol Biol 167 1983 57 75 (Pubitemid 13008362)
70. K.P. Davies, V.B. Carruthers, and G.A.M. Cross Manipulation of the VSG co-transposed region increases expression-site switching in Trypanosoma brucei Mol Biochem Parasitol 86 1997 163 177 (Pubitemid 27245178)
71. R.F. Aline, J.K. Scholler, and K. Stuart Transcripts from the co-transposed segment of variant surface glycoprotein genes are in Trypanosoma brucei polyribosomes Mol Biochem Parasitol 32 1989 169 178
72. A. Bernards, L.H.T. Van Der Ploeg, A.C.C. Frasch, P. Borst, J.C. Boothroyd, and S. Coleman et al. Activation of trypanosome surface glycoprotein genes involves a gene duplication-transposition leading to an altered 3′ end Cell 27 1981 497 505 (Pubitemid 12200786)
73. T.N. Siegel, K.S.W. Tan, and G.A.M. Cross A systematic study of sequence motifs for RNA trans-splicing in Trypanosoma brucei Mol Cell Biol 25 2005 9586 9594 (Pubitemid 41507857)
74. G.S. Lamont, R.S. Tucker, and G.A.M. Cross Analysis of antigen switching rates in Trypanosoma brucei Parasitology 92 1986 355 367 (Pubitemid 16112677)
75. D. Horn, and G.A.M. Cross Analysis of Trypanosoma brucei VSG expression site switching in vitro Mol Biochem Parasitol 84 1997 189 201 (Pubitemid 27092982)
76. C.E. Boothroyd, O. Dreesen, T. Leonova, K.I. Ly, L.M. Figueiredo, and G.A.M. Cross et al. A yeast-endonuclease-generated DNA break induces antigenic switching in Trypanosoma brucei Nature 459 2009 278 281
77. R.L. Barnes, and R. Mcculloch Trypanosoma brucei homologous recombination is dependent on substrate length and homology, though displays a differential dependence on mismatch repair as substrate length decreases Nucl Acids Res 35 2007 3478 3493 (Pubitemid 47073608)
78. L. Glover, R. Mcculloch, and D. Horn Sequence homology and microhomology dominate chromosomal double-strand break repair in African trypanosomes Nucl Acids Res 36 2008 2608 2618 (Pubitemid 351659575)
79. L. Glover, J. Jun, and D. Horn Microhomology-mediated deletion and gene conversion in African trypanosomes Nucl Acids Res 39 2011 1372 1380
80. Y. Lu, T. Hall, L.S. Gay, and J.E. Donelson Point mutations are associated with a gene duplication leading to the bloodstream reexpression of a trypanosome metacyclic VSG Cell 72 1993 397 406 (Pubitemid 23059409)
81. Y. Lu, C.M. Alarcon, T. Hall, L.V. Reddy, and J.E. Donelson A strand bias occurs in point mutations associated with variant surface glycoprotein gene conversion in Trypanosoma rhodesiense Mol Cell Biol 14 1994 3971 3980 (Pubitemid 24160803)
82. N.G. Kolev, J.B. Franklin, S. Carmi, H.F. Shi, S. Michaeli, and C. Tschudi The transcriptome of the human pathogen Trypanosoma brucei at single-nucleotide resolution PLoS Pathogens 6 2010 e1001090
83. N.B. Murphy, A. Pays, P. Tebabi, H. Coquelet, M. Gyaux, and M. Steinert et al. Trypanosoma brucei repeated element with unusual structural and transcriptional properties J Mol Biol 195 1987 855 871
84. D.J. Lacount, N.M. El-Sayed, S. Kaul, D. Wanless, C.M. Turner, and J.E. Donelson Analysis of a donor gene region for a variant surface glycoprotein and its expression site in African trypanosomes Nucl Acids Res 29 2001 2012 2019 (Pubitemid 32472070)
85. S.V. Graham, S. Terry, and J.D. Barry A structural and transcription pattern for variant surface glycoprotein gene expression sites used in metacyclic stage Trypanosoma brucei Mol Biochem Parasitol 103 1999 141 154 (Pubitemid 29469769)
86. M.L. Ginger, P.A. Blundell, A.M. Lewis, A. Browitt, A. Gunzl, and J.D. Barry Ex vivo and in vitro identification of a consensus promoter for VSG genes expressed by metacyclic-stage trypanosomes in the tsetse fly Euk Cell 1 2002 1000 1009 (Pubitemid 36557720)
87. C.M. Alarcon, H.J. Son, T. Hall, and J.E. Donelson A monocistronic transcript for a trypanosome variant surface glycoprotein Mol Cell Biol 14 1994 5579 5591 (Pubitemid 24235986)
88. Y.L. Nagoshi, C.M. Alarcon, and J.E. Donelson The putative promoter for a metacyclic VSG gene in African trypanosomes Mol Biochem Parasitol 72 1995 33 45
89. K.S. Kim, and J.E. Donelson Co-duplication of a variant surface glycoprotein gene and its promoter to an expression site in African trypanosomes J Biol Chem 272 1997 24637 24645 (Pubitemid 27418681)
90. L. Vanhamme, A. Pays, P. Tebabi, S. Alexandre, and E. Pays Specific binding of proteins to the noncoding strand of a crucial element of the variant surface glycoprotein, procyclin, and ribosomal promoters of Trypanosoma brucei Mol Cell Biol 15 1995 5598 5606
91. J. Brandenburg, B. Schimanski, E. Nogoceke, T.N. Nguyen, J.C. Padovan, and B.T. Chait et al. Multifunctional class I transcription in Trypanosoma brucei depends on a novel protein complex EMBO J 26 2007 4856 4866 (Pubitemid 350191303)
92. D.R. Sherman, L. Janz, M. Hug, and C. Clayton Anatomy of the parp gene promoter of Trypanosoma brucei EMBO J 10 1991 3379 3386 (Pubitemid 21905363)
93. L. Janz, C. Clayton, and P.A.R.P. The and rRNA promoters of Trypanosoma brucei are composed of dissimilar sequence elements that are functionally interchangeable Mol Cell Biol 14 1994 5804 5811 (Pubitemid 24264409)