RAP1 Is Essential for Silencing Telomeric Variant Surface Glycoprotein Genes in Trypanosoma brucei

Cell

Volumn 137, Issue 1, 2009, Pages 99-109

  Yang, Xiaofeng ^a,b   Figueiredo, Luisa M ^c   Espinal, Amin ^c   Okubo, Eiji ^c   Li, Bibo ^a,c  

^a CLEVELAND STATE UNIVERSITY   (United States)

^b MEDICAL SCHOOL OF XI AN JIAOTONG UNIVERSITY   (China)

^c ROCKEFELLER UNIVERSITY   (United States)

Author keywords

CELLBIO; DNA; HUMDISEASE

Indexed keywords

RAP1 PROTEIN; VARIANT SURFACE GLYCOPROTEIN;

ARTICLE; COMPLEX FORMATION; EPIGENETICS; GENE CONTROL; GENE DISRUPTION; GENE IDENTIFICATION; GENE LOCATION; GENE SILENCING; GENETIC VARIABILITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE VIRULENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TELOMERE; TRYPANOSOMA BRUCEI;

MAMMALIA; TRYPANOSOMA BRUCEI;

EID: 63049115947     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2009.01.037     Document Type: Article

References (68)

1. Alsford S., Kawahara T., Glover L., and Horn D. Tagging a T. brucei RRNA locus improves stable transfection efficiency and circumvents inducible expression position effects. Mol. Biochem. Parasitol. 144 (2005) 142-148
2. Alsford S., Kawahara T., Isamah C., and Horn D. A sirtuin in the African trypanosome is involved in both DNA repair and telomeric gene silencing but is not required for antigenic variation. Mol. Microbiol. 63 (2007) 724-736
3. Alsford S., Wickstead B., Ersfeld K., and Gull K. Diversity and dynamics of the minichromosomal karyotype in Trypanosoma brucei. Mol. Biochem. Parasitol. 113 (2001) 79-88
4. Barry J.D., and McCulloch R. Antigenic variation in trypanosomes: enhanced phenotypic variation in a eukaryotic parasite. Adv. Parasitol. 49 (2001) 1-70
5. Bastin P., Bagherzadeh A., Matthews K.R., and Gull K. A novel epitope tag system to study protein targeting and organelle biogenesis in Trypanosoma brucei. Mol. Biochem. Parasitol. 77 (1996) 235-239
6. Berriman M., Ghedin E., Hertz-Fowler C., Blandin G., Renauld H., Bartholomeu D.C., Lennard N.J., Caler E., Hamlin N.E., Haas B., et al. The genome of the African trypanosome Trypanosoma brucei. Science 309 (2005) 416-422
7. Bork P., Hofmann K., Bucher P., Neuwald A.F., Altschul S.F., and Koonin E.V. A superfamily of conserved domains in DNA damage-responsive cell cycle checkpoint proteins. FASEB J. 11 (1997) 68-76
8. Boulton S.J., and Jackson S.P. Components of the Ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing. EMBO J. 17 (1998) 1819-1828
9. Broccoli D., Smogorzewska A., Chong L., and de Lange T. Human telomeres contain two distinct Myb-related proteins, TRF1 and TRF2. Nat. Genet. 17 (1997) 231-235
10. Callebaut I., and Mornon J.P. From BRCA1 to RAP1: a widespread BRCT module closely associated with DNA repair. FEBS Lett. 400 (1997) 25-30
11. Chaves I., Rudenko G., Dirks-Mulder A., Cross M., and Borst P. Control of variant surface glycoprotein gene-expression sites in Trypanosoma brucei. EMBO J. 18 (1999) 4846-4855
12. Conway C., McCulloch R., Ginger M.L., Robinson N.P., Browitt A., and Barry J.D. 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
13. de Lange T. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 19 (2005) 2100-2110
14. de Lange T., and Borst P. Genomic environment of the expression-linked extra copies of genes for surface antigens of Trypanosoma brucei resembles the end of a chromosome. Nature 299 (1982) 451-453
15. Dreesen O., Li B., and Cross G.A.M. Telomere structure and function in trypanosomes: a proposal. Nat. Rev. Microbiol. 5 (2007) 70-75
16. Dreesen O., Li B., and Cross G.A.M. Telomere structure and shortening in telomerase-deficient Trypanosoma brucei. Nucleic Acids Res. 33 (2005) 4536-4543
17. Duraisingh M.T., Voss T.S., Marty A.J., Duffy M.F., Good R.T., Thompson J.K., Freitas-Junior L.H., Scherf A., Crabb B.S., and Cowman A.F. Heterochromatin silencing and locus repositioning linked to regulation of virulence genes in Plasmodium falciparum. Cell 121 (2005) 13-24
18. Evans S.K., Sistrunk M.L., Nugent C.I., and Lundblad V. Telomerase, Ku, and telomeric silencing in Saccharomyces cerevisiae. Chromosoma 107 (1998) 352-358
19. Figueiredo L.M., Janzen C.J., and Cross G.A.M. A histone methyltransferase modulates antigenic variation in African trypanosomes. PLoS Biol. 6 (2008) e161
20. Freitas-Junior L.H., Hernandez-Rivas R., Ralph S.A., Montiel-Condado D., Ruvalcaba-Salazar O.K., Rojas-Meza A.P., Mâncio-Silva L., Leal-Silvestre R.J., Gontijo A.M., Shorte S., and Scherf A. Telomeric heterochromatin propagation and histone acetylation control mutually exclusive expression of antigenic variation genes in malaria parasites. Cell 121 (2005) 25-36
21. Gao Q., Reynolds G.E., Innes L., Pedram M., Jones E., Junabi M., Gao D.W., Ricoul M., Sabatier L., Van Brocklin H., et al. Telomeric transgenes are silenced in adult mouse tissues and embryo fibroblasts, but are expressed in embryonic stem cells. Stem Cells 25 (2007) 3085-3092
22. Gasser S.M., and Cockell M.M. The molecular biology of the SIR proteins. Gene 279 (2001) 1-16
23. Glover L., Alsford S., Beattie C., and Horn D. Deletion of a trypanosome telomere leads to loss of silencing and progressive loss of terminal DNA in the absence of cell cycle arrest. Nucleic Acids Res. 35 (2007) 872-880
24. Glover L., and Horn D. Repression of polymerase I-mediated gene expression at Trypanosoma brucei telomeres. EMBO Rep. 7 (2006) 93-99
25. Gommers-Ampt J., Lutgerink J., and Borst P. A novel DNA nucleotide in Trypanosoma brucei only present in the mammalian phase of the life-cycle. Nucleic Acids Res. 19 (1991) 1745-1751
26. Gottschling D.E., Aparicio O.M., Billington B.L., and Zakian V.A. Position effect at S. cerevisiae telomeres: reversible repression of pol II transcription. Cell 63 (1990) 751-762
27. Grunstein M. Molecular model for telomeric heterochromatin in yeast. Curr. Opin. Cell Biol. 9 (1997) 383-387
28. Gunzl A., Bruderer T., Laufer G., Schimanski B., Tu L.C., Chung H.M., Lee P.T., and Lee M.G. RNA polymerase I transcribes procyclin genes and variant surface glycoprotein gene expression sites in Trypanosoma brucei. Eukaryot. Cell 2 (2003) 542-551
29. Hanaoka S., Nagadoi A., Yoshimura S., Aimoto S., Li B., de Lange T., and Nishimura Y. NMR structure of the hRap1 Myb motif reveals a canonical three-helix bundle lacking the positive surface charge typical of Myb DNA-binding domains. J. Mol. Biol. 312 (2001) 167-175
30. Hertz-Fowler C., Figueiredo L.M., Quail M.A., Becker M., Jackson A., Bason N., Brooks K., Churcher C., Fahkro S., and Goodhead I. Telomeric expression sites are highly conserved in Trypanosoma brucei. PLoS ONE 3 (2008) e3527
31. Hoek M., Zanders T., and Cross G.A.M. Trypanosoma brucei expression-site-associated-gene 8 protein interacts with a Pumilio family protein. Mol. Biochem. Parasitol. 120 (2002) 269-283
32. Horn D., and Barry J.D. The central roles of telomeres and subtelomeres in antigenic variation in African trypanosomes. Chromosome Res. 13 (2005) 525-533
33. Horn D., and Cross G.A.M. A developmentally regulated position effect at a telomeric locus in Trypanosoma brucei. Cell 83 (1995) 555-561
34. Horn D., and Cross G.A.M. Position-dependent and promoter-specific regulation of gene expression in Trypanosoma brucei. EMBO J. 16 (1997) 7422-7431
35. Hughes K., Wand M., Foulston L., Young R., Harley K., Terry S., Ersfeld K., and Rudenko G. A novel ISWI is involved in VSG expression site downregulation in African trypanosomes. EMBO J. 26 (2007) 2400-2410
36. Janzen C.J., Lander F., Dreesen O., and Cross G.A.M. Telomere length regulation and transcriptional silencing in KU80-deficient Trypanosoma brucei. Nucleic Acids Res. 32 (2004) 6575-6584
37. Kanoh J., and Ishikawa F. spRap1 and spRif1, recruited to telomeres by Taz1, are essential for telomere function in fission yeast. Curr. Biol. 11 (2001) 1624-1630
38. Konig P., Giraldo R., Chapman L., and Rhodes D. The crystal structure of the DNA-binding domain of yeast RAP1 in complex with telomeric DNA. Cell 85 (1996) 125-136
39. Konig P., and Rhodes D. Recognition of telomeric DNA. Trends Biochem. Sci. 22 (1997) 43-47
40. Kyte J., and Doolittle R.F. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157 (1982) 105-132
41. Landeira D., and Navarro M. Nuclear repositioning of the VSG promoter during developmental silencing in Trypanosoma brucei. J. Cell Biol. 176 (2007) 133-139
42. Li B., Espinal A., and Cross G.A.M. Trypanosome telomeres are protected by a homologue of mammalian TRF2. Mol. Cell. Biol. 25 (2005) 5011-5021
43. Li B., Oestreich S., and de Lange T. Identification of human Rap1: implications for telomere evolution. Cell 101 (2000) 471-483
44. Li B., and Lustig A.J. A novel mechanism for telomere size control in Saccharomyces cerevisiae. Genes Dev. 10 (1996) 1310-1326
45. Lowell J.E., and Cross G.A.M. A variant histone H3 is enriched at telomeres in Trypanosoma brucei. J. Cell Sci. 117 (2004) 5937-5947
46. Marcello L., and Barry J.D. 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
47. Michishita E., McCord R.A., Berber E., Kioi M., Padilla-Nash H., Damian M., Cheung P., Kusumoto R., Kawahara T.L., and Barrett J.C. SIRT6 is a histone H3 lysine 9 deacetylase that modulates telomeric chromatin. Nature 452 (2008) 492-496
48. Mishra K., and Shore D. Yeast Ku protein plays a direct role in telomeric silencing and counteracts inhibition by Rif proteins. Curr. Biol. 9 (1999) 1123-1126
49. Navarro M., and Cross G.A.M. DNA rearrangements associated with multiple consecutive directed antigenic switches in Trypanosoma brucei. Mol. Cell. Biol. 16 (1996) 3615-3625
50. Navarro M., and Gull K. A pol I transcriptional body associated with VSG mono-allelic expression in Trypanosoma brucei. Nature 414 (2001) 759-763
51. Ogata K., Morikawa S., Nakamura H., Sekikawa A., Inoue T., Kanai H., Sarai A., Ishii S., and Nishimura Y. Solution structure of a specific DNA complex of the Myb DNA-binding domain with cooperative recognition helices. Cell 79 (1994) 639-648
52. Park M.J., Jang Y.K., Choi E.S., Kim H.S., and Park S.D. Fission yeast Rap1 homolog is a telomere-specific silencing factor and interacts with Taz1p. Mol. Cells 13 (2002) 327-333
53. Pays E., Vanhamme L., and Perez-Morga D. Antigenic variation in Trypanosoma brucei: facts, challenges and mysteries. Curr. Opin. Microbiol. 7 (2004) 369-374
54. Pedram M., Sprung C.N., Gao Q., Lo A.W., Reynolds G.E., and Murnane J.P. Telomere position effect and silencing of transgenes near telomeres in the mouse. Mol. Cell. Biol. 26 (2006) 1865-1878
55. Pina B., Fernandez-Larrea J., Garcia-Reyero N., and Idrissi F.Z. The different (sur)faces of Rap1p. Mol. Genet. Genomics 268 (2003) 791-798
56. Pryde F.E., and Louis E.J. Limitations of silencing at native yeast telomeres. EMBO J. 18 (1999) 2538-2550
57. Renauld H., Aparicio O.M., Zierath P.D., Billington B.L., Chhablani S.K., and Gottschling D.E. Silent domains are assembled continuously from the telomere and are defined by promoter distance and strength, and by SIR3 dosage. Genes Dev. 7 (1993) 1133-1145
58. Sheader K., Vaughan S., Minchin J., Hughes K., Gull K., and Rudenko G. Variant surface glycoprotein RNA interference triggers a precytokinesis cell cycle arrest in African trypanosomes. Proc. Natl. Acad. Sci. USA 102 (2005) 8716-8721
59. Shore D. RAP1: a protean regulator in yeast. Trends Genet. 10 (1994) 408-412
60. Siegel T.N., Tan K.S., and Cross G.A.M. Systematic study of sequence motifs for RNA trans splicing in Trypanosoma brucei. Mol. Cell. Biol. 25 (2005) 9586-9594
61. Teixeira M.T., and Gilson E. Telomere maintenance, function and evolution: the yeast paradigm. Chromosome Res. 13 (2005) 535-548
62. van der Ploeg L.H.T., Liu A.Y.C., and Borst P. Structure of the growing telomeres of trypanosomes. Cell 36 (1984) 459-468
63. van Leeuwen F., Wijsman E.R., Kuyl-Yeheskiely E., van der Marel G.A., van Boom J.H., and Borst P. The telomeric GGGTAA repeats of Trypanosoma brucei contain the hypermodified base J in both strands. Nucleic Acids Res. 24 (1996) 2476-2482
64. Vanhamme L., Poelvoorde P., Pays A., Tebabi P., Van Xong H., and Pays E. Differential RNA elongation controls the variant surface glycoprotein gene expression sites of Trypanosoma brucei. Mol. Microbiol. 36 (2000) 328-340
65. Vojtek A.B., Hollenberg S.M., and Cooper J.A. Mammalian Ras interacts directly with the serine/threonine kinase Raf. Cell 74 (1993) 205-214
66. Wang R.C., Smogorzewska A., and de Lange T. Homologous recombination generates T-loop-sized deletions at human telomeres. Cell 119 (2004) 355-368
67. Wirtz E., Leal S., Ochatt C., and Cross G.A.M. A tightly regulated inducible expression system for dominant negative approaches in Trypanosoma brucei. Mol. Biochem. Parasitol. 99 (1999) 89-101
68. Zhang X., Morera S., Bates P.A., Whitehead P.C., Coffer A.I., Hainbucher K., Nash R.A., Sternberg M.J., Lindahl T., and Freemont P.S. Structure of an XRCC1 BRCT domain: a new protein-protein interaction module. EMBO J. 17 (1998) 6404-6411