Home LiteratureArticle Details
PMID: 19846312 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Review

Plasticity of telomere maintenance mechanisms in yeast.

Trends in biochemical sciences ·Vol. 35 ·No. 1 ·2010-01-00 ·Pages 8-17

Lue NF

Abstract

Telomeres, the nucleoprotein structures located at linear eukaryotic chromosomal termini, are essential for chromosome stability and are maintained by the special reverse transcriptase named telomerase. In the Saccharomycotina subphylum of budding yeast, telomere repeat sequences and binding factors, as well as telomerase components, are exceptionally diverse and distinct from those found in other eukaryotes. In this survey, I report a comparative analysis of the domain structures of telomere and telomerase-related factors made possible by the recent sequencing of multiple yeast genomes. This analysis revealed both conserved and variable aspects of telomere maintenance. Based on these findings, I propose a plausible series of evolutionary events in budding yeast to account for its exceptional telomere structural divergence.

MeSH Terms
Chromosomal Proteins, Non-Histone/metabolism Saccharomycetales/classification,cytology,genetics,metabolism Telomerase/metabolism Telomere/chemistry,metabolism
Chemicals
Chromosomal Proteins, Non-Histone Telomerase
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Lue Neal F
Department of Microbiology and Immunology, Weill Medical College of Cornell University, New York, NY 10065, USA. nflue@med.cornell.edu
References (85)
85 references, click to expand
  1. Telomerase: what are the Est proteins doing?
    Curr Opin Cell Biol. 2003 Jun;15(3):275-80 PMID: 12787768
  2. Beginning to understand the end of the chromosome.
    Cell. 2004 Jan 23;116(2):273-9 PMID: 14744437
  3. Identification of the single-strand telomeric DNA binding domain of the Saccharomyces cerevisiae Cdc13 protein.
    Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6457-62 PMID: 10841551
  4. Saccharomyces cerevisiae RAP1 binds to telomeric sequences with spatial flexibility.
    Nucleic Acids Res. 2000 Jun 15;28(12):2292-301 PMID: 10871358
  5. The origin of protein interactions and allostery in colocalization.
    Nature. 2007 Dec 13;450(7172):983-90 PMID: 18075577
  6. Subtelomeric proteins negatively regulate telomere elongation in budding yeast.
    EMBO J. 2006 Feb 22;25(4):846-56 PMID: 16467854
  7. Pot1, the putative telomere end-binding protein in fission yeast and humans.
    Science. 2001 May 11;292(5519):1171-5 PMID: 11349150
  8. Structural and functional studies of the Rap1 C-terminus reveal novel separation-of-function mutants.
    J Mol Biol. 2008 Jul 11;380(3):520-31 PMID: 18538788
  9. An emerging consensus for telomerase RNA structure.
    Proc Natl Acad Sci U S A. 2004 Oct 12;101(41):14683-4 PMID: 15466703
  10. [Principle of marginotomy in template synthesis of polynucleotides].
    Dokl Akad Nauk SSSR. 1971;201(6):1496-9 PMID: 5158754
  11. SMG7 is a 14-3-3-like adaptor in the nonsense-mediated mRNA decay pathway.
    Mol Cell. 2005 Feb 18;17(4):537-47 PMID: 15721257
  12. The crystal structure of the DNA-binding domain of yeast RAP1 in complex with telomeric DNA.
    Cell. 1996 Apr 5;85(1):125-36 PMID: 8620531
  13. Multiple interactions in Sir protein recruitment by Rap1p at silencers and telomeres in yeast.
    Mol Cell Biol. 2001 Dec;21(23):8082-94 PMID: 11689698
  14. PTOP interacts with POT1 and regulates its localization to telomeres.
    Nat Cell Biol. 2004 Jul;6(7):673-80 PMID: 15181449
  15. Conserved functions of yeast genes support the duplication, degeneration and complementation model for gene duplication.
    Genetics. 2005 Dec;171(4):1455-61 PMID: 15965245
  16. A fungal phylogeny based on 42 complete genomes derived from supertree and combined gene analysis.
    BMC Evol Biol. 2006 Nov 22;6:99 PMID: 17121679
  17. Telomere protection by mammalian Pot1 requires interaction with Tpp1.
    Nat Struct Mol Biol. 2007 Aug;14(8):754-61 PMID: 17632522
  18. A human homolog of yeast Est1 associates with telomerase and uncaps chromosome ends when overexpressed.
    Curr Biol. 2003 Apr 1;13(7):568-74 PMID: 12676087
  19. From RPA to BRCA2: lessons from single-stranded DNA binding by the OB-fold.
    Curr Opin Struct Biol. 2004 Feb;14(1):36-42 PMID: 15102447
  20. The origin recognition complex localizes to telomere repeats and prevents telomere-circle formation.
    Curr Biol. 2007 Nov 20;17(22):1989-95 PMID: 18006317
  21. The structure and function of telomerase reverse transcriptase.
    Annu Rev Biochem. 2006;75:493-517 PMID: 16756500
  22. Proteins that bind to double-stranded regions of telomeric DNA.
    Trends Cell Biol. 1997 Aug;7(8):317-24 PMID: 17708967
  23. A RAP1/TRF2 complex inhibits nonhomologous end-joining at human telomeric DNA ends.
    Mol Cell. 2007 May 11;26(3):323-34 PMID: 17499040
  24. The Saccharomyces telomere-binding protein Cdc13p interacts with both the catalytic subunit of DNA polymerase alpha and the telomerase-associated est1 protein.
    Genes Dev. 2000 Jul 15;14(14):1777-88 PMID: 10898792
  25. Rap1 affects the length and heterogeneity of human telomeres.
    Mol Biol Cell. 2003 Dec;14(12):5060-8 PMID: 14565979
  26. Interaction of Saccharomyces Cdc13p with Pol1p, Imp4p, Sir4p and Zds2p is involved in telomere replication, telomere maintenance and cell growth control.
    Nucleic Acids Res. 2004 Jan 23;32(2):511-21 PMID: 14742666
  27. The POT1-TPP1 telomere complex is a telomerase processivity factor.
    Nature. 2007 Feb 1;445(7127):506-10 PMID: 17237768
  28. RPA-like proteins mediate yeast telomere function.
    Nat Struct Mol Biol. 2007 Mar;14(3):208-14 PMID: 17293872
  29. Evidence that a complex of SIR proteins interacts with the silencer and telomere-binding protein RAP1.
    Genes Dev. 1994 Oct 1;8(19):2257-69 PMID: 7958893
  30. A critical stem-loop structure in the CR4-CR5 domain of mammalian telomerase RNA.
    Nucleic Acids Res. 2002 Jan 15;30(2):592-7 PMID: 11788723
  31. Switching human telomerase on and off with hPOT1 protein in vitro.
    J Biol Chem. 2005 May 27;280(21):20449-56 PMID: 15792951
  32. Functional conservation of the telomerase protein Est1p in humans.
    Curr Biol. 2003 Apr 15;13(8):698-704 PMID: 12699629
  33. Shelterin: the protein complex that shapes and safeguards human telomeres.
    Genes Dev. 2005 Sep 15;19(18):2100-10 PMID: 16166375
  34. Cdc13 both positively and negatively regulates telomere replication.
    Genes Dev. 2001 Feb 15;15(4):404-14 PMID: 11230149
  35. Mutual dependence of Candida albicans Est1p and Est3p in telomerase assembly and activation.
    Eukaryot Cell. 2007 Aug;6(8):1330-8 PMID: 17545315
  36. Purification of human telomerase complexes identifies factors involved in telomerase biogenesis and telomere length regulation.
    Mol Cell. 2007 Dec 14;28(5):773-85 PMID: 18082603
  37. TIN2 binds TRF1 and TRF2 simultaneously and stabilizes the TRF2 complex on telomeres.
    J Biol Chem. 2004 Nov 5;279(45):47264-71 PMID: 15316005
  38. How shelterin protects mammalian telomeres.
    Annu Rev Genet. 2008;42:301-34 PMID: 18680434
  39. A human telomerase holoenzyme protein required for Cajal body localization and telomere synthesis.
    Science. 2009 Jan 30;323(5914):644-8 PMID: 19179534
  40. The maintenance and masking of chromosome termini.
    Curr Opin Cell Biol. 2006 Jun;18(3):247-53 PMID: 16682180
  41. Protein RNA and protein protein interactions mediate association of human EST1A/SMG6 with telomerase.
    Nucleic Acids Res. 2007;35(20):7011-22 PMID: 17940095
  42. A bulged stem tethers Est1p to telomerase RNA in budding yeast.
    Genes Dev. 2002 Nov 1;16(21):2800-12 PMID: 12414733
  43. A proposed OB-fold with a protein-interaction surface in Candida albicans telomerase protein Est3.
    Nat Struct Mol Biol. 2008 Sep;15(9):985-9 PMID: 19172753
  44. Cdc13 delivers separate complexes to the telomere for end protection and replication.
    Cell. 2001 Feb 9;104(3):387-96 PMID: 11239396
  45. The biogenesis and regulation of telomerase holoenzymes.
    Nat Rev Mol Cell Biol. 2006 Jul;7(7):484-94 PMID: 16829980
  46. Telomere length predicts replicative capacity of human fibroblasts.
    Proc Natl Acad Sci U S A. 1992 Nov 1;89(21):10114-8 PMID: 1438199
  47. STN1 protects chromosome ends in Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 2008 Dec 16;105(50):19815-20 PMID: 19064932
  48. Telomere replication: an Est fest.
    Curr Biol. 2003 May 27;13(11):R439-41 PMID: 12781153
  49. Yeast telomerase RNA: a flexible scaffold for protein subunits.
    Proc Natl Acad Sci U S A. 2004 Jul 6;101(27):10024-9 PMID: 15226497
  50. Analysis of telomerase in Candida albicans: potential role in telomere end protection.
    Eukaryot Cell. 2002 Dec;1(6):967-77 PMID: 12477797
  51. The Est3 protein associates with yeast telomerase through an OB-fold domain.
    Nat Struct Mol Biol. 2008 Sep;15(9):990-7 PMID: 19172754
  52. The telomerase reverse transcriptase: components and regulation.
    Genes Dev. 1998 Apr 15;12(8):1073-85 PMID: 9553037
  53. Modeling and structure function analysis of the putative anchor site of yeast telomerase.
    Nucleic Acids Res. 2007;35(15):5213-22 PMID: 17670795
  54. Proteasome-dependent degradation of Est1p regulates the cell cycle-restricted assembly of telomerase in Saccharomyces cerevisiae.
    Nat Struct Mol Biol. 2006 Aug;13(8):720-8 PMID: 16862158
  55. A dynamic molecular link between the telomere length regulator TRF1 and the chromosome end protector TRF2.
    Curr Biol. 2004 Sep 21;14(18):1621-31 PMID: 15380063
  56. POT1-interacting protein PIP1: a telomere length regulator that recruits POT1 to the TIN2/TRF1 complex.
    Genes Dev. 2004 Jul 15;18(14):1649-54 PMID: 15231715
  57. Evolution of pathogenicity and sexual reproduction in eight Candida genomes.
    Nature. 2009 Jun 4;459(7247):657-62 PMID: 19465905
  58. Chromosome end protection plasticity revealed by Stn1p and Ten1p bypass of Cdc13p.
    Nat Cell Biol. 2006 Jul;8(7):748-55 PMID: 16767082
  59. Multiple pathways inhibit NHEJ at telomeres.
    Genes Dev. 2008 May 1;22(9):1153-8 PMID: 18451106
  60. Origin of concatemeric T7 DNA.
    Nat New Biol. 1972 Oct 18;239(94):197-201 PMID: 4507727
  61. Identification of human Rap1: implications for telomere evolution.
    Cell. 2000 May 26;101(5):471-83 PMID: 10850490
  62. Telomeres and telomerase: the path from maize, Tetrahymena and yeast to human cancer and aging.
    Nat Med. 2006 Oct;12(10):1133-8 PMID: 17024208
  63. Distinct roles for yeast Stn1 in telomere capping and telomerase inhibition.
    EMBO J. 2008 Sep 3;27(17):2328-39 PMID: 19172739
  64. Regulation of telomere structure and functions by subunits of the INO80 chromatin remodeling complex.
    Mol Cell Biol. 2007 Aug;27(16):5639-49 PMID: 17562861
  65. Telomere maintenance, function and evolution: the yeast paradigm.
    Chromosome Res. 2005;13(5):535-48 PMID: 16132818
  66. spRap1 and spRif1, recruited to telomeres by Taz1, are essential for telomere function in fission yeast.
    Curr Biol. 2001 Oct 16;11(20):1624-30 PMID: 11676925
  67. Linear chromosome maintenance in the absence of essential telomere-capping proteins.
    Nat Cell Biol. 2006 Jul;8(7):734-40 PMID: 16767084
  68. The meiotic chromosomal bouquet: SUN collects flowers.
    Cell. 2006 Apr 7;125(1):19-21 PMID: 16615884
  69. TPP1 is a homologue of ciliate TEBP-beta and interacts with POT1 to recruit telomerase.
    Nature. 2007 Feb 1;445(7127):559-62 PMID: 17237767
  70. A phylogenetically based secondary structure for the yeast telomerase RNA.
    Curr Biol. 2004 Jul 13;14(13):1148-58 PMID: 15242611
  71. A universal telomerase RNA core structure includes structured motifs required for binding the telomerase reverse transcriptase protein.
    Proc Natl Acad Sci U S A. 2004 Oct 12;101(41):14713-8 PMID: 15371596
  72. TIN2 mediates functions of TRF2 at human telomeres.
    J Biol Chem. 2004 Oct 15;279(42):43799-804 PMID: 15292264
  73. The Est1 subunit of Saccharomyces cerevisiae telomerase makes multiple contributions to telomere length maintenance.
    Genetics. 2002 Nov;162(3):1101-15 PMID: 12454059
  74. Identification and comparative analysis of telomerase RNAs from Candida species reveal conservation of functional elements.
    RNA. 2009 Apr;15(4):546-59 PMID: 19223441
  75. Ten1 functions in telomere end protection and length regulation in association with Stn1 and Cdc13.
    EMBO J. 2001 Mar 1;20(5):1173-83 PMID: 11230140
  76. Fission yeast Pot1-Tpp1 protects telomeres and regulates telomere length.
    Science. 2008 Jun 6;320(5881):1341-4 PMID: 18535244
  77. DNA binding and telomere length regulation of yeast RAP1 homologues.
    J Mol Biol. 2003 Sep 26;332(4):821-33 PMID: 12972254
  78. Crystal structure of the essential N-terminal domain of telomerase reverse transcriptase.
    Nat Struct Mol Biol. 2006 Mar;13(3):218-25 PMID: 16462747
  79. Break-induced replication and recombinational telomere elongation in yeast.
    Annu Rev Biochem. 2006;75:111-35 PMID: 16756487
  80. A critical three-way junction is conserved in budding yeast and vertebrate telomerase RNAs.
    Nucleic Acids Res. 2007;35(18):6280-9 PMID: 17855392
  81. Regulation of telomerase by telomeric proteins.
    Annu Rev Biochem. 2004;73:177-208 PMID: 15189140
  82. A triple helix within a pseudoknot is a conserved and essential element of telomerase RNA.
    Mol Cell Biol. 2007 Mar;27(6):2130-43 PMID: 17210648
  83. Transcription factor substitution during the evolution of fungal ribosome regulation.
    Mol Cell. 2008 Mar 14;29(5):552-62 PMID: 18342603
  84. TPR proteins: the versatile helix.
    Trends Biochem Sci. 2003 Dec;28(12):655-62 PMID: 14659697
  85. Structural basis for telomeric single-stranded DNA recognition by yeast Cdc13.
    J Mol Biol. 2004 Apr 23;338(2):241-55 PMID: 15066429
Article Info
Journal
Trends in biochemical sciences
Abbr.
Trends Biochem Sci
ISSN
0968-0004
DOI
10.1016/j.tibs.2009.08.006
Email
nflue@med.cornell.edu
Published
2010-01-00
Epub
2009-00-19
Pages
8-17
Language
English
Region
England
NLM ID
7610674
PMCID
PMC2818170
Subset
IM
Grants
NIGMS NIH HHS · GM062631 · United States
NIGMS NIH HHS · GM069507 · United States
NIGMS NIH HHS · R01 GM069507-04 · United States
NIGMS NIH HHS · R01 GM062631 · United States
NIGMS NIH HHS · R01 GM069507 · United States
NIGMS NIH HHS · R01 GM062631-08 · United States
External Links
PubMed source DOI: 10.1016/j.tibs.2009.08.006 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2