Telomere repeat binding proteins are functional components of Arabidopsis telomeres and interact with telomerase
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
24397874
PubMed Central
PMC4282523
DOI
10.1111/tpj.12428
Knihovny.cz E-zdroje
- Klíčová slova
- Arabidopsis thaliana, plant shelterin, telomerase, telomere, telomere protein interaction, telomere repeat binding (TRB),
- MeSH
- Arabidopsis enzymologie genetika MeSH
- proteiny huseníčku metabolismus MeSH
- proteiny vázající telomery metabolismus MeSH
- telomerasa metabolismus MeSH
- telomery metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- proteiny huseníčku MeSH
- proteiny vázající telomery MeSH
- telomerasa MeSH
Although telomere-binding proteins constitute an essential part of telomeres, in vivo data indicating the existence of a structure similar to mammalian shelterin complex in plants are limited. Partial characterization of a number of candidate proteins has not identified true components of plant shelterin or elucidated their functional mechanisms. Telomere repeat binding (TRB) proteins from Arabidopsis thaliana bind plant telomeric repeats through a Myb domain of the telobox type in vitro, and have been shown to interact with POT1b (Protection of telomeres 1). Here we demonstrate co-localization of TRB1 protein with telomeres in situ using fluorescence microscopy, as well as in vivo interaction using chromatin immunoprecipitation. Classification of the TRB1 protein as a component of plant telomeres is further confirmed by the observation of shortening of telomeres in knockout mutants of the trb1 gene. Moreover, TRB proteins physically interact with plant telomerase catalytic subunits. These findings integrate TRB proteins into the telomeric interactome of A. thaliana.
Zobrazit více v PubMed
Armstrong SJ, Franklin FC, Jones GH. Nucleolus-associated telomere clustering and pairing precede meiotic chromosome synapsis in Arabidopsis thaliana. J. Cell Sci. 2001;114:4207–4217. PubMed
Baumann P, Podell E, Cech TR. Human Pot1 (Protection of telomeres) protein: cytolocalization, gene structure, and alternative splicing. Mol. Cell. Biol. 2002;22:8079–8087. PubMed PMC
Bilaud T, Koering CE, Binet-Brasselet E, Ancelin K, Pollice A, Gasser SM, Gilson E. The telobox, a Myb-related telomeric DNA binding motif found in proteins from yeast, plants and human. Nucleic Acids Res. 1996;24:1294–1303. PubMed PMC
Blackburn EH, Gall JG. Tandemly repeated sequence at termini of extrachromosomal ribosomal RNA genes in Tetrahymena. J. Mol. Biol. 1978;120:33–53. PubMed
Bowler C, Benvenuto G, Laflamme P, Molino D, Probst AV, Tariq M, Paszkowski J. Chromatin techniques for plant cells. Plant J. 2004;39:776–789. PubMed
Brown JW, Shaw PJ. The role of the plant nucleolus in pre-mRNA processing. Curr. Top. Microbiol. Immunol. 2008;326:291–311. PubMed PMC
Chen LY, Redon S, Lingner J. The human CST complex is a terminator of telomerase activity. Nature. 2012;488:540–544. PubMed
Cifuentes-Rojas C, Kannan K, Tseng L, Shippen DE. Two RNA subunits and POT1a are components of Arabidopsis telomerase. Proc. Natl Acad. Sci. USA. 2011;108:73–78. PubMed PMC
Cifuentes-Rojas C, Nelson ADL, Boltz KA, Kannan K, She XT, Shippen DE. An alternative telomerase RNA in Arabidopsis modulates enzyme activity in response to DNA damage. Genes Dev. 2012;26:2512–2523. PubMed PMC
Citovsky V, Lee LY, Vyas S, Glick E, Chen MH, Vainstein A, Gafni Y, Gelvin SB, Tzfira T. Subcellular localization of interacting proteins by bimolecular fluorescence complementation in planta. J. Mol. Biol. 2006;362:1120–1131. PubMed
Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998;16:735–743. PubMed
Dvorackova M, Rossignol P, Shaw PJ, Koroleva OA, Doonan JH, Fajkus J. AtTRB1, a telomeric DNA-binding protein from Arabidopsis, is concentrated in the nucleolus and shows highly dynamic association with chromatin. Plant J. 2010;61:637–649. PubMed
Fajkus J, Fulneckova J, Hulanova M, Berkova K, Riha K, Matyasek R. Plant cells express telomerase activity upon transfer to callus culture, without extensively changing telomere lengths. Mol. Gen. Genet. 1998;260:470–474. PubMed
Fitzgerald MS, McKnight TD, Shippen DE. Characterization and developmental patterns of telomerase expression in plants. Proc. Natl Acad. Sci. USA. 1996;93:14422–14427. PubMed PMC
Gallego ME, Bleuyard JY, Daoudal-Cotterell S, Jallut N, White CI. Ku80 plays a role in non-homologous recombination but is not required for T-DNA integration in Arabidopsis. Plant J. 2003;35:557–565. PubMed
Gao H, Cervantes RB, Mandell EK, Otero JH, Lundblad V. RPA-like proteins mediate yeast telomere function. Nat. Struct. Mol. Biol. 2007;14:208–214. PubMed
Giraud-Panis MJ, Teixeira MT, Geli V, Gilson E. CST meets shelterin to keep telomeres in check. Mol. Cell. 2010;39:665–676. PubMed
Grant JD, Broccoli D, Muquit M, Manion FJ, Tisdall J, Ochs MF. Telometric: a tool providing simplified, reproducible measurements of telomeric DNA from constant field agarose gels. Biotechniques. 2001;31(1314–1316):1318. PubMed
Greider CW, Blackburn EH. Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell. 1985;43:405–413. PubMed
Greider CW, Blackburn EH. A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature. 1989;337:331–337. PubMed
Hofr C, Sultesova P, Zimmermann M, Mozgova I, Schrumpfova PP, Wimmerova M, Fajkus J. Single-Myb-histone proteins from Arabidopsis thaliana: a quantitative study of telomere-binding specificity and kinetics. Biochem. J. 2009;419:221–228. PubMed
Horak J, Grefen C, Berendzen KW, Hahn A, Stierhof YD, Stadelhofer B, Stahl M, Koncz C, Harter K. The Arabidopsis thaliana response regulator ARR22 is a putative AHP phospho-histidine phosphatase expressed in the chalaza of developing seeds. BMC Plant Biol. 2008;8:77. PubMed PMC
Hwang MG, Chung IK, Kang BG, Cho MH. Sequence-specific binding property of Arabidopsis thaliana telomeric DNA binding protein 1 (AtTBP1) FEBS Lett. 2001;503:35–40. PubMed
Hwang MG, Kim K, Lee WK, Cho MH. AtTBP2 and AtTRP2 in Arabidopsis encode proteins that bind plant telomeric DNA and induce DNA bending in vitro. Mol. Genet. Genomics. 2005;273:66–75. PubMed
Jurczyluk J, Nouwens AS, Holien JK, Adams TE, Lovrecz GO, Parker MW, Cohen SB, Bryan TM. Direct involvement of the TEN domain at the active site of human telomerase. Nucleic Acids Res. 2011;39:1774–1788. PubMed PMC
Kannan K, Nelson AD, Shippen DE. Dyskerin is a component of the Arabidopsis telomerase RNP required for telomere maintenance. Mol. Cell. Biol. 2008;28:2332–2341. PubMed PMC
Kappei D, Butter F, Benda C, et al. HOT1 is a mammalian direct telomere repeat-binding protein contributing to telomerase recruitment. EMBO J. 2013;32:1681–1701. PubMed PMC
Karamysheva ZN, Surovtseva YV, Vespa L, Shakirov EV, Shippen DE. A C–terminal Myb extension domain defines a novel family of double-strand telomeric DNA-binding proteins in Arabidopsis. J. Biol. Chem. 2004;279:47799–47807. PubMed
Karimi M, De Meyer B, Hilson P. Modular cloning in plant cells. Trends Plant Sci. 2005;10:103–105. PubMed
Kazda A, Zellinger B, Rossler M, Derboven E, Kusenda B, Riha K. Chromosome end protection by blunt-ended telomeres. Genes Dev. 2012;26:1703–1713. PubMed PMC
Kuchar M, Fajkus J. Interactions of putative telomere-binding proteins in Arabidopsis thaliana: identification of functional TRF2 homolog in plants. FEBS Lett. 2004;578:311–315. PubMed
Kwon C, Chung IK. Interaction of an Arabidopsis RNA-binding protein with plant single-stranded telomeric DNA modulates telomerase activity. J. Biol. Chem. 2004;279:12812–12818. PubMed
Lai CK, Mitchell JR, Collins K. RNA binding domain of telomerase reverse transcriptase. Mol. Cell. Biol. 2001;21:990–1000. PubMed PMC
de Lange T. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 2005;19:2100–2110. PubMed
de Lange T. How telomeres solve the end-protection problem. Science. 2009;326:948–952. PubMed PMC
Lo SJ, Lee CC, Lai HJ. The nucleolus: reviewing oldies to have new understandings. Cell Res. 2006;16:530–538. PubMed
Lue NF. A physical and functional constituent of telomerase anchor site. J. Biol. Chem. 2005;280:26586–26591. PubMed PMC
Marian CO, Bordoli SJ, Goltz M, Santarella RA, Jackson LP, Danilevskaya O, Beckstette M, Meeley R, Bass HW. The maize Single myb histone 1 gene, Smh1, belongs to a novel gene family and encodes a protein that binds telomere DNA repeats in vitro. Plant Physiol. 2003;133:1336–1350. PubMed PMC
McKeown P, Pendle AF, Shaw PJ. Preparation of Arabidopsis nuclei and nucleoli. Methods Mol. Biol. 2008;463:67–75. PubMed
Mozgova I, Schrumpfova PP, Hofr C, Fajkus J. Functional characterization of domains in AtTRB1, a putative telomere-binding protein in Arabidopsis thaliana. Phytochemistry. 2008;69:1814–1819. PubMed
Mozgova I, Mokros P, Fajkus J. Dysfunction of chromatin assembly factor 1 induces shortening of telomeres and loss of 45S rDNA in Arabidopsis thaliana. Plant Cell. 2010;22:2768–2780. PubMed PMC
Nandakumar J, Bell CF, Weidenfeld I, Zaug AJ, Leinwand LA, Cech TR. The TEL patch of telomere protein TPP1 mediates telomerase recruitment and processivity. Nature. 2012;492:285–289. PubMed PMC
Nelson AD, Shippen DE. Blunt-ended telomeres: an alternative ending to the replication and end protection stories. Genes Dev. 2012a;26:1648–1652. PubMed PMC
Nelson AD, Shippen DE. Surprises from the chromosome front: lessons from Arabidopsis on telomeres and telomerase; Cold Spring Harb. Symp. Quant. Biol; 2012b. pp. 7–15. PubMed PMC
Peska V, Sykorova E, Fajkus J. Two faces of Solanaceae telomeres: a comparison between Nicotiana and Cestrum telomeres and telomere-binding proteins. Cytogenet. Genome Res. 2008;122:380–387. PubMed
Peska V, Schrumpfova PP, Fajkus J. Using the telobox to search for plant telomere binding proteins. Curr. Protein Peptide Sci. 2011;12:75–83. PubMed
Pinto AR, Li H, Nicholls C, Liu JP. Telomere protein complexes and interactions with telomerase in telomere maintenance. Front. Biosci. 2011;16:187–207. PubMed
Price CM, Boltz KA, Chaiken MF, Stewart JA, Beilstein MA, Shippen DE. Evolution of CST function in telomere maintenance. Cell Cycle. 2010;9:3157–3165. PubMed PMC
Riha K, Fajkus J, Siroky J, Vyskot B. Developmental control of telomere lengths and telomerase activity in plants. Plant Cell. 1998;10:1691–1698. PubMed PMC
Riha K, McKnight TD, Fajkus J, Vyskot B, Shippen DE. Analysis of the G–overhang structures on plant telomeres: evidence for two distinct telomere architectures. Plant J. 2000;23:633–641. PubMed
Rotkova G, Sykorova E, Fajkus J. Protect and regulate: recent findings on plant POT1-like proteins. Biol. Plant. 2009;53:1–4.
Ruckova E, Friml J, Prochazkova Schrumpfova P, Fajkus J. Role of alternative telomere lengthening unmasked in telomerase knock-out mutant plants. Plant Mol. Biol. 2008;66:637–646. PubMed
Santos JH, Meyer JN, Skorvaga M, Annab LA, Van Houten B. Mitochondrial hTERT exacerbates free-radical-mediated mtDNA damage. Aging Cell. 2004;3:399–411. PubMed
Schrumpfova P, Kuchar M, Mikova G, Skrisovska L, Kubicarova T, Fajkus J. Characterization of two Arabidopsis thaliana Myb-like proteins showing affinity to telomeric DNA sequence. Genome. 2004;47:316–324. PubMed
Schrumpfova PP, Kuchar M, Palecek J, Fajkus J. Mapping of interaction domains of putative telomere-binding proteins AtTRB1 and AtPOT1b from Arabidopsis thaliana. FEBS Lett. 2008;582:1400–1406. PubMed
Schrumpfova PP, Fojtova M, Mokros P, Grasser KD, Fajkus J. Role of HMGB proteins in chromatin dynamics and telomere maintenance in Arabidopsis thaliana. Curr. Protein Peptide Sci. 2011;12:105–111. PubMed
Sealey DC, Zheng L, Taboski MA, Cruickshank J, Ikura M, Harrington LA. The N–terminus of hTERT contains a DNA-binding domain and is required for telomerase activity and cellular immortalization. Nucleic Acids Res. 2010;38:2019–2035. PubMed PMC
Sealey DC, Kostic AD, LeBel C, Pryde F, Harrington L. The TPR-containing domain within Est1 homologs exhibits species-specific roles in telomerase interaction and telomere length homeostasis. BMC Mol. Biol. 2011;12:45. PubMed PMC
Sfeir A, Kosiyatrakul ST, Hockemeyer D, MacRae SL, Karlseder J, Schildkraut CL, de Lange T. Mammalian telomeres resemble fragile sites and require TRF1 for efficient replication. Cell. 2009;138:90–103. PubMed PMC
Shakirov EV, Surovtseva YV, Osbun N, Shippen DE. The Arabidopsis Pot1 and Pot2 proteins function in telomere length homeostasis and chromosome end protection. Mol. Cell. Biol. 2005;25:7725–7733. PubMed PMC
Silhavy D, Molnar A, Lucioli A, Szittya G, Hornyik C, Tavazza M, Burgyan J. A viral protein suppresses RNA silencing and binds silencing-generated, 21- to 25-nucleotide double-stranded RNAs. EMBO J. 2002;21:3070–3080. PubMed PMC
Surovtseva YV, Churikov D, Boltz KA, Song XY, Lamb JC, Warrington R, Leehy K, Heacock M, Price CM, Shippen DE. Conserved telomere maintenance component 1 interacts with STN1 and maintains chromosome ends in higher eukaryotes. Mol. Cell. 2009;36:207–218. PubMed PMC
Surovtseva YV, Shakirov EV, Vespa L, Osbun N, Song X, Shippen DE. Arabidopsis POT1 associates with the telomerase RNP and is required for telomere maintenance. EMBO J. 2007;26:3653–3661. PubMed PMC
Sykorova E, Fajkus J. Structure–function relationships in telomerase genes. Biol. Cell. 2009;101:375–392. PubMed
Tani A, Murata M. Alternative splicing of Pot1 (Protection of telomere)-like genes in Arabidopsis thaliana. Genes Genet. Syst. 2005;80:41–48. PubMed
Voinnet O, Rivas S, Mestre P, Baulcombe D. An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 2003;33:949–956. PubMed
Wu FH, Shen SC, Lee LY, Lee SH, Chan MT, Lin CS. Tape-Arabidopsis sandwich – a simpler Arabidopsis protoplast isolation method. Plant Methods. 2009;5:16. PubMed PMC
Wu P, Takai H, de Lange T. Telomeric 3’ overhangs derive from resection by Exo1 and Apollo and fill-in by POT1b-associated CST. Cell. 2012;150:39–52. PubMed PMC
Wyatt HD, Lobb DA, Beattie TL. Characterization of physical and functional anchor site interactions in human telomerase. Mol. Cell. Biol. 2007;27:3226–3240. PubMed PMC
Yoo HH, Kwon C, Lee MM, Chung IK. Single-stranded DNA binding factor AtWHY1 modulates telomere length homeostasis in Arabidopsis. Plant J. 2007a;49:442–451. PubMed
Yoo SD, Cho YH, Sheen J. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 2007b;2:1565–1572. PubMed
Zachova D, Fojtova M, Dvorackova M, Mozgova I, Lermontova I, Peska V, Schubert I, Fajkus J, Sykorova E. Structure–function relationships during transgenic telomerase expression in Arabidopsis. Physiol. Plant. 2013;149:114–126. PubMed
Polycomb Repressive Complex 2 in Eukaryotes-An Evolutionary Perspective
Telomerase Interaction Partners-Insight from Plants
Composition and Function of Telomerase-A Polymerase Associated with the Origin of Eukaryotes
Tidying-up the plant nuclear space: domains, functions, and dynamics
Telomeres in Plants and Humans: Not So Different, Not So Similar
An armadillo-domain protein participates in a telomerase interaction network
Telomere- and Telomerase-Associated Proteins and Their Functions in the Plant Cell
Telomere binding protein TRB1 is associated with promoters of translation machinery genes in vivo