Structure of Dictyostelium discoideum telomeres. Analysis of possible replication mechanisms
Autoři:
Javier Rodriguez-Centeno aff001; Cristina Manguán-García aff001; Rosario Perona aff001; Leandro Sastre aff001
Působiště autorů:
Instituto de Investigaciones Biomédicas CSIC/UAM, C/ Arturo Duperier, IdiPaz, C/Pedro Rico, Madrid, Spain
aff001; CIBER de Enfermedades Raras (CIBERER), Madrid, Spain
aff002
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0222909
Souhrn
Telomeres are nucleo-protein structures that protect the ends of eukaryotic chromosomes. They are not completely synthesized during DNA replication and are elongated by specific mechanisms. The structure of the telomeres and the elongation mechanism have not been determined in Dictyostelium discoideum. This organism presents extrachromosomal palindromic elements containing two copies of the rDNA, also present at the end of the chromosomes. In this article the structure of the terminal region of the rDNA is shown to consist of repetitions of the A(G)n sequence where the number of Gs is variable. These repeats extend as a 3’ single stranded region. The G-rich region is preceded by four tandem repetitions of two different DNA motifs. D. discoideum telomere reverse transcriptase homologous protein (TERTHP) presented RNase-sensitive enzymatic activity and was required to maintain telomere structure since terthp-mutant strains presented reorganizations of the DNA terminal regions. These modifications were different in several terthp-mutants and changed with their prolonged culture and subcloning. However, the terthp gene is not essential for D. discoideum proliferation. Telomeres could be maintained in terthp-mutant strains by homologous recombination mechanisms such as ALT (Alternative Lengthening of Telomeres) or HAATI (heterochromatin amplification-mediated and telomerase-independent). In agreement with this hypothesis, the expression of mRNAs coding for several proteins involved in homologous recombination was induced in terthp-mutant strains. Extrachromosomal rDNA could serve as substrate in these DNA homologous recombination reactions.
Klíčová slova:
DNA sequence analysis – Polymerase chain reaction – Sequence motif analysis – Telomeres – Dictyostelium discoideum – Repeated sequences – Mutant strains – Nucleotide sequencing
Zdroje
1. de Lange T, Shiue L, Myers RM, Cox DR, Naylor SL, Killery AM, et al. Structure and variability of human chromosome ends. Mol Cell Biol. 1990 Feb;10(2):518–27. doi: 10.1128/mcb.10.2.518 2300052
2. Savage SA. Human telomeres and telomere biology disorders. Prog Mol Biol Transl Sci. 2014;125:41–66. doi: 10.1016/B978-0-12-397898-1.00002-5 24993697
3. Bertuch AA. The Molecular Genetics of the Telomere Biology Disorders. RNA Biol. 2016 Sep 23;13(8):696. doi: 10.1080/15476286.2015.1094596 26400640
4. Lazzerini-Denchi E, Sfeir A. Stop pulling my strings—what telomeres taught us about the DNA damage response. Nat Rev Mol Cell Biol. 2016 Jun;17(6):364–78. doi: 10.1038/nrm.2016.43 27165790
5. Perona R, Iarriccio L, Pintado-Berninches L, Rodriguez-Centeno J, Manguan-Garcia C, Garcia E, et al. Molecular diagnosis and precission therapeutic approaches for telomere biology disorders. In: Larramendy M, Soloneski S, editors. Telomeres: INTECH; 2016. p. 77–117.
6. McElligott R, Wellinger RJ. The terminal DNA structure of mammalian chromosomes. EMBO J. 1997 Jun 16;16(12):3705–14. doi: 10.1093/emboj/16.12.3705 9218811
7. Blasco MA. Telomeres and human disease: ageing, cancer and beyond. Nat Rev Genet. 2005 Aug;6(8):611–22. doi: 10.1038/nrg1656 16136653
8. Shampay J, Szostak JW, Blackburn EH. DNA sequences of telomeres maintained in yeast. Nature. 1984 Jul 12–18;310(5973):154–7. doi: 10.1038/310154a0 6330571
9. Sepsiova R, Necasova I, Willcox S, Prochazkova K, Gorilak P, Nosek J, et al. Evolution of Telomeres in Schizosaccharomyces pombe and Its Possible Relationship to the Diversification of Telomere Binding Proteins. PLoS One. 2016;11(4):e0154225. doi: 10.1371/journal.pone.0154225 27101289
10. Fajkus P, Peska V, Sitova Z, Fulneckova J, Dvorackova M, Gogela R, et al. Allium telomeres unmasked: the unusual telomeric sequence (CTCGGTTATGGG)n is synthesized by telomerase. Plant J. 2016 Feb;85(3):337–47. doi: 10.1111/tpj.13115 26716914
11. Henderson ER, Blackburn EH. An overhanging 3' terminus is a conserved feature of telomeres. Mol Cell Biol. 1989 Jan;9(1):345–8. doi: 10.1128/mcb.9.1.345 2927395
12. de Lange T. T-loops and the origin of telomeres. Nat Rev Mol Cell Biol. 2004 Apr;5(4):323–9. doi: 10.1038/nrm1359 15071557
13. de Lange T. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 2005 Sep 15;19(18):2100–10. doi: 10.1101/gad.1346005 16166375
14. Martinez P, Blasco MA. Replicating through telomeres: a means to an end. Trends Biochem Sci. 2015 Sep;40(9):504–15. doi: 10.1016/j.tibs.2015.06.003 26188776
15. Greider CW, Blackburn EH. The telomere terminal transferase of Tetrahymena is a ribonucleoprotein enzyme with two kinds of primer specificity. Cell. 1987 Dec 24;51(6):887–98. doi: 10.1016/0092-8674(87)90576-9 3319189
16. Schmidt JC, Cech TR. Human telomerase: biogenesis, trafficking, recruitment, and activation. Genes Dev. 2015 Jun 1;29(11):1095–105. doi: 10.1101/gad.263863.115 26063571
17. Fulcher N, Derboven E, Valuchova S, Riha K. If the cap fits, wear it: an overview of telomeric structures over evolution. Cell Mol Life Sci. 2014 Mar;71(5):847–65. doi: 10.1007/s00018-013-1469-z 24042202
18. Casacuberta E, Pardue ML. HeT-A and TART, two Drosophila retrotransposons with a bona fide role in chromosome structure for more than 60 million years. Cytogenet Genome Res. 2005;110(1–4):152–9. doi: 10.1159/000084947 16093667
19. Casacuberta E. Drosophila: Retrotransposons Making up Telomeres. Viruses. 2017 Jul 19;9(7).
20. Jain D, Cooper JP. Telomeric strategies: means to an end. Annu Rev Genet. 2010;44:243–69. doi: 10.1146/annurev-genet-102108-134841 21047259
21. Nabetani A, Ishikawa F. Alternative lengthening of telomeres pathway: recombination-mediated telomere maintenance mechanism in human cells. J Biochem. 2010 Jan;149(1):5–14. doi: 10.1093/jb/mvq119 20937668
22. O'Sullivan RJ, Almouzni G. Assembly of telomeric chromatin to create ALTernative endings. Trends Cell Biol. 2014 Nov;24(11):675–85. doi: 10.1016/j.tcb.2014.07.007 25172551
23. Cesare AJ, Reddel RR. Alternative lengthening of telomeres: models, mechanisms and implications. Nat Rev Genet. 2010 May;11(5):319–30. doi: 10.1038/nrg2763 20351727
24. Henson JD, Neumann AA, Yeager TR, Reddel RR. Alternative lengthening of telomeres in mammalian cells. Oncogene. 2002 Jan 21;21(4):598–610. doi: 10.1038/sj.onc.1205058 11850785
25. Chung I, Osterwald S, Deeg KI, Rippe K. PML body meets telomere: the beginning of an ALTernate ending? Nucleus. 2012 May-Jun;3(3):263–75. doi: 10.4161/nucl.20326 22572954
26. Maringele L, Lydall D. Telomerase- and recombination-independent immortalization of budding yeast. Genes Dev. 2004 Nov 1;18(21):2663–75. doi: 10.1101/gad.316504 15489288
27. Jain D, Hebden AK, Nakamura TM, Miller KM, Cooper JP. HAATI survivors replace canonical telomeres with blocks of generic heterochromatin. Nature. 2010 Sep 9;467(7312):223–7. doi: 10.1038/nature09374 20829796
28. Williams JG. Dictyostelium finds new roles to model. Genetics. 2010 Jul;185(3):717–26. doi: 10.1534/genetics.110.119297 20660652
29. Schaap P. Evolution of developmental cyclic adenosine monophosphate signaling in the Dictyostelia from an amoebozoan stress response. Dev Growth Differ. 2011 May;53(4):452–62. doi: 10.1111/j.1440-169X.2011.01263.x 21585352
30. Loomis WF. Cell signaling during development of Dictyostelium. Dev Biol. 2014 Jul 1;391(1):1–16. doi: 10.1016/j.ydbio.2014.04.001 24726820
31. Eichinger L, Pachebat JA, Glockner G, Rajandream M, Sucgang R, Berriman M, et al. The genome of the social amoeba Dictyostelium discoideum. Nature. 2005;435:43–57. doi: 10.1038/nature03481 15875012
32. Firtel RA, Cockburn A, Frankel G, Hershfield V. Structural organization of the genome of Dictyostelium discoideum: Analysis by EcoRI restriction endonuclease. J Mol Biol. 1976;102:831–52. doi: 10.1016/0022-2836(76)90294-1 781265
33. Sucgang R, Chen G, Liu W, Lindsay R, Lu J, Muzny D, et al. Sequence and structure of the extrachromosomal palindrome encoding the ribosomal RNA genes in Dictyostelium. Nucleic Acids Res. 2003 May 1;31(9):2361–8. doi: 10.1093/nar/gkg348 12711681
34. Emery HS, Weiner AM. An irregular satellite sequence is found at the termini of the linear extrachromosomal rDNA in Dictyostelium discoideum. Cell. 1981;26:411–9. doi: 10.1016/0092-8674(81)90210-5 6276016
35. Heidel AJ, Lawal HM, Felder M, Schilde C, Helps NR, Tunggal B, et al. Phylogeny-wide analysis of social amoeba genomes highlights ancient origins for complex intercellular communication. Genome Res. 2011 Nov;21(11):1882–91. doi: 10.1101/gr.121137.111 21757610
36. Pang KM, Lynes MA, Knecht DA. Variables controlling the expression level of exogenous genes in Dictyostelium. Plasmid. 1999;41:187–97. doi: 10.1006/plas.1999.1391 10366524
37. Hughes JE, Welker DL. A mini-screen technique for analyzing nuclear DNA from a single Dictyostelium colony. Nucl Acids Res. 1988;16:2338. doi: 10.1093/nar/16.5.2338 3357783
38. Faix J, Kreppel L, Shaulsky G, Schleicher M, Kimmel AR. A rapid and efficient method to generate multiple gene disruptions in Dictyostelium discoideum using a single selectable marker and the Cre-loxP system. Nucleic Acids Res. 2004;32(19):e143. doi: 10.1093/nar/gnh136 15507682
39. Kim NW, Wu F. Advances in quantification and characterization of telomerase activity by the telomeric repeat amplification protocol (TRAP). Nucleic Acids Res. 1997 Jul 1;25(13):2595–7. doi: 10.1093/nar/25.13.2595 9185569
40. Galardi-Castilla M, Pergolizzi B, Bloomfield G, Skelton J, Ivens A, Kay RR, et al. SrfB, a member of the Serum Response Factor family of transcription factors, regulates starvation response and early development in Dictyostelium. Dev Biol. 2008;316(2):260–74. doi: 10.1016/j.ydbio.2008.01.026 18339368
41. O'Sullivan RJ, Karlseder J. Telomeres: protecting chromosomes against genome instability. Nat Rev Mol Cell Biol. 2010 Mar;11(3):171–81. doi: 10.1038/nrm2848 20125188
42. Counter CM, Avilion AA, LeFeuvre CE, Stewart NG, Greider CW, Harley CB, et al. Telomere shortening associated with chromosome instability is arrested in immortal cells which express telomerase activity. EMBO J. 1992 May;11(5):1921–9. 1582420
43. Kyrion G, Boakye KA, Lustig AJ. C-terminal truncation of RAP1 results in the deregulation of telomere size, stability, and function in Saccharomyces cerevisiae. Mol Cell Biol. 1992 Nov;12(11):5159–73. doi: 10.1128/mcb.12.11.5159 1406688
44. Lundblad V, Blackburn EH. An alternative pathway for yeast telomere maintenance rescues est1- senescence. Cell. 1993 Apr 23;73(2):347–60. doi: 10.1016/0092-8674(93)90234-h 8477448
45. Henson JD, Reddel RR. Assaying and investigating Alternative Lengthening of Telomeres activity in human cells and cancers. FEBS Lett. 2010 Sep 10;584(17):3800–11. doi: 10.1016/j.febslet.2010.06.009 20542034
46. Tokutake Y, Matsumoto T, Watanabe T, Maeda S, Tahara H, Sakamoto S, et al. Extra-chromosomal telomere repeat DNA in telomerase-negative immortalized cell lines. Biochem Biophys Res Commun. 1998 Jun 29;247(3):765–72. doi: 10.1006/bbrc.1998.8876 9647768
47. Linger BR, Price CM. Conservation of telomere protein complexes: shuffling through evolution. Crit Rev Biochem Mol Biol. 2009 Nov-Dec;44(6):434–46. doi: 10.3109/10409230903307329 19839711
48. Broccoli D, Smogorzewska A, Chong L, de Lange T. Human telomeres contain two distinct Myb-related proteins, TRF1 and TRF2. Nat Genet. 1997 Oct;17(2):231–5. doi: 10.1038/ng1097-231 9326950
49. Poulet A, Pisano S, Faivre-Moskalenko C, Pei B, Tauran Y, Haftek-Terreau Z, et al. The N-terminal domains of TRF1 and TRF2 regulate their ability to condense telomeric DNA. Nucleic Acids Res. 2012 Mar;40(6):2566–76. doi: 10.1093/nar/gkr1116 22139926
50. Wu L, Multani AS, He H, Cosme-Blanco W, Deng Y, Deng JM, et al. Pot1 deficiency initiates DNA damage checkpoint activation and aberrant homologous recombination at telomeres. Cell. 2006 Jul 14;126(1):49–62. doi: 10.1016/j.cell.2006.05.037 16839876
51. Giraud-Panis MJ, Pisano S, Benarroch-Popivker D, Pei B, Le Du MH, Gilson E. One identity or more for telomeres? Front Oncol. 2013;3:48. doi: 10.3389/fonc.2013.00048 23509004
52. Nassir N, Hyde GJ, Baskar R. A telomerase with novel non-canonical roles: TERT controls cellular aggregation and tissue size in Dictyostelium. PLoS Genet. 2019 Jun;15(6):e1008188. doi: 10.1371/journal.pgen.1008188 31237867
53. Lustig AJ, Petes TD. Identification of yeast mutants with altered telomere structure. Proc Natl Acad Sci U S A. 1986 Mar;83(5):1398–402. doi: 10.1073/pnas.83.5.1398 3513174
54. Jiang WQ, Zhong ZH, Henson JD, Neumann AA, Chang AC, Reddel RR. Suppression of alternative lengthening of telomeres by Sp100-mediated sequestration of the MRE11/RAD50/NBS1 complex. Mol Cell Biol. 2005 Apr;25(7):2708–21. doi: 10.1128/MCB.25.7.2708-2721.2005 15767676
55. Zhong ZH, Jiang WQ, Cesare AJ, Neumann AA, Wadhwa R, Reddel RR. Disruption of telomere maintenance by depletion of the MRE11/RAD50/NBS1 complex in cells that use alternative lengthening of telomeres. J Biol Chem. 2007 Oct 5;282(40):29314–22. doi: 10.1074/jbc.M701413200 17693401
56. Potts PR, Yu H. The SMC5/6 complex maintains telomere length in ALT cancer cells through SUMOylation of telomere-binding proteins. Nat Struct Mol Biol. 2007 Jul;14(7):581–90. doi: 10.1038/nsmb1259 17589526
Článek vyšel v časopise
PLOS One
2019 Číslo 9
- I mozek má svou krizi středního věku. Jak tyto změny souvisejí s rizikem demence ve stáří?
- Přerušovaný půst může mít významná zdravotní rizika
- Jak nám pocit vděčnosti pomáhá snáze se rozloučit se životem
- Jak a kdy u celiakie začíná reakce na lepek? Možnou odpověď poodkryla čerstvá kanadská studie
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?