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: 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

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Krvácení v důsledku portální hypertenze při jaterní cirhóze – od pohledu záchranné služby až po závěrečný hepato-gastroenterologický pohled
nový kurz
Autoři: PhDr. Petr Jaššo, MBA, MUDr. Hynek Fiala, Ph.D., prof. MUDr. Radan Brůha, CSc., MUDr. Tomáš Fejfar, Ph.D., MUDr. David Astapenko, Ph.D., prof. MUDr. Vladimír Černý, Ph.D.

Rozšíření možností lokální terapie atopické dermatitidy v ordinaci praktického lékaře či alergologa
Autoři: MUDr. Nina Benáková, Ph.D.

Léčba bolesti v ordinaci praktického lékaře
Autoři: MUDr. PhDr. Zdeňka Nováková, Ph.D.

Revmatoidní artritida: včas a k cíli
Autoři: MUDr. Heřman Mann

Jistoty a nástrahy antikoagulační léčby aneb kardiolog - neurolog - farmakolog - nefrolog - právník diskutují
Autoři: doc. MUDr. Štěpán Havránek, Ph.D., prof. MUDr. Roman Herzig, Ph.D., doc. MUDr. Karel Urbánek, Ph.D., prim. MUDr. Jan Vachek, MUDr. et Mgr. Jolana Těšínová, Ph.D.

Všechny kurzy
Kurzy Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Nemáte účet?  Registrujte se

Zapomenuté heslo

Zadejte e-mailovou adresu se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se