SUMOylation regulates telomere length by targeting the shelterin subunit Tpz1Tpp1 to modulate shelterin-Stn1 interaction in fission yeast

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 16, 2014, Pages 5950-5955

  Miyagawa, Keisuke ^a   Low, Ross S ^b   Santosa, Venny ^a   Tsuji, Hiroki ^a   Moser, Bettina A ^b   Fujisawa, Shiho ^a   Harland, Jennifer L ^b   Raguimova, Olga N ^b   Go, Andrew ^b   Ueno, Masaru ^c   Matsuyama, Akihisa ^d   Yoshida, Minoru ^d,e   Nakamura, Toru M ^b   Tanaka, Katsunori ^a  

^a KWANSEI GAKUIN UNIVERSITY   (Japan)

^b UNIVERSITY OF ILLINOIS   (United States)

^c HIROSHIMA UNIVERSITY   (Japan)

^d RIKEN Center for Sustainable Resource Science   (Japan)

^e JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Cell cycle; CST complex; DNA replication; S phase

Indexed keywords

LYSINE; SCHIZOSACCHAROMYCES POMBE PROTEIN; SHELTERIN PROTEIN; STN1 PROTEIN; SUMO PROTEIN; TELOMERASE; TEN1 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; ENZYME ACTIVITY; ENZYME SUBUNIT; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; REGULATORY MECHANISM; SCHIZOSACCHAROMYCES POMBE; SEQUENCE HOMOLOGY; SHELTERIN SUBUNIT; SUMOYLATION; TELOMERE HOMEOSTASIS;

CELL CYCLE; CST COMPLEX; DNA REPLICATION; S-PHASE;

CARRIER PROTEINS; G2 PHASE; LYSINE; MODELS, BIOLOGICAL; PROTEIN BINDING; PROTEIN SUBUNITS; S PHASE; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SUMOYLATION; TELOMERASE; TELOMERE; TELOMERE HOMEOSTASIS; TELOMERE SHORTENING; TELOMERE-BINDING PROTEINS; UBIQUITIN-PROTEIN LIGASES;

EID: 84899052640     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1401359111     Document Type: Article

References (44)

1. Verdun RE, Karlseder J (2007) Replication and protection of telomeres. Nature 447(7147):924-931. (Pubitemid 46975759)
2. Palm W, de Lange T (2008) How shelterin protects mammalian telomeres. Annu Rev Genet 42:301-334.
3. Cesare AJ, Reddel RR (2010) Alternative lengthening of telomeres: Models, mechanisms and implications. Nat Rev Genet 11(5):319-330.
4. Armanios M, Blackburn EH (2012) The telomere syndromes. Nat Rev Genet 13(10): 693-704.
5. Sfeir A, de Lange T (2012) Removal of shelterin reveals the telomere end-protection problem. Science 336(6081):593-597.
6. Denchi EL, de Lange T (2007) Protection of telomeres through independent control of ATM and ATR by TRF2 and POT1. Nature 448(7157):1068-1071. (Pubitemid 47345583)
7. Miyoshi T, Kanoh J, Saito M, Ishikawa F (2008) Fission yeast Pot1-Tpp1 protects telomeres and regulates telomere length. Science 320(5881):1341-1344. (Pubitemid 351929470)
8. Baumann P, Cech TR (2001) Pot1, the putative telomere end-binding protein in fission yeast and humans. Science 292(5519):1171-1175. (Pubitemid 32440940)
9. Cooper JP, Nimmo ER, Allshire RC, Cech TR (1997) Regulation of telomere length and function by a Myb-domain protein in fission yeast. Nature 385(6618):744-747. (Pubitemid 27098098)
10. ATR kinases promote Ccq1-Est1 interaction to maintain telomeres in fission yeast. Nat Struct Mol Biol 18(12):1408-1413.
11. Giraud-Panis MJ, Teixeira MT, Geli V, Gilson E (2010) CST meets shelterin to keep telomeres in check. Mol Cell 39(5):665-676.
12. Price CM, et al. (2010) Evolution of CST function in telomere maintenance. Cell Cycle 9(16):3157-3165.
13. Martin V, Du LL, Rozenzhak S, Russell P (2007) Protection of telomeres by a conserved Stn1-Ten1 complex. Proc Natl Acad Sci USA 104(35):14038-14043. (Pubitemid 350003331)
14. Peuscher MH, Jacobs JJ (2012) Posttranslational control of telomere maintenance and the telomere damage response. Cell Cycle 11(8):1524-1534.
15. Gareau JR, Lima CD (2010) The SUMO pathway: Emerging mechanisms that shape specificity, conjugation and recognition. Nat Rev Mol Cell Biol 11(12):861-871.
16. Geiss-Friedlander R, Melchior F (2007) Concepts in sumoylation: A decade on. Nat Rev Mol Cell Biol 8(12):947-956. (Pubitemid 350176509)
17. Johnson ES (2004) Protein modification by SUMO. Annu Rev Biochem 73:355-382.
18. Potts PR, Yu H (2007) The SMC5/6 complex maintains telomere length in ALT cancer cells through SUMOylation of telomere-binding proteins. Nat Struct Mol Biol 14(7): 581-590. (Pubitemid 47037066)
19. Chavez A, George V, Agrawal V, Johnson FB (2010) Sumoylation and the structural maintenance of chromosomes (Smc) 5/6 complex slow senescence through recombination intermediate resolution. J Biol Chem 285(16):11922-11930.
20. Lu CY, Tsai CH, Brill SJ, Teng SC (2010) Sumoylation of the BLM ortholog, Sgs1, promotes telomere-telomere recombination in budding yeast. Nucleic Acids Res 38(2): 488-498.
21. Hang LE, Liu X, Cheung I, Yang Y, Zhao X (2011) SUMOylation regulates telomere length homeostasis by targeting Cdc13. Nat Struct Mol Biol 18(8):920-926.
22. Tanaka K, et al. (1999) Characterization of a fission yeast SUMO-1 homologue, Pmt3p, required for multiple nuclear events, including the control of telomere length and chromosome segregation. Mol Cell Biol 19(12):8660-8672. (Pubitemid 30414058)
23. Xhemalce B, et al. (2007) Role of SUMO in the dynamics of telomere maintenance in fission yeast. Proc Natl Acad Sci USA 104(3):893-898. (Pubitemid 46154707)
24. Andrews EA, et al. (2005) Nse2, a component of the Smc5-6 complex, is a SUMO ligase required for the response to DNA damage. Mol Cell Biol 25(1):185-196. (Pubitemid 40039810)
25. Lehmann AR (1996) Molecular biology of DNA repair in the fission yeast Schizosaccharomyces pombe. Mutat Res 363(3):147-161.
26. ATR phosphorylate the telomere protein Ccq1 to recruit telomerase and elongate telomeres in fission yeast. Genes Dev 26(3):241-246.
27. Chen LY, Redon S, Lingner J (2012) The human CST complex is a terminator of telomerase activity. Nature 488(7412):540-544.
28. Moser BA, et al. (2009) Differential arrival of leading and lagging strand DNA polymerases at fission yeast telomeres. EMBO J 28(7):810-820.
29. ATR kinase to limit telomere extension. PLoS Genet 9(11): e1003936.
30. Wu P, Takai H, de Lange T (2012) Telomeric 3′ overhangs derive from resection by Exo1 and Apollo and fill-in by POT1b-associated CST. Cell 150(1):39-52.
31. Wang F, et al. (2012) Human CST has independent functions during telomere duplex replication and C-strand fill-in. Cell Rep 2(5):1096-1103.
32. Dahlen M, Sunnerhagen P, Wang TS (2003) Replication proteins influence the maintenance of telomere length and telomerase protein stability. Mol Cell Biol 23(9): 3031-3042. (Pubitemid 36459219)
33. Adams-Martin A, Dionne I, Wellinger RJ, Holm C (2000) The function of DNA polymerase α at telomeric G tails is important for telomere homeostasis. Mol Cell Biol 20(3):786-796. (Pubitemid 30044215)
34. Puglisi A, Bianchi A, Lemmens L, Damay P, Shore D (2008) Distinct roles for yeast Stn1 in telomere capping and telomerase inhibition. EMBO J 27(17):2328-2339.
35. Qi H, Zakian VA (2000) The Saccharomyces telomere-binding protein Cdc13p interacts with both the catalytic subunit of DNA polymerase α and the telomerase-associated Est1 protein. Genes Dev 14(14):1777-1788. (Pubitemid 30602996)
36. Wan M, Qin J, Songyang Z, Liu D (2009) OB fold-containing protein 1 (OBFC1), a human homolog of yeast Stn1, associates with TPP1 and is implicated in telomere length regulation. J Biol Chem 284(39):26725-26731.
37. Moreno S, Klar A, Nurse P (1991) Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol 194:795-823.
38. Shiozaki K, Russell P (1997) Stress-activated protein kinase pathway in cell cycle control of fission yeast. Methods Enzymol 283:506-520. (Pubitemid 27339805)
39. Bentley NJ, et al. (1996) The Schizosaccharomyces pombe rad3 checkpoint gene. EMBO J 15(23):6641-6651. (Pubitemid 26413796)
40. Webb CJ, Zakian VA (2008) Identification and characterization of the Schizosaccharomyces pombe TER1 telomerase RNA. Nat Struct Mol Biol 15(1):34-42.
41. ATR promote telomere protection and telomerase recruitment. PLoS Genet 5(8):e1000622.
42. Krawchuk MD, Wahls WP (1999) High-efficiency gene targeting in Schizosaccharomyces pombe using a modular, PCR-based approach with long tracts of flanking homology. Yeast 15(13):1419-1427. (Pubitemid 29445815)
43. +. Genetics 152(4): 1501-1512.
44. Khair L, Subramanian L, Moser BA, Nakamura TM (2010) Roles of heterochromatin and telomere proteins in regulation of fission yeast telomere recombination and telomerase recruitment. J Biol Chem 285(8):5327-5337.