Dynamics of the hp1β-pcna-containing complexes in DNA replication and repair

Nucleus (United States)

Volumn 4, Issue 1, 2013, Pages 74-82

  Trembecka Lucas, Dominika O ^a   Szczurek, Aleksander T ^a   Dobrucki, Jurek W ^a  

^a JAGIELLONIAN UNIVERSITY   (Poland)

Author keywords

DNA repair; DNA replication; FRAP; FRET FLIM; HP1 ; PCNA; Protein interactions

Indexed keywords

CYCLINE; GREEN FLUORESCENT PROTEIN; HETEROCHROMATIN PROTEIN 1; HETEROCHROMATIN PROTEIN 1 BETA; UNCLASSIFIED DRUG; YELLOW FLUORESCENT PROTEIN; CHAF1A PROTEIN, HUMAN; CHROMATIN ASSEMBLY FACTOR 1; DNA; HETEROCHROMATIN SPECIFIC NONHISTONE CHROMOSOMAL PROTEIN HP 1; HETEROCHROMATIN-SPECIFIC NONHISTONE CHROMOSOMAL PROTEIN HP-1; NONHISTONE PROTEIN;

ARTICLE; COMPLEX FORMATION; CONFOCAL MICROSCOPY; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DYNAMICS; FLUORESCENCE MICROSCOPY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; PROTEIN INTERACTION; CELL NUCLEUS; DIMERIZATION; FRAP; FRET-FLIM; HELA CELL; HP1Β; METABOLISM; PCNA; PROTEIN BINDING; PROTEIN INTERACTIONS; PROTEIN SUBUNIT;

DNA REPAIR; DNA REPLICATION; FRAP; FRET-FLIM; HP1Β; PCNA; PROTEIN INTERACTIONS;

CELL NUCLEUS; CHROMATIN ASSEMBLY FACTOR-1; CHROMOSOMAL PROTEINS, NON-HISTONE; DIMERIZATION; DNA; DNA REPAIR; DNA REPLICATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; HELA CELLS; HUMANS; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTEIN BINDING; PROTEIN SUBUNITS;

EID: 84873563888     PISSN: 19491034     EISSN: 19491042     Source Type: Journal    
DOI: 10.4161/nucl.23683     Document Type: Article

References (43)

1. James TC, Elgin SC. Identification of a nonhistone chromosomal protein associated with heterochromatin in Drosophila melanogaster and its gene. Mol Cell Biol 1986; 6:3862-3872; PMID:3099166.
2. Eissenberg JC, Elgin SC. The HP1 protein family: getting a grip on chromatin. Curr Opin Genet Dev 2000; 10:204-210; PMID:10753776; http://dx.doi.org/10.1016/S0959-437X(00)00058-7.
3. Tachibana M, Sugimoto K, Nozaki M, Ueda J, Ohta T, Ohki M, et al. G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev 2002; 16:1779-1791; PMID:12130538; http://dx.doi.org/10.1101/gad.989402.
4. Cheutin T, McNairn AJ, Jenuwein T, Gilbert DM, Singh PB, Misteli T. Maintenance of stable heterochromatin domains by dynamic HP1 binding. Science 2003; 299:721-725; PMID:12560555; http://dx.doi.org/10.1126/science.1078572.
5. Brasher SV, Smith BO, Fogh RH, Nietlispach D, Thiru A, Nielsen PR, et al. The structure of mouse HP1 suggests a unique mode of single peptide recognition by the shadow chromo domain dimer. EMBO J 2000; 19:1587-1597; PMID:10747027; http://dx.doi.org/10.1093/emboj/19.7.1587.
6. Thiru A, Nietlispach D, Mott HR, Okuwaki M, Lyon D, Nielsen PR, et al. Structural basis of HP1/ PXVXL motif peptide interactions and HP1 localisation to heterochromatin. EMBO J 2004; 23:489-499; PMID:14765118; http://dx.doi.org/10.1038/sj.emboj.7600088.
7. Bolderson E, Savage KI, Mahen R, Pisupati V, Graham ME, Richard DJ, et al. Kruppel-associated Box (KRAB)-associated co-repressor (KAP-1) Ser-473 phosphorylation regulates heterochromatin protein 1β (HP1-β) mobilization and DNA repair in heterochromatin. J Biol Chem 2012; 287:28122-28131; PMID:22715096; http://dx.doi.org/10.1074/jbc.M112.368381.
8. Lomberk G, Wallrath L, Urrutia R. The heterochromatin protein 1 family. Genome Biol 2006; 7:228; PMID:17224041; http://dx.doi.org/10.1186/gb-2006-7-7-228.
9. Dormann HL, Tseng BS, Allis CD, Funabiki H, Fischle W. Dynamic regulation of effector protein binding to histone modifications: the biology of HP1 switching. Cell Cycle 2006; 5:2842-2851; PMID:17172865; http://dx.doi.org/10.4161/cc.5.24.3540.
10. LeRoy G, Weston JT, Zee BM, Young NL. Plazas-Mayorca MD, Garcia BA. Heterochromatin protein 1 is extensively decorated with histone code-like posttranslational modifications. Mol Cell Proteomics 2009; 8:2432-2442; PMID:19567367; http://dx.doi.org/10.1074/mcp.M900160-MCP200.
11. Zarebski M, Wiernasz E, Dobrucki JW. Recruitment of heterochromatin protein 1 to DNA repair sites. Cytometry A 2009; 75:619-625; PMID:19479850; http://dx.doi.org/10.1002/cyto.a.20734.
12. Mortusewicz O, Leonhardt H. XRCC1 and PCNA are loading platforms with distinct kinetic properties and different capacities to respond to multiple DNA lesions. BMC Mol Biol 2007; 8:81; PMID:17880707; http://dx.doi.org/10.1186/1471-2199-8-81.
13. Levin DS, Bai W, Yao N, O'Donnell M, Tomkinson AE. An interaction between DNA ligase I and proliferating cell nuclear antigen: implications for Okazaki fragment synthesis and joining. Proc Natl Acad Sci U S A 1997; 94:12863-12868; PMID:9371766; http://dx.doi.org/10.1073/pnas.94.24.12863.
14. Trembecka-Lucas DO, Dobrucki JW. A heterochromatin protein 1 (HP1) dimer and a proliferating cell nuclear antigen (PCNA) protein interact in vivo and are parts of a multiprotein complex involved in DNA replication and DNA repair. Cell Cycle 2012; 11:2170-2175; PMID:22617335; http://dx.doi.org/10.4161/cc.20673.
15. Kerppola TK. Visualization of molecular interactions using bimolecular fluorescence complementation analysis: characteristics of protein fragment complementation. Chem Soc Rev 2009; 38:2876-2886; PMID:19771334; http://dx.doi.org/10.1039/b909638h.
16. Swaminathan R, Hoang CP, Verkman AS. Photobleaching recovery and anisotropy decay of green fluorescent protein GFP-S65T in solution and cells: cytoplasmic viscosity probed by green fluorescent protein translational and rotational diffusion. Biophys J 1997; 72:1900-1907; PMID:9083693; http://dx.doi.org/10.1016/S0006-3495(97)78835-0.
17. Verkman AS. Solute and macromolecule diffusion in cellular aqueous compartments. Trends Biochem Sci 2002; 27:27-33; PMID:11796221; http://dx.doi.org/10.1016/S0968-0004(01)02003-5.
18. Phair RD, Misteli T. High mobility of proteins in the mammalian cell nucleus. Nature 2000; 404:604-609; PMID:10766243; http://dx.doi.org/10.1038/35007077.
19. Essers J, Theil AF, Baldeyron C, van Cappellen WA, Houtsmuller AB, Kanaar R, et al. Nuclear dynamics of PCNA in DNA replication and repair. Mol Cell Biol 2005; 25:9350-939; PMID:16227586; http://dx.doi.org/10.1128/MCB.25.21.9350-9359.2005.
20. Festenstein R, Pagakis SN, Hiragami K, Lyon D, Verreault A, Sekkali B, et al. Modulation of heterochromatin protein 1 dynamics in primary Mammalian cells. Science 2003; 299:719-721; PMID:12560554; http://dx.doi.org/10.1126/science.1078694.
21. Krishna TSR, Kong XP, Gary S, Burgers PM, Kuriyan J. Crystal structure of the eukaryotic DNA polymerase processivity factor PCNA. Cell 1994; 79:1233-1243; PMID:8001157; http://dx.doi.org/10.1016/0092-8674(94)90014-0.
22. Kelman Z, O'Donnell M. Structural and functional similarities of prokaryotic and eukaryotic DNA polymerase sliding clamps. Nucleic Acids Res 1995; 23:3613-3620; PMID:7478986; http://dx.doi.org/10.1093/nar/23.18.3613.
23. Yao N, Turner J, Kelman Z, Stukenberg PT, Dean F, Shechter D, et al. Clamp loading, unloading and intrinsic stability of the PCNA, beta and gp45 sliding clamps of human, E. coli and T4 replicases. Genes Cells 1996; 1:101-113; PMID:9078370; http://dx.doi.org/10.1046/j.1365-2443.1996.07007.x.
24. Bravo R, Frank R, Blundell PA, Macdonald-Bravo H. Cyclin/PCNA is the auxiliary protein of DNA polymerase-δ. Nature 1987; 326:515-517; PMID:2882423; http://dx.doi.org/10.1038/326515a0.
25. Bravo R, Macdonald-Bravo H. Existence of two populations of cyclin/proliferating cell nuclear antigen during the cell cycle: association with DNA replication sites. J Cell Biol 1987; 105:1549-1554; PMID:2889739; http://dx.doi.org/10.1083/jcb.105.4.1549.
26. Schmiedeberg L, Weisshart K, Diekmann S, Meyer Zu Hoerste G, Hemmerich P. High- and lowmobility populations of HP1 in heterochromatin of mammalian cells. Mol Biol Cell 2004; 15:2819-2833; PMID:15064352; http://dx.doi.org/10.1091/mbc.E03-11-0827.
27. Luijsterburg MS, Dinant C, Lans H, Stap J, Wiernasz E, Lagerwerf S, et al. Heterochromatin protein 1 is recruited to various types of DNA damage. J Cell Biol 2009; 185:577-586; PMID:19451271; http://dx.doi.org/10.1083/jcb.200810035.
28. Hoege C, Pfander B, Moldovan GL, Pyrowolakis G, Jentsch S. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 2002; 419:135-141; PMID:12226657; http://dx.doi.org/10.1038/nature00991.
29. Ayoub N, Jeyasekharan AD, Bernal JA, Venkitaraman AR. HP1-beta mobilization promotes chromatin changes that initiate the DNA damage response. Nature 2008; 453:682-686; PMID:18438399; http://dx.doi.org/10.1038/nature06875.
30. Ayoub N, Jeyasekharan AD, Venkitaraman AR. Mobilization and recruitment of HP1: a bimodal response to DNA breakage. Cell Cycle 2009; 8:2945-2950; PMID:19657222; http://dx.doi.org/10.4161/cc.8.18.9486.
31. Solarczyk KJ, Zarebski M, Dobrucki JW. Inducing local DNA damage by visible light to study chromatin repair. DNA Repair (Amst) 2012; 11:996-1002; PMID:23089313; http://dx.doi.org/10.1016/j.dnarep.2012.09.008.
32. Lakowicz JR. Principles of Fluorescence Spectroscopy, Springer, 2006, p. 954.
33. Vilenchik MM, Knudson AG. Endogenous DNA double-strand breaks: production, fidelity of repair, and induction of cancer. Proc Natl Acad Sci U S A 2003; 100:12871-12876; PMID:14566050; http://dx.doi.org/10.1073/pnas.2135498100.
34. Kwon SH, Workman JL. The changing faces of HP1: From heterochromatin formation and gene silencing to euchromatic gene expression: HP1 acts as a positive regulator of transcription. Bioessays 2011; 33:280-289; PMID:21271610; http://dx.doi.org/10.1002/bies.201000138.
35. Vakoc CR, Mandat SA, Olenchock BA, Blobel GA. Histone H3 lysine 9 methylation and HP1gamma are associated with transcription elongation through mammalian chromatin. Mol Cell 2005; 19:381-391; PMID:16061184; http://dx.doi.org/10.1016/j.molcel.2005.06.011.
36. Murzina N, Verreault A, Laue E, Stillman B. Heterochromatin dynamics in mouse cells: interaction between chromatin assembly factor 1 and HP1 proteins. Mol Cell 1999; 4:529-540; PMID:10549285; http://dx.doi.org/10.1016/S1097-2765(00)80204-X.
37. Hoek M, Stillman B. Chromatin assembly factor 1 is essential and couples chromatin assembly to DNA replication in vivo. Proc Natl Acad Sci U S A 2003; 100:12183-12188; PMID:14519857; http://dx.doi.org/10.1073/pnas.1635158100.
38. Shibahara K, Stillman B. Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell 1999; 96:575-85; PMID:10052459; http://dx.doi.org/10.1016/S0092-8674(00)80661-3.
39. Hu CD, Chinenov Y, Kerppola TK. Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol Cell 2002; 9:789-798; PMID:11983170; http://dx.doi.org/10.1016/S1097-2765(02)00496-3.
40. Trembecka DO, Kuzak M, Dobrucki JW. Conditions for using FRAP as a quantitative technique--influence of the bleaching protocol. Cytometry A 2010; 77:366-370; PMID:20131402; http://dx.doi.org/10.1002/cyto.a.20866.
41. Zacharias DA, Violin JD, Newton AC, Tsien RY. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 2002; 296:913-916; PMID:11988576; http://dx.doi.org/10.1126/science.1068539.
42. Periasamy A. FLIM Microscopy in Biology and Medicine. Taylot & Francis-CRC Press, 2010, p. 407.
43. Sillen A, Engelborghs Y. The Correct Use of "Average" Fluorescence Parameters. Photochem Photobiol 1998; 67:475-486.