The structure and function of replication protein A in DNA replication

Sub-Cellular Biochemistry

Volumn 62, Issue , 2012, Pages 171-196

  Prakash, Aishwarya ^a   Borgstahl, Gloria E O ^b  

^a UNIVERSITY OF VERMONT   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

DNA replication; G quadruplex; OB fold; Protein protein interaction; Replication protein A; Single stranded DNA binding protein

Indexed keywords

EUKARYOTA;

DNA; MULTIPROTEIN COMPLEX; REPLICATION FACTOR A;

ANIMAL; BIOSYNTHESIS; CHEMISTRY; DNA REPAIR; DNA REPLICATION; GENETIC RECOMBINATION; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; REVIEW; STRUCTURE ACTIVITY RELATION;

ANIMALS; DNA; DNA REPAIR; DNA REPLICATION; HUMANS; MULTIPROTEIN COMPLEXES; RECOMBINATION, GENETIC; REPLICATION PROTEIN A; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84894489800     PISSN: 03060225     EISSN: None     Source Type: Journal    
DOI: 10.1007/978-94-007-4572-8_10     Document Type: Article

References (134)

1. Anciano Granadillo VJ, Earley JN, Shuck SC, Georgiadis MM, Fitch RW, Turchi JJ (2010) Targeting the OB-folds of replication protein A with small molecules. J Nucleic Acids 2010: 304035.
2. Arunkumar AI, Klimovich V, Jiang X, Ott RD, Mizoue L, Fanning E, Chazin WJ (2005) Insights into hRPA32 C-terminal domain-mediated assembly of the simian virus 40 replisome. Nat Struct Mol Biol 12: 332-339.
3. Bae SH, Bae KH, Kim JA, Seo YS (2001) RPA governs endonuclease switching during processing of Okazaki fragments in eukaryotes. Nature 412: 456-461.
4. Bae KH, Kim HS, Bae SH, Kang HY, Brill S, Seo YS (2003) Bimodal interaction between replication-protein A and Dna2 is critical for Dna2 function both in vivo and in vitro. Nucleic Acids Res 31: 3006-3015.
5. Bansbach CE, Betous R, Lovejoy CA, Glick GG, Cortez D (2009) The annealing helicase SMARCAL1 maintains genome integrity at stalled replication forks. Genes Dev 23: 2405-2414.
6. Bastin-Shanower SA, Brill SJ (2001) Functional analysis of the four DNA binding domains of replication protein A. The role of RPA2 in ssDNA binding. J Biol Chem 276: 36446-36453.
7. Binz SK, Sheehan AM, Wold MS (2004) Replication protein A phosphorylation and the cellular response to DNA damage. DNA Repair (Amst) 3: 1015-1024.
8. Bissler JJ (2007) Triplex DNA and human disease. Front Biosci 12: 4536-4546.
9. Blackwell LJ, Borowiec JA, Mastrangelo IA (1996) Single-stranded-DNA binding alters human replication protein A structure and facilitates interaction with DNA-dependent protein kinase. Mol Cell Biol 16: 4798-4807.
10. Bochkarev A, Bochkareva E (2004) From RPA to BRCA2: lessons from single-stranded DNA binding by the OB-fold. Curr Opin Struct Biol 14: 36-42.
11. Bochkarev A, Pfuetzner RA, Edwards AM, Frappier L (1997) Structure of the single-stranded-DNA-binding domain of replication protein A bound to DNA. Nature 385: 176-181.
12. Bochkarev A, Bochkareva E, Frappier L, Edwards AM (1999) The crystal structure of the complex of replication protein A subunits RPA32 and RPA14 reveals a mechanism for single-stranded DNA binding. EMBO J 18: 4498-4504.
13. Bochkareva E, Korolev S, Bochkarev A (2000) The role for zinc in replication protein A. J Biol Chem 275: 27332-27338.
14. Bochkareva E, Belegu V, Korolev S, Bochkarev A (2001) Structure of the major single-stranded DNA-binding domain of replication protein A suggests a dynamic mechanism for DNA binding. EMBO J 20: 612-618.
15. Bochkareva E, Korolev S, Lees-Miller SP, Bochkarev A (2002) Structure of the RPA trimerization core and its role in the multistep DNA-binding mechanism of RPA. EMBO J 21: 1855-1863.
16. Bochkareva E, Kaustov L, Ayed A, Yi GS, Lu Y, Pineda-Lucena A, Liao JC, Okorokov AL, Milner J, Arrowsmith CH, Bochkarev A (2005) Single-stranded DNA mimicry in the p53 transactivation domain interaction with replication protein A. Proc Natl Acad Sci USA 102: 15412-15417.
17. Braun KA, Lao Y, He Z, Ingles CJ, Wold MS (1997) Role of protein-protein interactions in the function of replication protein A (RPA): RPA modulates the activity of DNA polymerase α by multiple mechanisms. Biochemistry 36: 8443-8454.
18. Broderick S, Rehmet K, Concannon C, Nasheuer HP (2010) Eukaryotic single-stranded DNA binding proteins: central factors in genome stability. Subcell Biochem 50: 143-163.
19. Brosey CA, Chagot ME, Ehrhardt M, Pretto DI, Weiner BE, Chazin WJ (2009) NMR analysis of the architecture and functional remodeling of a modular multidomain protein, RPA. J Am Chem Soc 131: 6346-6347.
20. Brosh RM Jr, Orren DK, Nehlin JO, Ravn PH, Kenny MK, Machwe A, Bohr VA (1999) Functional and physical interaction between WRN helicase and human replication protein A. J Biol Chem 274: 18341-18350.
21. Campbell JL (1986) Eukaryotic DNA replication. Annu Rev Biochem 55: 733-771.
22. Chedin F, Seitz EM, Kowalczykowski SC (1998) Novel homologs of replication protein A in archaea: implications for the evolution of ssDNA-binding proteins. Trends Biochem Sci 23: 273-277.
23. Clugston CK, McLaughlin K, Kenny MK, Brown R (1992) Binding of human single-stranded DNA binding protein to DNA damaged by the anticancer drug cis-diamminedichloroplatinum (II). Cancer Res 52: 6375-6379.
24. Constantinou A, Tarsounas M, Karow JK, Brosh RM, Bohr VA, Hickson ID, West SC (2000) Werner's syndrome protein (WRN) migrates Holliday junctions and co-localizes with RPA upon replication arrest. EMBO Rep 1: 80-84.
25. Cummings CJ, Zoghbi HY (2000) Fourteen and counting: unraveling trinucleotide repeat diseases. Hum Mol Genet 9: 909-916.
26. Dai J, Hatzakis E, Hurley LH, Yang D (2010) i-motif structures formed in the human c-MYC promoter are highly dynamic-insights into sequence redundancy and i-motif stability. PLoS One 5: e11647.
27. de Laat WL, Appeldoorn E, Sugasawa K, Weterings E, Jaspers NG, Hoeijmakers JH (1998) DNAbinding polarity of human replication protein A positions nucleases in nucleotide excision repair. Genes Dev 12: 2598-2609.
28. Deng X, Habel JE, Kabaleeswaran V, Snell EH, Wold MS, Borgstahl GE (2007) Structure of the full-length human RPA14/32 complex gives insights into the mechanism of DNA binding and complex formation. J Mol Biol 374: 865-876.
29. Deng X, Prakash A, Dhar K, Baia GS, Kolar C, Oakley GG, Borgstahl GE (2009) Human replication protein A-Rad52-single-stranded DNA complex: stoichiometry and evidence for strand transfer regulation by phosphorylation. Biochemistry 48: 6633-6643.
30. Dickson AM, Krasikova Y, Pestryakov P, Lavrik O, Wold MS (2009) Essential functions of the 32 kDa subunit of yeast replication protein A. Nucleic Acids Res 37: 2313-2326.
31. Din S, Brill SJ, Fairman MP, Stillman B (1990) Cell-cycle-regulated phosphorylation of DNA replication factor A from human and yeast cells. Genes Dev 4: 968-977.
32. Doherty KM, Sommers JA, Gray MD, Lee JW, von Kobbe C, Thoma NH, Kureekattil RP, Kenny MK, Brosh RM Jr (2005) Physical and functional mapping of the replication protein a interaction domain of the Werner and Bloom syndrome helicases. J Biol Chem 280: 29494-29505.
33. Dornreiter I, Erdile LF, Gilbert IU, von Winkler D, Kelly TJ, Fanning E (1992) Interaction of DNA polymerase α-primase with cellular replication protein A and SV40 T antigen. EMBO J 11: 769-776.
34. Eddy J, Maizels N (2006) Gene function correlates with potential for G4 DNA formation in the human genome. Nucleic Acids Res 34: 3887-3896.
35. Eddy J, Maizels N (2009) Selection for the G4 DNA motif at the 5ʹ end of human genes. Mol Carcinog 48: 319-325.
36. Fairman MP, Stillman B (1988) Cellular factors required for multiple stages of SV40 DNA replication in vitro. EMBO J 7: 1211-1218.
37. Fan JH, Bochkareva E, Bochkarev A, Gray DM (2009) Circular dichroism spectra and electrophoretic mobility shift assays show that human replication protein A binds and melts intramolecular G-quadruplex structures. Biochemistry 48: 1099-1111.
38. Fanning E, Klimovich V, Nager AR (2006) A dynamic model for replication protein A (RPA) function in DNA processing pathways. Nucleic Acids Res 34: 4126-4137.
39. Fotedar R, Roberts JM (1992) Cell cycle regulated phosphorylation of RPA-32 occurs within the replication initiation complex. EMBO J 11: 2177-2187.
40. Gellert M, Lipsett MN, Davies DR (1962) Helix formation by guanylic acid. Proc Natl Acad Sci USA 48: 2013-2018.
41. Glanzer JG, Liu S, Oakley GG (2011) Small molecule inhibitor of the RPA70 N-terminal protein interaction domain discovered using in silico and in vitro methods. Bioorg Med Chem 19: 2589-2595.
42. Gomes XV, Wold MS (1995) Structural analysis of human replication protein A. Mapping functional domains of the 70-kDa subunit. J Biol Chem 270: 4534-4543.
43. Gomes XV, Wold MS (1996) Functional domains of the 70-kilodalton subunit of human replication protein A. Biochemistry 35: 10558-10568.
44. Gomes XV, Henricksen LA, Wold MS (1996) Proteolytic mapping of human replication protein A: evidence for multiple structural domains and a conformational change upon interaction with single-stranded DNA. Biochemistry 35: 5586-5595.
45. Gottifredi V, Prives C (2005) The S phase checkpoint: when the crowd meets at the fork. Semin Cell Dev Biol 16: 355-368.
46. Grudic A, Jul-Larsen A, Haring SJ, Wold MS, Lonning PE, Bjerkvig R, Boe SO (2007) Replication protein A prevents accumulation of single-stranded telomeric DNA in cells that use alternative lengthening of telomeres. Nucleic Acids Res 35: 7267-7278.
47. Han Y, Loo YM, Militello KT, Melendy T (1999) Interactions of the papovavirus DNA replication initiator proteins, bovine papillomavirus type 1 E1 and simian virus 40 large T antigen, with human replication protein A. J Virol 73: 4899-4907.
48. Haring SJ, Mason AC, Binz SK, Wold MS (2008) Cellular functions of human RPA1. Multiple roles of domains in replication, repair, and checkpoints. J Biol Chem 283: 19095-19111.
49. Haring SJ, Humphreys TD, Wold MS (2010) A naturally occurring human RPA subunit homolog does not support DNA replication or cell-cycle progression. Nucleic Acids Res 38: 846-858.
50. He Z, Brinton BT, Greenblatt J, Hassell JA, Ingles CJ (1993) The transactivator proteins VP16 and GAL4 bind replication factor A. Cell 73: 1223-1232.
51. He Z, Henricksen LA, Wold MS, Ingles CJ (1995) RPA involvement in the damage-recognition and incision steps of nucleotide excision repair. Nature 374: 566-569.
52. Hermanson-Miller IL, Turchi JJ (2002) Strand-specific binding of RPA and XPA to damaged duplex DNA. Biochemistry 41: 2402-2408.
53. Huppert JL (2008) Four-stranded nucleic acids: structure, function and targeting of G-quadruplexes. Chem Soc Rev 37: 1375-1384.
54. Huppert JL, Balasubramanian S (2007) G-quadruplexes in promoters throughout the human genome. Nucleic Acids Res 35: 406-413.
55. Hyrien O (2000) Mechanisms and consequences of replication fork arrest. Biochimie 82: 5-17.
56. Iftode C, Daniely Y, Borowiec JA (1999) Replication protein A (RPA): the eukaryotic SSB. Crit Rev Biochem Mol Biol 34: 141-180.
57. Jackson D, Dhar K, Wahl JK, Wold MS, Borgstahl GE (2002) Analysis of the human replication protein A: Rad52 complex: evidence for crosstalk between RPA32, RPA70, Rad52 and DNA. J Mol Biol 321: 133-148.
58. Jacobs DM, Lipton AS, Isern NG, Daughdrill GW, Lowry DF, Gomes X, Wold MS (1999) Human replication protein A: global fold of the N-terminal RPA-70 domain reveals a basic cleft andflexible C-terminal linker. J Biomol NMR 14: 321-331.
59. Jain A, Wang G, Vasquez KM (2008) DNA triple helices: biological consequences and therapeutic potential. Biochimie 90: 1117-1130.
60. Jiang X, Klimovich V, Arunkumar AI, Hysinger EB, Wang Y, Ott RD, Guler GD, Weiner B, Chazin WJ, Fanning E (2006) Structural mechanism of RPA loading on DNA during activation of a simple pre-replication complex. EMBO J 25: 5516-5526.
61. Kanakis D, Levidou G, Gakiopoulou H, Eftichiadis C, Thymara I, Fragkou P, Trigka EA, Boviatsis E, Patsouris E, Korkolopoulou P (2011) Replication protein A: a reliable biologic marker of prognostic and therapeutic value in human astrocytic tumors. Hum Pathol 10: 1545-1553.
62. Kemp M, Sancar A (2009) DNA distress: just ring 9-1-1. Curr Biol 19: R733-R734.
63. Kemp MG, Mason AC, Carreira A, Reardon JT, Haring SJ, Borgstahl GE, Kowalczykowski SC, Sancar A, Wold MS (2010) An alternative form of replication protein a expressed in normal human tissues supports DNA repair. J Biol Chem 285: 4788-4797.
64. Kenny MK, Schlegel U, Furneaux H, Hurwitz J (1990) The role of human single-stranded DNA binding protein and its individual subunits in simian virus 40 DNA replication. J Biol Chem 265: 7693-7700.
65. Kim HS, Brill SJ (2001) Rfc4 interacts with Rpa1 and is required for both DNA replication and DNA damage checkpoints in Saccharomyces cerevisiae. Mol Cell Biol 21: 3725-3737.
66. Kim C, Snyder RO, Wold MS (1992) Binding properties of replication protein A from human and yeast cells. Mol Cell Biol 12: 3050-3059.
67. Kim C, Paulus BF, Wold MS (1994) Interactions of human replication protein A with oligonucleotides. Biochemistry 33: 14197-14206.
68. Kobayashi Y, Sato K, Kibe T, Seimiya H, Nakamura A, Yukawa M, Tsuchiya E, Ueno M (2010) Expression of mutant RPA in human cancer cells causes telomere shortening. Biosci Biotechnol Biochem 74: 382-385.
69. Kolpashchikov DM, Ivanova TM, Boghachev VS, Nasheuer HP, Weisshart K, Favre A, Pestryakov PE, Lavrik OI (2000a) Synthesis of base-substituted dUTP analogues carrying a photoreactive group and their application to study human replication protein A. Bioconjug Chem 11: 445-451.
70. Kolpashchikov DM, Pestryakov PE, Wlassoff WA, Khodyreva SN, Lavrik OI (2000b) Study of interaction of human replication factor A with DNA using new photoreactive analogs of dTTP. Biochemistry (Mosc) 65: 160-163.
71. Krishna SS, Majumdar I, Grishin NV (2003) Structural classification of zincfingers: survey and summary. Nucleic Acids Res 31: 532-550.
72. Kunkel TA, Burgers PM (2008) Dividing the workload at a eukaryotic replication fork. Trends Cell Biol 18: 521-527.
73. Lahue RS, Slater DL (2003) DNA repair and trinucleotide repeat instability. Front Biosci 8: s653-s665.
74. Liu Y, Vaithiyalingam S, Shi Q, Chazin WJ, Zinkel SS (2011) BID binds to replication protein A and stimulates ATR function following replicative stress. Mol Cell Biol 31: 4298-4309.
75. Lopes J, Piazza A, Bermejo R, Kriegsman B, Colosio A, Teulade-Fichou MP, Foiani M, Nicolas A (2011) G-quadruplex-induced instability during leading-strand replication. EMBO J 30: 4033-4046.
76. Machwe A, Lozada E, Wold MS, Li GM, Orren DK (2011) Molecular cooperation between the Werner syndrome protein and replication protein A in relation to replication fork blockage. J Biol Chem 286: 3497-3508.
77. MacNeill SA (2001) DNA replication: partners in the Okazaki two-step. Curr Biol 11: R842-R844.
78. Marathias VM, Bolton PH (1999) Determinants of DNA quadruplex structural type: sequence and potassium binding. Biochemistry 38: 4355-4364.
79. Mariappan SV, Silks LA 3rd, Chen X, Springer PA, Wu R, Moyzis RK, Bradbury EM, Garcia AE, Gupta G (1998) Solution structures of the Huntington's disease DNA triplets, (CAG)n. J Biomol Struct Dyn 15: 723-744.
80. Mason AC, Roy R, Simmons DT, Wold MS (2010) Functions of alternative replication protein A in initiation and elongation. Biochemistry 49: 5919-5928.
81. Masuda-Sasa T, Polaczek P, Peng XP, Chen L, Campbell JL (2008) Processing of G4 DNA by Dna2 helicase/nuclease and replication protein A (RPA) provides insights into the mechanism of Dna2/RPA substrate recognition. J Biol Chem 283: 24359-24373.
82. McElhinny AS, Li JL, Wu L (2008) Mastermind-like transcriptional co-activators: emerging roles in regulating cross talk among multiple signaling pathways. Oncogene 27: 5138-5147.
83. Melendy T, Stillman B (1993) An interaction between replication protein A and SV40 T antigen appears essential for primosome assembly during SV40 DNA replication. J Biol Chem 268: 3389-3395.
84. Mer G, Bochkarev A, Chazin WJ, Edwards AM (2000a) Three-dimensional structure and function of replication protein A. Cold Spring Harb Symp Quant Biol 65: 193-200.
85. Mer G, Bochkarev A, Gupta R, Bochkareva E, Frappier L, Ingles CJ, Edwards AM, Chazin WJ (2000b) Structural basis for the recognition of DNA repair proteins UNG2, XPA, and RAD52 by replication factor RPA. Cell 103: 449-456.
86. Mirkin S (1999) Structure and biology of H DNA. In: Malvy C, Harel-Bellan A (eds) Triple helix forming oligonucleotides. Kluwer Academic, Norwell, pp 193-222.
87. Mirkin SM (2006) DNA structures, repeat expansions and human hereditary disorders. Curr Opin Struct Biol 16: 351-358.
88. Mirkin SM (2007) Expandable DNA repeats and human disease. Nature 447: 932-940.
89. Mirkin SM (2008) Discovery of alternative DNA structures: a heroic decade (1979-1989). Front Biosci 13: 1064-1071.
90. Nuss JE, Sweeney DJ, Alter GM (2006) Reactivity-based analysis of domain structures in native replication protein A. Biochemistry 45: 9804-9818.
91. Nuss JE, Sweeney DJ, Alter GM (2009) Prediction of and experimental support for the threedimensional structure of replication protein A. Biochemistry 48: 7892-7905.
92. Oakley GG, Patrick SM (2010) Replication protein A: directing traffic at the intersection of replication and repair. Front Biosci 15: 883-900.
93. Oakley GG, Loberg LI, Yao J, Risinger MA, Yunker RL, Zernik-Kobak M, Khanna KK, Lavin MF, Carty MP, Dixon K (2001) UV-induced hyperphosphorylation of replication protein a depends on DNA replication and expression of ATM protein. Mol Biol Cell 12: 1199-1213.
94. Parrilla-Castellar ER, Karnitz LM (2003) Cut5 is required for the binding of ATR and DNA polymerase α to genotoxin-damaged chromatin. J Biol Chem 278: 45507-45511.
95. Patel DJ, Phan AT, Kuryavyi V (2007) Human telomere, oncogenic promoter and 5ʹ-UTR G-quadruplexes: diverse higher order DNA and RNA targets for cancer therapeutics. Nucleic Acids Res 35: 7429-7455.
96. Patrick SM, Turchi JJ (1998) Human replication protein A preferentially binds cisplatin-damaged duplex DNA in vitro. Biochemistry 37: 8808-8815.
97. Pestryakov PE, Lavrik OI (2008) Mechanisms of single-stranded DNA-binding protein functioning in cellular DNA metabolism. Biochemistry (Mosc) 73: 1388-1404.
98. Pestryakov PE, Weisshart K, Schlott B, Khodyreva SN, Kremmer E, Grosse F, Lavrik OI, Nasheuer HP (2003) Human replication protein A. The C-terminal RPA70 and the central RPA32 domains are involved in the interactions with the 3ʹ-end of a primer-template DNA. J Biol Chem 278: 17515-17524.
99. Pestryakov PE, Khlimankov DY, Bochkareva E, Bochkarev A, Lavrik OI (2004) Human replication protein A (RPA) binds a primer-template junction in the absence of its major ssDNAbinding domains. Nucleic Acids Res 32: 1894-1903.
100. Pestryakov PE, Krasikova YS, Petruseva IO, Khodyreva SN, Lavrik OI (2007) The role of p14 subunit of replication protein A in binding to single-stranded DNA. Dokl Biochem Biophys 412: 4-7.
101. Pfuetzner RA, Bochkarev A, Frappier L, Edwards AM (1997) Replication protein A. Characterization and crystallization of the DNA binding domain. J Biol Chem 272: 430-434.
102. Potterton L, McNicholas S, Krissinel E, Gruber J, Cowtan K, Emsley P, Murshudov GN, Cohen S, Perrakis A, Noble M (2004) Developments in the CCP4 molecular-graphics project. Acta Crystallogr D Biol Crystallogr 60: 2288-2294.
103. Prakash A, Kieken F, Marky LA, Borgstahl GE (2011a) Stabilization of a G-quadruplex from unfolding by replication protein A using potassium and the porphyrin TMPyP4. J Nucleic Acids 2011: 529828.
104. Prakash A, Natarajan A, Marky LA, Ouellette MM, Borgstahl GE (2011b) Identification of the DNA-binding domains of human replication protein A that recognize G-quadruplex DNA. J Nucleic Acids 2011: 896947.
105. Pretto DI, Tsutakawa S, Brosey CA, Castillo A, Chagot ME, Smith JA, Tainer JA, Chazin WJ (2010) Structural dynamics and single-stranded DNA binding activity of the three N-terminal domains of the large subunit of replication protein A from small angle X-ray scattering. Biochemistry 49: 2880-2889.
106. Richard DJ, Bolderson E, Cubeddu L, Wadsworth RI, Savage K, Sharma GG, Nicolette ML, Tsvetanov S, McIlwraith MJ, Pandita RK, Takeda S, Hay RT, Gautier J, West SC, Paull TT, Pandita TK, White MF, Khanna KK (2008) Single-stranded DNA-binding protein hSSB1 is critical for genomic stability. Nature 453: 677-681.
107. Sakaguchi K, Ishibashi T, Uchiyama Y, Iwabata K (2009) The multi-replication protein A (RPA) system-a new perspective. FEBS J 276: 943-963.
108. Salas TR, Petruseva I, Lavrik O, Bourdoncle A, Mergny JL, Favre A, Saintome C (2006) Human replication protein A unfolds telomeric G-quadruplexes. Nucleic Acids Res 34: 4857-4865.
109. Salas TR, Petruseva I, Lavrik O, Saintome C (2009) Evidence for direct contact between the RPA3 subunit of the human replication protein A and single-stranded DNA. Nucleic Acids Res 37: 38-46.
110. Schweizer U, Hey T, Lipps G, Krauss G (1999) Photocrosslinking locates a binding site for the large subunit of human replication protein A to the damaged strand of cisplatin-modified DNA. Nucleic Acids Res 27: 3183-3189.
111. Seroussi E, Lavi S (1993) Replication protein A is the major single-stranded DNA binding protein detected in mammalian cell extracts by gel retardation assays and UV cross-linking of long and short single-stranded DNA molecules. J Biol Chem 268: 7147-7154.
112. Shuck SC, Turchi JJ (2010) Targeted inhibition of replication protein A reveals cytotoxic activity, synergy with chemotherapeutic DNA-damaging agents, and insight into cellular function. Cancer Res 70: 3189-3198.
113. Sleeth KM, Sorensen CS, Issaeva N, Dziegielewski J, Bartek J, Helleday T (2007) RPA mediates recombination repair during replication stress and is displaced from DNA by checkpoint signalling in human cells. J Mol Biol 373: 38-47.
114. Sogo JM, Lopes M, Foiani M (2002) Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 297: 599-602.
115. Stigger E, Drissi R, Lee SH (1998) Functional analysis of human replication protein A in nucleotide excision repair. J Biol Chem 273: 9337-9343.
116. Taneja P, Boche I, Hartmann H, Nasheuer HP, Grosse F, Fanning E, Weisshart K (2007) Different activities of the largest subunit of replication protein A cooperate during SV40 DNA replication. FEBS Lett 581: 3973-3978.
117. Treuner K, Ramsperger U, Knippers R (1996) Replication protein A induces the unwinding of long double-stranded DNA regions. J Mol Biol 259: 104-112.
118. Turchi JJ, Henkels KM, Hermanson IL, Patrick SM (1999) Interactions of mammalian proteins with cisplatin-damaged DNA. J Inorg Biochem 77: 83-87.
119. Vassin VM, Wold MS, Borowiec JA (2004) Replication protein A (RPA) phosphorylation prevents RPA association with replication centers. Mol Cell Biol 24: 1930-1943.
120. Voineagu I, Narayanan V, Lobachev KS, Mirkin SM (2008) Replication stalling at unstable inverted repeats: interplay between DNA hairpins and fork stabilizing proteins. Proc Natl Acad Sci USA 105: 9936-9941.
121. Voineagu I, Freudenreich CH, Mirkin SM (2009) Checkpoint responses to unusual structures formed by DNA repeats. Mol Carcinog 48: 309-318.
122. Waga S, Stillman B (1994) Anatomy of a DNA replication fork revealed by reconstitution of SV40 DNA replication in vitro. Nature 369: 207-212.
123. Weinberg DH, Collins KL, Simancek P, Russo A, Wold MS, Virshup DM, Kelly TJ (1990) Reconstitution of simian virus 40 DNA replication with purified proteins. Proc Natl Acad Sci USA 87: 8692-8696.
124. Weisshart K, Taneja P, Fanning E (1998) The replication protein A binding site in simian virus 40 (SV40) T antigen and its role in the initial steps of SV40 DNA replication. J Virol 72: 9771-9781.
125. Weisshart K, Pestryakov P, Smith RW, Hartmann H, Kremmer E, Lavrik O, Nasheuer HP (2004) Coordinated regulation of replication protein A activities by its subunits p14 and p32. J Biol Chem 279: 35368-35376.
126. Wells RD (2007) Non-B DNA conformations, mutagenesis and disease. Trends Biochem Sci 32: 271-278.
127. Wold MS (1997) Replication protein A: a heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism. Annu Rev Biochem 66: 61-92.
128. Wold MS (2010) Eukaryotic replication protein A. Encyclopedia of life science. Wiley, Chichester.
129. Wold MS, Kelly T (1988) Purification and characterization of replication protein A, a cellular protein required for in vitro replication of simian virus 40 DNA. Proc Natl Acad Sci USA 85: 2523-2527.
130. Wu Y, Rawtani N, Thazhathveetil AK, Kenny MK, Seidman MM, Brosh RM Jr (2008) Human replication protein A melts a DNA triple helix structure in a potent and specific manner. Biochemistry 47: 5068-5077.
131. Xu X, Vaithiyalingam S, Glick GG, Mordes DA, Chazin WJ, Cortez D (2008) The basic cleft of RPA70N binds multiple checkpoint proteins, including RAD9, to regulate ATR signaling. Mol Cell Biol 28: 7345-7353.
132. Yuzhakov A, Kelman Z, Hurwitz J, O'Donnell M (1999) Multiple competition reactions for RPA order the assembly of the DNA polymerase δ holoenzyme. EMBO J 18: 6189-6199.
133. Zou L, Elledge SJ (2003) Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300: 1542-1548.
134. Zou Y, Liu Y, Wu X, Shell SM (2006) Functions of human replication protein A (RPA): from DNA replication to DNA damage and stress responses. J Cell Physiol 208: 267-273.