Development of bimolecular fluorescence complementation using dronpa for visualization of protein-protein interactions in cells

Molecular Imaging and Biology

Volumn 12, Issue 5, 2010, Pages 468-478

  Lee, You Ri ^a   Park, Jong Hwa ^a   Hahm, Soo Hyun ^a   Kang, Lin Woo ^a   Chung, Ji Hyung ^b   Nam, Ki Hyun ^c   Hwang, Kwang Yeon ^c   Kwon, Ick Chan ^d   Han, Ye Sun ^a  

^a Konkuk University   (South Korea)

^b Yonsei University College of Medicine   (South Korea)

^c Korea University   (South Korea)

^d Korea Institute of Science and Technology   (South Korea)

Author keywords

Bimolecular fluorescence complementation; Dronpa; hHus1; hRad1; Human MutY homolog; Protein protein interaction; Reversible photoswitching activity

Indexed keywords

CELL PROTEIN; DNA GLYCOSYLASE MUTY; DRONPA; FLUORESCENT DYE; HUS1 PROTEIN; MYC PROTEIN; PROTEIN RAD1; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BIMOLECULAR FLUORESCENCE COMPLEMENTATION; CARBOXY TERMINAL SEQUENCE; CELL STRAIN HEK293; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; EXPRESSION VECTOR; FLUORESCENCE ANALYSIS; GENE SEQUENCE; GENE STRUCTURE; GENETIC CODE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LIGHT ABSORPTION; MOLECULAR IMAGING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROCESS DEVELOPMENT; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; WESTERN BLOTTING;

AMINO ACID SEQUENCE; BLOTTING, WESTERN; CELL LINE; FLUORESCENCE; HUMANS; IMMUNOPRECIPITATION; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 78049348351     PISSN: 15361632     EISSN: 18602002     Source Type: Journal    
DOI: 10.1007/s11307-010-0312-2     Document Type: Article

References (48)

1. TK Kerppola 2006 Complementary methods for studies of protein interactions in living cells Nat Methods 3 969 971 1:CAS:528:DC%2BD28Xht1WqurfP 10.1038/nmeth1206-969 17117150 (Pubitemid 44782690)
2. TK Kerppola 2006 Design and implementation of bimolecular fluorescence complementation (BiFC) assays for the visualization of protein interactions in living cells Nat Protoc 1 1278 1286 10.1038/nprot.2006.201 17406412
3. F Ciruela 2008 Fluorescence-based methods in the study of protein-protein interactions in living cells Curr Opin Biotech 19 338 343 1:CAS:528: DC%2BD1cXhtValsL7K 10.1016/j.copbio.2008.06.003 18602005
4. I Ghosh AD Hamilton L Regan 2000 Antiparallel leucine zipper-directed protein reassembly: application to the green fluorescent protein J Am Chem Soc 122 5658 5659 1:CAS:528:DC%2BD3cXjsF2qs78%3D 10.1021/ja994421w (Pubitemid 30431094)
5. SW Michnick 2003 Protein fragment complementation strategies for biochemical network mapping Curr Opin Biotech 14 610 617 1:CAS:528: DC%2BD3sXps1Oqt7c%3D 10.1016/j.copbio.2003.10.014 14662390 (Pubitemid 37518439)
6. R Paulmurugan SS Gambhir 2003 Monitoring protein-protein interactions using split synthetic Renilla luciferase protein-fragment-assisted complementation Anal Chem 75 1584 1589 1:CAS:528:DC%2BD3sXhslSlsro%3D 10.1021/ac020731c 12705589 (Pubitemid 36512595)
7. CD Hu Y Chinenov TK Kerppola 2002 Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation Mol Cell 9 789 798 1:CAS:528:DC%2BD38XjsFWgsLY%3D 10.1016/S1097-2765(02)00496-3 11983170 (Pubitemid 34454889)
8. KE Luker MC Smith GD Luker, et al. 2004 Kinetics of regulated protein-protein interactions revealed with firefly luciferase complementation imaging in cells and living animals Proc Natl Acad Sci USA 101 12288 12293 1:CAS:528:DC%2BD2cXntFekt7k%3D 10.1073/pnas.0404041101 15284440 (Pubitemid 39145436)
9. Y Kodama M Wada 2009 Simultaneous visualization of two protein complexes in a single plant cell using multicolor fluorescence complementation analysis Plant Mol Biol 70 211 217 1:CAS:528:DC%2BD1MXktFShs7Y%3D 10.1007/s11103-009- 9467-0 19219406
10. KP Skarp X Zhao M Weber J Jantti 2008 Use of bimolecular fluorescence complementation in yeast Saccharomyces cerevisiae Methods Mol Biol 457 165 175 1:CAS:528:DC%2BD1cXht1CmtLzJ 19066026
11. SM Hiatt YJ Shyu HM Duren, et al. 2008 Bimolecular fluorescence complementation (BiFC) analysis of protein interactions in Caenorhabditis elegans Methods 45 185 191 1:CAS:528:DC%2BD1cXpsVGnsL4%3D 10.1016/j.ymeth.2008. 06.003 18586101
12. KH Nam OY Kwon K Sugiyama, et al. 2007 Structural characterization of the photoswitchable fluorescent protein Dronpa-C62S Biochem Biophys Res Commun 354 962 967 1:CAS:528:DC%2BD2sXhs1Snt7o%3D 10.1016/j.bbrc.2007.01.086 17276392 (Pubitemid 46216226)
13. R Ando H Mizuno A Miyawaki 2004 Regulated fast nucleocytoplasmic shuttling observed by reversible protein highlighting Science 306 1370 1373 1:CAS:528:DC%2BD2cXpvVekt7o%3D 10.1126/science.1102506 15550670 (Pubitemid 39532513)
14. H Mizuno TK Mal M Walchli, et al. 2008 Light-dependent regulation of structure flexibility in a photochromic fluorescent protein Proc Natl Acad Sci USA 105 9927 9932 10.1073/pnas.0709599105
15. S Aramaki K Hatta 2006 Visualizing neurons one-by-one in vivo: optical dissection and reconstruction of neural networks with reversible fluorescent proteins Dev Dyn 235 2192 2199 1:CAS:528:DC%2BD28XptVeisbw%3D 10.1002/dvdy.20826 16607643 (Pubitemid 44205053)
16. C Venclovas MP Thelen 2000 Structure-based predictions of Rad1, Rad9, Hus1 and Rad17 participation in sliding clamp and clamp-loading complexes Nucleic Acids Res 28 2481 2493 1:CAS:528:DC%2BD3cXlvFWqs7s%3D 10.1093/nar/28.13.2481 10871397
17. L Zou D Cortez SJ Elledge 2002 Regulation of ATR substrate selection by Rad17-dependent loading of Rad9 complexes onto chromatin Genes Dev 16 198 208 1:CAS:528:DC%2BD38Xos1erug%3D%3D 10.1101/gad.950302 11799063 (Pubitemid 34075812)
18. Y Shiomi A Shinozaki D Nakada, et al. 2002 Clamp and clamp loader structures of the human checkpoint protein complexes, Rad9-1-1 and Rad17-RFC Genes Cells 7 861 868 1:CAS:528:DC%2BD38Xmslyisrw%3D 10.1046/j.1365-2443.2002. 00566.x 12167163 (Pubitemid 34947088)
19. VP Bermudez LA Lindsey-Boltz 2003 Cesare, A.J.; et al. Loading of the human 9-1-1 checkpoint complex onto DNA by the checkpoint clamp loader hRad17-replication factor C complex in vitro Proc Natl Acad Sci USA 100 1633 1638 1:CAS:528:DC%2BD3sXhsFGktLo%3D 10.1073/pnas.0437927100 12578958 (Pubitemid 36254499)
20. S Bao T Lu X Wang, et al. 2004 Disruption of the Rad9/Rad1/Hus1 (9-1-1) complex leads to checkpoint signaling and replication defects Oncogene 23 5586 5593 1:CAS:528:DC%2BD2cXlvVehsLY%3D 10.1038/sj.onc.1207753 15184880 (Pubitemid 39093036)
21. J Lee A Kumagai WG Dunphy 2007 The Rad9-Hus1-Rad1 checkpoint clamp regulates interaction of TopBP1 with ATR J Biol Chem 282 28036 28044 1:CAS:528:DC%2BD2sXhtVeisr3I 10.1074/jbc.M704635200 17636252 (Pubitemid 47529479)
22. A Gembka M Toueille E Smirnova, et al. 2007 The checkpoint clamp, Rad9-Rad1-Hus1 complex, preferentially stimulates the activity of apurinic/apyrimidinic endonuclease 1 and DNA polymerase beta in long patch base excision repair Nucleic Acids Res 35 2596 2608 1:CAS:528:DC%2BD2sXmt1WqsL0%3D 10.1093/nar/gkl1139 17426133 (Pubitemid 47073673)
23. W Wang P Brandt ML Rossi, et al. 2004 The human Rad9-Rad1-Hus1 checkpoint complex stimulates flap endonuclease 1 Proc Natl Acad Sci USA 101 16762 16767 1:CAS:528:DC%2BD2cXhtFansrzE 10.1073/pnas.0407686101 15556996 (Pubitemid 39601312)
24. E Friedrich-Heineken M Toueile B Tannler, et al. 2005 The two DNA clamps Rad9/Rad1/Hus1 complex and proliferating cell nuclear antigen differentially relate flap endonuclease I activity J Mol Biol 353 980 989 1:CAS:528: DC%2BD2MXhtFKms7fM 10.1016/j.jmb.2005.09.018 16216273 (Pubitemid 41503266)
25. M Toueille N El-Andaloussi I Frouin, et al. 2004 The human Rad9/Rad1/Hus1 damage sensor clamp interacts with DNA polymerase beta and increases its DNA substrate utilization efficiency: implications for DNA repair Nucleic Acid Res 32 3316 3324 1:CAS:528:DC%2BD2cXltlyju70%3D 10.1093/nar/gkh652 15314187 (Pubitemid 39117448)
26. E Smirnova M Toueille E Markkanen, et al. 2005 The human checkpoint sensor and alternative DNA clamp Rad9-Rad1-Hus1 modulates the activity of DNA ligase I, a component of the long-patch base excision repair machinery Biochem J 389 13 17 1:CAS:528:DC%2BD2MXmt1yktbg%3D 10.1042/BJ20050211 15871698 (Pubitemid 40978002)
27. G Shi DY Chang CC Cheng, et al. 2006 Physical and functional interactions between MutY homolog (MYH) and checkpoint proteins Rad9-Rad1-Hus1 Biochem J 400 53 62 1:CAS:528:DC%2BD28XhtFaksLjF 10.1042/BJ20060774 16879101 (Pubitemid 44763819)
28. X Guan H Bai G Shi, et al. 2007 The human checkpoint sensor Rad9-Rad1-Hus1 interacts with and stimulates NEIL1 glycosylase Nucleic Acids Res 35 2463 2472 1:CAS:528:DC%2BD2sXmt1Wqsrc%3D 10.1093/nar/gkm075 17395641 (Pubitemid 47073661)
29. X Guan A Madabushi DY Chang, et al. 2007 The human checkpoint sensor Rad9-Rad1-Hus1 interacts with and stimulates DNA repair enzyme TDG glycosylase Nucleic Acids Res 35 6207 6218 1:CAS:528:DC%2BD2sXht1ejsL3I 10.1093/nar/gkm678 17855402 (Pubitemid 350018582)
30. MM Slupska C Baikalov WM Luther, et al. 1996 Cloning and sequencing a human homolog (hMYH) of the Escherichia coli mutY gene whose function is required for the repair of oxidative DNA damage J Bacteriol 178 3885 3892 1:CAS:528:DyaK28XjvFegtrc%3D 8682794
31. T Ohtsubo K Nishioka Y Imaiso, et al. 2000 Identification of human MutY homolog (hMYH) as a repair enzyme for 2-hydroxyadenine in DNA and detection of multiple forms of hMYH located in nuclei and mitochondria Nucleic Acid Res 28 1355 1364 1:CAS:528:DC%2BD3cXit1GgsL8%3D 10.1093/nar/28.6.1355 10684930
32. K Shinmura H Kasai A Sasaki, et al. 1997 8-hydroxyguanine (7, 8-dihydro-8-oxoguanine) DNA glycosylase and AP lyase activities of hOGG1 protein and their substrate specificity Mutat Res 385 75 82 1:CAS:528: DyaK2sXlvVKqs7w%3D 9372850
33. K Sakumi M Furuichi T Tsuzuki, et al. 1993 Cloning and expression of cDNA for a human enzyme that hydrolyzes 8-oxo-dGTP, a mutagenic substrate for DNA synthesis J Biol Chem 268 23524 23530 1:CAS:528:DyaK3sXlvFKqurg%3D 8226881
34. A Parker Y Gu W Mahoney, et al. 2001 Human homolog of the MutY repair protein (hMYH) physically interacts with proteins involved in long patch DNA base excision repair J Biol Chem 276 5547 5555 1:CAS:528:DC%2BD3MXhs1KmsLs%3D 10.1074/jbc.M008463200 11092888
35. Y Gu A Parker TM Wilson, et al. 2002 Human MutY homolog, a DNA glycosylase involved in base excision repair, physically and functionally interacts with mismatch repair proteins human MutS homolog 2/human MutS homolog 6 J Biol Chem 277 11135 11142 1:CAS:528:DC%2BD38Xis1Khu7Y%3D 10.1074/jbc.M108618200 11801590 (Pubitemid 34952874)
36. DY Chang AL Lu 2005 Interaction of checkpoint proteins Hus1/Rad1/Rad9 with DNA base excision repair enzyme MutY homolog in fission yeast, Schizosaccharomyces pombe J Biol Chem 280 408 417 1:CAS:528:DC%2BD2cXhtFGgu7jL 15533944
37. PJ Lupardus KA Cimprich 2006 Phosphorylation of Xenopus Rad1 and Hus1 defines a readout for ATR activation that is independent of claspin and the Rad9 carboxy terminus Mol Biol Cell 17 1559 1569 1:CAS:528:DC%2BD28XltlSqu7o%3D 10.1091/mbc.E05-09-0865 16436514 (Pubitemid 44011576)
38. AT Brünger PD Adams GM Clore, et al. 1998 Crystallography & NMR system: A new software suite for macromolecular structure determination Acta Crystallogr D Biol Crystallogr 54 905 921 10.1107/S0907444998003254 9757107 (Pubitemid 28443603)
39. RE Campbell O Tour AE Palmer, et al. 2002 A monomeric red fluorescent protein Proc Natl Acad Sci USA 99 7877 7882 1:CAS:528:DC%2BD38XkvVGjsbw%3D 10.1073/pnas.082243699 12060735 (Pubitemid 34650973)
40. G Jach M Pesch K Richter, et al. 2006 An improved mRFP1 adds red to bimolecular fluorescence complementation Nat Methods 3 597 600 1:CAS:528:DC%2BD28XntFCgtLc%3D 10.1038/nmeth901 16862132 (Pubitemid 44123424)
41. I Hirai T Sasaki HG Wang 2004 Human hRad1 but not hRad9 protects hHus1 from ubiquitin-proteosomal degradation Oncogene 23 5124 5130 1:CAS:528:DC%2BD2cXlt1OksbY%3D 10.1038/sj.onc.1207658 15122316 (Pubitemid 38980345)
42. AS Doré ML Kilkenny NJ Rzechorzek LH Pearl 2009 Crystal structure of the Rad9-Rad1-Hus1 DNA damage checkpoint complex-implications for clamp loading and regulation Molecular Cell 34 735 745 10.1016/j.molcel.2009.04.027 19446481
43. SY Sohn Y Cho 2009 Crystal structure of the human Rad9-Rad1-Hus1 clamp J Mol Biol 390 490 502 1:CAS:528:DC%2BD1MXnsl2itb0%3D 10.1016/j.jmb.2009.05.028 19464297
44. CD Hu TK Kerppola 2003 Simultaneous visualization of multiple protein interactions in living cells using multicolor fluorescence complementation analysis Nat Biotechnol 21 539 545 1:CAS:528:DC%2BD3sXjt1OnsLk%3D 10.1038/nbt816 12692560 (Pubitemid 36532019)
45. DM Chudakov S Lukyanov KA Lukyanov 2005 Fluorescent proteins as a toolkit for in vivo imaging Trends Biotechnol 23 605 613 1:CAS:528:DC%2BD2MXht1Omu7vE 10.1016/j.tibtech.2005.10.005 16269193 (Pubitemid 41682374)
46. BN Giepmans SR Adams MH Ellisman, et al. 2006 The fluorescent toolbox for assessing protein location and function Science 312 217 224 1:CAS:528:DC%2BD28XjtlOjs70%3D 10.1126/science.1124618 16614209
47. MD Allen J Xhang 2006 Subcellular dynamics of protein kinase A activity visualized by FRET-based reporter Biochem Biophys Res Commun 348 716 721 1:CAS:528:DC%2BD28Xot1aiur0%3D 10.1016/j.bbrc.2006.07.136 16895723 (Pubitemid 44188622)
48. KA Lukyanov DM Chudakov S Lukyanov, et al. 2005 Innovation: Photoactivatable fluorescent proteins Nat Rev Mol Cell Biol 6 885 891 1:CAS:528:DC%2BD2MXhtFKlsLzJ 10.1038/nrm1741 16167053 (Pubitemid 41568737)