Molecular and cellular approaches for the detection of protein-protein interactions: Latest techniques and current limitations

Plant Journal

Volumn 53, Issue 4, 2008, Pages 610-635

  Lalonde, Sylvie ^a   Ehrhardt, David W ^a   Loqué, Dominique ^a   Chen, Jin ^a   Rhee, Seung Y ^a   Frommer, Wolf B ^a  

^a GEOPHYSICAL LABORATORY   (United States)

Author keywords

Co localization; Fluorescence correlation spectroscopy; Fluorescence resonance energy transfer; Protein interaction; Split GFP; Split ubiquitin

Indexed keywords

FLUORESCENCE SPECTROSCOPY; MASS SPECTROMETRY; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; SIGNAL TRANSDUCTION; SURFACE PLASMON RESONANCE; YEAST;

CO-LOCALIZATION; FLUORESCENCE CORRELATION SPECTROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; PROTEIN INTERACTION; SPLIT UBIQUITIN;

PROTEINS;

VEGETABLE PROTEIN;

BIOLOGICAL MODEL; CHEMISTRY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETICS; MASS SPECTROMETRY; METABOLISM; METHODOLOGY; PROTEIN ANALYSIS; PROTEIN BINDING; REVIEW; SURFACE PLASMON RESONANCE; TWO HYBRID SYSTEM;

FLUORESCENCE RESONANCE ENERGY TRANSFER; MASS SPECTROMETRY; MODELS, BIOLOGICAL; PLANT PROTEINS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; SURFACE PLASMON RESONANCE; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 38949195338     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2007.03332.x     Document Type: Review

References (199)

1. Adai, A.T., Date, S.V., Wieland, S. Marcotte, E.M. (2004) LGL: creating a map of protein function with an algorithm for visualizing very large biological networks. J. Mol. Biol., 340, 179 190.
2. Adjobo-Hermans, M.J., Goedhart, J. Gadella, T.W., Jr. (2006) Plant G protein heterotrimers require dual lipidation motifs of Gα and Gγ and do not dissociate upon activation. J. Cell Sci., 119, 5087 5097.
3. Ai, H.W., Henderson, J.N., Remington, S.J. Campbell, R.E. (2006) Directed evolution of a monomeric, bright and photostable version of Clavularia cyan fluorescent protein: structural characterization and applications in fluorescence imaging. Biochem. J. 400, 531 540.
4. Aker, J., Borst, J.W., Karlova, R. de Vries, S. (2006) The Arabidopsis thaliana AAA protein CDC48A interacts in vivo with the somatic embryogenesis receptor-like kinase 1 receptor at the plasma membrane. J. Struct. Biol. 156, 62 71.
5. Aker, J., Hesselink, R., Engel, R., Karlova, R. et al. (2007) In vivo hexamerization and characterization of the Arabidopsis AAA ATPase CDC48A-complex using FRET-FLIM and FCS. Plant Physiol., 145, 339 350.
6. Alberts, B. (1998) The cell as a collection of protein machines: preparing the next generation of molecular biologists. Cell, 92, 291 294.
7. Alon, U. (2003) Biological networks: the tinkerer as an engineer. Science, 301, 1866 1867.
8. Bacia, K., Kim, S.A. Schwille, P. (2006) Fluorescence cross-correlation spectroscopy in living cells. Nat. Methods, 3, 83 89.
9. Bader, G.D. Hogue, C.W. (2003) An automated method for finding molecular complexes in large protein interaction networks. BMC Bioinformatics, 4, 2.
10. Bader, J.S., Chaudhuri, A., Rothberg, J.M. Chant, J. (2004) Gaining confidence in high-throughput protein interaction networks. Nat. Biotechnol., 22, 78 85.
11. Barabasi, A.L. Albert, R. (1999) Emergence of scaling in random networks. Science, 286, 509 512.
12. Bartel, P.L., Roecklein, J.A., SenGupta, D. Fields, S. (1996) A protein linkage map of Escherichia coli bacteriophage T7. Nat. Genet. 12, 72 77.
13. Bastiaens, P.I.H. Squire, A. (1999) Fluorescence lifetime imaging microscopy: spatial resolution of biochemical processes in the cell. Trends Cell Biol. 9, 48 52.
14. Batagelj, V. Mrvar, A. (1998) Pajek - program for large network analysis. Connections, 21, 47 57.
15. Baxter, I., Ouzzani, M., Orcun, S., Kennedy, B. et al. (2007) Purdue Ionomics Information Management System. An integrated functional genomics platform. Plant Physiol. 143, 600 611.
16. Berney, C. Danuser, G. (2003) FRET or no FRET: a quantitative comparison. Biophys. J. 84, 3992 4010.
17. Bibi, E. Kaback, H.R. (1992) Functional complementation of internal deletion mutants in the lactose permease of Escherichia coli. Proc. Natl Acad. Sci. USA, 89, 1524 1528.
18. Biskup, C., Zimmer, T., Kelbauskas, L., Hoffmann, B. et al. (2007) Multi-dimensional fluorescence lifetime and FRET measurements. Microsc. Res. Tech. 70, 442 451.
19. Boozer, C., Kim, G., Cong, S.X., Guan, H.W. et al. (2006) Looking towards label-free biomolecular interaction analysis in a high-throughput format: a review of new surface plasmon resonance technologies. Curr. Opin. Biotechnol. 17, 400 405.
20. Breitkreutz, B.J., Stark, C. Tyers, M. (2003) Osprey: a network visualization system. Genome Biol. 4, R22.
21. Burz, D.S., Dutta, K., Cowburn, D. Shekhtman, A. (2006) Mapping structural interactions using in-cell NMR spectroscopy (STINT-NMR). Nat. Methods, 3, 91 93.
22. Cabantous, S., Terwilliger, T.C. Waldo, G.S. (2005) Protein tagging and detection with engineered self-assembling fragments of green fluorescent protein. Nat. Biotechnol. 23, 102 107.
23. Chatr-Aryamontri, A., Ceol, A., Montecchi Palazzi, L., Nardelli, G. et al. (2007) MINT: the Molecular INTeraction database. Nucleic Acids Res. 35, D572 D574.
24. Chattopadhyaya, R. Pal, A. (2004) Improved model of a LexA repressor dimer bound to recA operator. J. Biomol. Struct. Dyn. 21, 681 689.
25. Chen, H., Puhl, H.L., Koushik, S.V., Vogel, S.S. et al. (2006) Measurement of FRET efficiency and ratio of donor to acceptor concentration in living cells. Biophys. J. 91, L39 L41.
26. Cusick, M.E., Klitgord, N., Vidal, M. Hill, D.E. (2005) Interactome: gateway into systems biology. Hum. Mol. Genet. 14, R171 R181.
27. de Folter, S., Immink, R.G.H., Kieffer, M., Parenicova, L. et al. (2005) Comprehensive interaction map of the Arabidopsis MADS box transcription factors. Plant Cell, 17, 1424 1433.
28. de Prat-Gay, G. (1996) Association of complementary fragments and the elucidation of protein folding pathways. Protein Eng. 9, 843 847.
29. Demidov, V. Broude, N. (2006) Profluorescent protein fragments for fast bimolecular fluorescence complementation in vitro. Nat. Protoc. 1, 714 719.
30. Deuschle, K., Chaudhuri, B., Okumoto, S., Lager, I. et al. (2006) Rapid metabolism of glucose detected with FRET glucose nanosensors in epidermal cells and intact roots of Arabidopsis RNA-silencing mutants. Plant Cell, 18, 2314 2325.
31. Dixit, R., Cyr, R. Gilroy, S. (2006) Using intrinsically fluorescent proteins for plant cell imaging. Plant J. 45, 599 615.
32. Donaldson, I., Martin, J., de Bruijn, B., Wolting, C. et al. (2003) PreBIND and Textomy - mining the biomedical literature for protein-protein interactions using a support vector machine. BMC Bioinformatics, 4, 11.
33. Fehr, M., Okumoto, S., Deuschle, K., Lager, I. et al. (2005) Development and use of fluorescent nanosensors for metabolite imaging in living cells. Biochem. Soc. Trans. 33, 287 290.
34. Fields, S. Song, O.K. (1989) A novel genetic system to detect protein-protein interactions. Nature, 340, 245 246.
35. Formstecher, E., Aresta, S., Colluar, V., Hamburger, A. et al. (2005) Protein interaction mapping: a Drosophila case study. Genome Res. 15, 376 384.
36. Förster, T. (1948) Intermolecular energy migration and fluorescence. Ann. Phys. 2, 55 75.
37. Franca-Koh, J., Kamimura, Y. Devreotes, P. (2006) Navigating signaling networks: chemotaxis in Dictyostelium discoideum. Curr. Opin. Genet. Dev. 16, 333 338.
38. Frommer, W. Ninnemann, O. (1995) Heterologous expression of genes in bacterial, fungal, animal, and plant cells. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46, 419 444.
39. Fung, B.K.K. Stryer, L. (1978) Surface density determination in membranes by fluorescence energy-transfer. Biochemistry, 17, 5241 5248.
40. Galarneau, A., Primeau, M., Trudeau, L.E. Michnick, S.W. (2002) β-Lactamase protein fragment complementation assays as in vivo and in vitro sensors of protein-protein interactions. Nat. Biotechnol. 20, 619 622.
41. Gansner, E.R. North, S.C. (2000) An open graph visualization system and its applications to software engineering. Software Pract. Exp. 30, 1203 1233.
42. Gavin, A.C., Bosche, M., Krause, R., Grandi, P. et al. (2002) Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature, 415, 141 147.
43. Gavin, A.C., Aloy, P., Grandi, P., Krause, R. et al. (2006) Proteome survey reveals modularity of the yeast cell machinery. Nature, 440, 631 636.
44. Geisler-Lee, J., O'Toole, N., Ammar, R., Provart, N.J. et al. (2007) A predicted interactome for arabidopsis. Plant Physiol., 145, 317 329.
45. Gerhart, J. Kirschner, M. (1997) Cells, Embryos, and Evolution: Toward a Cellular and Developmental Understanding of Phenotypic Variation and Evolutionary Adaptability. Oxford: Blackwell Science.
46. Ghosh, I., Hamilton, A.D. Regan, L. (2000) Antiparallel leucine zipper-directed protein reassembly: application to the green fluorescent protein. J. Am. Chem. Soc. 122, 5658 5659.
47. Gilbert, D. (2005) Biomolecular interaction network database. Brief Bioinformatics, 6, 194 198.
48. Giot, L., Bader, J.S., Brouwer, C., Chaudhuri, A. et al. (2003) A protein interaction map of Drosophila melanogaster. Science, 302, 1727 1736.
49. Goedhart, J., Hink, M.A., Visser, A., Bisseling, T. et al. (2000) In vivo fluorescence correlation microscopy (FCM) reveals accumulation and immobilization of Nod factors in root hair cell walls. Plant J. 21, 109 119.
50. Gordon, G.W., Berry, G., Liang, X.H., Levine, B. et al. (1998) Quantitative fluorescence resonance energy transfer measurements using fluorescence microscopy. Biophys. J. 74, 2702 2713.
51. Gratton, E., Breusegem, S., Sutin, J., Ruan, Q. et al. (2003) Fluorescence lifetime imaging for the two-photon microscope: time-domain and frequency-domain methods. J. Biomed. Opt. 8, 381 390.
52. Grefen, C., Lalonde, S. Obrdlik, P. (2007) Split-ubiquitin system for identifying protein-protein interactions in membrane and full-length proteins. Curr. Protoc. Neurosci. Unit 5.27, 5.27.1 5.27.40.
53. Griesbeck, O., Baird, G.S., Campbell, R.E., Zacharias, D.A. et al. (2001) Reducing the environmental sensitivity of yellow fluorescent protein. Mechanism and applications. J. Biol. Chem. 276, 29188 29194.
54. Grigoriev, A. (2003) On the number of protein-protein interactions in the yeast proteome. Nucleic Acids Res. 31, 4157 4161.
55. Gu, H., Lalonde, S., Okumoto, S., Looger, L.L. et al. (2006) A novel analytical method for in vivo phosphate tracking. FEBS Lett. 580, 5885 5893.
56. Guelzim, N., Bottani, S., Bourgine, P. Kepes, F. (2002) Topological and causal structure of the yeast transcriptional regulatory network. Nat. Genet. 31, 60 63.
57. Harary, F. (1969) Graph Theory. Boston: Addison-Wesley.
58. Hartuv, E., Schmitt, A.O., Lange, J., Meier-Ewert, S. et al. (2000) An algorithm for clustering cDNA fingerprints. Genomics, 66, 249 256.
59. Heim, N. Griesbeck, O. (2004) Genetically encoded indicators of cellular calcium dynamics based on troponin C and green fluorescent protein. J. Biol. Chem. 279, 14280 14286.
60. Hermjakob, H., Montecchi-Palazzi, L., Bader, G., Wojcik, R. et al. (2004a) The HUPO PSI's molecular interaction format - a community standard for the representation of protein interaction data. Nat. Biotechnol. 22, 177 183.
61. Hermjakob, H., Montecchi-Palazzi, L., Lewington, C., Mudali, S. et al. (2004b) IntAct: an open source molecular interaction database. Nucleic Acids Res. 32, D452 D455.
62. Hink, M.A., Borst, J.W. Visser, A. (2003) Fluorescence correlation spectroscopy of GFP fusion proteins in living plant cells. Method Enzymol. 361, 93 112.
63. Hinterdorfer, P. Dufrene, Y.F. (2006) Detection and localization of single molecular recognition events using atomic force microscopy. Nat. Methods, 3, 347 355.
64. Ho, Y., Gruhler, A., Heilbut, A., Bader, G.D. et al. (2002) Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature, 415, 180 183.
65. Hu, C.-D., Chinenov, Y. Kerppola, T.K. (2002) Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol. Cell, 9, 789 798.
66. Huang, X.Y., Holden, H.M. Raushel, F.M. (2001) Channeling of substrates and intermediates in enzyme-catalyzed reactions. Annu. Rev. Biochem. 70, 149 180.
67. Islam, M., Wallin, R., Wynn, R., Conway, M. et al. (2007) A novel branched-chain amino acid metabolon: Protein-protein interactions in a supramolecular complex. J. Biol. Chem., 282, 11893 11903.
68. Ito, T., Tashiro, K., Muta, S., Ozawa, R. et al. (2000) Toward a protein-protein interaction map of the budding yeast: A comprehensive system to examine two-hybrid interactions in all possible combinations between the yeast proteins. Proc. Natl Acad. Sci. USA, 97, 1143 1147.
69. Ito, T., Chiba, T., Ozawa, R., Yoshida, M. et al. (2001) A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc. Natl Acad. Sci. USA, 98, 4569 4574.
70. Jares-Erijman, E.A. Jovin, T.M. (2003) FRET imaging. Nat. Biotechnol. 21, 1387 1395.
71. Jares-Erijman, E.A. Jovin, T.M. (2006) Imaging molecular interactions in living cells by FRET microscopy. Curr. Opin. Chem. Biol. 10, 409 416.
72. Jeong, H., Mason, S.P., Barabasi, A.L. Oltvai, Z.N. (2001) Lethality and centrality in protein networks. Nature, 411, 41 42.
73. Ji, Z.L., Chen, X., Zhen, C.J., Yao, L.X. et al. (2003) KDBI: Kinetic Data of Bio-molecular Interactions database. Nucleic Acids Res., 31, 255 257.
74. Jin, F.L., Hazbun, T., Michaud, G.A., Salcius, M. et al. (2006) A pooling-deconvolution strategy for biological network elucidation. Nat. Methods, 3, 183 189.
75. Johnsson, N. Varshavsky, A. (1994) Split Ubiquitin as a sensor of protein interactions in vivo. Proc. Natl Acad. Sci. USA, 91, 10340 10344.
76. 1A receptors. IUBMB Life, 57, 505 512.
77. Karasawa, S., Araki, T., Nagai, T., Mizuno, H. et al. (2004) Cyan-emitting and orange-emitting fluorescent proteins as a donor/acceptor pair for fluorescence resonance energy transfer. Biochem. J. 381, 307 312.
78. Kashtan, N., Itzkovitz, S., Milo, R. Alon, U. (2004) Efficient sampling algorithm for estimating subgraph concentrations and detecting network motifs. Bioinformatics, 20, 1746 1758.
79. Kerrien, S., Alam-Faruque, Y., Aranda, B., Bancarz, I. et al. (2007) IntAct - open source resource for molecular interaction data. Nucleic Acids Res. 35, D561 565.
80. Köhler, R.H., Cao, J., Zipfel, W.R., Webb, W.W. et al. (1997) Exchange of protein molecules through connections between higher plant plastids. Science, 276, 2039 2042.
81. Köhler, R.H., Schwille, P., Webb, W.W. Hanson, M.R. (2000) Active protein transport through plastid tubules: velocity quantified by fluorescence correlation spectroscopy. J. Cell Sci., 113, 3921 3930.
82. Korf, U. Wiemann, S. (2005) Protein microarrays as a discovery tool for studying protein-protein interactions. Expert Rev. Proteomics, 2, 13 26.
83. Koushik, S.V., Chen, H., Thaler, C., Puhl, H.L. et al. (2006) Cerulean, Venus, and Venus(Y67C) FRET reference standards. Biophys. J. 91, L99 L101.
84. Kozer, N., Kuttner, Y.Y., Haran, G. Schreiber, G. (2007) Protein-protein association in polymer solutions: from dilute to semidilute to concentrated. Biophys. J. 92, 2139 2149.
85. Krishnaswamy, S.R., Williams, E.R. Kirsch, J.F. (2006) Free energies of protein-protein association determined by electrospray ionization mass spectrometry correlate accurately with values obtained by solution methods. Protein Sci. 15, 1465 1475.
86. Krogan, N.J., Cagney, G., Yu, H.Y., Zhong, G.Q. et al. (2006) Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature, 440, 637 643.
87. Kumaran, S. Jez, J.M. (2007) Thermodynamics of the interaction between O-acetylserine sulfhydrylase and the C-terminus of serine acetyltransferase. Biochemistry, 46, 5586 5594.
88. Kuramochi, M. Karypis, G. (2004) Finding Frequent Patterns in a Large Sparse Graph. Lake Buena Vista, Florida: SIAM International Conference on Data Mining.
89. Lakey, J.H. Raggett, E.M. (1998) Measuring protein-protein interactions. Curr. Opin. Struct. Biol. 8, 119 123.
90. Lakowicz, J.R. (2006) Principles of Fluorescence Spectroscopy, 3rd edn. New York: Springer.
91. Lalonde, S., Ehrhardt, D.W. Frommer, W.B. (2005) Shining light on signaling and metabolic networks by genetically encoded biosensors. Curr. Opin. Plant Biol. 8, 574 581.
92. Li, S.M., Armstrong, C.M., Bertin, N., Ge, H. et al. (2004) A map of the interactome network of the metazoan C. elegans. Science, 303, 540 543.
93. Lin, S., Chen, J., Huang, L. Lin, H. (2005) Measurements of the forces in protein interactions with atomic force microscopy. Curr. Proteomics, 2, 55.
94. Lipson, H., Pollack, J.B. Suh, N.P. (2002) On the origin of modular variation. Evolution, 56, 1549 1556.
95. + channel. Science, 309, 897 903.
96. Loqué, D., Lalonde, S., Looger, L., von Wirén, N. et al. (2007) Trans-activation and cooperativity in an ammonium transporter complex. Nature, 446, 195 198.
97. + uniporters. J. Biol. Chem. 278, 45603 45610.
98. MacKinnon, R. (1991) Determination of the subunit stoichiometry of a voltage-activated potassium channel. Nature, 350, 232 235.
99. Magliery, T.J., Wilson, C.G.M., Pan, W.L., Mishler, D. et al. (2005) Detecting protein-protein interactions with a green fluorescent protein fragment reassembly trap: scope and mechanism. J. Am. Chem. Soc., 127, 146 157.
100. McDonnell, J.M. (2001) Surface plasmon resonance: towards an understanding of the mechanisms of biological molecular recognition. Curr. Opin. Chem. Biol., 5, 572 577.
101. Mena, M.A., Treynor, T.P., Mayo, S.L. Daugherty, P.S. (2006) Blue fluorescent proteins with enhanced brightness and photostability from a structurally targeted library. Nat. Biotechnol., 24, 1569 1571.
102. Meseth, U., Wohland, T., Rigler, R. Vogel, H. (1999) Resolution of fluorescence correlation measurements. Biophys. J. 76, 1619 1631.
103. Meyer, R., Steinfath, M., Lisec, J., Becher, M. et al. (2007) The metabolic signature related to high plant growth rate in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA, 104, 4759 4764.
104. Miernyk, J.A. Thelen, J.J. (2008) Biochemical approaches for discovering protein-protein interactions. Plant J. 53, 597 609.
105. Miller, J.P., Lo, R.S., Ben-Hur, A., Desmarais, C. et al. (2005) Large-scale identification of yeast integral membrane protein interactions. Proc. Natl Acad. Sci. USA, 102, 12123 12128.
106. Milo, R., Shen-Orr, S., Itzkovitz, S., Kashtan, N. et al. (2002) Network motifs: simple building blocks of complex networks. Science, 298, 824 827.
107. Mitra, R.D., Silva, C.M. Youvan, D.C. (1996) Fluorescence resonance energy transfer between blue-emitting and red-shifted excitation derivatives of the green fluorescent protein. Gene, 173, 13 17.
108. Mitra, R.M., Gleason, C.A., Edwards, A., Hadfield, J. et al. (2004) A Ca2 + /calmodulin-dependent protein kinase required for symbiotic nodule development: Gene identification by transcript-based cloning. Proc. Natl Acad. Sci. USA, 101, 4701 4705.
109. Müller, J.D., Chen, Y. Gratton, E. (2003) Fluorescence correlation spectroscopy. Methods Enzymol. 361, 69 92.
110. Nagai, T., Ibata, K., Park, E.S., Kubota, M. et al. (2002) A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat. Biotechnol. 20, 8790.
111. Nguyen, A. Daugherty, P. (2005) Evolutionary optimization of fluorescent proteins for intracellular FRET. Nat. Biotechnol. 23, 355 360.
112. Nooren, I.M. Thornton, J.M. (2003) Diversity of protein-protein interactions. EMBO J. 22, 3486 3492.
113. Nühse, T.S., Stensballe, A., Jensen, O.N. Peck, S.C. (2004) Phosphoproteomics of the arabidopsis plasma membrane and a new phosphorylation site database. Plant Cell, 16, 2394 2405.
114. + channel interactions detected by a genetic system optimized for systematic studies of membrane protein interactions. Proc. Natl Acad. Sci. USA, 101, 12242 12247.
115. Okumoto, S., Looger, L.L., Micheva, K.D., Reimer, R.J. et al. (2005) Detection of glutamate release from neurons by genetically encoded surface-displayed FRET nanosensors. Proc. Natl Acad. Sci. USA, 102, 8740 8745.
116. Pagel, P., Kovac, S., Oesterheld, M., Brauner, B. et al. (2005) The MIPS mammalian protein-protein interaction database. Bioinformatics, 21, 832 834.
117. Paulmurugan, R., Umezawa, Y. Gambhir, S.S. (2002) Non-invasive imaging of protein-protein interactions in living subjects by using reporter protein complementation and reconstitution strategies. Proc. Natl Acad. Sci. USA, 99, 15608 15613.
118. Pelet, S., Previte, M.J.R. So, P.T.C. (2006) Comparing the quantification of Förster resonance energy transfer measurement accuracies based on intensity, spectral, and lifetime imaging. J. Biomed. Opt., 11, 34017.
119. Pelletier, J.N., Campbell-Valois, F.X. Michnick, S.W. (1998) Oligomerization domain-directed reassembly of active dihydrofolate reductase from rationally designed fragments. Proc. Natl Acad. Sci. USA, 95, 12141 12146.
120. Pelletier, J.N., Arndt, K.M., Pluckthun, A. Michnick, S.W. (1999) An in vivo library-versus-library selection of optimized protein-protein interactions. Nat. Biotechnol. 17, 683 690.
121. Pellicena, P. Kuriyan, J. (2006) Protein-protein interactions in the allosteric regulation of protein kinases. Curr. Opin. Struct. Biol. 16, 702 709.
122. Perozzo, R., Folkers, G. Scapozza, L. (2004) Thermodynamics of protein-ligand interactions: history, presence, and future aspects. J. Recept. Signal Transduct. 24, 1 52.
123. Philip, J. Carlsson, K. (2003) Theoretical investigation of the signal-to-noise ratio in fluorescence lifetime imaging. J. Opt. Soc. Am. A, 20, 368 379.
124. Popescu, S., Popescu, G., Bachan, S., Zhang, Z. et al. (2007) Differential binding of calmodulin-related proteins to their targets revealed through high-density Arabidopsis protein microarrays. Proc. Natl Acad. Sci. USA, 104, 4730 4735.
125. Przulj, N., Wigle, D.A. Jurisica, I. (2004) Functional topology in a network of protein interactions. Bioinformatics, 20, 340 348.
126. Rain, J.C., Selig, L., De Reuse, H., Battaglia, V. et al. (2001) The protein-protein interaction map of Helicobacter pylori. Nature, 409, 211 215.
127. Raquet, X., Eckert, J.H., Muller, S. Johnsson, N. (2001) Detection of altered protein conformations in living cells. J. Mol. Biol., 305, 927 938.
128. Redford, G.I. Clegg, R.M. (2005) Polar plot representation for frequency-domain analysis of fluorescence lifetimes. J. Fluoresc. 15, 805 815.
129. Reichmann, D., Rahat, O., Albeck, S., Meged, R. et al. (2005) The modular architecture of protein-protein binding interfaces. Proc. Natl Acad. Sci. USA, 102, 57 62.
130. Reichmann, D., Rahat, O., Cohen, M., Neuvirth, H. et al. (2007) The molecular architecture of protein-protein binding sites. Curr. Opin. Struct. Biol. 17, 67 76.
131. Reinders, A., Schulze, W., Kühn, C., Barker, L. et al. (2002a) Protein-protein interactions between sucrose transporters of different affinities co-localized in the same enucleate sieve element. Plant Cell, 14, 1567 1577.
132. Reinders, A., Schulze, W., Thaminy, S., Stagljar, I. et al. (2002b) Intra- and intermolecular interactions in sucrose transporters at the plasma membrane detected by split-ubiquitin system and functional assays. Structure, 10, 763 772.
133. Remy, I. Michnick, S.W. (2006) A highly sensitive protein-protein interaction assay based on Gaussia luciferase. Nat. Methods, 3, 977 979.
134. Rich, R.L. Myszka, D.G. (2000) Advances in surface plasmon resonance biosensor analysis. Curr. Opin. Biotechnol. 11, 54 61.
135. Rizzo, M.A., Springer, G.H., Granada, B. Piston, D.W. (2004) An improved cyan fluorescent protein variant useful for FRET. Nat. Biotechnol. 22, 445 449.
136. Rizzo, M.A., Springer, G., Segawa, K., Zipfel, W.R. et al. (2006) Optimization of pairings and detection conditions for measurement of FRET between cyan and yellow fluorescent proteins. Microsc. Microanal. 12, 238 254.
137. 2+/CaM kinase II. FEBS Lett. 273, 682 694.
138. Rossi, F., Charlton, C.A. Blau, H.M. (1997) Monitoring protein-protein interactions in intact eukaryotic cells by beta-galactosidase complementation. Proc. Natl Acad. Sci. USA, 94, 8405 8410.
139. Rual, J.F., Venkatesan, K., Hao, T., Hirozane-Kishikawa, T. et al. (2005) Towards a proteome-scale map of the human protein-protein interaction network. Nature, 437, 1173 1178.
140. Russinova, E., Borst, J.W., Kwaaitaal, M., Cano-Delgado, A. et al. (2004) Heterodimerization and endocytosis of Arabidopsis brassinosteroid receptors BRI1 and AtSERK3 (BAK1). Plant Cell, 16, 3216 3229.
141. Saito, R., Suzuki, H. Hayashizaki, Y. (2002) Interaction generality, a measurement to assess the reliability of a protein-protein interaction. Nucleic Acids Res. 30, 1163 1168.
142. Saito, R., Suzuki, H. Hayashizaki, Y. (2003) Construction of reliable protein-protein interaction networks with a new interaction generality measure. Bioinformatics, 19, 756 763.
143. Schevitz, R.W., Otwinowski, Z., Joachimiak, A., Lawson, C.L. et al. (1985) The 3-dimensional structure of Trp repressor. Nature, 317, 782 786.
144. Schonberger, O., Knox, C., Bibi, E. Pines, O. (1996) Split invertase polypeptides form functional complexes in the yeast periplasm in vivo. Proc. Natl Acad. Sci. USA, 93, 9612 9617.
145. Schreiber, F. Schwobbermeyer, H. (2004) Towards Motif Detection in Networks: Frequency Concepts and Flexible Search. Camerino, Italy: NETTAB'04.
146. Schuck, P. (1997a) Use of surface plasmon resonance to probe the equilibrium and dynamic aspects of interactions between biological macromolecules. Annu. Rev. Biophys. Biomol. Struct. 26, 541 566.
147. Schuck, P. (1997b) Reliable determination of binding affinity and kinetics using surface plasmon resonance biosensors. Curr. Opin. Biotechnol. 8, 498 502.
148. Schwacke, R., Schneider, A., van der Graaff, E., Fischer, K. et al. (2003) ARAMEMNON, a novel database for Arabidopsis integral membrane proteins. Plant Physiol. 131, 16 26.
149. Schwille, P., Meyer-Almes, F.J. Rigler, R. (1997) Dual-color fluorescence cross-correlation spectroscopy for multicomponent diffusional analysis in solution. Biophys. J. 72, 1878 1886.
150. Schwille, P., Haupts, U., Maiti, S. Webb, W.W. (1999) Molecular dynamics in living cells observed by fluorescence correlation spectroscopy with one- and two-photon excitation. Biophys. J. 77, 2251 2265.
151. Shaner, N.C., Campbell, R.E., Steinbach, P.A., Giepmans, B.N.G. et al. (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp red fluorescent protein. Nat. Biotechnol. 22, 1567 1572.
152. Shaner, N.C., Steinbach, P.A. Tsien, R.Y. (2005) A guide to choosing fluorescent proteins. Nat. Methods, 2, 905 909.
153. Shannon, P., Markiel, A., Ozier, O., Baliga, N.S. et al. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498 2504.
154. Shaw, S.L. (2006) Imaging the live plant cell. Plant J. 45, 573 598.
155. Shen, K., Teruel, M.N., Connor, J.H., Shenolikar, S. et al. (2000) Molecular memory by reversible translocation of calcium/calmodulin-dependent protein kinase II. Nat. Neurosci. 3, 881 886.
156. Shen, Q.H., Saijo, Y., Mauch, S., Biskup, C. et al. (2007) Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science, 315, 1098 1103.
157. Shoemaker, B. Panchenko, A. (2007) Deciphering protein-protein interactions. Part I. Experimental techniques and databases. PLoS Comput. Biol. 3, e42.
158. Spotts, J.M., Dolmetscht, R.E. Greenberg, M.E. (2002) Time-lapse imaging of a dynamic phosphorylation dependent protein-protein interaction in mammalian cells. Proc. Natl Acad. Sci. USA, 99, 15142 15147.
159. Sprangers, R. Kay, L.E. (2007) Quantitative dynamics and binding studies of the 20S proteasome by NMR. Nature, 445, 618 622.
160. Stagljar, I., Korostensky, C., Johnsson, N. te Heesen, S. (1998) A genetic system based on split-ubiquitin for the analysis of interactions between membrane proteins in vivo. Proc. Natl Acad. Sci. USA, 95, 5187 5192.
161. Stanyon, C.A., Liu, G.Z., Mangiola, B.A., Patel, N. et al. (2004) A Drosophila protein-interaction map centered on cell-cycle regulators. Genome Biol. 5, R96.
162. Stark, C., Breitkreutz, B.J., Reguly, T., Boucher, L. et al. (2006) BioGRID: a general repository of interaction datasets. Nucleic Acids Res. 34, D535 D539.
163. Stelzl, U., Worm, U., Lalowski, M., Haenig, C. et al. (2005) A human protein-protein interaction network: a resource for annotating the proteome. Cell, 122, 957 968.
164. Stryer, L. (1978) Fluorescence energy transfer as a spectroscopic ruler. Annu. Rev. Biochem. 47, 819 846.
165. Subramaniam, V., Hanley, Q.S., Clayton, A.H.A. Jovin, T.M. (2003) Photophysics of green and red fluorescent proteins: Implications for quantitative microscopy. In Methods Enzymol. 360, 178 201.
166. Subramanian, C., Kim, B.H., Lyssenko, N.N., Xu, X. et al. (2004) The Arabidopsis repressor of light signaling, COP1, is regulated by nuclear exclusion: Mutational analysis by bioluminescence resonance energy transfer. Proc. Natl Acad. Sci. USA, 101, 6798 6802.
167. Subramanian, C., Woo, J., Cai, X., Xu, X.D. et al. (2006) A suite of tools and application notes for in vivo protein interaction assays using bioluminescence resonance energy transfer (BRET). Plant J. 48, 138 152.
168. Thaler, C., Koushik, S.V., Blank, P.S. Vogel, S.S. (2005) Quantitative multiphoton spectral imaging and its use for measuring resonance energy transfer. Biophys. J. 89, 2736 2749.
169. Trakselis, M.A., Alley, S.C. Ishmael, F.T. (2005) Identification and mapping of protein-protein interactions by a combination of cross-linking, cleavage, and proteomics. Bioconjug. Chem. 16, 741 750.
170. Uetz, P., Giot, L., Cagney, G., Mansfield, T.A. et al. (2000) A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature, 403, 623 627.
171. van Munster, E.B. Gadella, T.W.J. (2005) Fluorescence lifetime imaging microscopy (FLIM). Adv. Biochem. Engin./Biotechnol. 95, 143 175.
172. Vasilescu, J. Figeys, D. (2006) Mapping protein-protein interactions by mass spectrometry. Curr. Opin. Biotechnol. 17, 394 399.
173. Vaughan, C.K., Buckle, A.M. Fersht, A.R. (1999) Structural response to mutation at a protein-protein interface. J. Mol. Biol. 286, 1487 1506.
174. Vidal, M. (2005) Interactome modeling. FEBS Lett. 579, 1834 1838.
175. Vidalain, P.O., Boxem, M., Ge, H., Li, S.M. et al. (2004) Increasing specificity in high-throughput yeast two-hybrid experiments. Methods, 32, 363 370.
176. Vogel, S.S., Thaler, C. Koushik, S.V. (2006) Fanciful FRET. Sci. STKE, 2006, re2.
177. Wagner, A. (2003) Does selection mold molecular networks? Sci. STKE, 202, pe41.
178. Walhout, A.J.M., Sordella, R., Lu, X.W., Hartley, J.L. et al. (2000) Protein interaction mapping in C. elegans using proteins involved in vulval development. Science, 287, 116 122.
179. Walter, M., Chaban, C., Schutze, K., Batistic, O. et al. (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J. 40, 428 438.
180. Wang, T. Montell, C. (2007) Phototransduction and retinal degeneration in Drosophila. Eur. J. Physiol. 454, 821 847.
181. Watts, D.J. Strogatz, S.H. (1998) Collective dynamics of 'small-world' networks. Nature, 393, 440 442.
182. Wehr, M.C., Laage, R., Bolz, U., Fischer, T.M. et al. (2006) Monitoring regulated protein-protein interactions using split TEV. Nat. Methods, 3, 985 993.
183. Wei, N. Deng, X.W. (2003) The COP9 signalosome. Annu. Rev. Cell. Dev. Biol. 19, 261 286.
184. Wiechert, W., Schweissgut, O., Takanaga, H. Frommer, W.B. (2007) Fluxomics: mass spectrometry versus quantitative imaging. Curr. Opin. Plant Biol. 10, 323 330.
185. Wouters, F.S. (2006) The physics and biology of fluorescence microscopy in the life sciences. Contemp. Phys. 47, 239 255.
186. Wrubel, W., Stochaj, U. Ehring, R. (1994) Construction and in vivo analysis of new split lactose permeases. FEBS Lett. 349, 433 438.
187. Xenarios, I., Salwinski, L., Duan, X.Q.J., Higney, P. et al. (2002) DIP, the Database of Interacting Proteins: a research tool for studying cellular networks of protein interactions. Nucleic Acids Res. 30, 303 305.
188. Xia, Y., Lu, L.J. Gerstein, M. (2006) Integrated prediction of the helical membrane protein interactome in yeast. J. Mol. Biol. 357, 339 349.
189. Xu, X.D., Soutto, M., Xie, Q., Servick, S. et al. (2007) Imaging protein interactions with bioluminescence resonance energy transfer (BRET) in plant and mammalian cells and tissues. Proc. Natl Acad. Sci. USA, 104, 10264 10269.
190. Xu, Y., Piston, D.W. Hirschie Johnson, C. (1999) A bioluminescence resonance energy transfer (BRET) system: application to interacting circadian clock proteins. Proc. Natl Acad. Sci. USA, 96, 151 156.
191. Yanes, O., Villanueva, J., Querol, E. Aviles, F.X. (2007) Detection of non-covalent protein interactions by 'intensity fading' MALDI-TOF mass spectrometry: applications to proteases and protease inhibitors. Nat. Protoc. 2, 119 130.
192. Yeger-Lotem, E., Sattath, S., Kashtan, N., Itzkovitz, S. et al. (2004) Network motifs in integrated cellular networks of transcription-regulation and protein-protein interaction. Proc. Natl Acad. Sci. USA, 101, 5934 5939.
193. Yersin, A., Hirling, H., Steiner, P., Magnin, S. et al. (2003) Interactions between synaptic vesicle fusion proteins explored by atomic force microscopy. Proc. Natl Acad. Sci. USA, 100, 8736 8741.
194. Yu, J., Wang, J., Lin, W., Li, S. et al. (2005) The Genomes of Oryza sativa: a history of duplications. PLoS Biol. 3, e38.
195. Zacharias, D.A., Violin, J.D., Newton, A.C. Tsien, R.Y. (2002) Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science, 296, 913 916.
196. Zamyatnin, A.A., Solovyev, A.G., Bozhkov, P.V., Valkonen, J.P.T. et al. (2006) Assessment of the integral membrane protein topology in living cells. Plant J. 46, 145 154.
197. Zhong, J.H., Zhang, H.M., Stanyon, C.A., Tromp, G. et al. (2003) A strategy for constructing large protein interaction maps using the yeast two-hybrid system: regulated expression arrays and two-phase mating. Genome Res. 13, 2691 2699.
198. Zimmermann, T., Rietdorf, J., Girod, A., Georget, V. et al. (2002) Spectral imaging and linear un-mixing enables improved FRET efficiency with a novel GFP2-YFP FRET pair. FEBS Lett. 531, 245 249.
199. Zimmermann, T., Rietdorf, J. Pepperkok, R. (2003) Spectral imaging and its applications in live cell microscopy. FEBS Lett. 546, 87 92.