Optical sensors to gain mechanistic insights into signaling assemblies

Current Opinion in Structural Biology

Volumn 41, Issue , 2016, Pages 203-210

  Tenner, Brian ^a,b   Mehta, Sohum ^a   Zhang, Jin ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; GREEN FLUORESCENT PROTEIN; MULTIPROTEIN COMPLEX; SIGNALOSOME; UNCLASSIFIED DRUG;

BIOSENSOR; COMPLEX FORMATION; FLUOROMETRY; FORSTER RESONANCE ENERGY TRANSFER; GENETICALLY ENCODED OPTICAL SENSOR; HUMAN; INTRACELLULAR SIGNALING; MOLECULAR DYNAMICS; NONHUMAN; OPTICAL SENSOR; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN STRUCTURE; REVIEW; SIGNAL NOISE RATIO; SIGNAL TRANSDUCTION; GENETIC PROCEDURES; LIGHT RELATED PHENOMENA; PROCEDURES;

BIOSENSING TECHNIQUES; OPTICAL PHENOMENA; SIGNAL TRANSDUCTION;

EID: 84985011825     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2016.07.021     Document Type: Review

References (64)

1. 1 Cebecauer, M., Spitaler, M., Sergé, A., Magee, A.I., Signalling complexes and clusters: functional advantages and methodological hurdles. J Cell Sci 123 (2010), 309–320.
2. 2 Dean, K.M., Palmer, A.E., Advances in fluorescence labeling strategies for dynamic cellular imaging. Nat Chem Biol 10 (2014), 512–523.
3. 3 Altschuler, S.J., Wu, L.F., Cellular heterogeneity: do differences make a difference?. Cell 141 (2010), 559–563.
4. 4 DiPilato, L.M., Zhang, J., Fluorescent protein-based biosensors: resolving spatiotemporal dynamics of signaling. Curr Opin Chem Biol 14 (2010), 37–42.
5. 5 Cheng, S., Li, Y., Yang, Y., Feng, D., Yang, L., Ma, Q., Zheng, S., Meng, R., Wang, S., Wang, S., et al. Breast cancer-derived K172N, D301V mutations abolish Na+/H + exchanger regulatory factor 1 inhibition of platelet-derived growth factor receptor signaling. FEBS Lett 587 (2013), 3289–3295.
6. 6 Selkoe, D.J., Cell biology of protein misfolding: the examples of Alzheimer's and Parkinson's diseases. Nat Cell Biol 6 (2004), 1054–1061.
7. 7 Stryer, L., Haugland, R.P., Energy transfer: a spectroscopic ruler. Proc Natl Acad Sci U S A 58 (1967), 719–726.
8. 8 Tsien, R.Y., The green fluorescent protein. Proteins 67 (1998), 509–544.
9. 9 Clister, T., Mehta, S., Zhang, J., Single-cell analysis of G-protein signal transduction. J Biol Chem 290 (2015), 6681–6688.
10. 10 Lohse, M.J., Nuber, S., Hoffmann, C., Fluorescence/bioluminescence resonance energy transfer techniques to study g-protein-coupled receptor activation and signaling. Pharmacol Rev 64 (2012), 299–336.
11. 11 Vilardaga, J.-P., Bünemann, M., Krasel, C., Castro, M., Lohse, M.J., Measurement of the millisecond activation switch of G protein-coupled receptors in living cells. Nat Biotechnol 21 (2003), 807–812.
12. 12 Salahpour, A., Espinoza, S., Masri, B., Lam, V., Barak, L.S., Gainetdinov, R.R., BRET biosensors to study GPCR biology, pharmacology, and signal transduction. Front Endocrinol (Lausanne) 3 (2012), 1–9.
13. 13 Chen, H., Puhl, H.L., Koushik, S.V., Vogel, S.S., Ikeda, S.R., Measurement of FRET efficiency and ratio of donor to acceptor concentration in living cells. Biophys J 91 (2006), L39–L41.
14. 14 Hofman, E.G., Bader, A.N., Voortman, J., Van Den Heuvel, D.J., Sigismund, S., Verkleij, A.J., Gerritsen, H.C., Van Bergen en Henegouwen, P.M.P., Ligand-induced EGF receptor oligomerization is kinase-dependent and enhances internalization. J Biol Chem 285 (2010), 39481–39489.
15. 15 Bader, A.N., Hofman, E.G., Voortman, J., Van Bergen En Henegouwen, P.M.P., Gerritsen, H.C., Homo-FRET imaging enables quantification of protein cluster sizes with subcellular resolution. Biophys J 97 (2009), 2613–2622.
16. 16 Bader, A.N., Hoetzl, S., Hofman, E.G., Voortman, J., Van Bergen En Henegouwen, P.M.P., Van Meer, G., Gerritsen, H.C., Homo-FRET imaging as a tool to quantify protein and lipid clustering. ChemPhysChem 12 (2011), 475–483.
17. 17 De Heus, C., Kagie, N., Heukers, R., Van Bergen En Henegouwen, P.M.P., Gerritsen, H.C., Analysis of EGF Receptor Oligomerization by Homo-FRET. 2013, Elsevier Inc.
18. 18 Pauker, M.H., Hassan, N., Noy, E., Reicher, B., Barda-Saad, M., Studying the dynamics of SLP-76, Nck, and Vav1 multimolecular complex formation in live human cells with triple-color FRET. Sci Signal, 5, 2012 rs3-rs3.
19. 19 Hoppe, A.D., Scott, B.L., Welliver, T.P., Straight, S.W., Swanson, J.A., N-Way FRET microscopy of multiple protein-protein interactions in live cells. PLoS One, 2013, 8.
20. 20 Sun, Y., Wallrabe, H., Booker, C.F., Day, R.N., Periasamy, A., Three-color spectral FRET microscopy localizes three interacting proteins in living cells. Biophys J 99 (2010), 1274–1283.
21. 21 Woehler, A., Wlodarczyk, J., Neher, E., Signal/noise analysis of FRET-based sensors. Biophys J 99 (2010), 2344–2354.
22. 22 Berney, C., Danuser, G., FRET or no FRET: a quantitative comparison. Biophys J 84 (2003), 3992–4010.
23. 23 Piston, D.W.D.W., Kremers, G.-J.G.J., Fluorescent protein FRET: the good, the bad and the ugly. Trends Biochem Sci 32 (2007), 407–414.
24. 24 Grünberg, R., Burnier, J.V., Ferrar, T., Beltran-Sastre, V., Stricher, F., van der Sloot, A.M., Garcia-Olivas, R., Mallabiabarrena, A., Sanjuan, X., Zimmermann, T., et al. Engineering of weak helper interactions for high-efficiency FRET probes. Nat Methods 10 (2013), 1021–1027.
25. 25 Barilá, D., Superti-Furga, G., An intramolecular SH3-domain interaction regulates c-Abl activity. Nat Genet 18 (1998), 280–282.
26. 26 Morell, M., Espargaró, A., Avilés, F.X., Ventura, S., Detection of transient protein-protein interactions by bimolecular fluorescence complementation: the Abl-SH3 case. Proteomics 7 (2007), 1023–1036.
27. 27 Michnick, S.W., Detection of protein-protein interactions by protein fragment complementation strategies. Methods Enzymol 4 (2015), 615–624.
28. 28 Kerppola, T.K., Design and implementation of bimolecular fluorescence complementation (BiFC) assays for the visualization of protein interactions in living cells. Nat Protoc 1 (2006), 1278–1286.
29. 29 Kodama, Y., Hu, C.D., Bimolecular fluorescence complementation (BiFC): a 5-year update and future perspectives. Biotechniques 53 (2012), 285–298.
30. 30 Vidi, P., Chemel, B.R., Hu, C., Watts, V.J., Ligand-dependent oligomerization of dopamine D 2 and adenosine A 2A receptors in living neuronal cells. Mol Pharmacol 74 (2008), 544–551.
31. 31 Hancock, J.F., Parton, R.G., Ras plasma membrane signalling platforms. Biochem J 389 (2005), 1–11.
32. 32 Kholodenko, B.N., Hancock, J.F., Kolch, W., Signalling ballet in space and time. Nat Rev Mol Cell Biol 11 (2010), 414–426.
33. 33 Cambi, A., Lidke, D.S., Nanoscale membrane organization: where biochemistry meets advanced microscopy. ACS Chem Biol 7 (2012), 139–149.
34. 34 Harding, A., Hancock, J.F., Ras nanoclusters: Combining digital and analog signaling. Cell Cycle 7 (2008), 127–134.
35. 35•• Nickerson, A., Huang, T., Lin, L.J., Nan, X., Photoactivated localization microscopy with Bimolecular Fluorescence Complementation (BiFC-PALM) for nanoscale imaging of protein-protein interactions in cells. PLoS One, 2014, 9 The authors successfully split a photoactivatable FP and used the system to map fixed PPIs below the spatial resolution of traditional imaging methods.
36. 36• Hertel, F., Mo, G.C.H., Duwe, S., Dedecker, P., Zhang, J., RefSOFI for mapping nanoscale organization of protein-protein interactions in living cells. Cell Rep 14 (2016), 390–400 The authors utilized a BiFC approach and SOFI analysis to obtain a super-resolved map of PPIs in living cells.
37. 37 Miller, K.E., Kim, Y., Huh, W.K., Park, H.O., Bimolecular fluorescence complementation (BiFC) analysis: advances and recent applications for genome-wide interaction studies. J Mol Biol 427 (2015), 2039–2055.
38. 38 Manning, B.D., Cantley, L.C., AKT/PKB signaling: navigating downstream. Cell 129 (2007), 1261–1274.
39. 39 Remy, I., Michnick, S.W., Regulation of apoptosis by the Ft1 protein, a new modulator of protein kinase B/Akt. Mol Cell Biol 24 (2004), 1493–1504.
40. 40 Poe, J.A., Vollmer, L., Vogt, A., Smithgall, T.E., Development and validation of a high-content bimolecular fluorescence complementation assay for small-molecule inhibitors of HIV-1 Nef dimerization. J Biomol Screen 19 (2014), 556–565.
41. 41• Cabantous, S., Nguyen, H.B., Pedelacq, J.-D., Koraïchi, F., Chaudhary, A., Ganguly, K., Lockard, M.A., Favre, G., Terwilliger, T.C., Waldo, G.S., A new protein-protein interaction sensor based on tripartite split-GFP association. Sci Rep, 3, 2013, 2854 By splitting GFP into three non-fluorescent fragments, the authors were able to decrease non-specific reconstitution and monitor the interaction between three proteins.
42. 42 Kerppola, T.K., Multicolor bimolecular fluorescence complementation (BiFC) analysis of protein interactions with alternative partners. Cold Spring Harb Protoc 2013 (2013), 798–803.
43. 43• Filonov, G.S., Verkhusha, V.V., A near-infrared bifc reporter for in vivo imaging of protein-protein interactions. Chem Biol 20 (2013), 1078–1086 The authors were able to split a near-infrared FP from bacteria and use the probe to detect PPIs in deep tissue where other wavelengths of light cannot reach.
44. 44 VanEngelenburg, S.B., Palmer, A.E., Fluorescent biosensors of protein function. Curr Opin Chem Biol 12 (2008), 60–65.
45. 45 Herbst, K.J., Ni, Q., Zhang, J., Dynamic visualization of signal transduction in living cells: From second messengers to kinases. IUBMB Life 61 (2009), 902–908.
46. 46 Newman, R.H., Fosbrink, M.D., Zhang, J., Genetically-encodable fluorescent biosensors for tracking signalling dynamics in livivng cells. Chem Rev 111 (2011), 3614–3666.
47. 47 Mehta, S., Zhang, J., Reporting from the field: genetically encoded fluorescent reporters uncover signaling dynamics in living biological systems. Annu Rev Biochem 80 (2011), 375–401.
48. 48 Miyawaki a, Llopis, J., Heim, R., McCaffery, J.M., Adams, J.a, Ikura, M., Tsien, R.Y., Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 388 (1997), 882–887.
49. 49 Tian, L., Hires, S.A., Mao, T., Huber, D., Chiappe, M.E., Chalasani, S.H., Petreanu, L., Akerboom, J., McKinney, S.A., Schreiter, E.R., et al. Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat Methods 6 (2009), 875–881.
50. 50•• Akerboom, J., Carreras Calderón, N., Tian, L., Wabnig, S., Prigge, M., Tolö, J., Gordus, A., Orger, M.B., Severi, K.E., Macklin, J.J., et al. Genetically encoded calcium indicators for multi-color neural activity imaging and combination with optogenetics. Front Mol Neurosci, 6, 2013, 2 The authors extended the color palette of single-color calcium reporters based on the GCaMP design by making blue, yellow, and red variants.
51. 51 Zhang, J., Ma, Y., Taylor, S.S., Tsien, R.Y., Genetically encoded reporters of protein kinase A activity reveal impact of substrate tethering. Proc Natl Acad Sci U S A 98 (2001), 14997–15002.
52. 52• Koçer, S.S., Wang, H.-Y., Malbon, C.C., Shaping” of cell signaling via AKAP-tethered PDE4D: Probing with AKAR2-AKAP5 biosensor. J Mol Signal, 7, 2012, 4 By fusing the PKA activity sensor AKAR to a PKA anchoring protein, the authors demonstrated that PKA signaling around the protein is both accelerated and amplified.
53. 53• Greenwald, E.C., M, Redden, J., Dodge-Kafka, K.L., Saucerman, J.J., Scaffold state switching amplifies, accelerates, and insulates protein kinase c signaling. J Biol Chem 289 (2014), 2353–2360 The authors determined that scaffolded PKC “insulates” PKC from certain competitive inhibitors using a fused biosensor.
54. 54• Zlobovskaya, O.A., Sarkisyan, K.S., Lukyanov, K.A., Infrared fluorescent protein iRFP as an acceptor for forster resonance energy transfer. Bioorg Khim 41 (2015), 299–304 An infrared FP was paired with far-red FPs in order to measure FRET in tissues and multiplex with other FRET-based sensors.
55. 55 Zlobovskaya, O.A., Sergeeva, T.F., Shirmanova, M.V., Dudenkova, V.V., Sharonov, G.V., Zagaynova, E.V., Lukyanov, K.A., Genetically encoded far-red fluorescent sensors for caspase-3 activity. Biotechniques 60 (2016), 62–68.
56. 56 Woehler, A., Simultaneous quantitative live cell imaging of multiple FRET-based biosensors. PLoS One, 2013, 8.
57. 57 Cameron, W.D., Bui, C.V., Hutchinson, A., Loppnau, P., Gräslund, S., Rocheleau, J.V., Apollo-NADP+: a spectrally tunable family of genetically encoded sensors for NADP+. Nat Methods 13 (2016), 352–358.
58. 58• Belal, A.S.F., Sell, B.R., Hoi, H., Davidson, M.W., Campbell, R.E., Optimization of a genetically encoded biosensor for cyclin B1-cyclin dependent kinase 1. Mol Biosyst 10 (2014), 191–195 By simultaneously expressing biosensors and an upstream activator for the biosensor within E.coli colonies, the authors were able to rapidly optimize the biosensor's dynamic range 4.5 fold.
59. 59• Davis, L.M.L., Lubbeck, J.L.J., Dean, K.K.M., Palmer, A.E., Jimenez, R., Microfluidic cell sorter for use in developing red fluorescent proteins with improved photostability. Lab Chip 13 (2013), 2320–2327 The authors built a microfluidic device that interfaces with a fluorescence microscope in order to quickly measure the dark-state conversion of many FP variants and sort these variants for further analysis.
60. 60• Ratz, M., Testa, I., Hell, S.W., Jakobs, S., CRISPR/Cas9-mediated endogenous protein tagging for RESOLFT super-resolution microscopy of living human cells. Sci Rep, 5, 2015, 9592 By using the CRISPR/Cas9 for knock-ins, the authors successfully tagged many endogenous proteins with reversible switching EGFP for superresolution imaging.
61. 61 Jain, A., Liu, R., Xiang, Y.K., Ha, T., Single-molecule pull-down for studying protein interactions. Nat Protoc 7 (2012), 445–452.
62. 62 Ishitsuka, Y., Azadfar, N., Kobitski, A.Y., Nienhaus, K., Johnsson, N., Nienhaus, G.U., Evaluation of genetically encoded chemical tags as orthogonal fluorophore labeling tools for single-molecule fret applications. J Phys Chem B 119 (2015), 6611–6619.
63. 63• Chen, T.-W., Wardill, T.J., Sun, Y., Pulver, S.R., Renninger, S.L., Baohan, A., Schreiter, E.R., Kerr, R.A., Orger, M.B., Jayaraman, V., et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499 (2013), 295–300 The authors optimized the single-color calcium reporter GCaMP in order to respond faster to measure transient calcium spikes in neurons.
64. 64• St-Pierre, F., Marshall, J.D., Yang, Y., Gong, Y., Schnitzer, M.J., Lin, M.Z., High-fidelity optical reporting of neuronal electrical activity with an ultrafast fluorescent voltage sensor. Nat Neurosci 17 (2014), 884–889 The authors created a single-color voltage sensor that is sensitive and responds quickly in order to detect individual action potentials.