Screening for in planta protein-protein interactions combining bimolecular fluorescence complementation with flow cytometry

Plant Methods

Volumn 8, Issue 1, 2012, Pages

  Berendzen, Kenneth W ^a   Böhmer, Maik ^b   Wallmeroth, Niklas ^a   Peter, Sébastien ^a   Vesić, Marko ^a   Zhou, Ying ^a   Tiesler, Franziska K E ^a   Schleifenbaum, Frank ^a   Harter, Klaus ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

BiFC; CPK3; FACS; In planta; In vivo; Protein protein interaction screen

Indexed keywords

ARABIDOPSIS;

EID: 84863645983     PISSN: None     EISSN: 17464811     Source Type: Journal    
DOI: 10.1186/1746-4811-8-25     Document Type: Article

References (63)

1. Braun P, Tasan M, Dreze M, Barrios-Rodiles M, Lemmens I, Yu H, Sahalie JM, Murray RR, Roncari L, de Smet AS, et al. An experimentally derived confidence score for binary protein-protein interactions. Nat Methods 2009, 6:91-97. 10.1038/nmeth.1281, 2976677, 19060903.
2. Grefen C, Obrdlik P, Harter K. The determination of protein-protein interactions by the mating-based split-ubiquitin system (mbSUS). Methods Mol Biol 2009, 479:217-233.
3. Young KH. Yeast two-hybrid: so many interactions, (in) so little time. Biol Reprod 1998, 58:302-311. 10.1095/biolreprod58.2.302, 9475380.
4. Fujikawa Y, Kato N. Split luciferase complementation assay to study protein-protein interactions in Arabidopsis protoplasts. Plant J 2007, 52:185-195. 10.1111/j.1365-313X.2007.03214.x, 17662028.
5. Morell M, Ventura S, Avilés FX. Protein complementation assays: Approaches for the in vivo analysis of protein interactions. FEBS Lett 2009, 583:1684-1691. 10.1016/j.febslet.2009.03.002, 19269288.
6. Walter M, Chaban C, Schütze K, Batistic O, Weckermann K, Näke C, Blazevic D, Grefen C, Schumacher K, Oecking C, et al. Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J 2004, 40:428-438. 10.1111/j.1365-313X.2004.02219.x, 15469500.
7. Kerppola TK. Bimolecular Fluorescence Complementation (BiFC) Analysis as a Probe of Protein Interactions in Living Cells. Annu Rev Biophys 2008, 37:465-487. 10.1146/annurev.biophys.37.032807.125842, 2829326, 18573091.
8. Boruc J, Inze D, Russinova E. A high-throughput bimolecular fluorescence complementation protein-protein interaction screen identifies functional Arabidopsis CDKA/B-CYCD4/5 complexes. Plant Signal Behav 2010, 5:1276-1281. 10.4161/psb.5.10.13037, 3115367, 20861687.
9. Boruc J, Van den Daele H, Hollunder J, Rombauts S, Mylle E, Hilson P, Inze D, De Veylder L, Russinova E. Functional modules in the Arabidopsis core cell cycle binary protein-protein interaction network. Plant Cell 2010, 22:1264-1280. 10.1105/tpc.109.073635, 2879739, 20407024.
10. Morell M, Espargaro A, Aviles FX, Ventura S. Detection of transient protein-protein interactions by bimolecular fluorescence complementation: the Abl-SH3 case. Proteomics 2007, 7:1023-1036. 10.1002/pmic.200600966, 17352427.
11. Li M, Berendzen KW, Schoffl F. Promoter specificity and interactions between early and late Arabidopsis heat shock factors. Plant Mol Biol 2010, 73:559-567. 10.1007/s11103-010-9643-2, 2882041, 20458611.
12. Li M, Doll J, Weckermann K, Oecking C, Berendzen KW, Schoffl F. Detection of in vivo interactions between Arabidopsis class A-HSFs, using a novel BiFC fragment, and identification of novel class B-HSF interacting proteins. Eur J Cell Biol 2010, 89:126-132. 10.1016/j.ejcb.2009.10.012, 19945192.
13. von Behrens I, Komatsu M, Zhang Y, Berendzen KW, Niu X, Sakai H, Taramino G, Hochholdinger F. Rootless with undetectable meristem 1 encodes a monocot-specific AUX/IAA protein that controls embryonic seminal and post-embryonic lateral root initiation in maize. Plant J 2011, 66:341-353. 10.1111/j.1365-313X.2011.04495.x, 21219511.
14. Edwards K, Johnstone C, Thompson C. A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Res 1991, 19:1349. 10.1093/nar/19.6.1349, 333874, 2030957.
15. Kerppola TK. Visualization of molecular interactions using bimolecular fluorescence complementation analysis: Characteristics of protein fragment complementation. Chem Soc Rev 2009, 38:2876. 10.1039/b909638h, 2980501, 19771334.
16. Geiger D, Scherzer S, Mumm P, Marten I, Ache P, Matschi S, Liese A, Wellmann C, Al-Rasheid KA, Grill E, et al. Guard cell anion channel SLAC1 is regulated by CDPK protein kinases with distinct Ca2+ affinities. Proc Natl Acad Sci USA 2010, 107:8023-8028. 10.1073/pnas.0912030107, 2867891, 20385816.
17. Haweker H, Rips S, Koiwa H, Salomon S, Saijo Y, Chinchilla D, Robatzek S, von Schaewen A. Pattern recognition receptors require N-glycosylation to mediate plant immunity. J Biol Chem 2010, 285:4629-4636. 10.1074/jbc.M109.063073, 2836068, 20007973.
18. Hass C, Lohrmann J, Albrecht V, Sweere U, Hummel F, Yoo SD, Hwang I, Zhu T, Schafer E, Kudla J, Harter K. The response regulator 2 mediates ethylene signalling and hormone signal integration in Arabidopsis. EMBO J 2004, 23:3290-3302. 10.1038/sj.emboj.7600337, 514511, 15282545.
19. Ottmann C, Weyand M, Wolf A, Kuhlmann J. Applicability of superfolder YFP bimolecular fluorescence complementation in vitro. Biol Chem 2009, 390:81-90.
20. Robida AM, Kerppola TK. Bimolecular fluorescence complementation analysis of inducible protein interactions: effects of factors affecting protein folding on fluorescent protein fragment association. J Mol Biol 2009, 394:391-409. 10.1016/j.jmb.2009.08.069, 2862259, 19733184.
21. Shyu YJ, Liu H, Deng X, Hu CD. Identification of new fluorescent protein fragments for bimolecular fluorescence complementation analysis under physiological conditions. Biotechniques 2006, 40:61-66. 10.2144/000112036, 16454041.
22. Dammann C. Subcellular Targeting of Nine Calcium-Dependent Protein Kinase Isoforms from Arabidopsis. Plant Physiol 2003, 132:1840-1848. 10.1104/pp.103.020008, 181270, 12913141.
23. Mehlmer N, Wurzinger B, Stael S, Hofmann-Rodrigues D, Csaszar E, Pfister B, Bayer R, Teige M. The Ca2 + -dependent protein kinase CPK3 is required for MAPK-independent salt-stress acclimation in Arabidopsis. Plant J 2010, 63:484-498.
24. Narendra S. The Arabidopsis ascorbate peroxidase 3 is a peroxisomal membrane-bound antioxidant enzyme and is dispensable for Arabidopsis growth and development. J Exp Bot 2006, 57:3033-3042. 10.1093/jxb/erl060, 16873450.
25. D'Andrea LD, Regan L. TPR proteins: the versatile helix. Trends Biochem Sci 2003, 28:655-662. 10.1016/j.tibs.2003.10.007, 14659697.
26. Heazlewood JL. Experimental Analysis of the Arabidopsis Mitochondrial Proteome Highlights Signaling and Regulatory Components, Provides Assessment of Targeting Prediction Programs, and Indicates Plant-Specific Mitochondrial Proteins. The Plant Cell Online 2004, 16:241-256.
27. Eubel H, Meyer EH, Taylor NL, Bussell JD, O'Toole N, Heazlewood JL, Castleden I, Small ID, Smith SM, Millar AH. Novel Proteins, Putative Membrane Transporters, and an Integrated Metabolic Network Are Revealed by Quantitative Proteomic Analysis of Arabidopsis Cell Culture Peroxisomes. Plant Physiol 2008, 148:1809-1829. 10.1104/pp.108.129999, 2593673, 18931141.
28. Umate P. Oxysterol binding proteins (OSBPs) and their encoding genes in Arabidopsis and rice. Steroids 2011, 76:524-529. 10.1016/j.steroids.2011.01.007, 21281657.
29. Lord JM, Spooner RA. Ricin Trafficking in Plant and Mammalian Cells. Toxins 2011, 3:787-801. 10.3390/toxins3070787, 3202855, 22069740.
30. Pedersen DS, Merkle T, Marktl B, Lildballe DL, Antosch M, Bergmann T, Tonsing K, Anselmetti D, Grasser KD. Nucleocytoplasmic Distribution of the Arabidopsis Chromatin-Associated HMGB2/3 and HMGB4 Proteins. Plant Physiol 2010, 154:1831-1841. 10.1104/pp.110.163055, 2996034, 20940346.
31. Alexandersson E, Saalbach G, Larsson C, Kjellbom P. Arabidopsis plasma membrane proteomics identifies components of transport, signal transduction and membrane trafficking. Plant Cell Physiol 2004, 45:1543-1556. 10.1093/pcp/pch209, 15574830.
32. Kanchiswamy CN, Takahashi H, Quadro S, Maffei ME, Bossi S, Bertea C, Zebelo SA, Muroi A, Ishihama N, Yoshioka H, et al. Regulation of Arabidopsis defense responses against Spodoptera littoralis by CPK-mediated calcium signaling. BMC Plant Biol 2010, 10:97. 10.1186/1471-2229-10-97, 3095362, 20504319.
33. Llères D, Swift S, Lamond AI. Detecting Protein-Protein Interactions In Vivo with FRET using Multiphoton Fluorescence Lifetime Imaging Microscopy (FLIM) 2007, , .
34. Bleckmann A, Weidtkamp-Peters S, Seidel CAM, Simon R. Stem Cell Signaling in Arabidopsis Requires CRN to Localize CLV2 to the Plasma Membrane. Plant Physiol 2009, 152:166-176. 2799354, 19933383.
35. Wanke D, Hohenstatt ML, Dynowski M, Bloss U, Hecker A, Elgass K, Hummel S, Hahn A, Caesar K, Schleifenbaum F, et al. Alanine zipper-like coiled-coil domains are necessary for homotypic dimerization of plant GAGA-factors in the nucleus and nucleolus. PLoS One 2011, 6:e16070. 10.1371/journal.pone.0016070, 3037368, 21347358.
36. Mori IC, Murata Y, Yang Y, Munemasa S, Wang YF, Andreoli S, Tiriac H, Alonso JM, Harper JF, Ecker JR, et al. CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca(2+)-permeable channels and stomatal closure. PLoS Biol 2006, 4:e327. 10.1371/journal.pbio.0040327, 1592316, 17032064.
37. DeFalco Thomas A, Bender Kyle W, Snedden Wayne A. Breaking the code: Ca2+sensors in plant signalling. Biochem J 2010, 425:27-40.
38. Böhmer M, Schroeder JI. Quantitative transcriptomic analysis of abscisic acid-induced and reactive oxygen species-dependent expression changes and proteomic profiling in Arabidopsis suspension cells. Plant J 2011, 67:105-118. 10.1111/j.1365-313X.2011.04579.x, 3125488, 21426425.
39. Cousson A. Arabidopsis Ca2 + -dependent protein kinase CPK3 mediates relationship of putative inositol triphosphate receptor with slow-type anion channel. Biologia Plantarum 2011, 55:507-521.
40. Arimura G, Sawasaki T. Arabidopsis CPK3 plays extensive roles in various biological and environmental responses. Plant Signal Behav 2010, 5:1263-1265. 10.4161/psb.5.10.12957, 3115363, 20798597.
41. Albertazzi L, Arosio D, Marchetti L, Ricci F, Beltram F. Quantitative FRET Analysis With the E0GFP-mCherry Fluorescent Protein Pair. Photochem Photobiol 2009, 85:287-297. 10.1111/j.1751-1097.2008.00435.x, 18764891.
42. Liu P, Ahmed S, Wohland T. The F-techniques: advances in receptor protein studies. Trends Endocrinol Metab 2008, 19:181-190. 10.1016/j.tem.2008.02.004, 18387308.
43. Kerppola TK. Visualization of molecular interactions by fluorescence complementation. Nat Rev Mol Cell Biol 2006, 7:449-456. 2512262, 16625152.
44. Fan JY, Cui ZQ, Wei HP, Zhang ZP, Zhou YF, Wang YP, Zhang XE. Split mCherry as a new red bimolecular fluorescence complementation system for visualizing protein-protein interactions in living cells. Biochem Biophys Res Commun 2008, 367:47-53. 10.1016/j.bbrc.2007.12.101, 18158915.
45. Fahnenstich H, Scarpeci TE, Valle EM, Flugge UI, Maurino VG. Generation of Hydrogen Peroxide in Chloroplasts of Arabidopsis Overexpressing Glycolate Oxidase as an Inducible System to Study Oxidative Stress. Plant Physiol 2008, 148:719-729. 10.1104/pp.108.126789, 2556821, 18685041.
46. Shen G, Kuppu S, Venkataramani S, Wang J, Yan J, Qiu X, Zhang H. ANKYRIN REPEAT-CONTAINING PROTEIN 2A Is an Essential Molecular Chaperone for Peroxisomal Membrane-Bound ASCORBATE PEROXIDASE3 in Arabidopsis. The Plant Cell Online 2010, 22:811-831.
47. Beh CT, Cool L, Phillips J, Rine J. Overlapping functions of the yeast oxysterol-binding protein homologues. Genetics 2001, 157:1117-1140. 1461579, 11238399.
48. Hartmann MA. Plant sterols and the membrane environment. Trends Plant Sci 1998, 3:170-175.
49. Endo Y, Tsurugi K. RNA N-glycosidase activity of ricin A-chain. Mechanism of action of the toxic lectin ricin on eukaryotic ribosomes. J Biol Chem 1987, 262:8128-8130.
50. Reeves R. Nuclear functions of the HMG proteins. Biochim Biophys Acta 2010, 1799:3-14. 10.1016/j.bbagrm.2009.09.001, 2818135, 19748605.
51. Reeves R, Nissen MS. The A.T-DNA-binding domain of mammalian high mobility group I chromosomal proteins. A novel peptide motif for recognizing DNA structure. J Biol Chem 1990, 265:8573-8582.
52. Launholt D, Merkle T, Houben A, Schulz A, Grasser KD. Arabidopsis Chromatin-Associated HMGA and HMGB Use Different Nuclear Targeting Signals and Display Highly Dynamic Localization within the Nucleus. The Plant Cell Online 2006, 18:2904-2918.
53. Fukamatsu Y, Mitsui S, Yasuhara M, Tokioka Y, Ihara N, Fujita S, Kiyosue T. Identification of LOV KELCH PROTEIN2 (LKP2)-interacting factors that can recruit LKP2 to nuclear bodies. Plant Cell Physiol 2005, 46:1340-1349. 10.1093/pcp/pci144, 15937324.
54. Milla MA, Townsend J, Chang IF, Cushman JC. The Arabidopsis AtDi19 gene family encodes a novel type of Cys2/His2 zinc-finger protein implicated in ABA-independent dehydration, high-salinity stress and light signaling pathways. Plant Mol Biol 2006, 61:13-30. 10.1007/s11103-005-5798-7, 16786289.
55. Alliotte T, Tire C, Engler G, Peleman J, Caplan A, Van Montagu M, Inze D. An Auxin-Regulated Gene of Arabidopsis thaliana Encodes a DNA-Binding Protein. Plant Physiol 1989, 89:743-752. 10.1104/pp.89.3.743, 1055917, 16666616.
56. Merkle T, Leclerc D, Marshallsay C, Nagy F. A plant in vitro system for the nuclear import of proteins. Plant J 1996, 10:1177-1186. 10.1046/j.1365-313X.1996.10061177.x, 9011099.
57. Negrutiu I, Shillito R, Potrykus I, Biasini G, Sala F. Hybrid genes in the analysis of transformation conditions. Plant Mol Biol 1987, 8:363-373.
58. Schutze K, Harter K, Chaban C. Bimolecular fluorescence complementation (BiFC) to study protein-protein interactions in living plant cells. Methods Mol Biol 2009, 479:189-202.
59. Orkin S. Molecular-Cloning - a Laboratory Manual, 2nd Edition - Sambrook, J, Fritsch, Ef, Maniatis, T. Nature 1990, 343:604-605.
60. Voinnet O, Rivas S, Mestre P, Baulcombe D. An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J 2003, 33:949-956. 10.1046/j.1365-313X.2003.01676.x, 12609035.
61. Weltmeier F, Ehlert A, Mayer CS, Dietrich K, Wang X, Schutze K, Alonso R, Harter K, Vicente-Carbajosa J, Droge-Laser W. Combinatorial control of Arabidopsis proline dehydrogenase transcription by specific heterodimerisation of bZIP transcription factors. EMBO J 2006, 25:3133-3143. 10.1038/sj.emboj.7601206, 1500977, 16810321.
62. Horak J, Grefen C, Berendzen KW, Hahn A, Stierhof YD, Stadelhofer B, Stahl M, Koncz C, Harter K. The Arabidopsis thaliana response regulator ARR22 is a putative AHP phospho-histidine phosphatase expressed in the chalaza of developing seeds. BMC Plant Biol 2008, 8:77. 10.1186/1471-2229-8-77, 2478664, 18625081.
63. Grefen C, Lalonde S, Obrdlik P. Split-ubiquitin system for identifying protein-protein interactions in membrane and full-length proteins. Curr Protoc Neurosci 2007, 41:1-5.