A high-definition native polyacrylamide gel electrophoresis system for the analysis of membrane complexes

Plant Journal

Volumn 67, Issue 1, 2011, Pages 181-194

  Ladig, Roman ^a   Sommer, Maik S ^b   Hahn, Alexander ^b   Leisegang, Matthias S ^b   Papasotiriou, Dimitrios G ^b   Ibrahim, Mohamed ^b   Elkehal, Rajae ^b   Karas, Michael ^b   Zickermann, Volker ^b   Gutensohn, Michael ^a,c   Brandt, Ulrich ^b   Klösgen, Ralf Bernd ^a   Schleiff, Enrico ^b  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b GOETHE UNIVERSITY   (Germany)

^c PURDUE UNIVERSITY   (United States)

Author keywords

chloroplasts; cyanobacteria; native polyacrylamide gel electrophoresis; outer inner envelope complexes; protein translocation; thylakoid complexes

Indexed keywords

CHLOROPLASTS; CYANOBACTERIA; NATIVE POLYACRYLAMIDE GEL ELECTROPHORESIS; OUTER/INNER ENVELOPE COMPLEXES; PROTEIN TRANSLOCATION; THYLAKOIDS;

AMINO ACIDS; BIOLOGICAL MEMBRANES; CHLOROPHYLL; GELS; MACHINERY; MASS SPECTROMETRY; MEMBRANES; PLANTS (BOTANY); PROTEINS;

ELECTROPHORESIS;

DEOXYCHOLIC ACID; HISTIDINE; MEMBRANE PROTEIN; MULTIPROTEIN COMPLEX;

ALFALFA; ANABAENA; ANIMAL; ARTICLE; CATTLE; CELL WALL; CHEMISTRY; CHLOROPLAST; CYANOBACTERIUM; HEART; ISOLATION AND PURIFICATION; MASS SPECTROMETRY; METHODOLOGY; MITOCHONDRION; MUSCLE; PEA; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN TRANSPORT; THYLAKOID; YARROWIA;

ANABAENA; ANIMALS; CATTLE; CELL WALL; CHLOROPLASTS; CYANOBACTERIA; DEOXYCHOLIC ACID; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HEART; HISTIDINE; MASS SPECTROMETRY; MEDICAGO SATIVA; MEMBRANE PROTEINS; MITOCHONDRIA; MULTIPROTEIN COMPLEXES; MUSCLES; PEAS; PROTEIN TRANSPORT; THYLAKOIDS; YARROWIA;

ANABAENA; ANABAENA SP.; BOVINAE; CYANOBACTERIA; MEDICAGO SATIVA; PISUM SATIVUM; YARROWIA LIPOLYTICA;

EID: 79959711557     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2011.04577.x     Document Type: Article

References (78)

1. Akita, M., Nielsen, E., and, Keegstra, K., (1997) Identification of protein transport complexes in the chloroplastic envelope membranes via chemical cross-linking. J. Cell Biol. 136, 983-994. (Pubitemid 27131731)
2. Amunts, A., and, Nelson, N., (2009) Plant photosystem I design in the light of evolution. Structure, 17, 637-650.
3. Arnon, D.I., (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in beta vulgaris. Plant Physiol. 24, 1-15.
4. Aro, E.M., Suorsa, M., Rokka, A., Allahverdiyeva, Y., Paakkarinen, V., Saleem, A., Battchikova, N., and, Rintamaki, E., (2005) Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes. J Exp. Bot. 56, 347-356. (Pubitemid 40263281)
5. Berghofer, J., and, Klösgen, R.B., (1999) Two distinct translocation intermediates can be distinguished during protein transport by the TAT (Delta ph) pathway across the thylakoid membrane. FEBS Lett. 460, 328-332. (Pubitemid 29495963)
6. Bölter, B., Soll, J., Hill, K., Hemmler, R., and, Wagner, R., (1999) A rectifying ATP-regulated solute channel in the chloroplastic outer envelope from pea. EMBO J. 18, 5505-5516. (Pubitemid 29486370)
7. Bredemeier, R., Schlegel, T., Ertel, F., Vojta, A., Borissenko, L., Bohnsack, M.T., Groll, M., von Haeseler, A., and, Schleiff, E., (2007) Functional and phylogenetic properties of the pore-forming beta-barrel transporters of the Omp85 family. J. Biol. Chem. 282, 1882-1890. (Pubitemid 47076709)
8. Bulseco, D.A., and, Wolf, D.E., (2003) Fluorescence correlation spectroscopy: molecular complexing in solution and in living cells. Methods Cell Biol. 72, 465-498.
9. Caliebe, A., Grimm, R., Kaiser, G., Lübeck, J., Soll, J., and, Heins, L., (1997) The chloroplastic protein import machinery contains a Rieske-type iron-sulfur cluster and a mononuclear iron-binding protein. EMBO J. 16, 7342-7350. (Pubitemid 28010494)
10. Cardona, T., Battchikova, N., Zhang, P., Stensjö, K., Aro, E.M., Lindblad, P., and, Magnuson, A., (2009) Electron transfer protein complexes in the thylakoid membranes of heterocysts from the cyanobacterium Nostoc punctiforme. Biochim. Biophys. Acta, 1787, 252-263.
11. Chen, K.Y., and, Li, H.M., (2007) Precursor binding to an 880-kDa Toc complex as an early step during active import of protein into chloroplasts. Plant J. 49, 149-158.
12. Cline, K., and, Mori, H., (2001) Thylakoid delta pH-dependent precursor proteins bind to a cpTatC-Hcf106 complex before Tha4-dependent transport. J. Cell Biol. 154, 719-729. (Pubitemid 34292954)
13. Crociani, O., (2010) Biochemical methods to study the interactions between integrins and ion channels. Adv. Exp. Med. Biol. 674, 23-32.
14. Danielsson, R., Suorsa, M., Paakkarinen, V., Albertsson, P.A., Styring, S., Aro, E.M., and, Mamedov, F., (2006) Dimeric and monomeric organization of photosystem II. Distribution of five distinct complexes in the different domains of the thylakoid membrane. J. Biol. Chem. 281, 14241-14249. (Pubitemid 43853025)
15. Drykova, D., Cenklova, V., Sulimenko, V., Volc, J., Draber, P., and, Binarova, P., (2003) Plant gamma-tubulin interacts with alpha beta-tubulin dimers and forms membrane-associated complexes. Plant Cell, 15, 465-480. (Pubitemid 36229998)
16. Ellis, J., (1987) Proteins as molecular chaperones. Nature, 328, 378-379.
17. Ertel, F., Mirus, O., Bredemeier, R., Moslavac, S., Becker, T., and, Schleiff, E., (2005) The evolutionarily related beta-barrel polypeptide transporters from Pisum sativum and Nostoc PCC7120 contain two distinct functional domains. J. Biol. Chem. 280, 28281-28289. (Pubitemid 41105724)
18. Groves, J.T., and, Kuriyan, J., (2010) Molecular mechanisms in signal transduction at the membrane. Nat. Struct. Mol. Biol. 17, 659-665.
19. Heazlewood, J.L., Whelan, J., and, Millar, A.H., (2003) The products of the mitochondrial orf25 and orfB genes are F-o components in the plant F1Fo ATP synthase. FEBS Lett. 540, 201-205. (Pubitemid 36398057)
20. Heinemeyer, J., Eubel, H., Wehmhoner, D., Jansch, L., and, Braun, H.P., (2004) Proteomic approach to characterize the supramolecular organization of photosystems in higher plants. Phytochemistry, 65, 1683-1692. (Pubitemid 38976518)
21. Hoffmann, J., Aslimovska, L., Bamann, C., Glaubitz, C., Bamberg, E., and, Brutschy, B., (2010) Studying the stoichiometries of membrane proteins by mass spectrometry: microbial rhodopsins and a potassium ion channel. Phys. Chem. Chem. Phys. 12, 3480-3485.
22. Huang, D., Everly, R.M., Cheng, R.H., Heymann, J.B., Schägger, H., Sled, V., Ohnishi, T., Baker, T.S., and, Cramer, W.A., (1994) Characterization of the chloroplast cytochrome-B(6)F complex as a structural and functional dimer. Biochemistry, 33, 4401-4409. (Pubitemid 24140629)
23. Hurley, J.H., and, Hanson, P.I., (2010) Membrane budding and scission by the ESCRT machinery: it's all in the neck. Nat. Rev. Mol. Cell Biol. 11, 556-566.
24. Irving, L.J., and, Robinson, D., (2006) A dynamic model of Rubisco turnover in cereal leaves. New Phytol. 169, 493-504.
25. Jansch, L., Kruft, V., Schmitz, U.K., and, Braun, H.P., (1995) Cytochrome-C reductase from potato does not comprise 3 core proteins but contains an additional low-molecular-mass subunit. Eur. J. Biochem. 228, 878-885.
26. Jansch, L., Kruft, V., Schmitz, U.K., and, Braun, H.P., (1998) Unique composition of the preprotein translocase of the outer mitochondrial membrane from plants. J. Biol. Chem. 273, 17251-17257. (Pubitemid 28311765)
27. Karpova, O.V., and, Newton, K.J., (1999) A partially assembled complex I in NAD4-deficient mitochondria of maize. Plant J. 17, 511-521.
28. Kashani-Poor, N., Kerscher, S., Zickermann, V., and, Brandt, U., (2001) Efficient large scale purification of his-tagged proton translocating NADH: ubiquinone oxidoreductase (complex I) from the strictly aerobic yeast Yarrowia lipolytica. Biochim. Biophys. Acta, 1504, 363-370. (Pubitemid 32201908)
29. Kikuchi, S., Hirohashi, T., and, Nakai, M., (2006) Characterization of the preprotein translocon at the outer envelope membrane of chloroplasts by blue native PAGE. Plant Cell Physiol. 47, 363-371.
30. Kikuchi, S., Oishi, M., Hirabayashi, Y., Lee, D.W., Hwang, I., and, Nakai, M., (2009) A 1-megadalton translocation complex containing Tic20 and Tic21 mediates chloroplast protein import at the inner envelope membrane. Plant Cell, 21, 1781-1797.
31. Kjell, J., Rasmusson, A.G., Larsson, H., and, Widell, S., (2004) Protein complexes of the plant plasma membrane resolved by blue native PAGE. Physiol. Plant, 121, 546-555. (Pubitemid 39123188)
32. Klostermann, E., Helling, I.D., Carde, J.P., and, Schünemann, D., (2002) The thylakoid membrane protein ALB3 associates with the cpSecY-translocase in Arabidopsis thaliana. Biochem. J. 368, 777-781. (Pubitemid 36042679)
33. Komenda, J., Reisinger, V., Müller, B.C., Dobáková, M., Granvogl, B., and, Eichacker, L.A., (2004) Accumulation of the D2 protein is a key regulatory step for assembly of the photosystem II reaction center complex in Synechocystis PCC 6803. J. Biol. Chem. 279, 48620-48629. (Pubitemid 39625737)
34. Kouranov, A., and, Schnell, D.J., (1997) Analysis of the interactions of preproteins with the import machinery over the course of protein import into chloroplasts. J. Cell Biol. 139, 1677-1685. (Pubitemid 28079233)
35. Küchler, M., Decker, S., Hormann, F., Soll, J., and, Heins, L., (2002) Protein import into chloroplasts involves redox-regulated proteins. EMBO J. 21, 6136-6145. (Pubitemid 35415330)
36. Kyhse-Andersen, J., (1984) Electroblotting of multiple gels: a simple apparatus without buffer tank for rapid transfer of proteins from polyacrylamide to nitrocellulose. J. Biochem. Biophys. Methods, 10, 203-209. (Pubitemid 15171298)
37. Ma, X., and, Cline, K., (2010) Multiple precursor proteins bind individual Tat receptor complexes and are collectively transported. EMBO J. 29, 1477-1488.
38. Maizel, J.V. Jr, (1966) Acrylamide-gel electrophorograms by mechanical fractionation: radioactive adenovirus proteins. Science, 151, 988-990.
39. Martin, J.R., Harwood, J.H., McCaffery, M., Fernandez, D.E., and, Cline, K., (2009) Localization and integration of thylakoid protein translocase subunit cpTatC. Plant J. 58, 831-842.
40. Millar, A.H., Mittova, V., Kiddle, G., Heazlewood, J.L., Bartoli, C.G., Theodoulou, F.L., and, Foyer, C.H., (2003) Control of ascorbate synthesis by respiration and its implications for stress responses. Plant Physiol. 133, 443-447. (Pubitemid 37325654)
41. Moslavac, S., Bredemeier, R., Mirus, O., Granvogl, B., Eichacker, L.A., and, Schleiff, E., (2005) Proteomic analysis of the outer membrane of Anabaena sp. strain PCC 7120. J. Proteome Res. 4, 1330-1338. (Pubitemid 41208689)
42. Moslavac, S., Reisinger, V., Berg, M., Mirus, O., Vosyka, O., Plöscher, M., Flores, E., Eichacker, L.A., and, Schleiff, E., (2007a) The proteome of the heterocyst cell wall in Anabaena sp. PCC 7120. Biol. Chem. 388, 823-829. (Pubitemid 47184840)
43. Moslavac, S., Nicolaisen, K., Mirus, O., Al Dehni, F., Pernil, R., Flores, E., Maldener, I., and, Schleiff, E., (2007b) A TolC-like protein is required for heterocyst development in Anabaena sp. strain PCC 7120. J. Bacteriol. 189, 7887-7895. (Pubitemid 350035097)
44. Nicolaisen, K., Hahn, A., and, Schleiff, E., (2009a) The cell wall in heterocyst formation by Anabaena sp. PCC 7120. J. Basic Microbiol. 49, 5-24.
45. Nicolaisen, K., Mariscal, V., Bredemeier, R., Pernil, R., Moslavac, S., Lõpez-Igual, R., Maldener, I., Herrero, A., Schleiff, E., and, Flores, E., (2009b) The outer membrane of a heterocyst-forming cyanobacterium is a permeability barrier for uptake of metabolites that are exchanged between cells. Mol. Microbiol. 74, 58-70.
46. Nielsen, E., Akita, M., Davila-Aponte, J., and, Keegstra, K., (1997) Stable association of chloroplastic precursors with protein translocation complexes that contain proteins from both envelope membranes and a stromal Hsp100 molecular chaperone. EMBO J. 16, 935-946. (Pubitemid 27113173)
47. Niepmann, M., and, Zheng, J., (2006) Discontinuous native protein gel electrophoresis. Electrophoresis, 27, 3949-3951. (Pubitemid 44680805)
48. Nübel, E., Wittig, I., Kerscher, S., Brandt, U., and, Schägger, H., (2009) Two-dimensional native electrophoretic analysis of respiratory supercomplexes from Yarrowia lipolytica. Proteomics, 9, 2408-2418.
49. Ossenbühl, F., Göhre, V., Meurer, J., Krieger-Liszkay, A., Rochaix, J.D., and, Eichacker, L.A., (2004) Efficient assembly of photosystem II in chlamydomonas reinhardtii requires Alb3.1p, a homolog of Arabidopsis ALBINO3. Plant Cell, 16, 1790-1800. (Pubitemid 38908776)
50. Pribil, M., Pesaresi, P., Hertle, A., Barbato, R., and, Leister, D., (2010) Role of plastid protein phosphatase TAP38 in LHCII dephosphorylation and thylakoid electron flow. PLoS Biol. 8, e1000288.
51. Qbadou, S., Becker, T., Bionda, T., Reger, K., Ruprecht, M., Soll, J., and, Schleiff, E., (2007) Toc64-a preprotein-receptor at the outer membrane with bipartide function. J. Mol. Biol. 367, 1330-1346. (Pubitemid 46420704)
52. Rehling, P., Brandner, K., and, Pfanner, N., (2004) Mitochondrial import and the twin-pore translocase. Nat. Rev. Mol. Cell Biol. 5, 519-530. (Pubitemid 38868581)
53. Reisinger, V., and, Eichacker, L.A., (2007) How to analyze protein complexes by 2D blue native SDS-PAGE. Proteomics, 7, 6-16. (Pubitemid 351547765)
54. Rexroth, S., Tittingdorf, R.M.W.M.Z., Schwassmann, H.J., Krause, F., Seelert, H., and, Dencher, N.A., (2004) Dimeric H+-ATP synthase in the chloroplast of Chlamydomonas reinhardtii. Biophys. Biochim. Acta, 1658, 202-211. (Pubitemid 39278484)
55. Sabar, M., Gagliardi, D., Balk, J., and, Leaver, C.J., (2003) ORFB is a subunit of F1FO-ATP synthase: insight into the basis of cytoplasmic male sterility in sunflower. EMBO Rep. 4, 381-386. (Pubitemid 36622003)
56. Schägger, H., and, Pfeiffer, K., (2000) Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. EMBO J. 19, 1777-1783. (Pubitemid 30204389)
57. Schägger, H., and, von Jagow, G., (1991) Blue native electrophoresis for isolation of membrane-protein complexes in enzymatically active form. Anal. Biochem. 199, 223-231.
58. Schägger, H., Cramer, W.A., and, von Jagow, G., (1994) Analysis of molecular masses and oligomeric states of protein complexes by blue native electrophoresis and isolation of membrane protein complexes by two-dimensional native electrophoresis. Anal. Biochem. 217, 220-230. (Pubitemid 24080754)
59. Schleiff, E., and, Becker, T., (2011) Common ground for protein translocation: access control for mitochondria and chloroplasts. Nat. Rev. Mol. Cell Biol. 12, 48-59.
60. Schleiff, E., and, Tampé, R., (2009) Membrane proteins take center stage in Frankfurt. Nat. Chem. Biol. 5, 135-139.
61. Schleiff, E., Soll, J., Küchler, M., Kühlbrandt, W., and, Harrer, R., (2003) Characterization of the translocon of the outer envelope of chloroplasts. J. Cell Biol. 160, 541-551. (Pubitemid 36254392)
62. Schmidt, O., Pfanner, N., and, Meisinger, C., (2010) Mitochondrial protein import: from proteomics to functional mechanisms. Nat. Rev. Mol. Cell Biol. 11, 655-667.
63. Schwenkert, S., Umate, P., Dal Bosco, C., Volz, S., Mlç ochová, L., Zoryan, M., Eichacker, L.A., Ohad, I., Herrmann, R.G., and, Meurer, J., (2006) PsbI affects the stability, function, and phosphorylation patterns of photosystem II assemblies in tobacco. J. Biol. Chem. 281, 34227-34238. (Pubitemid 46036631)
64. Seelert, H., Dencher, N.A., and, Müller, D.J., (2003) Fourteen protomers compose the oligomer III of the proton-rotor in spinach chloroplast ATP synthase. J. Mol. Biol. 333, 337-344. (Pubitemid 37188576)
65. Shevchenko, A., Tomas, H., Havli, J., Olsen, J.V., and, Mann, M., (2007) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc. 1, 2856-2860.
66. Slotboom, D.J., Duurkens, R.H., Olieman, K., and, Erkens, G.B., (2008) Static light scattering to characterize membrane proteins in detergent solution. Methods, 46, 73-82.
67. Smith, A.L., (1967) Preparation, properties and conditions for assay of mitochondria, small scale. Methods Enzymol. 10, 81-86.
68. Sohrt, K., and, Soll, J., (2000) Toc64, a new component of the protein translocon of chloroplasts. J. Cell Biol. 148, 1213-1221.
69. Suzuki, J.Y., Ytterberg, A.J., Beardslee, T.A., Allison, L.A., Wijk, K.J., and, Maliga, P., (2004) Affinity purification of the tobacco plastid RNA polymerase and in vitro reconstitution of the holoenzyme. Plant J. 40, 164-172. (Pubitemid 39342603)
70. Thidholm, E., Lindström, V., Tissier, C., Robinson, C., Schröder, W.P., and, Funk, C., (2002) Novel approach reveals localisation and assembly pathway of the PsbS and PsbW proteins into the photosystem II dimer. FEBS Lett. 513, 217-222. (Pubitemid 34251268)
71. Tree, J.J., Wolfson, E.B., Wang, D., Roe, A.J., and, Gally, D.L., (2009) Controlling injection: regulation of type III secretion in enterohaemorrhagic Escherichia coli. Trends Microbiol. 17, 361-370.
72. Van Coster, R., Smet, J., George, E., et al. (2001) Blue native polyacrylamide gel electrophoresis: a powerful tool in diagnosis of oxidative phosphorylation defects. Pediatr. Res. 50, 658-665. (Pubitemid 33009992)
73. Werhahn, W., Niemeyer, A., Jansch, L., Kruft, V., Schmitz, U.K., and, Braun, H.P., (2001) Purification and characterization of the preprotein translocase of the outer mitochondrial membrane from Arabidopsis. Identification of multiple forms of TOM20. Plant Physiol. 125, 943-954. (Pubitemid 32169901)
74. Werhahn, W., Jansch, L., and, Braun, H.P., (2003) Identification of novel subunits of the TOM complex from Arabidopsis thaliana. Plant Phys. Biochem. 41, 407-416. (Pubitemid 36708596)
75. Wittig, I., and, Schägger, H., (2008) Features and applications of blue-native and clear-native electrophoresis. Proteomics, 8, 3974-3990.
76. Wittig, I., Braun, H.P., and, Schägger, H., (2006) Blue native PAGE. Nat. Protoc. 1, 418-428.
77. Zhang, H.M., Whitelegge, J.P., and, Cramer, W.A., (2001) Ferredoxin: NADP(+) oxidoreductase is a subunit of the chloroplast cytochrome b(6)f complex. J. Biol. Chem. 276, 38159-38165.
78. Zickermann, V., Kerscher, S., Zwicker, K., Tocilescu, M.A., Radermacher, M., and, Brandt, U., (2009) Architecture of complex I and its implications for electron transfer and proton pumping. Biochim. Biophys. Acta, 1787, 574-583.