Structure and conservation of the periplasmic targeting factor Tic22 protein from plants and cyanobacteria

Journal of Biological Chemistry

Volumn 287, Issue 29, 2012, Pages 24164-24173

  Tripp, Joanna ^a   Hahn, Alexander ^a   Koenig, Patrick ^b,c   Flinner, Nadine ^a   Bublak, Daniela ^a   Brouwer, Eva M ^a   Ertel, Franziska ^a,d   Mirus, Oliver ^a   Sinning, Irmgard ^b   Tews, Ivo ^b,e   Schleiff, Enrico ^a  

^a GOETHE UNIVERSITY   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c GENENTECH INC   (United States)

^d MCGILL UNIVERSITY   (Canada)

^e UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANABAENA SP. PCC 7120; BACTERIAL PROTEIN; CHEMICAL CROSS-LINKING; ENDOSYMBIOTIC; EVOLUTIONARY CONSERVATIONS; HYDROPHOBIC POCKETS; IMMUNOPRECIPITATIONS; IN-VITRO; OUTER MEMBRANE; PERIPLASM; PHYSICAL INTERACTIONS; THREE-DIMENSIONAL STRUCTURE; THYLAKOIDS; TRANSLOCON;

BIOSYNTHESIS; CROSSLINKING;

PROTEINS;

BACTERIAL PROTEIN; PROTEIN BAMB; PROTEIN CLPS; PROTEIN OMP85; PROTEIN TIC22; TRANSLOCON; UNCLASSIFIED DRUG;

ANABAENA; ARTICLE; BACTERIAL STRAIN; BIOGENESIS; CHLOROPLAST; CONTROLLED STUDY; CROSS LINKING; CRYSTAL STRUCTURE; CYTOPLASM; ELECTRON MICROSCOPY; GENETIC CONSERVATION; HYDROPHOBICITY; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; MUTANT; NONHUMAN; PHENOTYPE; PLANT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; THYLAKOID;

ANABAENA; BACTERIAL PROTEINS; CYANOBACTERIA; MEMBRANE TRANSPORT PROTEINS; MICROSCOPY, ELECTRON; MOLECULAR CHAPERONES; PERIPLASM; PLANTS; PROTEIN TRANSPORT; THYLAKOIDS;

BACTERIA (MICROORGANISMS); CYANOBACTERIA; NOSTOC SP. PCC 7120;

EID: 84863802049     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.341644     Document Type: Article

References (57)

1. Cavalier-Smith, T. (2006) Origin of mitochondria by intracellular enslavement of a photosynthetic purple bacterium. Proc. Biol. Sci. 273, 1943-1952
2. Archibald, J. M. (2009) The puzzle of plastid evolution. Curr. Biol. 19, R81-R88
3. Alcock, F., Clements, A., Webb, C., and Lithgow, T. (2010) Evolution. Tinkering inside the organelle. Science. 327, 649-650
4. Bohnsack, M. T., and Schleiff, E. (2010) The evolution of protein targeting and translocation systems. Biochim. Biophys. Acta 1803, 1115-1130
5. Chacinska, A., Koehler, C. M., Milenkovic, D., Lithgow, T., and Pfanner, N. (2009) Importing mitochondrial proteins: Machineries and mechanisms. Cell 138, 628-644
6. 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
7. Kessler, F., and Schnell, D. (2009) Chloroplast biogenesis: Diversity and regulation of the protein import apparatus. Curr. Opin. Cell Biol. 21, 494-500
8. 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)
9. Kouranov, A., Chen, X., Fuks, B., and Schnell, D. J. (1998) Tic20 and Tic22 are new components of the protein import apparatus at the chloroplast inner envelope membrane. J. Cell Biol. 143, 991-1002 (Pubitemid 28547398)
10. Becker, T., Hritz, J., Vogel, M., Caliebe, A., Bukau, B., Soll, J., and Schleiff, E. (2004) Toc12, a novel subunit of the intermembrane space preprotein translocon of chloroplasts. Mol. Biol. Cell 15, 5130-5144 (Pubitemid 39392225)
11. Kalanon, M., and McFadden, G. I. (2008) The chloroplast protein translocation complexes of Chlamydomonas reinhardtii: A bioinformatic comparison of Toc and Tic components in plants, green algae, and red algae. Genetics. 179, 95-112
12. Hewitt, V., Alcock, F., and Lithgow, T. (2011) Minor modifications and major adaptations: The evolution of molecular machines driving mitochondrial protein import. Biochim. Biophys. Acta 1808, 947-954
13. Knowles, T. J., Scott-Tucker, A., Overduin, M., and Henderson, I. R. (2009) Membrane protein architects: The role of the BAM complex in outer membrane protein assembly. Nat. Rev. Microbiol. 7, 206-214
14. Schleiff, E., Maier, U. G., and Becker, T. (2011) Omp85 in eukaryotic systems: One protein family with distinct functions. Biol. Chem. 392, 21-27
15. Jacob-Dubuisson, F., Villeret, V., Clantin, B., Delattre, A. S., and Saint, N. (2009) First structural insights into the TpsB/Omp85 superfamily. Biol. Chem. 390, 675-684
16. 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)
17. Koenig, P., Mirus, O., Haarmann, R., Sommer, M. S., Sinning, I., Schleiff, E., and Tews, I. (2010) Conserved properties of polypeptide transport-associated (POTRA) domains derived from cyanobacterial Omp85. J. Biol. Chem. 285, 18016-18024
18. Fulda, S., Norling, B., Schoor, A., and Hagemann, M. (2002) The Slr0924 protein of Synechocystis sp. strain PCC 6803 resembles a subunit of the chloroplast protein import complex and is mainly localized in the thylakoid lumen. Plant Mol. Biol. 49, 107-118 (Pubitemid 34414194)
19. Fulda, S., Mikkat, S., Schröder, W., and Hagemann, M. (1999) Isolation of salt-induced periplasmic proteins from Synechocystis sp. strain PCC 6803. Arch. Microbiol. 171, 214-217 (Pubitemid 29142896)
20. Sriram, S. M., Kim, B. Y., and Kwon, Y. T. (2011) The N-end rule pathway: Emerging functions and molecular principles of substrate recognition. Nat. Rev. Mol. Cell Biol. 12, 735-747
21. Heuck, A., Schleiffer, A., and Clausen, T. (2011) Augmenting β-augmentation: Structural basis of how BamB binds BamA and may support folding of outer membrane proteins. J. Mol. Biol. 406, 659-666
22. Moslavac, S., Nicolaisen, K., Mirus, O., Al Dehni, F., Pernil, R., Flores, E., Maldener, I., and Schleiff, E. (2007) A TolC-like protein is required for heterocyst development in Anabaena sp. strain PCC 7120. J. Bacteriol. 189, 7887-7895 (Pubitemid 350035097)
23. Nicolaisen, K., Mariscal, V., Bredemeier, R., Pernil, R., Moslavac, S., López-Igual, R., Maldener, I., Herrero, A., Schleiff, E., and Flores, E. (2009) 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
24. Nicolaisen, K., Hahn, A., Valdebenito, M., Moslavac, S., Samborski, A., Maldener, I., Wilken, C., Valladares, A., Flores, E., Hantke, K., and Schleiff, E. (2010) The interplay between siderophore secretion and coupled iron and copper transport in the heterocyst-forming cyanobacterium Anabaena sp. PCC 7120. Biochim. Biophys. Acta 1798, 2131-2140
25. Bendtsen, J. D., Nielsen, H., von Heijne, G., and Brunak, S. (2004) Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340, 783-795 (Pubitemid 38829638)
26. Rippka, R., Deruelles, J., Waterbury, J. B., Herdman, M., and Stanier, R. Y. (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Microbiology 111, 1-61 (Pubitemid 9142236)
27. 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)
28. Black, K., Buikema, W. J., and Haselkorn, R. (1995) The hglK gene is required for localization of heterocyst-specific glycolipids in the cyanobacterium Anabaena sp. strain PCC 7120. J. Bacteriol. 177, 6440-6448
29. Van Duyne, G. D., Standaert, R. F., Karplus, P. A., Schreiber, S. L., and Clardy, J. (1993) Atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin. J. Mol. Biol. 229, 105-124 (Pubitemid 23037917)
30. Terwilliger, T. C., and Berendzen, J. (1999) Automated MAD and MIR structure solution. Acta Crystallogr. D 55, 849-861 (Pubitemid 29194533)
31. Emsley, P., and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (Pubitemid 41742764)
32. Murshudov, G. N., Vagin, A. A., Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D 53, 240-255 (Pubitemid 27235885)
33. Lamzin, V. S., and Wilson, K. S. (1999) Automated refinement for protein crystallography. Methods Enzymol. 276, 269-305 (Pubitemid 27390926)
34. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK: A program to check the stereochemical quality of protein structures. J. Appl. Cryst. 26, 283-291
35. Pernil, R., Picossi, S., Mariscal, V., Herrero, A., and Flores, E. (2008) ABC-type amino acid uptake transporters Bgt and N-II of Anabaena sp. strain PCC 7120 share an ATPase subunit and are expressed in vegetative cells and heterocysts. Mol. Microbiol. 67, 1067-1080 (Pubitemid 351207334)
36. Sklar, J. G., Wu, T., Kahne, D., and Silhavy, T. J. (2007) Defining the roles of the periplasmic chaperones SurA, Skp, and DegP in Escherichia coli. Genes Dev. 21, 2473-2484 (Pubitemid 47529375)
37. Knoblauch, N. T., Rüdiger, S., Schönfeld, H. J., Driessen, A. J., Schneider-Mergener, J., and Bukau, B. (1999) Substrate specificity of the SecB chaperone. J. Biol. Chem. 274, 34219-34225 (Pubitemid 129511760)
38. Dekker, C., de Kruijff, B., and Gros, P. (2003) Crystal structure of SecB from Escherichia coli. J. Struct. Biol. 144, 313-319 (Pubitemid 37468388)
39. Bechtluft, P., Nouwen, N., Tans, S. J., Driessen, A. J. (2010) SecB-a chaperone dedicated to protein translocation. Mol. Biosyst 6, 620-627
40. Xu, X., Wang, S., Hu, Y. X., and McKay, D. B. (2007) The periplasmic bacterial molecular chaperone SurA adapts its structure to bind peptides in different conformations to assert a sequence preference for aromatic residues. J. Mol. Biol. 373, 367-381 (Pubitemid 47445573)
41. Moslavac, S., Reisinger, V., Berg M., Mirus, O., Vosyka, O., Plöscher, M., Flores, E., Eichacker, L. A., and Schleiff, E. (2007) The proteome of the heterocyst cell wall in Anabaena sp. PCC 7120. Biol. Chem. 388, 823-829 (Pubitemid 47184840)
42. Nicolaisen, K., Hahn, A., and Schleiff, E. (2009) The cell wall in heterocyst formation by Anabaena sp. PCC 7120. J. Basic Microbiol. 49, 5-24
43. Flores, E., and Herrero, A. (2010) Compartmentalized function through cell differentiation in filamentous cyanobacteria. Nat. Rev. Microbiol. 8, 39-50
44. Ladig, R., Sommer, M. S., Hahn, A., Leisegang, M. S., Papasotiriou, D. G., Ibrahim, M., Elkehal, R., Karas, M., Zickermann, V., Gutensohn, M., Brandt, U., Klösgen, R. B., Schleiff, E. (2011) A high-definition native polyacrylamide gel electrophoresis system for the analysis of membrane complexes. Plant J. 67, 181-194
45. Ieva, R., Tian, P., Peterson, J. H., and Bernstein, H. D. (2011) Sequential and spatially restricted interactions of assembly factors with an autotransporter β domain. Proc. Natl. Acad. Sci. U.S.A. 108, E383-391
46. Vuong, P., Bennion, D., Mantei, J., Frost, D., and Misra, R. (2008) Analysis of YfgL and YaeT interactions through bioinformatics, mutagenesis, and biochemistry. J. Bacteriol. 190, 1507-1517 (Pubitemid 351304004)
47. Román-Hernández, G., Grant, R. A., Sauer, R. T., and Baker, T. A. (2009) Molecular basis of substrate selection by the N-end rule adaptor protein ClpS. Proc. Natl. Acad. Sci. U.S.A. 106, 8888-8893
48. Kim, K. H., and Paetzel, M. (2011) Crystal structure of Escherichia coli BamB, a lipoprotein component of the β-barrel assembly machinery complex. J. Mol. Biol. 406, 667-678
49. Noinaj, N., Fairman, J. W., and Buchanan, S. K. (2011) The crystal structure of BamB suggests interactions with BamA and its role within the BAM complex. J. Mol. Biol. 407, 248-260
50. Albrecht, R., and Zeth, K. (2011) Structural basis of outer membrane protein biogenesis in bacteria. J. Biol. Chem. 286, 27792-27803
51. Holm, L., and Rosenström, P. (2010) Dali server: Conservation mapping in three dimensions. Nucleic Acids Res. 38, W545-549
52. Cavalier-Smith, T. (2006) Rooting the tree of life by transition analyses. Biol. Direct. 1, 19
53. 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 β-barrel transporters of the Omp85 family. J. Biol. Chem. 282, 1882-1890 (Pubitemid 47076709)
54. Baker, N. A., Sept, D., Joseph, S., Holst, M. J., and McCammon, J. A. (2001) Electrostatics of nanosystems: Application to microtubules and the ribosome. Proc. Natl. Acad. Sci. U.S.A. 98, 10037-10041 (Pubitemid 32802969)
55. Kyte, J., and Doolittle, R. F. (1982) A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157, 105-132
56. Olmedo-Verd, E., Muro-Pastor, A. M., Flores, E., and Herrero, A. (2006) Localized induction of the ntcA regulatory gene in developing heterocysts of Anabaena sp. strain PCC 7120. J. Bacteriol. 188, 6694-6699 (Pubitemid 44412080)
57. Black, T. A., Cai, Y., and Wolk, C. P. (1993) Spatial expression and autoregulation of hetR, a gene involved in the control of heterocyst development in Anabaena. Mol. Microbiol. 9, 77-84 (Pubitemid 23217739)