In vitro interaction of the housekeeping SecA1 with the accessory SecA2 protein of Mycobacterium tuberculosis

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Prabudiansyah, Irfan ^a   Kusters, Ilja ^a,b   Driessen, Arnold J M ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; HETERODIMER; HOMODIMER; OLIGOMER; PROTEIN SECA1; PROTEIN SECA2; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE; CARRIER PROTEIN; PROTEIN BINDING; RECOMBINANT PROTEIN; SECA1 PROTEIN, MYCOBACTERIUM TUBERCULOSIS; SECA2 PROTEIN, MYCOBACTERIUM; SOLUTION AND SOLUBILITY; VIRULENCE FACTOR;

ARTICLE; CONTROLLED STUDY; DIMERIZATION; DISSOCIATION; FLUORESCENCE CORRELATION SPECTROSCOPY; IN VITRO STUDY; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; ESCHERICHIA COLI; ESSENTIAL GENE; GENE EXPRESSION; GENETICS; METABOLISM; MUTATION; PROTEIN MULTIMERIZATION; PROTEIN TRANSPORT; SOLUTION AND SOLUBILITY;

BACTERIA (MICROORGANISMS); CORYNEBACTERINEAE; MYCOBACTERIUM TUBERCULOSIS; POSIBACTERIA;

ADENOSINE TRIPHOSPHATASES; BACTERIAL PROTEINS; ESCHERICHIA COLI; GENE EXPRESSION; GENES, ESSENTIAL; MEMBRANE TRANSPORT PROTEINS; MUTATION; MYCOBACTERIUM TUBERCULOSIS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN TRANSPORT; RECOMBINANT PROTEINS; SOLUTIONS; VIRULENCE FACTORS;

EID: 84934973427     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0128788     Document Type: Article

References (59)

1. Driessen AJM, Nouwen N (2008) Protein translocation across the bacterial cytoplasmic membrane. Annu Rev Biochem 77: 643-667. PMID: 18078384
2. Du Plessis DJF, Nouwen N, Driessen AJM (2011) The Sec translocase. Biochim Biophys Acta 1808: 851-865. doi: 10.1016/j.bbamem.2010.08.016 PMID: 20801097
3. Lycklama a Nijeholt JA, Driessen AJM (2012) The bacterial Sec-translocase: structure and mechanism. Philos Trans R Soc Lond B Biol Sci 367: 1016-1028. doi: 10.1098/rstb.2011.0201 PMID: 22411975
4. Schiebel E, Driessen AJM, Hartl FU, Wickner W (1991) ΔμH+ and ATP function at different steps of the catalytic cycle of preprotein translocase. Cell 64: 927-939. PMID: 1825804
5. Economou A, Wickner W (1994) SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion. Cell 78: 835-843. PMID: 8087850
6. Van der Wolk JPW, De Wit JG, Driessen AJM (1997) The catalytic cycle of the Escherichia coli SecA ATPase comprises two distinct preprotein translocation events. EMBO J 16: 7297-7304. PMID: 9405359
7. Kusters I, Driessen AJM (2011) SecA, a remarkable nanomachine. Cell Mol Life Sci 68: 2053-2066. doi: 10.1007/s00018-011-0681-y PMID: 21479870
8. Fekkes P, de Wit JG, van der Wolk JPW, Kimsey HH, Kumamoto CA, Driessen AJM (1998) Preprotein transfer to the Escherichia coli translocase requires the co-operative binding of SecB and the signal sequence to SecA. Mol Microbiol 29: 1179-1190. PMID: 9767586
9. Bechtluft P, Nouwen N, Tans SJ, Driessen AJM (2010) SecB - a chaperone dedicated to protein translocation. Mol Biosyst 6: 620-627. doi: 10.1039/b915435c PMID: 20237639
10. Driessen AJM (1993) SecA, the peripheral subunit of the Escherichia coli precursor protein translocase, is functional as a dimer. Biochemistry 32: 13190-13197. PMID: 8241173
11. De Keyzer J, van der Sluis EO, Spelbrink REJ, Nijstad N, de Kruijff B, Nouwen N,et al. (2005) Covalently dimerized SecA is functional in protein translocation. J Biol Chem 280: 35255-35260. PMID: 16115882
12. Jilaveanu LB, Zito CR, Oliver D (2005) Dimeric SecA is essential for protein translocation. Proc Natl Acad Sci U S A 102: 7511-7516. PMID: 15897468
13. Gouridis G, Karamanou S, Sardis MF, Schärer MA, Capitani G, Economou A (2013) Quaternary dynamics of the SecA motor drive translocase catalysis. Mol Cell 52: 655-666. doi: 10.1016/j.molcel.2013.10.036 PMID: 24332176
14. Hunt JF, Weinkauf S, Henry L, Fak JJ, McNicholas P, Oliver DB, qt al. (2002) Nucleotide control of interdomain interactions in the conformational reaction cycle of SecA. Science 297: 2018-2026. PMID: 12242434
15. Ding H, Hunt JF, Mukerji I, Oliver D (2003) Bacillus subtilis SecA ATPase Exists as an Antiparallel Dimer in Solution. Biochemistry 42: 8729-8738. PMID: 12873133
16. Sharma V, Arockiasamy A, Ronning DR, Savva CG, Holzenburg A, Braunstein Met al. (2003) Crystal structure of Mycobacterium tuberculosis SecA, a preprotein translocating ATPase. Proc Natl Acad Sci U S A 100: 2243-2248. PMID: 12606717
17. Papanikolau Y, Papadovasilaki M, Ravelli RBG, McCarthy A, Cusack S, Economou A et al. (2007) Structure of dimeric SecA, the Escherichia coli preprotein translocase motor. J Mol Biol 366: 1545-1457. PMID: 17229438
18. Zimmer J, Li W, Rapoport TA (2006) A novel dimer interface and conformational changes revealed by an X-ray structure of B. subtilis SecA. J Mol Biol 364: 259-265. PMID: 16989859
19. Vassylyev DG, Mori H, Vassylyeva MN, Tsukazaki T, Kimura Y, Tahirov TH, et al. (2006) Crystal structure of the translocation ATPase SecA from Thermus thermophilus reveals a parallel, head-to-head dimer. J Mol Biol 364: 248-258. PMID: 17059823
20. Benach J, Chou Y-T, Fak JJ, Itkin A, Nicolae DD, Smith PC, et al. (2003) Phospholipid-induced monomerization and signal-peptide-induced oligomerization of SecA. J Biol Chem 278: 3628-3638. PMID: 12403785
21. Or E, Boyd D, Gon S, Beckwith J, Rapoport T (2005) The bacterial ATPase SecA functions as a monomer in protein translocation. J Biol Chem 280: 9097-9105. PMID: 15618215
22. Musial-Siwek M, Rusch SL, Kendall DA (2005) Probing the affinity of SecA for signal peptide in different environments. Biochemistry 44: 13987-13996. PMID: 16229488
23. Bu Z, Wang L, Kendall DA (2003) Nucleotide Binding Induces Changes in the Oligomeric State and Conformation of SecA in a Lipid Environment: A Small-angle Neutron-scattering Study. J Mol Biol 332: 23-30. PMID: 12946344
24. Wowor AJ, Yu D, Kendall DA, Cole JL (2011) Energetics of SecA dimerization. J Mol Biol 408: 87-98. doi: 10.1016/j.jmb.2011.02.006 PMID: 21315086
25. Kusters I, van den Bogaart G, Kedrov A, Krasnikov V, Fulyani F, Poolman B,et al. (2011) Quaternary structure of SecA in solution and bound to SecYEG probed at the single molecule level. Structure 19: 430-439. doi: 10.1016/j.str.2010.12.016 PMID: 21397193
26. Woodbury RL, Hardy SJS, Randall LL (2002) Complex behavior in solution of homodimeric SecA. Protein Sci 11: 875-882. PMID: 11910030
27. Braunstein M, Brown AM, Kurtz S Jr WRJ (2001) Two Nonredundant SecA Homologues Function in Mycobacteria. J Bacteriol 183: 6979-6990. PMID: 11717254
28. Bensing BA, Sullam PM (2002) An accessory sec locus of Streptococcus gordonii is required for export of the surface protein GspB and for normal levels of binding to human platelets. Mol Microbiol 44: 1081-1094. PMID: 12010500
29. Caspers M, Freudl R (2008) Corynebacterium glutamicum possesses two secA homologous genes that are essential for viability. Arch Microbiol 189: 605-610. doi: 10.1007/s00203-008-0351-0 PMID: 18246326
30. Feltcher ME, Braunstein M (2012) Emerging themes in SecA2-mediated protein export. Nat Rev Microbiol 10: 779-789. doi: 10.1038/nrmicro2874 PMID: 23000954
31. Bensing BA, Seepersaud R, Yen YT, Sullam PM (2014) Selective transport by SecA2: an expanding family of customized motor proteins. Biochim Biophys Acta 1843: 1674-1686. doi: 10.1016/j.bbamcr.2013.10.019 PMID: 24184206
32. Lenz LL, Mohammadi S, Geissler A, Portnoy DA (2003) SecA2-dependent secretion of autolytic enzymes promotes Listeria monocytogenes pathogenesis. Proc Natl Acad Sci U S A 100: 12432-12437. PMID: 14527997
33. Sullivan JT, Young EF, McCann JR, Braunstein M (2012) The Mycobacterium tuberculosis SecA2 system subverts phagosome maturation to promote growth in macrophages. Infect Immun 80: 996-1006. doi: 10.1128/IAI.05987-11 PMID: 22215736
34. Van der Woude AD, Stoop EJM, Stiess M, Wang S, Ummels R, van Stempvoort G, et al. (2014) Analysis of SecA2-dependent substrates in Mycobacterium marinum identifies protein kinase G (PknG) as a virulence effector. Cell Microbiol 16: 280-295. doi: 10.1111/cmi.12221 PMID: 24119166
35. Braunstein M, Espinosa BJ, Chan J, Belisle JT, Jacobs W R. (2003) SecA2 functions in the secretion of superoxide dismutase A and in the virulence of Mycobacterium tuberculosis. Mol Microbiol 48: 453-464. A PMID: 12675804
36. Hou JM, D'Lima NG, Rigel NW, Gibbons HS, McCann JR, Braunstein M, et al. (2008) ATPase activity of Mycobacterium tuberculosis SecA1 and SecA2 proteins and its importance for SecA2 function in macrophages. J Bacteriol 190: 4880-4887. doi: 10.1128/JB.00412-08 PMID: 18487341
37. Rigel NW, Gibbons HS, McCann JR, McDonough JA, Kurtz S, Braunstein M (2009) The Accessory SecA2 System of Mycobacteria Requires ATP Binding and the Canonical SecA1. J Biol Chem 284: 9927-9936. doi: 10.1074/jbc.M900325200 PMID: 19240020
38. Fagan RP, Fairweather NF (2011) Clostridium difficile has two parallel and essential Sec secretion systems. J Biol Chem 286: 27483-27493. doi: 10.1074/jbc.M111.263889 PMID: 21659510
39. D'Lima NG, Teschke CM (2014) ADP-dependent conformational changes distinguish Mycobacterium tuberculosis SecA2 from SecA1. J Biol Chem 289: 2307-2317. doi: 10.1074/jbc.M113.533323 PMID: 24297168
40. Rigel NW, Braunstein M (2008) A new twist on an old pathway: accessory Sec systems. Mol Microbiol 69: 291-302. doi: 10.1111/j.1365-2958.2008.06294.x PMID: 18544071
41. Zhou M, Zhang H, Zhu F, Wu H (2011) Canonical SecA associates with an accessory secretory protein complex involved in biogenesis of a streptococcal serine-rich repeat glycoprotein. J Bacteriol 193: 6560-6566. doi: 10.1128/JB.05668-11 PMID: 21965576
42. Halbedel S, Reiss S, Hahn B, Albrecht D, Mannala GK, Chakraborty T, et al. (2014) A systematic proteomic analysis of Listeria monocytogenes house-keeping protein secretion systems. Mol Cell Proteomics 13: 3063-3081. doi: 10.1074/mcp.M114.041327 PMID: 25056936
43. Hanahan D, Harbor CS (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166: 557-580. PMID: 6345791
44. Studier FW, Rosenberg AH, Dunn JJ, Dubendorff JW (1990) Use of T7 RNA Polymerase to Direct Expression of Cloned Genes. Methods Enzymol 185: 60-89. PMID: 2199796
45. Van der Does C, de Keyzer J, van der Laan M, Driessen AJM (2003) Reconstitution of Purified Bacterial Preprotein Translocase in Liposomes. Methods Enzymol 372: 86-98. PMID: 14610808
46. Wienken CJ, Baaske P, Rothbauer U, Braun D, Duhr S (2010) Protein-binding assays in biological liquids using microscale thermophoresis. Nat Commun 1: 100. doi: 10.1038/ncomms1093 PMID: 20981028
47. Jerabek-Willemsen M, Wienken CJ, Braun D, Baaske P, Duhr S (2011) Molecular interaction studies using microscale thermophoresis. Assay Drug Dev Technol 9: 342-353. doi: 10.1089/adt.2011.0380 PMID: 21812660
48. Seidel SAI, Dijkman PM, Lea WA, van den Bogaart G, Jerabek-Willemsen M, Lazic A, et al. (2013) Microscale Thermophoresis Quantifies Biomolecular Interactions under Previously Challenging Conditions. Methods 59: 301-315. doi: 10.1016/j.ymeth.2012.12.005 PMID: 23270813
49. Veldhuis G, Hink M, Krasnikov V, van den Bogaart G, Hoeboer J, Visser AJ, et al. (2006) The oligomeric state and stability of the mannitol transporter, EnzymeII mtl, from Escherichia coli: A fluorescence correlation spectroscopy study. Protein Sci 15: 1977-1986. PMID: 16823033
50. Akita M, Shinkai A, Matsuyama S, Mizushima S (1991) SecA, an essential component of the secretory machinery of Escherichia coli, exists as homodimer. Biochem Biophys Res Commun 174: 211-216. PMID: 1824919
51. Sardis MF, Economou A (2010) SecA: a tale of two protomers. Mol Microbiol 76: 1070-1081. doi: 10.1111/j.1365-2958.2010.07176.x PMID: 20444093
52. Duhr S, Braun D (2006) Why molecules move along a temperature gradient. Proc Natl Acad Sci U S A 103: 19678-19682. PMID: 17164337
53. Bacia K, Schwille P (2007) Practical guidelines for dual-color fluorescence cross-correlation spectroscopy. Nat Protoc 2: 2842-2856. PMID: 18007619
54. Cayley S, Lewis BA, Guttman HJ, Jry MTR (1991) Characterization of the Cytoplasm of Escherichia coli K-12 as a Function of External Osmolarity: Implications for Protein-DNA Interactions in Vivo. J Mol Biol 222: 281-300. PMID: 1960728
55. Or E, Navon A, Rapoport T (2002) Dissociation of the dimeric SecA ATPase during protein translocation across the bacterial membrane. EMBO J 21: 4470-4479. PMID: 12198149
56. Breukink E, Nouwen N, van Raalte A, Mizushima S, Tommassen J, de Kruijff B (1995) The C terminus of SecA is involved in both lipid binding and SecB binding. J Biol Chem 270: 7902-7907. PMID: 7713885
57. Zimmer J, Nam Y, Rapoport TA (2008) Structure of a complex of the ATPase SecA and the protein-translocation channel. Nature 455: 936-943. Available: doi: 10.1038/nature07335 PMID: 18923516
58. Das S, Oliver DB (2011) Mapping of the SecA SecY and SecA SecG interfaces by site-directed in vivo photocross-linking. J Biol Chem 286: 12371-12380. Available: doi: 10.1074/jbc.M110.182931 PMID: 21317284
59. Ligon LS, Rigel NW, Romanchuk A, Jones CD, Braunstein M (2013) Suppressor analysis reveals a role for SecY in the SecA2-dependent protein export pathway of Mycobacteria. J Bacteriol 195: 4456-4465. doi: 10.1128/JB.00630-13 PMID: 23913320