Leaving home ain't easy: Protein export systems in Gram-positive bacteria

Research in Microbiology

Volumn 164, Issue 6, 2013, Pages 664-674

  Freudl, Roland ^a  

^a FORSCHUNGSZENTRUM JÜLICH   (Germany)

Author keywords

Protein translocation; Sec pathway; Sec2 systems; Twin arginine translocation; Type VII secretion; WXG100 secretion

Indexed keywords

ARGININE; BACTERIAL PROTEIN; CARRIER PROTEIN; DOCKING PROTEIN; SEC TRANSLOCASE; SECY PROTEIN; SECY2 PROTEIN; SIGNAL PEPTIDASE; SIGNAL PEPTIDE; SIGNAL RECOGNITION PARTICLE; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG; YIDC PROTEIN;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL SECRETION SYSTEM; CARBOXY TERMINAL SEQUENCE; GRAM POSITIVE BACTERIUM; LISTERIA MONOCYTOGENES; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN STRUCTURE; PROTEIN TRANSPORT; STREPTOCOCCUS AGALACTIAE; STREPTOMYCES COELICOLOR;

PROTEIN TRANSLOCATION; SEC PATHWAY; SEC2 SYSTEMS; TWIN-ARGININE-TRANSLOCATION; TYPE VII SECRETION; WXG100 SECRETION;

BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; GRAM-POSITIVE BACTERIA; PROTEIN TRANSPORT;

NEGIBACTERIA; POSIBACTERIA;

EID: 84879882380     PISSN: 09232508     EISSN: 17697123     Source Type: Journal    
DOI: 10.1016/j.resmic.2013.03.014     Document Type: Article

References (100)

1. Abdallah A.M., van Pittius N.C., DiGiuseppe Champion P.A., Cox J., Luirink J., Vandenbroucke-Grauls C.M.J.E., Appelmelk B.J., Bitter W. Type VII secretion - mycobacteria show the way. Nat. Rev. Microbiol. 2007, 5:883-891.
2. Abdallah A.M., Verboom T., Weerdenburg E.M., van Pittius N.C.G., Mahasha P.W., Jimenez C., Parra M., Cadieux N., Brennan M.J., Appelmelk B.J., Bitter W. PPE and PE_PGRS proteins of Mycobacterium marinum are transported via the type VII secretion system ESX-5. Mol. Microbiol. 2009, 73:329-340.
3. Alami M., Lüke I., Deitermann S., Eisner G., Koch H.-G., Brunner J., Müller M. Differential interaction between a twin-arginine signal peptide and its translocase in Escherichia coli. Mol. Cell. 2003, 12:937-946.
4. Anderson M., Chen Y.-H., Butler E.K., Missiakas D.M. EsaD, a secretion factor for the Ess pathway in Staphylococcus aureus. J. Bacteriol. 2011, 193:1583-1589.
5. Archambaud C., Nahori M.A., Pizarro-Cerda J., Cossart P., Dussurget O. Control of Listeria superoxide dismutase by phosphorylation. J. Biol. Chem. 2006, 281:31812-31822.
6. Barnett J.P., Eijlander R.T., Kuipers O.P., Robinson C. A minimal Tat system from a Gram-positive organism. A bifunctional TatA subunit participates in discrete TatAC and TatA complexes. J. Biol. Chem. 2008, 283:2534-2542.
7. Baumgärtner M., Kärst U., Gerstel B., Loessner M., Wehland J., Jänsch L. Inactivation of Lgt allows systematic characterization of lipoproteins from Listeria monocytogenes. J. Bacteriol. 2007, 189:313-324.
8. Bechtluft P., Nouwen N., Tans S.J., Driessen A.J.M. SecB - a chaperone dedicated to protein translocation. Mol. BioSyst. 2010, 6:620-627.
9. Bendtsen J.D., Nielsen H., von Heijne G., Brunak S. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 2004, 340:783-795.
10. Bensing B.A., Sullam P.M. 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. 2002, 44:1081-1094.
11. Bensing B.A., Takamatsu D., Sullam P.M. Determinants of the streptococcal surface glycoprotein GspB that facilitate export by the accessory Sec system. Mol. Microbiol. 2005, 58:1468-1481.
12. Bensing B.A., Siboo I.R., Sullam P.M. Glycine residues in the hydrophobic core of the GspB signal sequence route export toward the accessory Sec pathway. J. Bacteriol. 2007, 189:3846-3854.
13. Bensing B.A., Sullam P.M. Transport of preproteins by the accessory Sec system requires a specific domain adjacent to the signal peptide. J. Bacteriol. 2010, 192:4223-4232.
14. Bensing B.A., Yen Y.T., Seepersaud R., Sullam P.M. A specific interaction between SecA2 and a region of the preprotein adjacent to the signal peptide occurs during transport via the accessory Sec system. J. Biol. Chem. 2012, 287:24438-24447.
15. Berks B.C. A common export pathway for proteins binding complex redox cofactors?. Mol. Microbiol. 1996, 22:393-404.
16. Berks B.C., Palmer T., Sargent F. The Tat protein translocation pathway and its role in microbial physiology. Adv. Microb. Physiol. 2003, 47:187-254.
17. Bitter W., Houben E.N.G., Bottai D., Brodin P., Brown E.J., Cox J.S., Derbyshire K., Fortune S.M., Gao L.-Y., Liu J., van Pittius N.C.G., Pym A.S., Rubin E.J., Sherman D.R., Cole S.T., Brosch R. Systematic genetic nomenclature for type VII secretion systems. PLoS Pathog. 2009, 5:e1000507.
18. Blaudeck N., Kreutzenbeck P., Freudl R., Sprenger G.A. Genetic analysis of pathway specificity during posttranslational protein translocation across the Escherichia coli plasma membrane. J. Bacteriol. 2003, 185:2811-2819.
19. Blaudeck N., Kreutzenbeck P., Müller M., Sprenger G.A., Freudl R. Isolation and characterization of bifunctional Escherichia coli TatA mutant proteins that allow efficient Tat-dependent protein translocation in the absence of TatB. J. Biol. Chem. 2005, 280:3426-3432.
20. Bolhuis A., Broekhuizen C.P., Sorokin A., van Roosmalen M.L., Venema G., Bron S., Quax W.J., van Dijl J.M. SecDF of Bacillus subtilis: a molecular Siamese twin required for efficient secretion of proteins. J. Biol. Chem. 1998, 273:21217-21244.
21. Bordes P., Cirinesi A.-M., Ummels R., Sala A., Sakr S., Bitter W., Genevaux P. SecB-like chaperone controls a toxin-antitoxin stress-responsive system in Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:8438-8443.
22. Braunstein M., Brown A.M., Kurtz S., Jacobs W.R. Two nonredundant SecA homologues function in mycobacteria. J. Bacteriol. 2001, 183:6979-6990.
23. Braunstein M., Espinosa B.J., Chan J., Belisle J.T., Jacobs W.R. SecA2 functions in the secretion of superoxide dismutase A and in the virulence of Mycobacterium tuberculosis. Mol. Microbiol. 2003, 48:453-464.
24. Brüser T., Sanders C. An alternative model of the twin arginine translocation system. Microbiol. Res. 2003, 158:7-17.
25. Burts M.L., Williams W.A., DeBord K., Missiakas D.M. EsxA and EsxB are secreted by an ESAT-6-like system that is required for the pathogenesis of Staphylococcus aureus infections. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:1169-1174.
26. Caspers M., Freudl R. Corynebacterium glutamicum possesses two secA homologous genes that are essential for viability. Arch. Microbiol. 2008, 189:605-610.
27. Chen Q., Wu H., Fives-Taylor P.M. Investigating the role of secA2 in secretion and glycosylation of a fimbrial adhesin in Streptococcus parasanguis FW213. Mol. Microbiol. 2004, 53:843-856.
28. Chen W., Huang Y.-j., Gundala S.R., Yang H., Li M., Tai P.C., Wang B. The first low μM SecA inhibitors. Bioorg. Med. Chem. 2010, 18:1617-1625.
29. Cregg K.M., Wilding E.I., Black M.T. Molecular cloning and expression of the spsB gene encoding an essential type I signal peptidase from Staphylococcus aureus. J. Bacteriol. 1996, 178:5712-5718.
30. Cristobal S., de Gier J.-W., Nielsen H., von Heijne G. Competition between Sec- and TAT-dependent protein translocation in Escherichia coli. EMBO J. 1999, 18:2982-2990.
31. Dalbey R.E., Wang P., Kuhn A. Assembly of bacterial inner membrane proteins. Annu. Rev. Biochem. 2011, 80:161-187.
32. Dalbey R.E., Wang P., van Dijl J.M. Membrane proteases in the bacterial protein secretion and quality control pathway. Microbiol. Mol. Biol. Rev. 2012, 76:311-350.
33. Daleke M.H., Ummels R., Bawono P., Heringa J., Vandenbroucke-Grauls C.M.J.E., Luirink J., Bitter W. General secretion signal for the mycobacterial type VII secretion pathway. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:11342-11347.
34. Desvaux M., Hebraud M., Talon R., Henderson I.R. Secretion and subcellular localizations of bacterial proteins: a semantic awareness issue. Trends Microbiol. 2009, 17:139-145.
35. DiGiuseppe Champion P.A., Stanley S.A., Champion M.M., Brown E.J., Cox J.S. C-terminal signal sequence promotes virulence factor secretion in Mycobacterium tuberculosis. Science 2006, 313:1632-1636.
36. Dramsi S., Bourdichon F., Cabanes D., Lecuit M., Fsihi H., Cossart P. FbpA, a novel multifunctional Listeria monocytogenes virulence factor. Mol. Microbiol. 2004, 53:639-649.
37. du Plessis D.J., Nouwen N., Driessen A.J.M. The Sec translocase. Biochim. Biophys. Acta 2011, 1808:851-865.
38. Fagan R.P., Fairweather N.F. Clostridium difficile has two parallel and essential Sec secretion systems. J. Biol. Chem. 2011, 286:27483-27493.
39. Feltcher M.E., Sullivan J.T., Braunstein M. Protein export systems of Mycobacterium tuberculosis: novel targets for drug development?. Future Microbiol. 2010, 5:1581-1597.
40. Feltcher M.E., Braunstein M. Emerging themes in SecA2-mediated protein export. Nat. Rev. Microbiol. 2012, 10:779-789.
41. Funes S., Hasona A., Bauerschmitt H., Grubbauer C., Kauff F., Collins R., Crowley P.J., Palmer S.R., Brady L.J., Herrmann J.M. Independent gene duplications of the YidC/Oxa/Alb3 family enabled a specialized cotranslational function. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:6656-6661.
42. Gibbons H.S., Wolschendorf F., Abshire M., Niederweis M., Braunstein M. Identification of two Mycobacterium smegmatis lipoproteins exported by a SecA2-dependent pathway. J. Bacteriol. 2007, 189:5090-5100.
43. Gohlke U., Pullan L., McDevitt C.A., Porcelli I., de Leeuw E., Palmer T., Saibil H.R., Berks B.C. The TatA component of the twin-arginine protein transport system forms channel complexes of variable diameter. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:10482-10486.
44. Gram H.C.J. Über die isolierte Färbung der Schizomyceten in Schnitt- und Trockenpräparaten. Fortschr. Med. 1884, 2:185-189.
45. Hasona A., Crowley P.J., Levesque C.M., Mair R.W., Cvitkovitch D.G., Bleiweis A.S., Brady L.J. Streptococcal viability and diminished stress tolerance in mutants lacking the signal recognition particle pathway or YidC2. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:17466-17471.
46. Henneke P., Dramsi S., Mancuso G., Chraibi K., Pellegrini E., Theilacker C., Hübner J., Santos-Sierra S., Teti G., Golenbock D.T., Poyart C., Trieu-Cuot P. Lipoproteins are critical TLR2 activating toxins in group B streptococcal sepsis. J. Immunol. 2008, 180:6149-6158.
47. Herbort M., Klein M., Manting E.H., Driessen A.J.M., Freudl R. Temporal expression of the Bacillus subtilis secA gene, encoding a central component of the preprotein translocase. J. Bacteriol. 1999, 181:493-500.
48. Hoffmann C., Leis A., Niederweis M., Plitzko J.M., Engelhardt H. Disclosure of the mycobacterial outer membrane: cryo-electron tomography and vitreous sections reveal the lipid bilayer structure. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:3963-3967.
49. Houben E.G., Bestebroer J., Ummels R., Wilson L., Piersma S.R., Jimenez C.R., Ottenhoff T.H.M., Luirink J., Bitter W. Composition of the type VII secretion system membrane complex. Mol. Microbiol. 2012, 86:472-484.
50. Hutchings M.I., Palmer T., Harrington D.J., Sutcliffe I.C. Lipoprotein biogenesis in Gram-positive bacteria: knowing when to hold 'em, knowing when to fold 'em. Trends Microbiol. 2009, 17:13-21.
51. Jack R.L., Sargent F., Berks B.C., Sawers G., Palmer T. Constitutive expression of Escherichia coli tat genes indicates an important role for the twin-arginine translocase during aerobic and anaerobic growth. J. Bacteriol. 2001, 183:1801-1804.
52. Jongbloed J.D.H., Martin U., Antelmann H., Hecker M., Tjalsma H., Venema G., Bron S., van Dijl J.M., Müller J. TatC is a specificity determinant for protein secretion via the twin-arginine translocation pathway. J. Biol. Chem. 2000, 275:41350-41357.
53. Kol S., Nouwen N., Driessen A.J.M. Mechanisms of YidC-mediated insertion and assembly of mulitmeric membrane protein complexes. J. Biol. Chem. 2008, 283:31269-31273.
54. Kudva R., Denks K., Kuhn P., Vogt A., Müller M., Koch H.-G. Protein translocation across the inner membrane of Gram-negative bacteria: the Sec- and Tat-dependent protein transport pathways. Res. Microbiol. 2013, 164. http://dx.doi.org/10.1016/j.resmic.2013.03.016.
55. Lausberg F., Fleckenstein S., Kreutzenbeck P., Fröbel J., Rose P., Müller M., Freudl R. Genetic evidence for a tight cooperation of TatB and TatC during productive recognition of twin-arginine (Tat) signal peptides in Escherichia coli. PLoS ONE 2012, 7:e39867.
56. Lenz L.L., Portnoy D.A. Identification of a second Listeria secA gene associated with protein secretion and the rough phenotype. Mol. Microbiol. 2002, 45:1043-1056.
57. Lenz L.L., Mohammadi S., Geissler A., Portnoy D.A. SecA2-dependent secretion of autolytic enzymes promotes Listeria monocytogenes pathogenesis. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:12432-12437.
58. Lüke I., Hanford J.I., Palmer T., Sargent F. Proteolytic processing of Escherichia coli twin-arginine signal peptides by LepB. Arch. Microbiol. 2009, 191:919-925.
59. Luthra A., Mahmood A., Arora A., Ramachandran R. Characterization of Rv3868, an essential hypothetical protein of the ESX-1 secretion system in Mycobacterium tuberculosis. J. Biol. Chem. 2008, 283:36532-36541.
60. Lyon W.R., Gibson C.M., Caparon M.G. A role for trigger factor and an Rgg-like regulator in the transcription, secretion and processing of the cysteine proteinase of Streptococcus pyogenes. EMBO J. 1998, 17:6263-6275.
61. Lycklama a Nijeholt J.A., Driessen A.J.M. The bacterial Sec-translocase: structure and mechanism. Phil. Trans. R. Soc. B 2012, 367:1016-1028.
62. Marchand C.H., Salmeron C., Raad R.B., Meniche X., Chami M., Masi M., Blanot D., Daffe M., Tropis M., Huc E., Le Marechal P., Decottignies P., Bayan N. Biochemical disclosure of the mycolate outer membrane of Corynebacterium glutamicum. J. Bacteriol. 2012, 194:587-597.
63. Mendel S., McCarthy A., Barnett J.P., Eijlander R.T., Nenninger A., Kuipers O.P., Robinson C. The Escherichia coli TatABC system and a Bacillus subtilis TatAC-type system recognise three distinct targeting determinants in twin-arginine signal peptides. J. Mol. Biol. 2008, 375:661-672.
64. Monteferrante C.G., Miethke M., van der Ploegh R., Glasner C., van Dijl J.M. Specific targeting of the metallophosphoesterase YkuE to the Bacillus cell wall requires the twin-arginine translocation system. J. Biol. Chem. 2012, 287:29789-29800.
65. Monteferrante C.G., Baglieri J., Robinson C., van Dijl J.M. TatAc, the third TatA subunit of Bacillus subtilis, can form active twin-arginine translocases with the TatCd and TatCy subunits. Appl. Environ. Microbiol. 2012, 78:4999-5001.
66. Mori H., Cline K. A twin arginine signal peptide and the pH gradient trigger reversible assembly of the thylakoid delta-pH/Tat translocase. J. Cell. Biol. 2002, 157:205-210.
67. Müller J., Walter F., van Dijl J.M., Behnke D. Suppression of the growth and export defects of an Escherichia coli secA(Ts) mutant by a gene cloned from Bacillus subtilis. Mol. Gen. Genet. 1992, 235:89-96.
68. Müller J.P., Ozegowski J., Vettermann S., Swaving J., van Wely K.H.M., Driessen A.J.M. Interaction of Bacillus subtilis CsaA with SecA and precursor proteins. Biochem. J. 2000, 348:367-373.
69. Nakayama H., Kurokawa K., Lee B.L. Lipoproteins in bacteria: structures and biosynthetic pathways. FEBS J. 2012, 279:4247-4268.
70. Nielsen H., Engelbrecht J., Brunak S., von Heijne G. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 1997, 10:1-6.
71. Nouaille S., Morello E., Cortez-Peres N., Le Loir Y., Commissaire J., Gratadoux J.J., Poumerol E., Gruss A., Langella P. Complementation of the Lactococcus lactis secretion machinery with Bacillus subtilis SecDF improves secretion of staphylococcal nuclease. Appl. Environ. Microbiol. 2006, 72:2272-2279.
72. Ollinger J., O'Malley T., Ahn J., Odingo J., Parish T. Inhibition of the sole type I signal peptidase in Mycobacterium tuberculosis is bactericidal under replicating and nonreplicating conditions. J. Bacteriol. 2012, 194:2614-2619.
73. Pallen M.J. The ESAT-6/WXG100 superfamily - and a new Gram-positive secretion system?. Trends Microbiol. 2002, 10:209-212.
74. Palmer T., Berks B.C. The twin-arginine translocation (Tat) protein export pathway. Nat. Rev. Microbiol. 2012, 10:483-496.
75. Rigel N.W., Braunstein M. A new twist on an old pathway - accessory secretion systems. Mol. Microbiol. 2008, 69:291-302.
76. Rigel N.W., Gibbons H.S., McCann J., McDonough J.A., Kurtz S., Braunstein M. The accessory SecA2 system of mycobacteria requires ATP binding and the canonical SecA1. J. Biol. Chem. 2009, 284:9927-9936.
77. Robinson C., Matos C.F.R.O., Beck D., Ren C., Lawrence J., Vasisht N., Mendel S. Transport and proofreading of proteins by the twin-arginine translocation (Tat) system in bacteria. Biochim. Biophys. Acta 2011, 1808:876-884.
78. Rusch S.L., Kendall D.A. Interactions that drive Sec-dependent bacterial protein transport. Biochemistry 2007, 46:9665-9673.
79. Saito A., Hizukuri Y., Matsuo E.-i., Chiba S., Mori H., Nishimura O., Ito K., Akiyama Y. Post-liberation cleavage of signal peptides is catalyzed by the site-2 protease (S2P) in bacteria. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:13740-13745.
80. Saraogi I., Shan S.-o. Molecular mechanism of co-translational protein targeting by the signal recognition particle. Traffic 2011, 12:535-542.
81. Sargent F., Bogsch E.G., Stanley N.R., Wexler M., Robinson C., Berks B.C., Palmer T. Overlapping functions of components of a bacterial Sec-independent protein export pathway. EMBO J. 1998, 17:3640-3650.
82. Schneewind O., Missiakas D.M. Protein secretion and surface display in Gram-positive bacteria. Phil. Trans. R. Soc. B 2012, 367:1123-1139.
83. Seepersaud R., Bensing B.A., Yen Y.T., Sullam P.M. Asp3 mediates multiple protein-protein interactions within the accessory Sec system of Streptococcus gordonii. Mol. Microbiol. 2010, 78:490-505.
84. Sibbald M.J.J.B., Ziebandt A.K., Engelmann S., Hecker M., de Jong A., Harmsen H.J.M., Raangs G.C., Stokroos I., Arends J.P., Dubois J.Y.F., van Dijl J.M. Mapping the pathways to staphylococcal pathogenesis by comparative secretomics. Microbiol. Mol. Biol. Rev. 2006, 70:755-788.
85. Siboo I., Chaffin D.O., Rubens C.E., Sullam P.M. Characterization of the accessory Sec system of Staphylococcus aureus. J. Bacteriol. 2008, 190:6188-6196.
86. Takamatsu D., Bensing B.A., Sullam P.M. Two additional components of the accessory Sec system mediating export of the Streptococcus gordonii platelet-binding protein GspB. J. Bacteriol. 2005, 187:3878-3883.
87. Tschumi A., Grau T., Albrecht D., Rezwan M., Antelmann H., Sander P. Functional analyses of mycobacterial lipoprotein diacylglyceryl transferase and comparative secretome analysis of a mycobacterial lgt mutant. J. Bacteriol. 2012, 194:3938-3949.
88. Tsukazaki T., Mori H., Echizen Y., Ishitani R., Fukai S., Tanaka T., Perederina A., Vassylyev D.G., Kohno T., Maturana A.D., Ito K., Nureki O. Structure and function of a membrane component SecDF that enhances protein export. Nature 2011, 474:235-238.
89. van der Ploeg R., Barnett J.P., Vasisht N., Goosens V.J., Pöther D.C., Robinson C., van Dijl J.M. Salt sensitivity of minimal twin arginine translocases. J. Biol. Chem. 2011, 286:43759-43770.
90. van Roosmalen M.L., Geukens N., Jongbloed J.D.H., Tjalsma H., Dubois J.-Y.F., Bron S., van Dijl J.M., Anné J. Type I signal peptidases of Gram-positive bacteria. Biochim. Biophys. Acta 2004, 1694:279-297.
91. van Stelten J., Silva F., Belin D., Silhavy T.J. Effects of antibiotics and a proto-oncogene homolog on destruction of protein translocator SecY. Science 2009, 325:753-756.
92. Vasil M.L., Tomaras A.P., Pritchard A.E. Identification and evaluation of twin-arginine translocase inhibitors. Antimicrob. Agents Chemother. 2012, 56:6223-6234.
93. von Heijne G. The structure of signal peptides from bacterial lipoproteins. Protein Eng. 1989, 2:531-534.
94. von Heijne G., Abrahmsén L. Species-specific variation in signal peptide design - implications for protein secretion in foreign hosts. FEBS Lett. 1989, 244:439-446.
95. Widdick D.A., Dilks K., Chandra G., Bottrill A., Naldrett M., Pohlschröder M., Palmer T. The twin-arginine translocation pathway is a major route of protein export in Streptomyces coelicolor. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:17927-17932.
96. Wu S.-C., Ye R., Wu X.-C., Ng S.-C., Wong S.-L. Enhanced secretory production of a single-chain antibody fragment from Bacillus subtilis by coproduction of molecular chaperones. J. Bacteriol. 1998, 180:2830-2835.
97. Yamazaki T., Yahagi S.-i., Nakamura K., Yamane K. Depletion of Bacillus subtilis histone-like protein, HBsu, causes defective protein translocation and induces upregulation of small cytoplasmic RNA. Biochem. Biophys. Res. Commun. 1999, 258:211-214.
98. Yen Y.T., Seepersaud R., Bensing B.A., Sullam P.M. Asp2 and Asp3 interact directly with GspB, the export substrate of the Streptococcus gordonii accessory Sec system. J. Bacteriol. 2011, 193:3165-3174.
99. Yuan J., Zweers J.C., van Dijl J.M., Dalbey R.E. Protein transport across and into cell membranes in bacteria and archaea. Cell. Mol. Life Sci. 2010, 67:179-199.
100. Zuber B., Chami M., Houssin C., Dubochet J., Griffiths G., Daffe M. Direct visualization of the outer membrane of mycobacteria and corynebacteria in their native state. J. Bacteriol. 2008, 190:5672-5680.