Abstract
Bacteria use an impressive arsenal of secretion systems (1-7) to infect their host cells by exporting proteins, DNA and DNA-protein complexes via cell membranes. They use chaperone-usher pathways for host colonization as well. To be targeted for transportation across one (Gram-positive) or two membranes (Gram-negative), clients must be selected, guided and unfolded to pass through type 3 (T3SS) or type 4 (T4SS) secretion systems. For these processes, bacteria count on secretory chaperones that guide macromolecular transport via membranes. Moreover, if we know how these processes occur, we might be able to stop them and avoid bacterial infections. Thus, structural and functional characterizations of secretory chaperones become interesting, as these proteins are the perfect targets for blocking bacteria action. Therefore, this review focuses on a story of known mechanisms of chaperone- secretion assisted transport with special attention on virulence proteins and DNA transport in bacteria.
Keywords: Bacteria, secretion systems, secretory chaperones, chaperone-assisted secretion, protein, secretion.
Graphical Abstract
[1]
Francis, M.S. In: Handbook of molecular chaperones: Roles, structures and mechanisms; Durante, P.; Colucci, L., Eds.; Nova Biomedical Books: New York, 2010, pp. 79-147.
[2]
Wattiau, P.; Woestyn, S.; Cornelis, G.R. Customized secretion chaperones in pathogenic bacteria. Mol. Microbiol., 1996, 20, 255-262.
[3]
Fattori, J.; Prando, A.; Martini, A.M.; Rodrigues, F.H.S.; Tasic, L. Bacterial secretion chaperones. Protein Pept. Lett., 2011, 18, 158-166.
[4]
Sayer, J.R.; Walldén, K.; Pesnot, T.; Campbell, F.; Gane, P.J.; Simone, M.; Koss, H.; Buelens, F.; Boyle, T.P.; Selwood, D.L.; Waksman, G.; Tabor, A.B. 2-and 3-substituted imidazo [1,2-α]pyrazines as inhibitors of bacterial type IV secretion. Bioorgan. Med. Chem., 2014, 22, 6459-6470.
[5]
Schneewin, O.; Missiakas, D.M. Protein secretion and surface display in Gram-positive bacteria. Phil. Trans. R. Soc., 2012, 367, 1123-1139.
[6]
Papanikou, E.; Karamanou, S.; Economou, A. Bacterial protein secretion through the translocase nanomachine. Nat. Rev. Microbiol., 2007, 5, 839-851.
[7]
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.
[8]
Natale, P.; Brüser, T.; Driessen, A.J.M. Sec- and Tat- mediated protein secretion across the bacterial cytoplasmic membrane distinct translocases and mechanisms. Biochim. Biophys. Acta, 2008, 1778, 1735-1756.
[10]
Tsirigotaki, A.; De Geyter, J.; Šoštaric, N.; Economou, A.; Karamanou, S. Protein export through the bacterial Sec pathway. Nat. Rev. Microbiol., 2017, 15, 21-36.
[11]
Lee, P.A.; Tullman-Ercek, D.; Georgiou, G. The bacterial twin-arginine translocation pathway. Annu. Rev. Microbiol., 2006, 60, 373-395.
[12]
Sargent, F.; Berks, B.C.; Palmer, T. Pathfinders and trailblazers: A prokaryotic targeting system for transport of folded proteins. FEMS Microbiol. Lett., 2006, 254, 198-207.
[13]
Palmer, T.; Berks, B.C. The twin-arginine translocation (Tat) protein export pathway. Nat. Rev. Microbiol., 2012, 10, 483-496.
[14]
Costa, T.R.D.; Felisberto-Rodrigues, C.; Meir, A.; Prevost, M.S.; Redzej, A.; Trokter, M.; Waksman, G. Secretion systems in Gram-negative bacteria: Structural and mechanistic insights. Nat. Rev. Microbiol., 2015, 13, 343-359.
[15]
Holland, I.B.; Schmitt, L.; Young, J. Type 1 protein secretion in bacteria, the ABC-transporter dependent pathway. Mol. Membr. Biol., 2005, 22, 29-39.
[16]
Herr, D.; Finley, K.D. In: Autophagy in health and disease; Gottlieb, R.A., Ed.; Elsevier: London, 2013, pp. 11-28.
[17]
Thomas, S.; Holland, I.B.; Schmitt, L. The type 1 secretion pathway - the hemolysin system and beyond. Biochim. Biophys. Acta, 2014, 1843, 1629-1641.
[18]
Chang, J.H.; Desveaux, D.; Creason, A.L. The ABCs and 123s of bacterial secretion systems in plant pathogenesis. Annu. Rev. Phytopathol., 2014, 52, 317-345.
[19]
Xu, L.; Liu, Y. Protein secretion systems in bacterial pathogens. Front. Biol., 2014, 9, 437-447.
[20]
Schwarz, C.K.W.; Landsberg, C.D.; Lenders, M.H.H.; Smits, S.H.J.; Schmit, L. Using an E. coli type 1 secretion system to secrete the mammalian, intracellular protein IFABP in its active form. J. Biotechnol., 2012, 159, 155-161.
[21]
Dalbey, R.E.; Kuhn, A. Protein traffic in gram-negative bacteria – How exported and secreted proteins find their way. FEMS Microbiol. Rev., 2012, 36, 1023-1045.
[22]
Kanonenberg, K.; Schwarz, C.K.W.; Schmitt, L. Type I secretion systems - a story of appendices. Res. Microbiol., 2013, 164, 596-604.
[23]
Masi, M.; Wandersman, C. Multiple signals direct the assembly and function of a type 1 secretion system. J. Bacteriol., 2010, 192, 3861-3869.
[24]
Satchell, K.J.F. MARTX, multifunctional autoprocessing repeats-in-toxin toxins. Infect. Immun., 2007, 75, 5079-5084.
[25]
Johnson, T.L.; Abendroth, J.; Hol, W.G.J.; Sandkvist, M. Type II secretion: From structure to function. FEMS Microbiol. Lett., 2006, 255, 175-186.
[26]
Korotkov, K.V.; Sandkvist, M.; Hol, W.G.J. The type II secretion system: Biogenesis, molecular architecture and mechanism. Nat. Rev. Microbiol., 2012, 10, 336-351.
[27]
Weber, B.S.; Kinsella, R.L.; Harding, C.M.; Feldman, M.F. The secrets of Acinetobacter secretion. Trends Microbiol., 2017, 25, 532-545.
[28]
Galán, E.J.; Lara-Tejero, M.; Marlovits, T.C.; Wagner, S. Bacterial type III secretion systems: Specialized nanomachines for protein delivery into target cells. Annu. Rev. Microbiol., 2014, 68, 348-415.
[29]
Büttner, D. Protein export according to schedule: Architecture, assembly, and regulation of type III secretion systems from plant- and animal-pathogenic bacteria. Microbiol. Mol. Biol. R., 2012, 76, 262-310.
[30]
Singer, A.U.; Rohde, J.R.; Lam, R.; Skarina, T.; Kagan, O.; Di Leo, R.; Chirgadze, N.Y.; Cuff, M.E.; Joachimiak, A.; Tyers, M.; Sansonetti, P.J.; Parsot, C.; Savchenko, A. Structure of the Shigella T3SS effector IpaH defines a new class of E3 ubiquitin ligases. Nat. Struct. Mol. Biol., 2008, 15, 1293-1301.
[31]
Job, V.; Matteï, P.J.; Lemaire, D.; Attree, I.; Dessen, A. Structural basis of chaperone recognition of type III secretion system minor translocator proteins. J. Biol. Chem., 2010, 285, 23224-23232.
[32]
Radics, J.; Königsmaier, L.; Marlovits, T.C. Structure of a pathogenic type III secretion system in action. Nat. Struct. Mol. Biol., 2014, 21, 82-87.
[33]
Martinez-Argudo, I.; Blocker, A.J. The Shigella T3SS needle transmits a signal for MxiC release, which controls secretion of effectors. Mol. Microbiol., 2010, 78, 1365-1378.
[34]
Fronzes, R.; Christie, P.J.; Waksman, G. The structural biology of type IV secretion systems. Nat. Rev. Microbiol., 2009, 7, 703-714.
[35]
Goessweiner-Mohr, N.; Arends, K.; Keller, W.; Grohmann, E. Conjugative Type 4 secretion system in gram-positive bacteria. Plasmid, 2013, 70, 289-302.
[36]
Segura, R.L.; Águila-Arcos, S.; Ugarte-Uribe, B.; Vecino, A.J.; de la Cruz, F.; Goñi, F.M.; Alkort, I. The transmembrane domain of the T4SS coupling protein TrwB and its role in protein-protein interactions. Biochim. Biophys. Acta, 2013, 1828, 2015-2025.
[37]
Bhatty, M.; Gomez, J.A.L.; Christie, P.J. The expanding bacterial type IV secretion lexicon. Res. Microbiol., 2013, 164, 620-639.
[38]
Delpino, M.V.; Comerci, D.J.; Wagner, M.A.; Eschenbrenner, M.; Mujer, C.V.; Ugalde, R.A.; Fossati, C.A.; Baldi, P.C.; Del Vecchio, V.G. Differential composition of culture supernatants from wild-type Brucella abortus and its isogenic virB mutants. Arch. Microbiol., 2009, 191, 571-581.
[39]
Zechner, E.L.; Lang, S.; Schildbach, J.F. Assembly and mechanisms of bacterial type IV secretion machines. Phil. Trans. R. Soc.B., 2012, 367, 1073-1087.
[40]
Cascales, E.; Chistie, P.J. The versatile bacterial type IV secretion systems. Nat. Rev. Microbiol., 2003, 1, 137-149.
[41]
Paredes-Cervantes, V.; Flores-Mejía, R.; Moreno-Lafont, M.C.; Lanz-Mendoza, H.; Tello-López, A.T.; Castillo-Vera, J.; Pando-Robles, V.; Hurtado-Sil, G.; González-González, E.; Rodríguez-Cortés, O.; Gutiérrez-Hoya, A.; Vega-Ramírez, M.T.; López-Santiago, R. Comparative proteome analysis of Brucella abortus 2308 and its virB type IV secretion system mutant reveals new T4SS-related candidate proteins. J. Proteomics, 2011, 74, 2959-2971.
[42]
Trokter, M.; Felisberto-Rodrigues, C.; Christie, P.J.; Waksman, G. Recent advances in the structural and molecular biology of type IV secretion system. Curr. Opin. Struct. Biol., 2014, 27, 16-23.
[43]
Tsai, Y-L.; Chiang, Y.R.; Narberhaus, F.; Baron, C.; Lai, E.M. The small heat-shock protein HspL is a VirB8 chaperone promoting type IV secretion-mediated DNA transfer. J. Biol. Chem., 2010, 285, 19757-19766.
[44]
Alvarez-Martinez, C.E.; Christie, P.J. Biological diversity of prokaryotic type IV secretion systems. Microbiol. Mol. Biol. R., 2009, 73, 775-808.
[45]
Guglielmini, J.; Néron, B.; Abby, S.S.; Garcillán-Barcia, M.P.; de la Cruz, F.; Rocha, E.P.C. Key components of the eight classes of type IV secretion systems involved in bacterial conjugation or protein secretion. Nucleic Acid Res., 2014, 42, 5715-5727.
[46]
Waksman, G.; Orlova, E.V. Structural organization of the type IV secretion systems. Curr. Opin. Microbiol., 2014, 17, 24-31.
[47]
Johnson, C.M.; Grossman, A.D. Integrative and conjugative elements (ICEs): What they do and how they work. Annu. Rev. Genet., 2015, 49, 577-601.
[48]
Li, M.; Shen, X.; Yan, J.; Han, H.; Zheng, B.; Liu, D.; Cheng, H.; Zhao, Y.; Rao, X.; Wang, C.; Tang, J.; Hu, F.; Gao, G.F. GI-type T4SS-mediated horizontal transfer of the 89K pathogenicity island in epidemic Streptococcus suis serotype 2mmi_7553. Mol. Microbiol., 2011, 79, 1670-1683.
[49]
Monzingo, A.F.; Ozburn, A.; Xia, S.; Meyer, R.J.; Robertus, J.D. The structure of the minimal relaxase domain of MobA at 2.1 Å resolution. J. Mol. Biol., 2007, 366, 165-178.
[50]
Chandran, V.; Fronzes, R.; Duquerroy, S.; Cronin, N.; Navaza, J.; Waksman, G. Structure of the outer membrane complex of a type IV secretion system. Nature, 2009, 462, 1011-1016.
[51]
Christie, P.J.; Atamakuri, K.; Kushmamoorthy, V.; Jakubowski, S.; Cascales, E. Biogenesis, architecture, and function of bacterial type IV secretion system. Annu. Rev. Microbiol., 2005, 59, 451-485.
[52]
Locht, C.; Coutte, L.; Mielcarek, N. The ins and outs of pertussis toxin. FEBS J., 2011, 278, 4668-4682.
[53]
Stingl, K.; Müller, S.; Scheidgen-Kleyboldt, G.; Clausen, M.; Maier, B. Composite system mediates two-step DNA uptake into Helicobacter pylori. PNAS, 2010, 107, 1184-1189.
[54]
Karnholz, A.; Hoefler, C.; Odenbreit, S.; Fischer, W.; Hofreuter, D.; Haas, R. Functional and topological characterization of novel components of the ComB DNA transformation competence system in Helicobacter pylori. J. Bacteriol., 2006, 188, 882-893.
[55]
Pattis, I.; Weiss, E.; Laugks, R.; Haas, R.; Fischer, W. The Helicobacter pylori CagF protein is a type IV secretion chaperone-like molecule that binds close to the C-terminal secretion signal of the CagA effector protein. Microbiology, 2007, 153, 2896-2909.
[56]
Juhas, M.; Crook, D.W.; Hood, D.W. Type IV secretion systems: Tools of bacterial horizontal gene transfer and virulence. Cell. Microbiol., 2008, 12, 2377-2386.
[57]
Bandyopadhyay, P.; Liu, S.; Gabbai, C.B.; Venitelli, Z.; Steinman, H.M. Environmental mimics and the Lvh type IVA secretion system contribute to virulence-related phenotypes of Legionella pneumophila. Infect. Immun., 2007, 75, 723-735.
[58]
Raychaudhury, S.; Farelli, J.D.; Montminy, T.P.; Matthews, M.; Ménétret, J-F.; Duménil, G.; Roy, C.R.; Head, J.F.; Isberg, R.R.; Akey, C.W. Structure and function of interacting IcmR-IcmQ domains from a type IVB secretion system in Legionella pneumophila. Structure, 2009, 17, 590-601.
[59]
Leo, J.C.; Grin, I.; Linke, D. Type V secretion: Mechanism(s) of autotransport through the bacterial outer membrane. Phil. Trans. R. Soc.B, 2012, 367, 1088-1101.
[60]
Dautin, N.; Bernstein, H.D. Protein secretion in gram-negative bacteria via the autotransporter pathway. Annu. Rev. Microbiol., 2007, 61, 89-112.
[61]
Leyton, D.L.; Rossiter, A.E.; Henderson, I.R. From self-sufficiency to dependence: Mechanisms and factors important for autotransporter biogenesis. Nat. Rev. Microbiol., 2012, 10, 213-225.
[62]
Cianfanelli, F.R.; Monlezun, L.; Coulthurst, S.J. Aim, load, fire: The type VI secretion system, a bacterial nanoweapon. Trends Microbiol., 2016, 24, 51-62.
[63]
Pukatzki, S.; Ma, A.T.; Revel, A.T.; Sturtevant, D.; Mekalanos, J.J. Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. PNAS, 2007, 104, 15508-15513.
[64]
Jani, A.J.; Cotte, P.A. Type VI secretion: Not just for pathogenesis anymore. Cell Host Microbe, 2010, 8, 2-6.
[65]
Hood, R.D. Singh, P.; Hsu, F.; Güvener, T.; Carl, M.A.; Trinidad, R.R.S.; Silverman, J.M.; Ohlson, B.B.; Hicks, K.G.; Plemel, R.L.; Li, M.; Schwarz, S.; Wang, W.Y.; Merz, A.J.; Goodlett, D.R.; Mougous, J.D. A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe, 2010, 7, 25-37.
[66]
MacIntyre, D.L.; Miyata, S.T.; Kitaoka, M.; Pukatzki, S. The Vibrio cholerae type VI secretion system displays antimicrobial properties. PNAS, 2010, 107, 19520-19524.
[67]
Silverman, J.M.; Agnello, D.M.; Zheng, H.; Andrews, B.T.; Li, M.; Catalano, C.E.; Gonen, T.; Mougous, J.D. Haemolysin coregulated protein is an exported receptor and chaperone of type VI secretion substrates. Mol. Cell, 2013, 51, 584-593.
[68]
Unterweger, D.; Kostiuk, B.; Pukatzki, S. Adaptor proteins of type VI secretion system effectors. Trends Microbiol., 2017, 25, 8-10.
[69]
Ma, J.; Sum, M.; Dong, W.; Pan, Z.; Lu, C.; Yao, H. PAAR-Rhs proteins harbor various C-terminal toxins to diversify the antibacterial pathways of type VI secretion systems. Environ. Microbiol., 2017, 19, 345-360.
[70]
Abdallah, A.M.; van Pittius, N.C.G.; Champion, P.A.D.; 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.
[71]
Bottai, D.; Serafini, A.; Cascioferro, A.; Brosch, R.; Manganelli, R. Targeting type VII/ESX secretion systems for development of novel antimycobacterial drugs. Curr. Pharm. Des., 2014, 20, 4346-4356.
[72]
Daleke, M.H.; van der Woude, A.D.; Parret, A.H.A.; Ummels, R.; de Groot, A.M.; Watson, D.; Piersma, S.R.; Jiménez, C.R.; Luirink, J.; Bitter, W.; Houben, E.N.G. Specific chaperones for the type VII protein secretion pathway. J. Biol. Chem., 2012, 287, 31939-31947.
[73]
Schmid, A.; Dittmann, S.; Grimminger, V.; Walter, S.; Heesemann, J.; Wilharm, G. Yersinia enterocolitica type III secretion chaperone SycD: Recombinant expression, purifcation and characterization of a homodimer. Protein Expres. Purif., 2006, 49, 176-182.
[74]
Lohou, D.; Lonjon, F.; Genin, S.; Vailleau, F. Type III chaperones and co in bacterial plant pathogens: A set of specialized bodyguards mediating effector delivery. Front. Plant Sci., 2013, 4, 1-8.
[75]
Triplett, L.R.; Wedemeyer, W.J.; Sundin, G.W. Homology-based modeling of the Erwinia amylovora type III secretion chaperone DspF used to identify amino acids required for virulence and interaction with the effector DspE. Res. Microbiol., 2010, 161, 613-618.
[76]
Brinkworth, A.J.; Malcolm, D.S.; Pedrosa, A.T.; Roguska, K.; Shahbazian, S.; Graham, J.E.; Hayward, R.D.; Carabeo, R.A. Chlamydia trachomatis Slc1 is a type III secretion chaperone that enhances the translocation of its invasion effector substrate TARPm. Mol. Microbiol., 2011, 82, 131-144.
[77]
Parsot, C.; Hamiaux, C.; Page, A.L. The various and varying roles of specific chaperones in type III secretion systems. Curr. Opin. Microbiol., 2003, 6, 7-14.
[78]
Zheng, Z.; Chen, G.; Joshi, S.; Brutinel, E.D.; Yahr, T.L.; Chen, L. Biochemical characterization of a regulatory cascade controlling transcription of the Pseudomonas aeruginosa type III secretion system. J. Biol. Chem., 2007, 282, 6136-6142.
[79]
Miki, T.; Shibagaki, Y.; Danbara, H.; Okada, N. Functional characterization of SsaE, a novel chaperone protein of the type III secretion system encoded by Salmonella pathogenicity island 2. J. Bacteriol., 2009, 191, 6843-6854.
[80]
Roblin, P.; Lebrun, P.; Rucktooa, P.; Dewitte, F.; Lens, Z.; Receveur-Brechot, V.; Bompard, C. The structural organization of the N-terminus domain of SopB, a virulence factor of Salmonella, depends on the nature of its protein partners. Biochim. Biophys. Acta, 2013, 1834, 2564-2572.
[81]
Tsai, C-L.; Burkinshaw, B.J.; Strynadka, N.C.J.; Tainer, J.A. The Salmonella type III secretion system virulence effector forms a new hexameric chaperone assembly for export of effector/chaperone complexes. J. Bacteriol., 2015, 197, 672-675.
[82]
Bröms, J.E.; Edqvist, P.J.; Forsberg, A.; Francis, M.S. Tetratricopeptide repeats are essential for PcrH chaperone function in Pseudomonas aeruginosa type III secretion. FEMS Microbiol. Lett., 2006, 256, 57-66.
[83]
Büttner, C.; Sorg, I.; Cornelis, G.; Heinz, D.; Niemann, H. Structure of the Yersinia enterocolitica type III secretion translocator chaperone SycD. J. Mol. Biol., 2008, 375, 997-1012.
[84]
Lunelli, M.; Lokareddy, R.; Zychlinsky, A.; Kolbe, M. IpaB-IpgC interaction defines binding motif for type III secretion translocator. Proc. Natl. Acad. Sci. USA, 2009, 106, 9661-9666.
[85]
Auvray, F.; Thomas, J.; Fraser, G.M.; Hughes, C. Flagellin polymerization control by a cytosolic export chaperone. J. Mol. Biol., 2001, 308, 221-229.
[86]
Lam, W.W.L.; Woo, E.J.; Kotaka, M.; Tam, W.K.; Leung, Y.C.; Ling, T.K.W.; Au, S.W.N. Molecular interaction of flagellar export chaperone FliS and co-chaperone HP1076 in Helicobacter pylori. FASEB J., 2010, 24, 4020-4032.
[87]
Evdokimov, A.G.; Phan, J.; Tropea, J.E.; Routzahn, K.M.; Peters, H.K.; Pokross, M.; Waugh, D.S. Similar modes of polypeptide recognition by export chaperones in flagellar biosynthesis and type III secretion. Nat. Struct. Biol., 2003, 10, 789-793.
[88]
Bennett, J.C.Q.; Thomas, J.; Fraser, G.M.; Hughes, C. Substrate complexes and domain organization of the Salmonella flagellar export chaperones FlgN and FliT. Mol. Microbiol., 2001, 39, 781-791.
[89]
Fattori, J.; Prando, A.; Assis, L.H.P.; Aparicio, R.; Tasic, L. Structural insights on two hypothetical secretion chaperones from Xanthomonas axonopodis pv. citri. Protein J., 2011, 30, 324-333.
[90]
Lynne, S. Cairns, L.S.; Marlow, V.L.; Kiley, T.B.; Birchall, C.; Ostrowski, A.; Aldridge, P.D.; Stanley-Wall, N.R. FlgN is required for flagellum-based motility by Bacillus subtilis. J. Bacteriol., 2014, 196, 2216-2226.
[91]
Remaut, H.; Waksman, G. Structural biology of bacterial pathogenesis. Curr. Opin. Struct. Biol., 2004, 14, 161-170.
[92]
Karuppiah, V.; Berry, J-L.; Derrick, J.P. Outer membrane translocons: Structural insights into channel formation. Trends Microbiol., 2011, 19, 40-48.
[93]
Whitfield, C.; Naismith, J.H. Periplasmic export machines for outer membrane assembly. Curr. Opin. Struct. Biol., 2008, 18, 466-474.
[94]
Cambronne, E.D.; Roy, C.R. Recognition and delivery of effector into eukaryotic cells by bacterial secretion systems. Traffic, 2006, 7, 929-939.
[95]
Filloux, A. Secretion signal and protein targeting in bacteria: A biological puzzle. J. Bacteriol., 2010, 192, 3847-3849.
[96]
Bardill, J.P.; Miller, J.L.; Vogel, J.P. IcmS-dependent translocation of SdeA into macrophages by the Legionella pneumophila type IV secretion system. Mol. Microbiol., 2005, 56, 90-103.
[97]
Geibel, S.; Waksman, G. The molecular dissection of the chaperone-usher pathway. Biochim. Biophys. Acta, 2014, 1843, 1559-1567.
[98]
Alperi, A.; Larrea, D.; Fernández-González, E.; Dehio, C.; Zechner, E.L.; Llosa, M. A translocation motif in relaxase TrwC specifically affects recruitment by its conjugative type IV secretion system. J. Bacteriol., 2013, 195, 4999-5006.
[99]
van Kregten, M.; Lindhout, B.I.; Hooykaas, P.J.J. van der Zaal. B.J. Agrobacterium-mediated T-DNA transfer and integration by minimal VirD2 consisting of the relaxase domain and a type IV secretion system translocation signal. Mol. Plant Microbe In., 2009, 22, 1356-1365.
[100]
Fattori, J. Structural insights on hypothetical proteins, secretion
chaperones from Xanthomonas axonopodis pv. citri. University of
Campinas: Campinas, September, 2011.
[101]
Prando, A. Biophysical studies on secretion chaperones and protein- ligand interaction. University of Campinas: Campinas, April. 2012.
[102]
Peterson, J.W. In: Medical microbiology;, Baron, S. Ed.; University
of Texas medical branch at Galveston: Galveston, 1996; pp. 1-32.
[103]
Beceiro, A.; Tomás, M.; Bou, G. Antimicrobial resistance and virulence: A successful or deleterious association in the bacterial world? Clin. Microbiol. Rev., 2013, 26, 185-230.
[104]
Casadevall, A.; Pirofski, L. Host-pathogen interactions: The attributes of virulence. J. Infect. Dis., 2001, 184, 337-344.
[105]
Carroll, K.C. In: Jawetz, Melnick, & Adelberg's Medical Microbiology;, Brooks, G.F.; Carroll, K.C.; Butel, J.S.; Morse, S.A.; Mietzner,
T.A. Eds.; The McGraw-Hill companies: New York, 2013
,
pp. 149-161.
[106]
Sharma, A.K.; Dhasmana, N.; Dubey, N.; Kumar, N.; Gangwal, A.; Gupta, M.; Singh, Y. Bacterial virulence factors: Secreted for survival. Indian J. Microbiol., 2016, 57, 1-10.
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