Take five - Type VII secretion systems of Mycobacteria

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1843, Issue 8, 2014, Pages 1707-1716

  Houben, Edith N G ^a,b   Korotkov, Konstantin V ^c   Bitter, Wilbert ^a,b  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Chaperone; Mycobacterium; Protease; Protein secretion; Secretion signal

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BACTERIAL PROTEIN; CHAPERONE;

ARTICLE; BACTERIAL GENE; BACTERIAL MEMBRANE; BACTERIAL OUTER MEMBRANE; BACTERIAL SECRETION SYSTEM; CELLULAR DISTRIBUTION; CORYNEBACTERIUM; ENZYME SPECIFICITY; GENE CLUSTER; GENE LOCUS; MYCOBACTERIUM; MYCOBACTERIUM BOVIS BCG; MYCOBACTERIUM LEPRAE; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; STRUCTURE ANALYSIS; TYPE VII SECRETION SYSTEM;

CHAPERONE; MYCOBACTERIUM; PROTEASE; PROTEIN SECRETION; SECRETION SIGNAL;

BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; CELL WALL; HUMANS; MOLECULAR CHAPERONES; MYCOBACTERIUM TUBERCULOSIS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; TUBERCULOSIS;

EID: 84902248633     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.11.003     Document Type: Article

References (91)

1. Goodfellow M., Jones A.L. Order Corynebacteriales ord. nov. Bergey's Manual of Systematic Bacteriology 2012, vol. 5:235-243. Springer Verlag, New York.
2. 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.
3. 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.
4. Faller M., Niederweis M., Schulz G.E. The structure of a mycobacterial outer-membrane channel. Science 2004, 303:1189-1192.
5. Marchand C.H., Salmeron C., Bou Raad R., 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.
6. Stanley S.A., Raghavan S., Hwang W.W., Cox J.S. Acute infection and macrophage subversion by Mycobacterium tuberculosis require a specialized secretion system. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:13001-13006.
7. Pym A.S., Brodin P., Brosch R., Huerre M., Cole S.T. Loss of RD1 contributed to the attenuation of the live tuberculosis vaccines Mycobacterium bovis BCG and Mycobacterium microti. Mol. Microbiol. 2002, 46:709-717.
8. Lewis K.N., Liao R., Guinn K.M., Hickey M.J., Smith S., Behr M.A., Sherman D.R. Deletion of RD1 from Mycobacterium tuberculosis mimics bacille Calmette-Guerin attenuation. J. Infect. Dis. 2003, 187:117-123.
9. Simeone R., Bottai D., Brosch R. ESX/type VII secretion systems and their role in host-pathogen interaction. Curr. Opin. Microbiol. 2009, 12:4-10.
10. Stoop E.J., Bitter W., van der Sar A.M. Tubercle bacilli rely on a type VII army for pathogenicity. Trends Microbiol. 2012, 20:477-484.
11. Gey Van Pittius N.C., Gamieldien J., Hide W., Brown G.D., Siezen R.J., Beyers A.D. The ESAT-6 gene cluster of Mycobacterium tuberculosis and other high G+C Gram-positive bacteria. Genome Biol. 2001, 2. (RESEARCH0044).
12. 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., Gey van Pittius N.C., 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.
13. Brown G.D., Dave J.A., Gey van Pittius N.C., Stevens L., Ehlers M.R., Beyers A.D. The mycosins of Mycobacterium tuberculosis H37Rv: a family of subtilisin-like serine proteases. Gene 2000, 254:147-155.
14. Sampson S.L. Mycobacterial PE/PPE proteins at the host-pathogen interface. Clin. Dev. Immunol. 2011, 2011:497203.
15. George K.M., Chatterjee D., Gunawardana G., Welty D., Hayman J., Lee R., Small P.L. Mycolactone: a polyketide toxin from Mycobacterium ulcerans required for virulence. Science 1999, 283:854-857.
16. Abdallah A.M., Verboom T., Hannes F., Safi M., Strong M., Eisenberg D., Musters R.J., Vandenbroucke-Grauls C.M., Appelmelk B.J., Luirink J., Bitter W. A specific secretion system mediates PPE41 transport in pathogenic mycobacteria. Mol. Microbiol. 2006, 62:667-679.
17. Siegrist M.S., Unnikrishnan M., McConnell M.J., Borowsky M., Cheng T.Y., Siddiqi N., Fortune S.M., Moody D.B., Rubin E.J. Mycobacterial ESX-3 is required for mycobactin-mediated iron acquisition. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:18792-18797.
18. Sorensen A.L., Nagai S., Houen G., Andersen P., Andersen A.B. Purification and characterization of a low-molecular-mass T-cell antigen secreted by Mycobacterium tuberculosis. Infect. Immun. 1995, 63:1710-1717.
19. Pallen M.J. The ESAT-6/WXG100 superfamily - and a new Gram-positive secretion system?. Trends Microbiol. 2002, 10:209-212.
20. Renshaw P.S., Lightbody K.L., Veverka V., Muskett F.W., Kelly G., Frenkiel T.A., Gordon S.V., Hewinson R.G., Burke B., Norman J., Williamson R.A., Carr M.D. Structure and function of the complex formed by the tuberculosis virulence factors CFP-10 and ESAT-6. EMBO J. 2005, 24:2491-2498.
21. Abdallah A.M., Verboom T., Weerdenburg E.M., Gey van Pittius N.C., 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.
22. Ilghari D., Lightbody K.L., Veverka V., Waters L.C., Muskett F.W., Renshaw P.S., Carr M.D. Solution structure of the Mycobacterium tuberculosis EsxG.EsxH complex: functional implications and comparisons with other M. tuberculosis Esx family complexes. J. Biol. Chem. 2011, 286:29993-30002.
23. Sundaramoorthy R., Fyfe P.K., Hunter W.N. Structure of Staphylococcus aureus EsxA suggests a contribution to virulence by action as a transport chaperone and/or adaptor protein. J. Mol. Biol. 2008, 383:603-614.
24. Carlsson F., Joshi S.A., Rangell L., Brown E.J. Polar localization of virulence-related ESX-1 secretion in mycobacteria. PLoS Pathog. 2009, 5:e1000285.
25. Champion P.A., Champion M.M., Manzanillo P., Cox J.S. ESX-1 secreted virulence factors are recognized by multiple cytosolic AAA ATPases in pathogenic mycobacteria. Mol. Microbiol. 2009, 73:950-962.
26. McLaughlin B., Chon J.S., MacGurn J.A., Carlsson F., Cheng T.L., Cox J.S., Brown E.J. A mycobacterium ESX-1-secreted virulence factor with unique requirements for export. PLoS Pathog. 2007, 3:e105.
27. Daleke M.H., Cascioferro A., de Punder K., Ummels R., Abdallah A.M., van der Wel N., Peters P.J., Luirink J., Manganelli R., Bitter W. Conserved Pro-Glu (PE) and Pro-Pro-Glu (PPE) protein domains target LipY lipases of pathogenic mycobacteria to the cell surface via the ESX-5 pathway. J. Biol. Chem. 2011, 286:19024-19034.
28. Strong M., Sawaya M.R., Wang S., Phillips M., Cascio D., Eisenberg D. Toward the structural genomics of complexes: crystal structure of a PE/PPE protein complex from Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:8060-8065.
29. Daleke M.H., Ummels R., Bawono P., Heringa J., Vandenbroucke-Grauls C.M., 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.
30. Cole S.T., Brosch R., Parkhill J., Garnier T., Churcher C., Harris D., Gordon S.V., Eiglmeier K., Gas S., Barry C.E., Tekaia F., Badcock K., Basham D., Brown D., Chillingworth T., Connor R., Davies R., Devlin K., Feltwell T., Gentles S., Hamlin N., Holroyd S., Hornsby T., Jagels K., Krogh A., McLean J., Moule S., Murphy L., Oliver K., Osborne J., Quail M.A., Rajandream M.A., Rogers J., Rutter S., Seeger K., Skelton J., Squares R., Squares S., Sulston J.E., Taylor K., Whitehead S., Barrell B.G. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 1998, 393:537-544.
31. van der Woude A.D., Mahendran K.R., Ummels R., Piersma S.R., Pham T.V., Jimenez C.R., de Punder K., van der Wel N.N., Winterhalter M., Luirink J., Bitter W., Houben E.N.G. Differential detergent extraction of Mycobacterium marinum cell envelope proteins identifies an extensively modified threonine-rich outer membrane protein with channel activity. J. Bacteriol. 2013, 195:2050-2059.
32. Sani M., Houben E.N.G., Geurtsen J., Pierson J., de Punder K., van Zon M., Wever B., Piersma S.R., Jiménez C.R., Daffé M., Appelmelk B.J., Bitter W., van der Wel N., Peters P.J. Direct visualization by cryo-EM of the mycobacterial capsular layer: a labile structure containing ESX-1-secreted proteins. PLoS Pathog. 2010, 6:e1000794.
33. Chen J.M., Zhang M., Rybniker J., Basterra L., Dhar N., Tischler A.D., Pojer F., Cole S.T. Phenotypic profiling of Mycobacterium tuberculosis EspA point-mutants reveals blockage of ESAT-6 and CFP-10 secretion in vitro does not always correlate with attenuation of virulence. J. Bacteriol. 2013, 195(24):5421-5430.
34. 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.
35. Serafini A., Boldrin F., Palu G., Manganelli R. Characterization of a Mycobacterium tuberculosis ESX-3 conditional mutant: essentiality and rescue by iron and zinc. J. Bacteriol. 2009, 191:6340-6344.
36. Raman S., Puyang X., Cheng T.Y., Young D.C., Moody D.B., Husson R.N. Mycobacterium tuberculosis SigM positively regulates Esx secreted protein and nonribosomal peptide synthetase genes and down regulates virulence-associated surface lipid synthesis. J. Bacteriol. 2006, 188:8460-8468.
37. Agarwal N., Woolwine S.C., Tyagi S., Bishai W.R. Characterization of the Mycobacterium tuberculosis sigma factor SigM by assessment of virulence and identification of SigM-dependent genes. Infect. Immun. 2007, 75:452-461.
38. Blasco B., Chen J.M., Hartkoorn R., Sala C., Uplekar S., Rougemont J., Pojer F., Cole S.T. Virulence regulator EspR of Mycobacterium tuberculosis is a nucleoid-associated protein. PLoS Pathog. 2012, 8:e1002621.
39. Buxton R.S., Green J., Hunt D.M., Kahramanoglou C., Stapleton M.R., Sweeney N.P. Long range transcriptional control of virulence critical genes in Mycobacterium tuberculosis by nucleoid-associated proteins?. Virulence 2012, 3:408-410.
40. Gordon B.R., Li Y., Wang L., Sintsova A., van Bakel H., Tian S., Navarre W.W., Xia B., Liu J. Lsr2 is a nucleoid-associated protein that targets AT-rich sequences and virulence genes in Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:5154-5159.
41. Pang X., Samten B., Cao G., Wang X., Tvinnereim A.R., Chen X.L., Howard S.T. MprAB regulates the espA operon in Mycobacterium tuberculosis and modulates ESX-1 function and host cytokine response. J. Bacteriol. 2013, 195:66-75.
42. Raghavan S., Manzanillo P., Chan K., Dovey C., Cox J.S. Secreted transcription factor controls Mycobacterium tuberculosis virulence. Nature 2008, 454:717-721.
43. Brodin P., Majlessi L., Marsollier L., de Jonge M.I., Bottai D., Demangel C., Hinds J., Neyrolles O., Butcher P.D., Leclerc C., Cole S.T., Brosch R. Dissection of ESAT-6 system 1 of Mycobacterium tuberculosis and impact on immunogenicity and virulence. Infect. Immun. 2006, 74:88-98.
44. Fortune S.M., Jaeger A., Sarracino D.A., Chase M.R., Sassetti C.M., Sherman D.R., Bloom B.R., Rubin E.J. Mutually dependent secretion of proteins required for mycobacterial virulence. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:10676-10681.
45. MacGurn J.A., Raghavan S., Stanley S.A., Cox J.S. A non-RD1 gene cluster is required for Snm secretion in Mycobacterium tuberculosis. Mol. Microbiol. 2005, 57:1653-1663.
46. Chen J.M., Zhang M., Rybniker J., Boy-Rottger S., Dhar N., Pojer F., Cole S.T. Mycobacterium tuberculosis EspB binds phospholipids and mediates EsxA-independent virulence. Mol. Microbiol. 2013, 89:1154-1166.
47. Fattori J., Prando A., Martins A.M., Rodrigues F.H., Tasic L. Bacterial secretion chaperones. Protein Pept. Lett. 2013, 18:158-166.
48. Phan J., Austin B.P., Waugh D.S. Crystal structure of the Yersinia type III secretion protein YscE. Protein Sci. 2005, 14:2759-2763.
49. Sun P., Tropea J.E., Austin B.P., Cherry S., Waugh D.S. Structural characterization of the Yersinia pestis type III secretion system needle protein YscF in complex with its heterodimeric chaperone YscE/YscG. J. Mol. Biol. 2008, 377:819-830.
50. De Leon J., Jiang G., Ma Y., Rubin E., Fortune S., Sun J. Mycobacterium tuberculosis ESAT-6 exhibits a unique membrane-interacting activity that is not found in its ortholog from non-pathogenic Mycobacterium smegmatis. J. Biol. Chem. 2012, 287:44184-44191.
51. de Jonge M.I., Pehau-Arnaudet G., Fretz M.M., Romain F., Bottai D., Brodin P., Honore N., Marchal G., Jiskoot W., England P., Cole S.T., Brosch R. ESAT-6 from Mycobacterium tuberculosis dissociates from its putative chaperone CFP-10 under acidic conditions and exhibits membrane-lysing activity. J. Bacteriol. 2007, 189:6028-6034.
52. Smith J., Manoranjan J., Pan M., Bohsali A., Xu J., Liu J., McDonald K.L., Szyk A., LaRonde-LeBlanc N., Gao L.Y. Evidence for pore formation in host cell membranes by ESX-1-secreted ESAT-6 and its role in Mycobacterium marinum escape from the vacuole. Infect. Immun. 2008, 76:5478-5487.
53. Hsu T., Hingley-Wilson S.M., Chen B., Chen M., Dai A.Z., Morin P.M., Marks C.B., Padiyar J., Goulding C., Gingery M., Eisenberg D., Russell R.G., Derrick S.C., Collins F.M., Morris S.L., King C.H., Jacobs W.R. The primary mechanism of attenuation of bacillus Calmette-Guerin is a loss of secreted lytic function required for invasion of lung interstitial tissue. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:12420-12425.
54. Chen J.M., Boy-Rottger S., Dhar N., Sweeney N., Buxton R.S., Pojer F., Rosenkrands I., Cole S.T. EspD is critical for the virulence-mediating ESX-1 secretion system in Mycobacterium tuberculosis. J. Bacteriol. 2012, 194:884-893.
55. Daleke M.H., van der Woude A.D., Parret A.H., Ummels R., de Groot A.M., Watson D., Piersma S.R., Jimenez 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.
56. Planet P.J., Kachlany S.C., DeSalle R., Figurski D.H. Phylogeny of genes for secretion NTPases: identification of the widespread tadA subfamily and development of a diagnostic key for gene classification. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:2503-2508.
57. Bonemann G., Pietrosiuk A., Diemand A., Zentgraf H., Mogk A. Remodelling of VipA/VipB tubules by ClpV-mediated threading is crucial for type VI protein secretion. EMBO J. 2009, 28:315-325.
58. Basler M., Pilhofer M., Henderson G.P., Jensen G.J., Mekalanos J.J. Type VI secretion requires a dynamic contractile phage tail-like structure. Nature 2012, 483:182-186.
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. Cerveny L., Straskova A., Dankova V., Hartlova A., Ceckova M., Staud F., Stulik J. Tetratricopeptide repeat motifs in the world of bacterial pathogens: role in virulence mechanisms. Infect. Immun. 2013, 81:629-635.
61. Wagner J.M., Evans T.J., Korotkov K.V. Crystal structure of the N-terminal domain of EccA ATPase from the ESX-1 secretion system of Mycobacterium tuberculosis. Proteins 2013, 10.1002/prot.24351.
62. Lapouge K., Smith S.J., Walker P.A., Gamblin S.J., Smerdon S.J., Rittinger K. Structure of the TPR domain of p67phox in complex with Rac.GTP. Mol. Cell 2000, 6:899-907.
63. Bottai D., Di Luca M., Majlessi L., Frigui W., Simeone R., Sayes F., Bitter W., Brennan M.J., Leclerc C., Batoni G., Campa M., Brosch R., Esin S. Disruption of the ESX-5 system of Mycobacterium tuberculosis causes loss of PPE protein secretion, reduction of cell wall integrity and strong attenuation. Mol. Microbiol. 2012, 83:1195-1209.
64. Gao L.Y., Guo S., McLaughlin B., Morisaki H., Engel J.N., Brown E.J. A mycobacterial virulence gene cluster extending RD1 is required for cytolysis, bacterial spreading and ESAT-6 secretion. Mol. Microbiol. 2004, 53:1677-1693.
65. Sassetti C.M., Boyd D.H., Rubin E.J. Genes required for mycobacterial growth defined by high density mutagenesis. Mol. Microbiol. 2003, 48:77-84.
66. Joshi S.A., Ball D.A., Sun M.G., Carlsson F., Watkins B.Y., Aggarwal N., McCracken J.M., Huynh K.K., Brown E.J. EccA1, a component of the Mycobacterium marinum ESX-1 protein virulence factor secretion pathway, regulates mycolic acid lipid synthesis. Chem. Biol. 2012, 19:372-380.
67. Houben E.N.G., Bestebroer J., Ummels R., Wilson L., Piersma S.R., Jiménez C.R., Ottenhoff T.H., Luirink J., Bitter W. Composition of the type VII secretion system membrane complex. Mol. Microbiol. 2012, 86:472-484.
68. Converse S.E., Cox J.S. A protein secretion pathway critical for Mycobacterium tuberculosis virulence is conserved and functional in Mycobacterium smegmatis. J. Bacteriol. 2005, 187:1238-1245.
69. Burton B., Dubnau D. Membrane-associated DNA transport machines. Cold Spring Harb. Perspect. Biol. 2010, 2:a000406.
70. Atmakuri K., Cascales E., Christie P.J. Energetic components VirD4, VirB11 and VirB4 mediate early DNA transfer reactions required for bacterial type IV secretion. Mol. Microbiol. 2004, 54:1199-1211.
71. Niederweis M., Danilchanka O., Huff J., Hoffmann C., Engelhardt H. Mycobacterial outer membranes: in search of proteins. Trends Microbiol. 2010, 18:109-116.
72. Mahfoud M., Sukumaran S., Hulsmann P., Grieger K., Niederweis M. Topology of the porin MspA in the outer membrane of Mycobacterium smegmatis. J. Biol. Chem. 2006, 281:5908-5915.
73. 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, 462:1011-1015.
74. Wirth S.E., Krywy J.A., Aldridge B.B., Fortune S.M., Fernandez-Suarez M., Gray T.A., Derbyshire K.M. Polar assembly and scaffolding proteins of the virulence-associated ESX-1 secretory apparatus in mycobacteria. Mol. Microbiol. 2012, 83:654-664.
75. Dave J.A., Gey van Pittius N.C., Beyers A.D., Ehlers M.R., Brown G.D. Mycosin-1, a subtilisin-like serine protease of Mycobacterium tuberculosis, is cell wall-associated and expressed during infection of macrophages. BMC Microbiol. 2002, 2:30.
76. Ohol Y.M., Goetz D.H., Chan K., Shiloh M.U., Craik C.S., Cox J.S. Mycobacterium tuberculosis MycP1 protease plays a dual role in regulation of ESX-1 secretion and virulence. Cell Host Microbe 2010, 7:210-220.
77. Solomonson M., Huesgen P.F., Wasney G.A., Watanabe N., Gruninger R.J., Prehna G., Overall C.M., Strynadka N.C. Structure of the mycosin-1 protease from the mycobacterial ESX-1 protein type VII secretion system. J. Biol. Chem. 2013, 288:17782-17790.
78. Wagner J.M., Evans T.J., Chen J., Zhu H., Houben E.N.G., Bitter W., Korotkov K.V. Understanding specificity of the mycosin proteases in ESX/type VII secretion by structural and functional analysis. J. Struct. Biol. 2013.
79. Shinde U., Inouye M. Folding mediated by an intramolecular chaperone: autoprocessing pathway of the precursor resolved via a substrate assisted catalysis mechanism. J. Mol. Biol. 1995, 247:390-395.
80. Coros A., Callahan B., Battaglioli E., Derbyshire K.M. The specialized secretory apparatus ESX-1 is essential for DNA transfer in Mycobacterium smegmatis. Mol. Microbiol. 2008, 69:794-808.
81. Flint J.L., Kowalski J.C., Karnati P.K., Derbyshire K.M. The RD1 virulence locus of Mycobacterium tuberculosis regulates DNA transfer in Mycobacterium smegmatis. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:12598-12603.
82. Gray T.A., Krywy J.A., Harold J., Palumbo M.J., Derbyshire K.M. Distributive conjugal transfer in mycobacteria generates progeny with meiotic-like genome-wide mosaicism, allowing mapping of a mating identity locus. PLoS Biol. 2013, 11:e1001602.
83. Cascales E., Atmakuri K., Sarkar M.K., Christie P.J. DNA substrate-induced activation of the Agrobacterium VirB/VirD4 type IV secretion system. J. Bacteriol. 2013, 195:2691-2704.
84. Punta M., Coggill P.C., Eberhardt R.Y., Mistry J., Tate J., Boursnell C., Pang N., Forslund K., Ceric G., Clements J., Heger A., Holm L., Sonnhammer E.L., Eddy S.R., Bateman A., Finn R.D. The Pfam protein families database. Nucleic Acids Res. 2012, 40:D290-D301.
85. 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.
86. Baptista C., Barreto H.C., Sao-Jose C. High levels of DegU-P activate an Esat-6-like secretion system in Bacillus subtilis. PLoS One 2013, 8:e67840.
87. Burts M.L., DeDent A.C., Missiakas D.M. EsaC substrate for the ESAT-6 secretion pathway and its role in persistent infections of Staphylococcus aureus. Mol. Microbiol. 2008, 69:736-746.
88. 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.
89. Garufi G., Butler E., Missiakas D. ESAT-6-like protein secretion in Bacillus anthracis. J. Bacteriol. 2008, 190:7004-7011.
90. Mueller-Cajar O., Stotz M., Wendler P., Hartl F.U., Bracher A., Hayer-Hartl M. Structure and function of the AAA+ protein CbbX, a red-type Rubisco activase. Nature 2011, 479:194-199.
91. Fisher S.J., Blakeley M.P., Cianci M., McSweeney S., Helliwell J.R. Protonation-state determination in proteins using high-resolution X-ray crystallography: effects of resolution and completeness. Acta Crystallogr. D Biol. Crystallogr. 2012, 68:800-809.