1887

Abstract

Non-tuberculous mycobacteria (NTM) are a large group of micro-organisms comprising more than 200 individual species. Most NTM are saprophytic organisms and are found mainly in terrestrial and aquatic environments. In recent years, NTM have been increasingly associated with infections in both immunocompetent and immunocompromised individuals, prompting significant efforts to understand the diverse pathogenic and signalling traits of these emerging pathogens. Since the discovery of Type VII secretion systems (T7SS), there have been significant developments regarding the role of these complex systems in mycobacteria. These specialised systems, also known as Early Antigenic Secretion (ESX) systems, are employed to secrete proteins across the inner membrane. They also play an essential role in virulence, nutrient uptake and conjugation. Our understanding of T7SS in mycobacteria has significantly benefited over the last few years, from the resolution of ESX-3 structure in , to ESX-5 structures in and . In addition, ESX-4, considered until recently as a non-functional system in both pathogenic and non-pathogenic mycobacteria, has been proposed to play an important role in the virulence of ; an increasingly recognized opportunistic NTM causing severe lung diseases. These major findings have led to important new insights into the functional mechanisms of these biological systems, their implication in virulence, nutrient acquisitions and cell wall shaping, and will be discussed in this review.

Funding
This study was supported by the:
  • LabexEpiGenMed (Award ANR-10-LABX-12-01)
    • Principle Award Recipient: MattD. Johansen
  • Joachim Herz Stiftung
    • Principle Award Recipient: FlorianP. Maurer
  • Joachim Herz Stiftung
    • Principle Award Recipient: MatthiasWilmanns
  • H2020 European Institute of Innovation and Technology (Award Marie Skłodowska-Curie grant no 846476)
    • Principle Award Recipient: CecilePetit
  • Association Vaincre la Mucoviscidose (Award RIF20190502522)
    • Principle Award Recipient: MarionLagune
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.001054
2021-07-05
2024-04-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/167/7/mic001054.html?itemId=/content/journal/micro/10.1099/mic.0.001054&mimeType=html&fmt=ahah

References

  1. Stanley SA, Raghavan S, Hwang WW, Cox JS. Acute infection and macrophage subversion by Mycobacterium tuberculosis require a specialized secretion system. Proc Natl Acad Sci U S A 2003; 100:13001–13006 [View Article] [PubMed]
    [Google Scholar]
  2. Mahairas GG, Sabo PJ, Hickey MJ, Singh DC, Stover CK. Molecular analysis of genetic differences between Mycobacterium bovis BCG and virulent M. bovis. J Bacteriol 1996; 178:1274–1282 [View Article] [PubMed]
    [Google Scholar]
  3. Behr MA, Wilson MA, Gill WP, Salamon H, Schoolnik GK et al. Comparative genomics of BCG vaccines by whole-genome DNA microarray. Science 1999; 284:1520–1523 [View Article] [PubMed]
    [Google Scholar]
  4. Gordon SV, Brosch R, Billault A, Garnier T, Eiglmeier K et al. Identification of variable regions in the genomes of tubercle bacilli using bacterial artificial chromosome arrays. Mol Microbiol 1999; 32:643–655 [View Article] [PubMed]
    [Google Scholar]
  5. Abdallah AM, Gey van Pittius NC, Champion PAD, Cox J, Luirink J et al. Type VII secretion--mycobacteria show the way. Nat Rev Microbiol 2007; 5:883–891 [View Article] [PubMed]
    [Google Scholar]
  6. Sørensen AL, Nagai S, Houen G, Andersen P, Andersen AB. Purification and characterization of a low-molecular-mass T-cell antigen secreted by Mycobacterium tuberculosis. Infect Immun 1995; 63:1710–1717 [View Article] [PubMed]
    [Google Scholar]
  7. Pai M, Riley LW, Colford JM. Interferon-γ assays in the immunodiagnosis of tuberculosis: a systematic review. Lancet Infect Dis 2004; 4:761–776 [View Article] [PubMed]
    [Google Scholar]
  8. Hsu T, Hingley-Wilson SM, Chen B, Chen M, Dai AZ et al. 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 USA 2003; 100:12420–12425 [View Article] [PubMed]
    [Google Scholar]
  9. Guinn KM, Hickey MJ, Mathur SK, Zakel KL, Grotzke JE et al. Individual RD1-region genes are required for export of ESAT-6/CFP-10 and for virulence of Mycobacterium tuberculosis. Mol Microbiol 2004; 51:359–370 [View Article] [PubMed]
    [Google Scholar]
  10. Brodin P, Majlessi L, Marsollier L, de Jonge MI, Bottai D et al. Dissection of ESAT-6 system 1 of Mycobacterium tuberculosis and impact on immunogenicity and virulence. Infect Immun 2006; 74:88–98 [View Article] [PubMed]
    [Google Scholar]
  11. Bitter W, Houben ENG, Bottai D, Brodin P, Brown EJ et al. Systematic genetic nomenclature for type VII secretion systems. PLoS Pathog 2009; 5:e1000507 [View Article] [PubMed]
    [Google Scholar]
  12. Houben ENG, Korotkov KV, Bitter W. Take five — Type VII secretion systems of Mycobacteria. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research 2014; 1843:1707–1716
    [Google Scholar]
  13. Bunduc CM, Bitter W, Houben ENG. Structure and function of the mycobacterial type VII secretion systems. Annu Rev Microbiol 2020; 74:315–335 [View Article] [PubMed]
    [Google Scholar]
  14. Unnikrishnan M, Constantinidou C, Palmer T, Pallen MJ. The enigmatic Esx proteins: Looking beyond mycobacteria. Trends Microbiol 2017; 25:192–204 [View Article] [PubMed]
    [Google Scholar]
  15. Bottai D, Gröschel MI, Brosch R. Type VII secretion systems in gram-positive bacteria. Curr Top Microbiol Immunol 2017; 404:235–265 [View Article] [PubMed]
    [Google Scholar]
  16. Chirakos AE, Balaram A, Conrad W, Champion PA. Modeling tubercular ESX-1 secretion using Mycobacterium marinum. Microbiol Mol Biol Rev 2020; 84:e00082 [View Article] [PubMed]
    [Google Scholar]
  17. Abdallah AM, Savage NDL, van Zon M, Wilson L, Vandenbroucke-Grauls C et al. The ESX-5 secretion system of Mycobacterium marinum modulates the macrophage response. J Immunol 2008; 181:7166–7175 [View Article] [PubMed]
    [Google Scholar]
  18. Lienard J, Nobs E, Lovins V, Movert E, Valfridsson C et al. The Mycobacterium marinum ESX-1 system mediates phagosomal permeabilization and type I interferon production via separable mechanisms. Proc Natl Acad Sci 20201160–1166
    [Google Scholar]
  19. Gray TA, Derbyshire KM. Blending genomes: distributive conjugal transfer in mycobacteria, a sexier form of HGT: Distributive conjugal transfer. Mol Microbiol 2018; 108:601–613 [View Article] [PubMed]
    [Google Scholar]
  20. Siegrist MS, Unnikrishnan M, McConnell MJ, Borowsky M, Cheng T-Y et al. Mycobacterial Esx-3 is required for mycobactin-mediated iron acquisition. Proc Natl Acad Sci U S A 2009; 106:18792–18797 [View Article]
    [Google Scholar]
  21. Serafini A, Boldrin F, Palù 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 [View Article]
    [Google Scholar]
  22. Ates LS, Ummels R, Commandeur S, van de Weerd R, van der Weerd R et al. Essential role of the ESX-5 secretion system in outer membrane permeability of pathogenic mycobacteria. PLoS Genet 2015; 11:e1005190 [View Article] [PubMed]
    [Google Scholar]
  23. Ates LS, van der Woude AD, Bestebroer J, van Stempvoort G, Musters RJP et al. The ESX-5 system of pathogenic mycobacteria is involved in capsule integrity and virulence through its substrate PPE10. PLoS Pathog 2016; 12:e1005696 [View Article] [PubMed]
    [Google Scholar]
  24. Beckham KSH, Ciccarelli L, Bunduc CM, Mertens HDT, Ummels R et al. Structure of the mycobacterial ESX-5 type VII secretion system membrane complex by single-particle analysis. Nat Microbiol 2017; 2:17047 [View Article] [PubMed]
    [Google Scholar]
  25. Famelis N, Rivera-Calzada A, Degliesposti G, Wingender M, Mietrach N et al. Architecture of the mycobacterial type VII secretion system. Nature 2019; 576:321–325 [View Article] [PubMed]
    [Google Scholar]
  26. Poweleit N, Czudnochowski N, Nakagawa R, Trinidad DD, Murphy KC et al. The structure of the endogenous ESX-3 secretion system. eLife 2019; 8:e52983 [View Article] [PubMed]
    [Google Scholar]
  27. Bunduc CM, Fahrenkamp D, Wald J, Ummels R, Bitter W et al. Structure and dynamics of the ESX-5 type VII secretion system of Mycobacterium tuberculosis. Nature 2021; 593:445–448
    [Google Scholar]
  28. Beckham KSH, Ritter C, Chojnowski G, Mullapudi E, Rettel M et al. Structure of the mycobacterial ESX-5 type VII secretion system hexameric pore complex. Microbiology 2020
    [Google Scholar]
  29. Laencina L, Dubois V, Moigne L, Viljoen A, Majlessi L et al. Identification of genes required for Mycobacterium abscessus growth in vivo with a prominent role of the ESX-4 locus. Proc Natl Acad Sci USA 2018; 115:1002–1011
    [Google Scholar]
  30. Johansen MD, Herrmann JL, Kremer L. Non-tuberculous mycobacteria and the rise of Mycobacterium abscessus. Nat Rev Microbiol 2020; 18:392–407 [View Article] [PubMed]
    [Google Scholar]
  31. Dumas E, Christina Boritsch E, Vandenbogaert M, Rodríguez de la Vega RC, Thiberge J-M et al. Mycobacterial pan-genome analysis suggests important role of plasmids in the radiation of type VII secretion systems. Genome Biol Evol 2016; 8:387–402 [View Article] [PubMed]
    [Google Scholar]
  32. Newton-Foot M, Warren RM, Sampson SL, van Helden PD, Gey van Pittius NC. The plasmid-mediated evolution of the mycobacterial ESX (Type VII) secretion systems. BMC Evol Biol 2016; 16:16–62 [View Article] [PubMed]
    [Google Scholar]
  33. Majlessi L, Prados-Rosales R, Casadevall A, Brosch R. Release of mycobacterial antigens. Immunol Rev 2015; 264:25–45 [View Article] [PubMed]
    [Google Scholar]
  34. Houben ENG, Bestebroer J, Ummels R, Wilson L, Piersma SR et al. Composition of the type VII secretion system membrane complex. Mol Microbiol 2012; 86:472–484 [View Article] [PubMed]
    [Google Scholar]
  35. Gey van Pittius NC, Sampson SL, Lee H, Kim Y, van Helden PD et al. Evolution and expansion of the mycobacterium tuberculosis PE and PPE multigene families and their association with the duplication of the esat-6 (ESX) gene cluster regions. BMC Evol Biol 2006; 6:95 [View Article] [PubMed]
    [Google Scholar]
  36. Gey Van Pittius NC, Gamieldien J, Hide W, Brown GD, Siezen RJ et al. The ESAT-6 gene cluster of Mycobacterium tuberculosis and other high G+C Gram-positive bacteria. Genome Biol 2001; 2:10RESEARCH0044
    [Google Scholar]
  37. Bottai D, Brosch R. Mycobacterial PE, PPE and ESX clusters: novel insights into the secretion of these most unusual protein families. Mol Microbiol 2009; 73:325–328 [View Article] [PubMed]
    [Google Scholar]
  38. Gröschel MI, Sayes F, Simeone R, Majlessi L, Brosch R. ESX secretion systems: mycobacterial evolution to counter host immunity. Nat Rev Microbiol 2016; 14:677–691 [View Article] [PubMed]
    [Google Scholar]
  39. Wagner JM, Chan S, Evans TJ, Kahng S, Kim J et al. Structures of EccB1 and EccD1 from the core complex of the mycobacterial ESX-1 type VII secretion system. BMC Struct Biol 201616
    [Google Scholar]
  40. Rosenberg OS, Dovala D, Li X, Connolly L, Bendebury A et al. Substrates control multimerization and activation of the multi-domain atpase motor of type vii secretion. Cell 2015; 161:501–512 [View Article]
    [Google Scholar]
  41. Bunduc CM, Ummels R, Bitter W, Houben ENG. Species-specific secretion of ESX-5 type VII substrates is determined by the linker 2 of EccC5. Mol Microbiol 2020; 114:66–76 [View Article] [PubMed]
    [Google Scholar]
  42. van Winden VJC, Ummels R, Piersma SR, Jiménez CR, Korotkov KV et al. Mycosins are required for the stabilization of the ESX-1 and ESX-5 type VII secretion membrane complexes. mBio 2016; 7:
    [Google Scholar]
  43. van Winden VJC, Damen MPM, Ummels R, Bitter W, Houben ENG. Protease domain and transmembrane domain of the type VII secretion mycosin protease determine system-specific functioning in mycobacteria. J Biol Chem 2019; 294:4806–4814 [View Article] [PubMed]
    [Google Scholar]
  44. van Winden VJC, Bunduc CM, Ummels R, Bitter W, Houben ENG. A chimeric EccB-MycP fusion protein is functional and a stable component of the ESX-5 type VII secretion system membrane complex. J Mol Biol 2020; 432:1265–1278 [View Article] [PubMed]
    [Google Scholar]
  45. Sun D, Liu Q, He Y, Wang C, Wu F et al. The putative propeptide of MycP1 in mycobacterial type VII secretion system does not inhibit protease activity but improves protein stability. Protein Cell 2013; 4:921–931 [View Article] [PubMed]
    [Google Scholar]
  46. Wagner JM, Evans TJ, Chen J, Zhu H, Houben ENG et al. Understanding specificity of the mycosin proteases in ESX/type VII secretion by structural and functional analysis. J Struct Biol 2013; 184:115–128 [View Article] [PubMed]
    [Google Scholar]
  47. Solomonson M, Huesgen PF, Wasney GA, Watanabe N, Gruninger RJ et al. Structure of the mycosin-1 protease from the mycobacterial ESX-1 protein type VII secretion system. J Biol Chem 2013; 288:17782–17790 [View Article] [PubMed]
    [Google Scholar]
  48. Ohol YM, Goetz DH, Chan K, Shiloh MU, Craik CS et al. Mycobacterium tuberculosis MycP1 protease plays a dual role in regulation of ESX-1 secretion and virulence. Cell Host Microbe 2010; 7:210–220 [View Article] [PubMed]
    [Google Scholar]
  49. Solomonson M, Setiaputra D, Makepeace KAT, Lameignere E, Petrotchenko EV et al. Structure of EspB from the ESX-1 type VII secretion system and insights into its export mechanism. Structure 2015; 23:571–583 [View Article] [PubMed]
    [Google Scholar]
  50. Poulsen C, Panjikar S, Holton SJ, Wilmanns M, Song YH. WXG100 protein superfamily consists of three subfamilies and exhibits an α-helical C-terminal conserved residue pattern. PLoS ONE 2014; 9:e89313 [View Article] [PubMed]
    [Google Scholar]
  51. Renshaw PS, Lightbody KL, Veverka V, Muskett FW, Kelly G et al. Structure and function of the complex formed by the tuberculosis virulence factors CFP-10 and ESAT-6. EMBO J 2005; 24:2491–2498 [View Article] [PubMed]
    [Google Scholar]
  52. Champion PAD, Stanley SA, Champion MM, Brown EJ, Cox JS. C-terminal signal sequence promotes virulence factor secretion in Mycobacterium tuberculosis. Science 2006; 313:1632–1636 [View Article] [PubMed]
    [Google Scholar]
  53. Daleke MH, Ummels R, Bawono P, Heringa J, Vandenbroucke-Grauls C et al. General secretion signal for the mycobacterial type VII secretion pathway. Proc Natl Acad Sci U S A 2012; 109:11342–11347 [View Article] [PubMed]
    [Google Scholar]
  54. Li Y, Miltner E, Wu M, Petrofsky M, Bermudez LE. A Mycobacterium avium PPE gene is associated with the ability of the bacterium to grow in macrophages and virulence in mice. Cell Microbiol 2005; 7:539–548 [View Article]
    [Google Scholar]
  55. Ripoll F, Pasek S, Schenowitz C, Dossat C, Barbe V et al. Non mycobacterial virulence genes in the genome of the emerging pathogen Mycobacterium abscessus. PLoS ONE 2009; 4:e5660 [View Article] [PubMed]
    [Google Scholar]
  56. Phan TH, Houben ENG. Bacterial secretion chaperones: The mycobacterial type VII case. FEMS Microbiol Lett 2018; 365: [View Article] [PubMed]
    [Google Scholar]
  57. Damen MPM, Phan TH, Ummels R, Rubio-Canalejas A, Bitter W et al. Modification of a PE/PPE substrate pair reroutes an Esx substrate pair from the mycobacterial ESX-1 type VII secretion system to the ESX-5 system. J Biol Chem 2020; 295:5960–5969 [View Article] [PubMed]
    [Google Scholar]
  58. Williamson ZA, Chaton CT, Ciocca WA, Korotkova N, Korotkov KV. PE5-PPE4-EspG3 heterotrimer structure from mycobacterial ESX-3 secretion system gives insight into cognate substrate recognition by ESX systems. J Biol Chem 2020; 295:12706–12715 [View Article] [PubMed]
    [Google Scholar]
  59. Ekiert DC, Cox JS. Structure of a PE–PPE–EspG complex from Mycobacterium tuberculosis reveals molecular specificity of ESX protein secretion. Proc Natl Acad Sci U S A 2014; 111:14758–14763 [View Article] [PubMed]
    [Google Scholar]
  60. Tuukkanen AT, Freire D, Chan S, Arbing MA, Reed RW et al. Structural variability of ESPG chaperones from mycobacterial ESX-1, ESX-3, and ESX-5 type VII secretion systems. J Mol Biol 2019; 431:289–307 [View Article] [PubMed]
    [Google Scholar]
  61. Raghavan S, Manzanillo P, Chan K, Dovey C, Cox JS. Secreted transcription factor controls Mycobacterium tuberculosis virulence. Nature 2008; 454:717–721 [View Article] [PubMed]
    [Google Scholar]
  62. Ates LS, Brosch R. Discovery of the type VII ESX-1 secretion needle?. Mol Microbiol 2017; 103:7–12 [View Article] [PubMed]
    [Google Scholar]
  63. Fortune SM, Jaeger A, Sarracino DA, Chase MR, Sassetti CM et al. Mutually dependent secretion of proteins required for mycobacterial virulence. Proc Natl Acad Sci U S A 2005; 102:10676–10681 [View Article] [PubMed]
    [Google Scholar]
  64. MacGurn JA, Raghavan S, Stanley SA, Cox JS. A non-RD1 gene cluster is required for Snm secretion in Mycobacterium tuberculosis. Mol Microbiol 2005; 57:1653–1663 [View Article] [PubMed]
    [Google Scholar]
  65. Gao L-Y, Guo S, McLaughlin B, Morisaki H, Engel JN et al. A mycobacterial virulence gene cluster extending RD1 is required for cytolysis, bacterial spreading and ESAT-6 secretion. Mol Microbiol 2004; 53:1677–1693 [View Article] [PubMed]
    [Google Scholar]
  66. Coros A, Callahan B, Battaglioli E, Derbyshire KM. The specialized secretory apparatus ESX-1 is essential for DNA transfer in Mycobacterium smegmatis. Mol Microbiol 2008; 69:794–808 [View Article] [PubMed]
    [Google Scholar]
  67. Sala C, Odermatt NT, Soler-Arnedo P, Gülen MF, von Schultz S et al. EspL is essential for virulence and stabilizes EspE, EspF and EspH levels in Mycobacterium tuberculosis. PLoS Pathog 2018; 14:e1007491 [View Article]
    [Google Scholar]
  68. Chirakos AE, Nicholson KR, Huffman A, Champion PA. Conserved ESX-1 substrates ESPE and ESPF are virulence factors that regulate gene expression. Infect Immun 2020; 88:e00289–20 [View Article] [PubMed]
    [Google Scholar]
  69. Sanchez KG, Ferrell MJ, Chirakos AE, Nicholson KR, Abramovitch RB et al. ESPM is a conserved transcription factor that regulates gene expression in response to the ESX-1 system. mBio 2020; 11:e02807–19 [View Article] [PubMed]
    [Google Scholar]
  70. 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 [View Article] [PubMed]
    [Google Scholar]
  71. Wagner JM, Evans TJ, Korotkov KV. Crystal structure of the N-terminal domain of EccA₁ ATPase from the ESX-1 secretion system of Mycobacterium tuberculosis. Proteins 2014; 82:159–163 [View Article] [PubMed]
    [Google Scholar]
  72. Champion PAD, Champion MM, Manzanillo P, Cox JS. ESX-1 secreted virulence factors are recognized by multiple cytosolic AAA ATPases in pathogenic mycobacteria. Mol Microbiol 2009; 73:950–962 [View Article] [PubMed]
    [Google Scholar]
  73. Joshi SA, Ball DA, Sun MG, Carlsson F, Watkins BY et al. 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 [View Article] [PubMed]
    [Google Scholar]
  74. Crosskey TD, Beckham KSH, Wilmanns M. The ATPases of the mycobacterial type VII secretion system: Structural and mechanistic insights into secretion. Prog Biophys Mol Biol 2019; 152:25–34 [View Article] [PubMed]
    [Google Scholar]
  75. Pym AS, Brodin P, Brosch R, Huerre M, Cole ST. Loss of RD1 contributed to the attenuation of the live tuberculosis vaccines Mycobacterium bovis BCG and Mycobacterium microti. Mol Microbiol 2002; 46:709–717 [View Article] [PubMed]
    [Google Scholar]
  76. Davis JM, Ramakrishnan L. The role of the granuloma in expansion and dissemination of early tuberculous infection. Cell 2009; 136:37–49 [View Article] [PubMed]
    [Google Scholar]
  77. Conrad WH, Osman MM, Shanahan JK, Chu F, Takaki KK et al. Mycobacterial ESX-1 secretion system mediates host cell lysis through bacterium contact-dependent gross membrane disruptions. Proc Natl Acad Sci U S A 2017; 114:1371–1376 [View Article] [PubMed]
    [Google Scholar]
  78. Houben D, Demangel C, van Ingen J, Perez J, Baldeón L et al. ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria. Cell Microbiol 2012; 14:1287–1298 [View Article] [PubMed]
    [Google Scholar]
  79. Simeone R, Bobard A, Lippmann J, Bitter W, Majlessi L et al. Phagosomal rupture by Mycobacterium tuberculosis results in toxicity and host cell death. PLoS Pathog 2012; 8:e1002507 [View Article] [PubMed]
    [Google Scholar]
  80. Smith J, Manoranjan J, Pan M, Bohsali A, Xu J et al. 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 [View Article] [PubMed]
    [Google Scholar]
  81. Augenstreich J, Arbues A, Simeone R, Haanappel E, Wegener A et al. ESX-1 and phthiocerol dimycocerosates of Mycobacterium tuberculosis act in concert to cause phagosomal rupture and host cell apoptosis. Cell Microbiol 2017; 19: [View Article] [PubMed]
    [Google Scholar]
  82. Quigley J, Hughitt VK, Velikovsky CA, Mariuzza RA, El-Sayed NM et al. The cell wall lipid PDIM contributes to phagosomal escape and host cell exit of Mycobacterium tuberculosis. mBio 2017; 8:e00148–17 [View Article] [PubMed]
    [Google Scholar]
  83. Osman MM, Pagán AJ, Shanahan JK, Ramakrishnan L. Mycobacterium marinum phthiocerol dimycocerosates enhance macrophage phagosomal permeabilization and membrane damage. PLoS One 2020; 15:e0233252 [View Article] [PubMed]
    [Google Scholar]
  84. Bosserman RE, Nicholson KR, Champion MM, Champion PA. A new ESX-1 substrate in Mycobacterium marinum that is required for hemolysis but not host cell lysis. J Bacteriol 2019; 201:e00760–18 [View Article] [PubMed]
    [Google Scholar]
  85. Volkman HE, Clay H, Beery D, Chang JCW, Sherman DR et al. Tuberculous granuloma formation is enhanced by a mycobacterium virulence determinant. PLoS Biol 2004; 2:e367 [View Article] [PubMed]
    [Google Scholar]
  86. Wang J, McIntosh F, Radomski N, Dewar K, Simeone R et al. Insights on the emergence of Mycobacterium tuberculosis from the analysis of Mycobacterium kansasii. Genome Biol Evol 2015; 7:856–870 [View Article] [PubMed]
    [Google Scholar]
  87. Guan Q, Ummels R, Ben-Rached F, Alzahid Y, Amini MS et al. Comparative genomic and transcriptomic analyses of mycobacterium kansasii subtypes provide new insights into their pathogenicity and taxonomy. Front Cell Infect Microbiol 2020; 10:122 [View Article] [PubMed]
    [Google Scholar]
  88. Roux A-L, Viljoen A, Bah A, Simeone R, Bernut A et al. The distinct fate of smooth and rough Mycobacterium abscessus variants inside macrophages. Open Biol 2016; 6:160185 [View Article]
    [Google Scholar]
  89. Dubois V, Viljoen A, Laencina L, Moigne L, Bernut A et al. MmpL8MAB controls Mycobacterium abscessus virulence and production of a previously unknown glycolipid family. Proc Natl Acad Sci U S A 2018; 115:E10147–56
    [Google Scholar]
  90. Abdallah AM, Verboom T, Weerdenburg EM, Gey van Pittius NC, Mahasha PW et al. PPE and PE_PGRS proteins of Mycobacterium marinum are transported via the type VII secretion system ESX-5. Mol Microbiol 2009; 73:329–340 [View Article] [PubMed]
    [Google Scholar]
  91. Abdallah AM, Verboom T, Hannes F, Safi M, Strong M et al. A specific secretion system mediates PPE41 transport in pathogenic mycobacteria. Mol Microbiol 2006; 62:667–679 [View Article] [PubMed]
    [Google Scholar]
  92. Abdallah AM, Bestebroer J, Savage NDL, de Punder K, van Zon M et al. Mycobacterial secretion systems ESX-1 and ESX-5 play distinct roles in host cell death and inflammasome activation. J Immunol 2011; 187:4744–4753 [View Article] [PubMed]
    [Google Scholar]
  93. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C et al. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 1998; 393:537–544 [View Article] [PubMed]
    [Google Scholar]
  94. Burggraaf MJ, Speer A, Meijers AS, Ummels R, van der Sar AM et al. Type VII Secretion Substrates of Pathogenic Mycobacteria Are Processed by a Surface Protease. mBio 2019; 10: [View Article] [PubMed]
    [Google Scholar]
  95. Dong D, Wang D, Li M, Wang H, Yu J et al. PPE38 modulates the innate immune response and is required for Mycobacterium marinum virulence. Infect Immun 2012; 80:43–54 [View Article] [PubMed]
    [Google Scholar]
  96. Wang H, Dong D, Tang S, Chen X, Gao Q. PPE38 of Mycobacterium marinum triggers the cross-talk of multiple pathways involved in the host response, as revealed by subcellular quantitative proteomics. J Proteome Res 2013; 12:2055–2066 [View Article] [PubMed]
    [Google Scholar]
  97. McNamara M, Danelishvili L, Bermudez LE. The Mycobacterium avium ESX-5 PPE protein, PPE25-MAV, interacts with an ESAT-6 family Protein, MAV_2921, and localizes to the bacterial surface. Microb Pathog 2012; 52:227–238 [View Article] [PubMed]
    [Google Scholar]
  98. Gray TA, Krywy JA, Harold J, Palumbo MJ, Derbyshire KM. 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 [View Article] [PubMed]
    [Google Scholar]
  99. Flint JL, Kowalski JC, Karnati PK, Derbyshire KM. The RD1 virulence locus of Mycobacterium tuberculosis regulates DNA transfer in Mycobacterium smegmatis. Proceedings of the National Academy of Sciences 2004; 101:12598–12603 [View Article]
    [Google Scholar]
  100. Gray TA, Clark RR, Boucher N, Lapierre P, Smith C et al. Intercellular communication and conjugation are mediated by ESX secretion systems in mycobacteria. Science 2016; 354:347–350 [View Article] [PubMed]
    [Google Scholar]
  101. Clark RR, Judd J, Lasek-Nesselquist E, Montgomery SA, Hoffmann JG et al. Direct cell-cell contact activates SigM to express the ESX-4 secretion system in Mycobacterium smegmatis. Proc Natl Acad Sci U S A 2018; 115:E6595–603 [View Article] [PubMed]
    [Google Scholar]
  102. Boritsch EC, Khanna V, Pawlik A, Honoré N, Navas VH et al. Key experimental evidence of chromosomal DNA transfer among selected tuberculosis-causing mycobacteria. Proc Natl Acad Sci USA 2016; 113:9876–9881 [View Article] [PubMed]
    [Google Scholar]
  103. Sapriel G, Konjek J, Orgeur M, Bouri L, Frézal L et al. Genome-wide mosaicism within Mycobacterium abscessus: evolutionary and epidemiological implications. BMC Genomics 2016; 17:118 [View Article] [PubMed]
    [Google Scholar]
  104. Ummels R, Abdallah AM, Kuiper V, Aâjoud A, Sparrius M et al. Identification of a novel conjugative plasmid in mycobacteria that requires both type IV and type VII secretion. mBio 2014; 5:e01744–01714 [View Article] [PubMed]
    [Google Scholar]
  105. Tufariello JM, Chapman JR, Kerantzas CA, Wong K-W, Vilchèze C et al. Separable roles for Mycobacterium tuberculosis ESX-3 effectors in iron acquisition and virulence. Proc Natl Acad Sci U S A 2016; 113:E348–57 [View Article] [PubMed]
    [Google Scholar]
  106. Kim YS, Yang C-S, Nguyen LT, Kim JK, Jin HS et al. Mycobacterium abscessus ESX-3 plays an important role in host inflammatory and pathological responses during infection. Microbes Infect 2017; 19:5–17 [View Article]
    [Google Scholar]
  107. Lai LY, Lin TL, Chen YY, Hsieh PF, Wang JT. Role of the Mycobacterium marinum ESX-1 secretion system in sliding motility and biofilm formation. Front Microbiol 2018; 9:1160 [View Article] [PubMed]
    [Google Scholar]
  108. Esteban J, García-Coca M. Mycobacterium biofilms. Front Microbiol 2017; 8:2651 [View Article] [PubMed]
    [Google Scholar]
  109. Everall I, Nogueira CL, Bryant JM, Sánchez-Busó L, Chimara E et al. Genomic epidemiology of a national outbreak of post-surgical mycobacterium abscessus wound infections in Brazil. Microb Genom mai 2017; 3:e000111
    [Google Scholar]
  110. Kim BJ, Cha GY, Kim BR, Kook YH, Kim BJ. Insights from the genome sequence of mycobacterium Paragordonae, a potential novel live vaccine for preventing mycobacterial infections: The putative role of type VII secretion systems for an intracellular lifestyle within free-living environmental predators. Front Microbiol 2019; 10:1524 [View Article]
    [Google Scholar]
  111. Daleke MH, Cascioferro A, de Punder K, Ummels R, Abdallah AM et al. 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 [View Article] [PubMed]
    [Google Scholar]
  112. Fang Z, Newton-Foot M, Sampson SL, Gey van Pittius NC. Two promoters in the esx 3 gene cluster of Mycobacterium smegmatis respond inversely to different iron concentrations in vitro. BMC Res Notes 2017; 10:426 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.001054
Loading
/content/journal/micro/10.1099/mic.0.001054
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error