DOI QR코드

DOI QR Code

Comparative Analysis of T4SS Molecular Architectures

  • Mishghan Zehra (Department of Biochemistry, University of Missouri) ;
  • Jiwon Heo (Department of Biotechnology, The Catholic University of Korea) ;
  • Jeong Min Chung (Department of Biotechnology, The Catholic University of Korea) ;
  • Clarissa L Durie (Department of Biochemistry, University of Missouri)
  • 투고 : 2023.07.06
  • 심사 : 2023.07.24
  • 발행 : 2023.12.28

초록

The recently published high-resolution R388 T4SS structure provides exciting new details about the complete complex of T4SS, including the components making up the stalk and arches, numerous symmetry mismatches between regions of the complex, and an intriguing interpretation of the closed stalk and radial symmetry of the inner membrane complex, which is related to pilus biogenesis assembly. However, there are a few unidentified densities in the electron microscopy map and portions of the identified component sequences for which the structure is not yet known. It is also unclear how well this minimized DNA-transporting T4SS predicts the structure of other T4SSs, such as expanded systems and those that transport proteins rather than DNA. In this review, we evaluate what can be inferred from the recent high-resolution structure of the R388 T4SS with respect to the Cag and Dot/Icm systems. These systems were selected because, given what is currently known about these systems, we expect them to present most structural differences compared to the R388 T4SS structure. Furthermore, we discuss bacterial physiology and diversity, the T4SS structures and their variations between different bacterial species. These insights may prove beneficial for researchers who elucidate the structure and functions of T4SS in different bacterial species.

키워드

과제정보

This work was supported by National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (NRF-2022R1C1C1003352) and the Catholic University of Korea, Research Fund, 2022.

참고문헌

  1. Fronzes R, Christie PJ, Waksman G. 2009. The structural biology of type IV secretion systems. Nat. Rev. Microbiol. 7: 703-714.
  2. Christie PJ. 2016. The mosaic type IV secretion systems. EcoSal Plus 7: 10.1128/ecosalplus.ESP-0020-2015.
  3. Christie PJ, Whitaker N, Gonzalez-Rivera C. 2014. Mechanism and structure of the bacterial type IV secretion systems. Biochim. Biophys. Acta 1843: 1578-1591.
  4. Durie CL, Sheedlo MJ, Chung JM, Byrne BG, Su M, Knight T, et al. 2020. Structural analysis of the Legionella pneumophila Dot/Icm type IV secretion system core complex. Elife 9: e59530.
  5. Voth DE, Broederdorf LJ, Graham JG. 2012. Bacterial type IV secretion systems: versatile virulence machines. Future Microbiol. 7: 241-257.
  6. Costa TRD, Harb L, Khara P, Zeng L, Hu B, Christie PJ. 2021. Type IV secretion systems: advances in structure, function, and activation. Mol. Microbiol. 115: 436-452.
  7. Ghosal D, Jeong KC, Chang Y-W, Gyore J, Teng L, Gardner A, et al. 2019. Molecular architecture, polar targeting and biogenesis of the Legionella Dot/Icm T4SS. Nat. Microbiol. 4: 1173-1182.
  8. Alvarez-Martinez CE, Christie PJ. 2009. Biological diversity of prokaryotic type IV secretion systems. Microbiol. Mol. Biol. Rev. MMBR 73: 775-808.
  9. Grohmann E, Christie PJ, Waksman G, Backert S. 2018. Type IV secretion in Gram-negative and Gram-positive bacteria. Mol. Microbiol. 107: 455-471.
  10. Gonzalez-Rivera C, Bhatty M, Christie PJ. 2016. Mechanism and function of type IV secretion during infection of the human host. Microbiol. Spectr. 4. 10.1128/microbiolspec.VMBF-0024-2015.
  11. Bhatty M, Laverde Gomez JA, Christie PJ. 2013. The expanding bacterial type IV secretion lexicon. Res. Microbiol. 164: 620-639.
  12. Chandran V, Fronzes R, Duquerroy S, Cronin N, Navaza J, Waksman G. 2009. Structure of the outer membrane complex of a type IV secretion system. Nature 462: 1011-1015.
  13. Nakano N, Kubori T, Kinoshita M, Imada K, Nagai H. 2010. Crystal structure of Legionella DotD: insights into the relationship between type IVB and type II/III secretion systems. PLoS Pathog. 6: e1001129.
  14. Durand E, Oomen C, Waksman G. 2010. Biochemical dissection of the ATPase TraB, the VirB4 homologue of the Escherichia coli pKM101 conjugation machinery. J. Bacteriol. 192: 2315-2323.
  15. Barden S, Lange S, Tegtmeyer N, Conradi J, Sewald N, Backert S, et al. 2013. A helical RGD motif promoting cell adhesion: crystal structures of the Helicobacter pylori Type IV secretion system pilus protein CagL. Structure 21: 1931-1941.
  16. Kuroda T, Kubori T, Thanh Bui X, Hyakutake A, Uchida Y, Imada K, et al. 2015. Molecular and structural analysis of Legionella DotI gives insights into an inner membrane complex essential for type IV secretion. Sci. Rep. 5: 10912.
  17. Casu B, Smart J, Hancock MA, Smith M, Sygusch J, Baron C. 2016. Structural analysis and inhibition of TraE from the pKM101 type IV secretion system. J. Biol. Chem. 291: 23817-23829.
  18. Meir A, Chetrit D, Liu L, Roy CR, Waksman G. 2018. Legionella DotM structure reveals a role in effector recruiting to the type 4B secretion system. Nat. Commun. 9: 507.
  19. Prevost MS, Waksman G. 2018. X-ray crystal structures of the type IVb secretion system DotB ATPases. Protein Sci. 27: 1464-1475.
  20. Wu X, Zhao Y, Sun L, Jiang M, Wang Q, Wang Q, et al. 2019. Crystal structure of CagV, the Helicobacter pylori homologue of the T4 SS protein VirB8. FEBS J. 286: 4294-4309.
  21. Fronzes R, Schafer E, Wang L, Saibil HR, Orlova EV, Waksman G. 2009. Structure of a type IV secretion system core complex. Science 323: 266-268.
  22. Kubori T, Koike M, Bui XT, Higaki S, Aizawa SI, Nagai H. 2014. Native structure of a type IV secretion system core complex essential for Legionella pathogenesis. Proc. Natl. Acad. Sci. USA 111: 11804-11809.
  23. Low HH, Gubellini F, Rivera-Calzada A, Braun N, Connery S, Dujeancourt A, et al. 2014. Structure of a type IV secretion system. Nature 508: 550-553.
  24. Gordon JE, Costa TRD, Patel RS, Gonzalez-Rivera C, Sarkar MK, Orlova EV, et al. 2017. Use of chimeric type IV secretion systems to define contributions of outer membrane subassemblies for contact-dependent translocation. Mol. Microbiol. 105: 273-293.
  25. Costa TRD, Felisberto-Rodrigues C, Meir A, Prevost MS, Redzej A, Trokter M, et al. 2015. Secretion systems in Gram-negative bacteria: structural and mechanistic insights. Nat. Rev. Microbiol. 13: 343-359.
  26. Sheedlo MJ, Ohi MD, Lacy DB, Cover TL. 2022. Molecular architecture of bacterial type IV secretion systems. PLoS Pathog. 18: e1010720.
  27. Mace K, Meir A, Lukoyanova N, Liu L, Chetrit D, Hospenthal MK, et al. 2022. Proteins DotY and DotZ modulate the dynamics and localization of the type IVB coupling complex of Legionella pneumophila. Mol. Microbiol. 117: 307-319.
  28. Mace K, Vadakkepat AK, Redzej A, Lukoyanova N, Oomen C, Braun N, et al. 2022. Cryo-EM structure of a type IV secretion system. Nature 607: 191-196.
  29. Avila P, de la Cruz F. 1988. Physical and genetic map of the IncW plasmid R388. Plasmid 20: 155-157.
  30. Llosa M, Bolland S, de la Cruz F. 1994. Genetic organization of the conjugal DNA processing region of the IncW plasmid R388. J. Mol. Biol. 235: 448-464.
  31. Cabezon E, Ripoll-Rozada J, Pena A, de la Cruz F, Arechaga I. 2014. Towards an integrated model of bacterial conjugation. FEMS Microbiol. Rev. 39: 81-95.
  32. Low HH, Gubellini F, Rivera-Calzada A, Braun N, Connery S, Dujeancourt A, et al. 2014. Structure of a type IV secretion system. Nature 508: 550-553.
  33. Redzej A, Ukleja M, Connery S, Trokter M, Felisberto-Rodrigues C, Cryar A, et al. 2017. Structure of a VirD4 coupling protein bound to a VirB type IV secretion machinery. EMBO J. 36: 3080-3095.
  34. Hu B, Khara P, Christie PJ. 2019. Structural bases for F plasmid conjugation and F pilus biogenesis in Escherichia coli. Proc. Natl. Acad. Sci. USA 116: 14222-14227.
  35. Khara P, Song L, Christie PJ, Hu B. 2021. In Situ visualization of the pKM101-encoded Type IV secretion system reveals a highly symmetric ATPase energy center. mBio 12: e02465-21.
  36. Sgro GG, Oka GU, Souza DP, Cenens W, Bayer-Santos E, Matsuyama BY, et al. 2019. Bacteria-killing type IV secretion systems. Front. Microbiol. 10: 1078.
  37. Yeo HJ, Yuan Q, Beck MR, Baron C, Waksman G. 2003. Structural and functional characterization of the VirB5 protein from the type IV secretion system encoded by the conjugative plasmid pKM101. Proc. Natl. Acad. Sci. USA 100: 15947-15952.
  38. Terradot L, Bayliss R, Oomen C, Leonard GA, Baron C, Waksman G. 2005. Structures of two core subunits of the bacterial type IV secretion system, VirB8 from Brucella suis and ComB10 from Helicobacter pylori. Proc. Natl. Acad. Sci. USA 102: 4596-4601.
  39. Chernyatina AA, Low HH. 2019. Core architecture of a bacterial type II secretion system. Nat. Commun. 10: 5437.
  40. Hu J, Worrall LJ, Hong C, Vuckovic M, Atkinson CE, Caveney N, et al. 2018. Cryo-EM analysis of the T3S injectisome reveals the structure of the needle and open secretin. Nat. Commun. 9: 3840.
  41. Cover TL, Lacy DB, Ohi MD. 2020. The Helicobacter pylori Cag Type IV secretion system. Trends Microbiol. 28: 682-695.
  42. Segal G, Purcell M, Shuman HA. 1998. Host cell killing and bacterial conjugation require overlapping sets of genes within a 22-kb region of the Legionella pneumophila genome. Proc. Natl. Acad. Sci. USA 95: 1669-1674.
  43. Vogel JP, Andrews HL, Wing SK, Isberg RR. 1998. Conjugative transfer by the virulence system of Legionella pneumophila. Science 279: 873-876.
  44. Nagai H, Kubori T. 2011. Type IVB secretion systems of legionella and other gram-negative bacteria. Front. Microbiol. 2: 136.
  45. Chung JM, Sheedlo MJ, Campbell AM, Sawhney N, Frick-Cheng AE, Lacy DB, et al. 2019. Structure of the Helicobacter pylori Cag type IV secretion system. ELife 8: e47644.
  46. Sheedlo MJ, Chung JM, Sawhney N, Durie CL, Cover TL, Ohi MD, et al. 2020. Cryo-EM reveals species-specific components within the Helicobacter pylori Cag type IV secretion system core complex. ELife 9: e59495.
  47. Sheedlo MJ, Durie CL, Chung JM, Chang L, Roberts J, Swanson M, et al. 2021. Cryo-EM reveals new species-specific proteins and symmetry elements in the Legionella pneumophila Dot/Icm T4SS. ELife 10: e70427.
  48. Hu B, Khara P, Song L, Lin AS, Frick-Cheng AE, Harvey ML, et al. 2019. In situ molecular architecture of the Helicobacter pylori Cag type IV secretion system. mBio 10: e00849-19.
  49. Ghosal D, Chang Y, Jeong KC, Vogel JP, Jensen GJ. 2017. In situ structure of the Legionella Dot/Icm type IV secretion system by electron cryotomography. EMBO Rep. 18: 726-732.
  50. Fischer W. 2011. Assembly and molecular mode of action of the Helicobacter pylori Cag type IV secretion apparatus. FEBS J. 278: 1203-1212.
  51. Lee MH, Yang JY, Cho Y, Woo HJ, Kwon HJ, Kim DH, et al. 2019. Inhibitory effects of menadione on Helicobacter pylori growth and Helicobacter pylori-induced inflammation via NF-κB inhibition. Int. J. Mol. Sci. 20: 1169.
  52. Ghosal D, Jeong KC, Chang Y-W, Gyore J, Teng L, Gardner A, et al. 2019. Molecular architecture, polar targeting and biogenesis of the Legionella Dot/Icm T4SS. Nat. Microbiol. 4: 1173-1182.
  53. Chetrit D, Hu B, Christie PJ, Roy CR, Liu J. 2018. A unique cytoplasmic ATPase complex defines the Legionella pneumophila type IV secretion channel. Nat. Microbiol. 3: 678-686.
  54. Park D, Chetrit D, Hu B, Roy CR, Liu J. 2020. Analysis of Dot/Icm type IVB secretion system subassemblies by cryoelectron tomography reveals conformational changes induced by DotB binding. mBio 11: e03328-19.
  55. Meir A, Mace K, Lukoyanova N, Chetrit D, Hospenthal MK, Redzej A, et al. 2020. Mechanism of effector capture and delivery by the type IV secretion system from Legionella pneumophila. Nat. Commun. 11: 2864.
  56. Buhrdorf R, Forster C, Haas R, Fischer W. 2003. Topological analysis of a putative virB8 homologue essential for the cag type IV secretion system in Helicobacter pylori. Int. J. Med. Microbiol. 293: 213-217.
  57. Liu X, Khara P, Baker ML, Christie PJ, Hu B. 2022. Structure of a type IV secretion system core complex encoded by multi-drug resistance F plasmids. Nat. Commun. 13: 379.
  58. Worrall LJ, Hong C, Vuckovic M, Deng W, Bergeron JRC, Majewski DD, et al. 2016. Near-atomic-resolution cryo-EM analysis of the Salmonella T3S injectisome basal body. Nature 540: 597-601.
  59. Sobti M, Walshe JL, Wu D, Ishmukhametov R, Zeng YC, Robinson CV, et al. 2020. Cryo-EM structures provide insight into how E. coli F1Fo ATP synthase accommodates symmetry mismatch. Nat. Commun. 11: 2615.
  60. Barrozo RM, Cooke CL, Hansen LM, Lam AM, Gaddy JA, Johnson EM, et al. 2013. Functional plasticity in the type IV secretion system of Helicobacter pylori. PLoS Pathog. 9: e1003189.
  61. Chang YW, Shaffer CL, Rettberg LA, Ghosal D, Jensen GJ. 2018. In vivo structures of the Helicobacter pylori cag Type IV secretion system. Cell Rep. 23: 673-681.
  62. Backert S, Selbach M. 2008. Role of type IV secretion in Helicobacter pylori pathogenesis. Cell. Microbiol. 10: 1573-1581.
  63. Bock D, Husler D, Steiner B, Medeiros JM, Welin A, Radomska KA, et al. 2021. The polar Legionella Icm/Dot T4SS establishes distinct contact sites with the pathogen vacuole membrane. mBio 12: e02180-21.
  64. Lai EM, Chesnokova O, Banta LM, Kado CI. 2000. Genetic and environmental factors affecting T-pilin export and T-pilus biogenesis in relation to flagellation of Agrobacterium tumefaciens. J. Bacteriol. 182: 3705-3716.
  65. Li YG, Christie PJ. 2018. The Agrobacterium VirB/VirD4 T4SS: mechanism and architecture defined through in vivo mutagenesis and chimeric systems. Curr. Top. Microbiol. Immunol. 418: 233-260.
  66. Sexton JA, Yeo HJ, Vogel JP. 2005. Genetic analysis of the Legionella pneumophila DotB ATPase reveals a role in type IV secretion system protein export. Mol. Microbiol. 57: 70-84.
  67. Xu J, Xu D, Wan M, Yin L, Wang X, Wu L, et al. 2017. Structural insights into the roles of the IcmS-IcmW complex in the type IVb secretion system of Legionella pneumophila. Proc. Natl. Acad. Sci. USA 114: 13543-13548.
  68. Wallden K, Rivera-Calzada A, Waksman G. 2010. Type IV secretion systems: versatility and diversity in function. Cell. Microbiol. 12: 1203-1212.
  69. Tegtmeyer N, Neddermann M, Lind J, Pachathundikandi SK, Sharafutdinov I, Gutierrez-Escobar AJ, et al. 2020. Toll-like receptor 5 activation by the CagY repeat domains of Helicobacter pylori. Cell Rep. 32: 108159.
  70. Barrozo RM, Hansen LM, Lam AM, Skoog EC, Martin ME, Cai LP, et al. 2016. CagY is an immune-sensitive regulator of the Helicobacter pylori Type IV secretion system. Gastroenterology 151: 1164-1175.e3.
  71. Skoog EC, Morikis VA, Martin ME, Foster GA, Cai LP, Hansen LM, et al. 2018. CagY-dependent regulation of type IV secretion in Helicobacter pylori is associated with alterations in integrin binding. mBio 9: e00717-18.
  72. Terradot L, Waksman G. 2011. Architecture of the Helicobacter pylori Cag-type IV secretion system. FEBS J. 278: 1213-1222.
  73. Viala J, Chaput C, Boneca IG, Cardona A, Girardin SE, Moran AP, et al. 2004. Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat. Immunol. 5: 1166-1174.
  74. Backert S, Meyer TF. 2006. Type IV secretion systems and their effectors in bacterial pathogenesis. Curr. Opin. Microbiol. 9: 207-217.
  75. Kwok T, Zabler D, Urman S, Rohde M, Hartig R, Wessler S, et al. 2007. Helicobacter exploits integrin for type IV secretion and kinase activation. Nature 449: 862-866.