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Structure of the Helicobacter pylori Cag type IV secretion system.

Chung JM, Sheedlo MJ, Campbell AM, Sawhney N, Frick-Cheng AE, Lacy DB, Cover TL, Ohi MD
Elife 8 (2019)
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Cited: 43 times
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Abstract

Bacterial type IV secretion systems (T4SSs) are molecular machines that can mediate interbacterial DNA transfer through conjugation and delivery of effector molecules into host cells. The Helicobacter pylori Cag T4SS translocates CagA, a bacterial oncoprotein, into gastric cells, contributing to gastric cancer pathogenesis. We report the structure of a membrane-spanning Cag T4SS assembly, which we describe as three sub-assemblies: a 14-fold symmetric outer membrane core complex (OMCC), 17-fold symmetric periplasmic ring complex (PRC), and central stalk. Features that differ markedly from those of prototypical T4SSs include an expanded OMCC and unexpected symmetry mismatch between the OMCC and PRC. This structure is one of the largest bacterial secretion system assemblies ever reported and illustrates the remarkable structural diversity that exists among bacterial T4SSs.

Reviews - 6oeg mentioned but not cited (1)

  1. The Helicobacter pylori Cag Type IV Secretion System. Cover TL, Lacy DB, Ohi MD. Trends Microbiol 28 682-695 (2020)

Articles - 6oeg mentioned but not cited (3)

  1. Structure of the Helicobacter pylori Cag type IV secretion system. Chung JM, Sheedlo MJ, Campbell AM, Sawhney N, Frick-Cheng AE, Lacy DB, Cover TL, Ohi MD. Elife 8 e47644 (2019)
  2. Lipoprotein Processing and Sorting in Helicobacter pylori. McClain MS, Voss BJ, Cover TL. mBio 11 e00911-20 (2020)
  3. A Proposal for a Consolidated Structural Model of the CagY Protein of Helicobacter pylori. López-Luis MA, Soriano-Pérez EE, Parada-Fabián JC, Torres J, Maldonado-Rodríguez R, Méndez-Tenorio A. Int J Mol Sci 24 16781 (2023)


Reviews citing this publication (14)

  1. Molecular anatomy and pathogenic actions of Helicobacter pylori CagA that underpin gastric carcinogenesis. Takahashi-Kanemitsu A, Knight CT, Hatakeyama M. Cell Mol Immunol 17 50-63 (2020)
  2. Type IV secretion systems: Advances in structure, function, and activation. Costa TRD, Harb L, Khara P, Zeng L, Hu B, Christie PJ. Mol Microbiol 115 436-452 (2021)
  3. Role of the Gastric Microbiome in Gastric Cancer: From Carcinogenesis to Treatment. Yang J, Zhou X, Liu X, Ling Z, Ji F. Front Microbiol 12 641322 (2021)
  4. Helicobacter pylori Virulence Factor Cytotoxin-Associated Gene A (CagA)-Mediated Gastric Pathogenicity. Ansari S, Yamaoka Y. Int J Mol Sci 21 E7430 (2020)
  5. Four Chromosomal Type IV Secretion Systems in Helicobacter pylori: Composition, Structure and Function. Fischer W, Tegtmeyer N, Stingl K, Backert S. Front Microbiol 11 1592 (2020)
  6. Multifunctional Role of S100 Protein Family in the Immune System: An Update. Singh P, Ali SA. Cells 11 2274 (2022)
  7. Molecular architecture of bacterial type IV secretion systems. Sheedlo MJ, Ohi MD, Lacy DB, Cover TL. PLoS Pathog 18 e1010720 (2022)
  8. Helicobacter pylori Infection, Its Laboratory Diagnosis, and Antimicrobial Resistance: a Perspective of Clinical Relevance. Ansari S, Yamaoka Y. Clin Microbiol Rev 35 e0025821 (2022)
  9. Secretion of Pertussis Toxin from Bordetella pertussis. Burns DL. Toxins (Basel) 13 574 (2021)
  10. Structural and functional diversity of type IV secretion systems. Costa TRD, Patkowski JB, Macé K, Christie PJ, Waksman G. Nat Rev Microbiol 22 170-185 (2024)
  11. Targeting bacterial pathogenesis by inhibiting virulence-associated Type III and Type IV secretion systems. Blasey N, Rehrmann D, Riebisch AK, Mühlen S. Front Cell Infect Microbiol 12 1065561 (2022)
  12. DNA Transport through the Dynamic Type IV Secretion System. Ryan ME, Damke PP, Shaffer CL. Infect Immun 91 e0043622 (2023)
  13. Comparative Analysis of T4SS Molecular Architectures. Zehra M, Heo J, Chung JM, Durie CL. J Microbiol Biotechnol 33 1543-1551 (2023)
  14. Primary architecture and energy requirements of Type III and Type IV secretion systems. Cabezón E, Valenzuela-Gómez F, Arechaga I. Front Cell Infect Microbiol 13 1255852 (2023)

Articles citing this publication (25)

  1. Structural analysis of the Legionella pneumophila Dot/Icm type IV secretion system core complex. Durie CL, Sheedlo MJ, Chung JM, Byrne BG, Su M, Knight T, Swanson M, Lacy DB, Ohi MD. Elife 9 e59530 (2020)
  2. Analysis of Dot/Icm Type IVB Secretion System Subassemblies by Cryoelectron Tomography Reveals Conformational Changes Induced by DotB Binding. Park D, Chetrit D, Hu B, Roy CR, Liu J. mBio 11 e03328-19 (2020)
  3. Cryo-EM reveals species-specific components within the Helicobacter pylori Cag type IV secretion system core complex. Sheedlo MJ, Chung JM, Sawhney N, Durie CL, Cover TL, Ohi MD, Lacy DB. Elife 9 e59495 (2020)
  4. Bacterial Energetic Requirements for Helicobacter pylori Cag Type IV Secretion System-Dependent Alterations in Gastric Epithelial Cells. Lin AS, Dooyema SDR, Frick-Cheng AE, Harvey ML, Suarez G, Loh JT, McDonald WH, McClain MS, Peek RM, Cover TL. Infect Immun 88 e00790-19 (2020)
  5. Cryo-EM reveals new species-specific proteins and symmetry elements in the Legionella pneumophila Dot/Icm T4SS. Sheedlo MJ, Durie CL, Chung JM, Chang L, Roberts J, Swanson M, Lacy DB, Ohi MD. Elife 10 e70427 (2021)
  6. Structure of a type IV secretion system core complex encoded by multi-drug resistance F plasmids. Liu X, Khara P, Baker ML, Christie PJ, Hu B. Nat Commun 13 379 (2022)
  7. In Situ Visualization of the pKM101-Encoded Type IV Secretion System Reveals a Highly Symmetric ATPase Energy Center. Khara P, Song L, Christie PJ, Hu B. mBio 12 e0246521 (2021)
  8. Evodiamine Inhibits Helicobacter pylori Growth and Helicobacter pylori-Induced Inflammation. Yang JY, Kim JB, Lee P, Kim SH. Int J Mol Sci 22 3385 (2021)
  9. Architecture of the outer-membrane core complex from a conjugative type IV secretion system. Amin H, Ilangovan A, Costa TRD. Nat Commun 12 6834 (2021)
  10. Bactericidal type IV secretion system homeostasis in Xanthomonas citri. Cenens W, Andrade MO, Llontop E, Alvarez-Martinez CE, Sgro GG, Farah CS. PLoS Pathog 16 e1008561 (2020)
  11. Temporal Control of the Helicobacter pylori Cag Type IV Secretion System in a Mongolian Gerbil Model of Gastric Carcinogenesis. Lin AS, McClain MS, Beckett AC, Caston RR, Harvey ML, Dixon BREA, Campbell AM, Shuman JHB, Sawhney N, Delgado AG, Loh JT, Piazuelo MB, Algood HMS, Cover TL. mBio 11 e01296-20 (2020)
  12. Inhibition of Type IV Secretion Activity and Growth of Helicobacter pylori by Cisplatin and Other Platinum Complexes. Lettl C, Schindele F, Testolin G, Bär A, Rehm T, Brönstrup M, Schobert R, Bilitewski U, Haas R, Fischer W. Front Cell Infect Microbiol 10 602958 (2020)
  13. Structural basis for effector recognition by an antibacterial type IV secretion system. Oka GU, Souza DP, Cenens W, Matsuyama BY, Cardoso MVC, Oliveira LC, da Silva Lima F, Cuccovia IM, Guzzo CR, Salinas RK, Farah CS. Proc Natl Acad Sci U S A 119 e2112529119 (2022)
  14. Electrostatic Switching Controls Channel Dynamics of the Sensor Protein VirB10 in A. tumefaciens Type IV Secretion System. Darbari VC, Ciccone J, Patel JS, Islam B, Agarwal PK, Haider S. ACS Omega 5 3271-3281 (2020)
  15. Type IV secretion of Helicobacter pylori CagA into oral epithelial cells is prevented by the absence of CEACAM receptor expression. Tegtmeyer N, Ghete TD, Schmitt V, Remmerbach T, Cortes MCC, Bondoc EM, Graf HL, Singer BB, Hirsch C, Backert S. Gut Pathog 12 25 (2020)
  16. Bacterial injection machines: Evolutionary diverse but functionally convergent. Bleves S, Galán JE, Llosa M. Cell Microbiol 22 e13157 (2020)
  17. Identification of Pathogenicity Island Genes Associated with Loss of Type IV Secretion Function during Murine Infection with Helicobacter pylori. Hansen LM, Dekalb DJ, Cai LP, Solnick JV. Infect Immun 88 e00801-19 (2020)
  18. Identification of an Essential LolD-Like Protein in Helicobacter pylori. McClain MS, Bryant KN, McDonald WH, Algood HMS, Cover TL. J Bacteriol 205 e0005223 (2023)
  19. Unique TLR9 Activation by Helicobacter pylori Depends on the cag T4SS, But Not on VirD2 Relaxases or VirD4 Coupling Proteins. Tegtmeyer N, Linz B, Yamaoka Y, Backert S. Curr Microbiol 79 121 (2022)
  20. A Comprehensive Phenotypic Screening Strategy to Identify Modulators of Cargo Translocation by the Bacterial Type IVB Secretion System. Cheng E, Dorjsuren D, Lehman S, Larson CL, Titus SA, Sun H, Zakharov A, Rai G, Heinzen RA, Simeonov A, Machner MP. mBio 13 e0024022 (2022)
  21. Mouse Gastric Epithelial Cells Resist CagA Delivery by the Helicobacter pylori Type IV Secretion System. Shrestha R, Murata-Kamiya N, Imai S, Yamamoto M, Tsukamoto T, Nomura S, Hatakeyama M. Int J Mol Sci 23 2492 (2022)
  22. Role of the CagY antenna projection in Helicobacter pylori Cag type IV secretion system activity. Tran SC, McClain MS, Cover TL. Infect Immun 91 e0015023 (2023)
  23. Tracking bacterial effector protein delivery into host cells. Cover TL. Mol Microbiol 116 724-728 (2021)
  24. Designed Ankyrin Repeat Proteins provide insights into the structure and function of CagI and are potent inhibitors of CagA translocation by the Helicobacter pylori type IV secretion system. Blanc M, Lettl C, Guérin J, Vieille A, Furler S, Briand-Schumacher S, Dreier B, Bergé C, Plückthun A, Vadon-Le Goff S, Fronzes R, Rousselle P, Fischer W, Terradot L. PLoS Pathog 19 e1011368 (2023)
  25. Remodeling of the gastric environment in Helicobacter pylori-induced atrophic gastritis. Shuman JHB, Lin AS, Westland MD, Bryant KN, Piazuelo MB, Reyzer ML, Judd AM, McDonald WH, McClain MS, Schey KL, Algood HMS, Cover TL. mSystems 9 e0109823 (2024)


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