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Staphylococcus aureus SdrE captures complement factor H's C-terminus via a novel 'close, dock, lock and latch' mechanism for complement evasion.

Zhang Y, Wu M, Hang T, Wang C, Yang Y, Pan W, Zang J, Zhang M, Zhang X
Biochem J 474 1619-1631 (2017)
Cited: 25 times
EuropePMC logo PMID: 28258151

Abstract

Complement factor H (CFH) is a soluble complement regulatory protein essential for the down-regulation of the alternative pathway on interaction with specific markers on the host cell surface. It recognizes the complement component 3b (C3b) and 3d (C3d) fragments in addition to self cell markers (i.e. glycosaminoglycans, sialic acid) to distinguish host cells that deserve protection from pathogens that should be eliminated. The Staphylococcus aureus surface protein serine-aspartate repeat protein E (SdrE) was previously reported to bind human CFH as an immune-evasion tactic. However, the molecular mechanism underlying SdrE-CFH-mediated immune evasion remains unknown. In the present study, we identified a novel region at CFH's C-terminus (CFH1206-1226), which binds SdrE N2 and N3 domains (SdrEN2N3) with high affinity, and determined the crystal structures of apo-SdrEN2N3 and the SdrEN2N3-CFH1206-1226 complex. Comparison of the structure of the CFH-SdrE complex with other CFH structures reveals that CFH's C-terminal tail flips from the main body to insert into the ligand-binding groove of SdrE. In addition, SdrEN2N3 adopts a 'close' state in the absence of CFH, which undergoes a large conformational change on CFH binding, suggesting a novel 'close, dock, lock and latch' (CDLL) mechanism for SdrE to recognize its ligand. Our findings imply that SdrE functions as a 'clamp' to capture CFH's C-terminal tail via a unique CDLL mechanism and sequesters CFH on the surface of S. aureus for complement evasion.

Articles - 5wtb mentioned but not cited (4)

  1. Staphylococcus aureus SdrE captures complement factor H's C-terminus via a novel 'close, dock, lock and latch' mechanism for complement evasion. Zhang Y, Wu M, Hang T, Wang C, Yang Y, Pan W, Zang J, Zhang M, Zhang X. Biochem J 474 1619-1631 (2017)
  2. Mechanical Stabilization of a Bacterial Adhesion Complex. Huang W, Le S, Sun Y, Lin DJ, Yao M, Shi Y, Yan J. J Am Chem Soc 144 16808-16818 (2022)
  3. Protein structure prediction in the era of AI: Challenges and limitations when applying to in silico force spectroscopy. Gomes PSFC, Gomes DEB, Bernardi RC. Front Bioinform 2 983306 (2022)
  4. Structural insights into the intermolecular interaction of the adhesin SdrC in the pathogenicity of Staphylococcus aureus. Wang J, Zhang M, Wang M, Zang J, Zhang X, Hang T. Acta Crystallogr F Struct Biol Commun 77 47-53 (2021)


Reviews citing this publication (10)

  1. Pathogenicity and virulence of Staphylococcus aureus. Cheung GYC, Bae JS, Otto M. Virulence 12 547-569 (2021)
  2. Staphylococcal Biofilm Development: Structure, Regulation, and Treatment Strategies. Schilcher K, Horswill AR. Microbiol Mol Biol Rev 84 e00026-19 (2020)
  3. Hijacking Factor H for Complement Immune Evasion. Moore SR, Menon SS, Cortes C, Ferreira VP. Front Immunol 12 602277 (2021)
  4. Staphylococcus aureus host interactions and adaptation. Howden BP, Giulieri SG, Wong Fok Lung T, Baines SL, Sharkey LK, Lee JYH, Hachani A, Monk IR, Stinear TP. Nat Rev Microbiol 21 380-395 (2023)
  5. Searching for the Secret of Stickiness: How Biofilms Adhere to Surfaces. Jiang Z, Nero T, Mukherjee S, Olson R, Yan J. Front Microbiol 12 686793 (2021)
  6. A Review of Biofilm Formation of Staphylococcus aureus and Its Regulation Mechanism. Peng Q, Tang X, Dong W, Sun N, Yuan W. Antibiotics (Basel) 12 12 (2022)
  7. Staphylococcus aureus-A Known Opponent against Host Defense Mechanisms and Vaccine Development-Do We Still Have a Chance to Win? Wójcik-Bojek U, Różalska B, Sadowska B. Int J Mol Sci 23 948 (2022)
  8. Complement Evasion Strategies of Human Pathogenic Bacteria. Sharma S, Bhatnagar R, Gaur D. Indian J Microbiol 60 283-296 (2020)
  9. The Role of Staphylococcal Biofilm on the Surface of Implants in Orthopedic Infection. Lu Y, Cai WJ, Ren Z, Han P. Microorganisms 10 1909 (2022)
  10. A genetic regulatory see-saw of biofilm and virulence in MRSA pathogenesis. Patel H, Rawat S. Front Microbiol 14 1204428 (2023)

Articles citing this publication (11)

  1. Molecular mechanism of extreme mechanostability in a pathogen adhesin. Milles LF, Schulten K, Gaub HE, Bernardi RC. Science 359 1527-1533 (2018)
  2. Sortases, Surface Proteins, and Their Roles in Staphylococcus aureus Disease and Vaccine Development. Schneewind O, Missiakas D. Microbiol Spectr 7 (2019)
  3. Enolase From Aspergillus fumigatus Is a Moonlighting Protein That Binds the Human Plasma Complement Proteins Factor H, FHL-1, C4BP, and Plasminogen. Dasari P, Koleci N, Shopova IA, Wartenberg D, Beyersdorf N, Dietrich S, Sahagún-Ruiz A, Figge MT, Skerka C, Brakhage AA, Zipfel PF. Front Immunol 10 2573 (2019)
  4. Biofilm Formation of Multidrug-Resistant MRSA Strains Isolated from Different Types of Human Infections. Silva V, Almeida L, Gaio V, Cerca N, Manageiro V, Caniça M, Capelo JL, Igrejas G, Poeta P. Pathogens 10 970 (2021)
  5. The N2N3 domains of ClfA, FnbpA and FnbpB in Staphylococcus aureus bind to human complement factor H, and their antibodies enhance the bactericidal capability of human blood. Mao X, Kim J, Zhang Q, Jiang T, Ahn DH, Jung Y, Matsushita M, Bae T, Lee BL. J Biochem 169 543-553 (2021)
  6. Comparative Analysis of Virulence and Toxin Expression of Vancomycin-Intermediate and Vancomycin-Sensitive Staphylococcus aureus Strains. Jin Y, Yu X, Zhang S, Kong X, Chen W, Luo Q, Zheng B, Xiao Y. Front Microbiol 11 596942 (2020)
  7. Interaction of the Staphylococcus aureus Surface Protein FnBPB with Corneodesmosin Involves Two Distinct, Extremely Strong Bonds. Paiva TO, Viljoen A, da Costa TM, Geoghegan JA, Dufrêne YF. ACS Nanosci Au 3 58-66 (2023)
  8. A Factor H-Fc fusion protein increases complement-mediated opsonophagocytosis and killing of community associated methicillin-resistant Staphylococcus aureus. Sage MAG, Cranmer KD, Semeraro ML, Ma S, Galkina EV, Tran Y, Wycoff KL, Sharp JA. PLoS One 17 e0265774 (2022)
  9. Adhesive Virulence Factors of Staphylococcus aureus Resist Digestion by Coagulation Proteases Thrombin and Plasmin. Risser F, López-Morales J, Nash MA. ACS Bio Med Chem Au 2 586-599 (2022)
  10. High-force catch bonds between the Staphylococcus aureus surface protein SdrE and complement regulator factor H drive immune evasion. Paiva TO, Geoghegan JA, Dufrêne YF. Commun Biol 6 302 (2023)
  11. May the force be with you: The role of hyper-mechanostability of the bone sialoprotein binding protein during early stages of Staphylococci infections. Gomes PSFC, Forrester M, Pace M, Gomes DEB, Bernardi RC. Front Chem 11 1107427 (2023)


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