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An arginine switch in the species B adenovirus knob determines high-affinity engagement of cellular receptor CD46.

Persson BD, Müller S, Reiter DM, Schmitt BB, Marttila M, Sumowski CV, Schweizer S, Scheu U, Ochsenfeld C, Arnberg N, Stehle T
J Virol 83 673-86 (2009)
Related entries: 3exw, 3f0y

Cited: 39 times
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Abstract

Adenoviruses (Ads) are icosahedral, nonenveloped viruses with a double-stranded DNA genome. The 51 known Ad serotypes exhibit profound variations in cell tropism and disease types. The number of observed Ad infections is steadily increasing, sometimes leading to fatal outcomes even in healthy individuals. Species B Ads can cause kidney infections, hemorrhagic cystitis, and severe respiratory infections, and most of them use the membrane cofactor protein CD46 as a cellular receptor. The crystal structure of the human Ad type 11 (Ad11) knob complexed with CD46 is known; however, the determinants of CD46 binding in related species B Ads remain unclear. We report here a structural and functional analysis of the Ad11 knob, as well as the Ad7 and Ad14 knobs, which are closely related in sequence to the Ad11 knob but have altered CD46-binding properties. The comparison of the structures of the three knobs, which we determined at very high resolution, provides a platform for understanding these differences and allows us to propose a mechanism for productive high-affinity engagement of CD46. At the center of this mechanism is an Ad knob arginine that needs to switch its orientation in order to engage CD46 with high affinity. Quantum chemical calculations showed that the CD46-binding affinity of Ad11 is significantly higher than that of Ad7. Thus, while Ad7 and Ad14 also bind CD46, the affinity and kinetics of these interactions suggest that these Ads are unlikely to use CD46 productively. The proposed mechanism is likely to determine the receptor usage of all CD46-binding Ads.

Articles - 3exv mentioned but not cited (4)

  1. An arginine switch in the species B adenovirus knob determines high-affinity engagement of cellular receptor CD46. Persson BD, Müller S, Reiter DM, Schmitt BB, Marttila M, Sumowski CV, Schweizer S, Scheu U, Ochsenfeld C, Arnberg N, Stehle T. J Virol 83 673-686 (2009)
  2. Human species D adenovirus hexon capsid protein mediates cell entry through a direct interaction with CD46. Persson BD, John L, Rafie K, Strebl M, Frängsmyr L, Ballmann MZ, Mindler K, Havenga M, Lemckert A, Stehle T, Carlson LA, Arnberg N. Proc Natl Acad Sci U S A 118 e2020732118 (2021)
  3. CryoEM structure of adenovirus type 3 fibre with desmoglein 2 shows an unusual mode of receptor engagement. Vassal-Stermann E, Effantin G, Zubieta C, Burmeister W, Iseni F, Wang H, Lieber A, Schoehn G, Fender P. Nat Commun 10 1181 (2019)
  4. Broadly neutralizing monoclonal antibodies against human adenovirus types 55, 14p, 7, and 11 generated with recombinant type 11 fiber knob. Tian X, Fan Y, Liu Z, Zhang L, Liao J, Zhou Z, Li X, Liu T, Liu W, Qiu H, Zhou R. Emerg Microbes Infect 7 206 (2018)


Reviews citing this publication (8)

  1. Latest insights on adenovirus structure and assembly. San Martín C. Viruses 4 847-877 (2012)
  2. Human adenovirus binding to host cell receptors: a structural view. Stasiak AC, Stehle T. Med Microbiol Immunol 209 325-333 (2020)
  3. A comparative review of viral entry and attachment during large and giant dsDNA virus infections. Sobhy H. Arch Virol 162 3567-3585 (2017)
  4. An adenovirus traffic update: from receptor engagement to the nuclear pore. Henaff D, Salinas S, Kremer EJ. Future Microbiol 6 179-192 (2011)
  5. Glycomics and Proteomics Approaches to Investigate Early Adenovirus-Host Cell Interactions. Lasswitz L, Chandra N, Arnberg N, Gerold G. J Mol Biol 430 1863-1882 (2018)
  6. Specificity switching in virus-receptor complexes. Stehle T, Casasnovas JM. Curr Opin Struct Biol 19 181-188 (2009)
  7. Adenovirus entry: Stability, uncoating, and nuclear import. Greber UF, Suomalainen M. Mol Microbiol 118 309-320 (2022)
  8. [Significance of quantum chemical interactions for medicinal science and design of β-secretase inhibitors]. Hamada Y. Yakugaku Zasshi 133 1113-1120 (2013)

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  1. Desmoglein 2 is a receptor for adenovirus serotypes 3, 7, 11 and 14. Wang H, Li ZY, Liu Y, Persson J, Beyer I, Möller T, Koyuncu D, Drescher MR, Strauss R, Zhang XB, Wahl JK, Urban N, Drescher C, Hemminki A, Fender P, Lieber A. Nat Med 17 96-104 (2011)
  2. Macropinocytotic uptake and infection of human epithelial cells with species B2 adenovirus type 35. Kälin S, Amstutz B, Gastaldelli M, Wolfrum N, Boucke K, Havenga M, DiGennaro F, Liska N, Hemmi S, Greber UF. J Virol 84 5336-5350 (2010)
  3. Structural basis and specificity of acetylated transcription factor GATA1 recognition by BET family bromodomain protein Brd3. Gamsjaeger R, Webb SR, Lamonica JM, Billin A, Blobel GA, Mackay JP. Mol Cell Biol 31 2632-2640 (2011)
  4. Structure of the extracellular portion of CD46 provides insights into its interactions with complement proteins and pathogens. Persson BD, Schmitz NB, Santiago C, Zocher G, Larvie M, Scheu U, Casasnovas JM, Stehle T. PLoS Pathog 6 e1001122 (2010)
  5. Avidity binding of human adenovirus serotypes 3 and 7 to the membrane cofactor CD46 triggers infection. Trinh HV, Lesage G, Chennamparampil V, Vollenweider B, Burckhardt CJ, Schauer S, Havenga M, Greber UF, Hemmi S. J Virol 86 1623-1637 (2012)
  6. A structure-guided mutation in the major capsid protein retargets BK polyomavirus. Neu U, Allen SA, Blaum BS, Liu Y, Frank M, Palma AS, Ströh LJ, Feizi T, Peters T, Atwood WJ, Stehle T. PLoS Pathog 9 e1003688 (2013)
  7. Congress Survey of the 2009 commercial optical biosensor literature. Rich RL, Myszka DG. J Mol Recognit 24 892-914 (2011)
  8. Human adenovirus 52 uses sialic acid-containing glycoproteins and the coxsackie and adenovirus receptor for binding to target cells. Lenman A, Liaci AM, Liu Y, Årdahl C, Rajan A, Nilsson E, Bradford W, Kaeshammer L, Jones MS, Frängsmyr L, Feizi T, Stehle T, Arnberg N. PLoS Pathog 11 e1004657 (2015)
  9. Infection and killing of multiple myeloma by adenoviruses. Senac JS, Doronin K, Russell SJ, Jelinek DF, Greipp PR, Barry MA. Hum Gene Ther 21 179-190 (2010)
  10. Structure of the HCMV UL16-MICB complex elucidates select binding of a viral immunoevasin to diverse NKG2D ligands. Müller S, Zocher G, Steinle A, Stehle T. PLoS Pathog 6 e1000723 (2010)
  11. Structure of adenovirus type 21 knob in complex with CD46 reveals key differences in receptor contacts among species B adenoviruses. Cupelli K, Müller S, Persson BD, Jost M, Arnberg N, Stehle T. J Virol 84 3189-3200 (2010)
  12. The crystal structure of dynein intermediate chain-light chain roadblock complex gives new insights into dynein assembly. Hall J, Song Y, Karplus PA, Barbar E. J Biol Chem 285 22566-22575 (2010)
  13. Structural basis for catalytic activation of a serine recombinase. Keenholtz RA, Rowland SJ, Boocock MR, Stark WM, Rice PA. Structure 19 799-809 (2011)
  14. Enteric Species F Human Adenoviruses use Laminin-Binding Integrins as Co-Receptors for Infection of Ht-29 Cells. Rajan A, Persson BD, Frängsmyr L, Olofsson A, Sandblad L, Heino J, Takada Y, Mould AP, Schnapp LM, Gall J, Arnberg N. Sci Rep 8 10019 (2018)
  15. The Reorientation of T-Cell Polarity and Inhibition of Immunological Synapse Formation by CD46 Involves Its Recruitment to Lipid Rafts. Ludford-Menting MJ, Crimeen-Irwin B, Oliaro J, Pasam A, Williamson D, Pedersen N, Guillaumot P, Christansen D, Manie S, Gaus K, Russell SM. J Lipids 2011 521863 (2011)
  16. Human Desmoglein-2 and Human CD46 Mediate Human Adenovirus Type 55 Infection, but Human Desmoglein-2 Plays the Major Roles. Feng Y, Yi C, Liu X, Qu L, Su W, Shu T, Zheng X, Ye X, Luo J, Hao M, Sun X, Li L, Liu X, Yang C, Guan S, Chen L, Feng L. J Virol 94 e00747-20 (2020)
  17. Native and engineered tropism of vectors derived from a rare species D adenovirus serotype 43. Belousova N, Mikheeva G, Xiong C, Stagg LJ, Gagea M, Fox PS, Bassett RL, Ladbury JE, Braun MB, Stehle T, Li C, Krasnykh V. Oncotarget 7 53414-53429 (2016)
  18. Quantum-chemical and combined quantum-chemical/molecular-mechanical studies on the stabilization of a twin arginine pair in adenovirus Ad11. Sumowski CV, Schmitt BB, Schweizer S, Ochsenfeld C. Angew Chem Int Ed Engl 49 9951-9955 (2010)
  19. Utilization of Multi-Immunization and Multiple Selection Strategies for Isolation of Hapten-Specific Antibodies from Recombinant Antibody Phage Display Libraries. Tullila A, Nevanen TK. Int J Mol Sci 18 E1169 (2017)
  20. Ex Vivo and In Vivo CD46 Receptor Utilization by Species D Human Adenovirus Serotype 26 (HAdV26). Hemsath JR, Liaci AM, Rubin JD, Parrett BJ, Lu SC, Nguyen TV, Turner MA, Chen CY, Cupelli K, Reddy VS, Stehle T, Liszewski MK, Atkinson JP, Barry MA. J Virol 96 e0082621 (2022)
  21. Lactoferrin-Hexon Interactions Mediate CAR-Independent Adenovirus Infection of Human Respiratory Cells. Persson BD, Lenman A, Frängsmyr L, Schmid M, Ahlm C, Plückthun A, Jenssen H, Arnberg N. J Virol 94 e00542-20 (2020)
  22. Binding Mechanism Elucidation of the Acute Respiratory Disease Causing Agent Adenovirus of Serotype 7 to Desmoglein-2. Hograindleur MA, Effantin G, Fenel D, Mas C, Lieber A, Schoehn G, Fender P, Vassal-Stermann E. Viruses 12 E1075 (2020)
  23. A novel bladder cancer - specific oncolytic adenovirus by CD46 and its effect combined with cisplatin against cancer cells of CAR negative expression. Cao W, Tian J, Li C, Gao Y, Liu X, Lu J, Wang Y, Wang Z, Svatek RS, Rodriguez R. Virol J 14 149 (2017)
  24. Adenovirus interactions with CD46 on transgenic mouse erythrocytes. Andersson EK, Mei YF, Wadell G. Virology 402 20-25 (2010)
  25. Electrostatic Interactions between Complement Regulator CD46(SCR1-2) and Adenovirus Ad11/Ad21 Fiber Protein Knob. Chen CZ, Gorham RD, Gaieb Z, Morikis D. Mol Biol Int 2015 967465 (2015)
  26. Immunological Study of Reconstructed Common Ancestral Sequence of Adenovirus Hexon Protein. Wang Y, Zhang Z, Shang L, Gao H, Du X, Li F, Gao Y, Qi G, Guo W, Qu Z, Dong T. Front Microbiol 12 717047 (2021)
  27. Toward the understanding of DSG2 and CD46 interaction with HAdV-11 fiber, a super-complex analysis. Effantin G, Hograindleur M-A, Fenel D, Fender P, Vassal-Stermann E. J Virol 97 e0091023 (2023)


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