1887

Journal of General Virology header logo

Volume 88, Issue 11

Species B adenovirus serotypes 3, 7, 11 and 35 share similar binding sites on the membrane cofactor protein CD46 receptor Free

Abstract

We recently characterized the domains of the human cofactor protein CD46 involved in binding species B2 adenovirus (Ad) serotype 35. Here, the CD46 binding determinants are mapped for the species B1 Ad serotypes 3 and 7 and for the species B2 Ad11. Ad3, 7 and 11 bound and transduced CD46-positive rodent BHK cells at levels similar to Ad35. By using antibody-blocking experiments, hybrid CD46–CD4 receptor constructs and CD46 single point mutants, it is shown that Ad3, 7 and 11 share many of the Ad35-binding features on CD46. Both CD46 short consensus repeat domains SCR I and SCR II were necessary and sufficient for optimal binding and transgene expression, provided that they were positioned at an appropriate distance from the cell membrane. Similar to Ad35, most of the putative binding residues of Ad3, 7 and 11 were located on the same glycan-free, solvent-exposed face of the SCR I or SCR II domains, largely overlapping with the binding surface of the recently solved fiber knob Ad11–SCR I–II three-dimensional structure. Differences between species B1 and B2 Ads were documented with competition experiments based on anti-CD46 antibodies directed against epitopes flanking the putative Ad-binding sites, and with competition experiments based on soluble CD46 protein. It is concluded that the B1 and B2 species of Ad engage CD46 through similar binding surfaces.

  • Received:
  • Accepted:
  • Published Online:
SGM
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.83142-0
2007-11-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/jgv/88/11/2925.html?itemId=/content/journal/jgv/10.1099/vir.0.83142-0&mimeType=html&fmt=ahah

References

  1. Benkő M., Harrach B., Russell W. C. 2000; Family Adenoviridae . In Virus Taxonomy: Seventh Report of the International Committee on Taxonomy of Viruses . pp 227–238 Edited by van Regenmortel M. H. V., Fauquet C. M., Bishop D. H. L., Carstens E. B., Estes M. K., Lemon S. M., Maniloff J., Mayo M. A., McGeoch D. J., Pringle C. R., Wickner E. B. San Diego, CA: Academic Press;
  2. Bergelson J. M., Cunningham J. A., Droguett G., Kurt-Jones E. A., Krithivas A., Hong J. S., Horwitz M. S., Crowell R. L., Finberg R. W. 1997; Isolation of a common receptor for coxsackie B viruses and adenoviruses 2 and 5. Science 275:1320–1323 [CrossRef]
     [Google Scholar]
  3. Bork P., Downing A. K., Kieffer B., Campbell I. D. 1996; Structure and distribution of modules in extracellular proteins. Q Rev Biophys 29:119–167 [CrossRef]
     [Google Scholar]
  4. Buchholz C. J., Schneider U., Devaux P., Gerlier D., Cattaneo R. 1996; Cell entry by measles virus: long hybrid receptors uncouple binding from membrane fusion. J Virol 70:3716–3723
     [Google Scholar]
  5. Buchholz C. J., Koller D., Devaux P., Mumenthaler C., Schneider-Schaulies J., Braun W., Gerlier D., Cattaneo R. 1997; Mapping of the primary binding site of measles virus to its receptor CD46. J Biol Chem 272:22072–22079 [CrossRef]
     [Google Scholar]
  6. Casasnovas J. M., Larvie M., Stehle T. 1999; Crystal structure of two CD46 domains reveals an extended measles virus-binding surface. EMBO J 18:2911–2922 [CrossRef]
     [Google Scholar]
  7. Cattaneo R. 2004; Four viruses, two bacteria and one receptor: membrane cofactor protein (CD46) as pathogens' magnet. J Virol 78:4385–4388 [CrossRef]
     [Google Scholar]
  8. Chroboczek J., Ruigrok R. W. H., Cusack S. 1995; Adenovirus fiber. In The Molecular Repertoire of Adenoviruses , part I. pp 163–200 Edited by Doerfler W., Böhm P. Berlin: Springer;
  9. Defer C., Belin M. T., Caillet-Boudin M. L., Boulanger P. 1990; Human adenovirus-host cell interactions: comparative study with members of subgroups B and C. J Virol 64:3661–3673
     [Google Scholar]
  10. Devaux P., Buchholz C. J., Schneider U., Escoffier C., Cattaneo R., Gerlier D. 1997; CD46 short consensus repeats III and IV enhance measles virus binding but impair soluble hemagglutinin binding. J Virol 71:4157–4160
     [Google Scholar]
  11. Ebbinghaus C., Al-Jaibaji A., Operschall E., Schoffel A., Peter I., Greber U. F., Hemmi S. 2001; Functional and selective targeting of adenovirus to high-affinity Fc γ receptor I-positive cells by using a bispecific hybrid adapter. J Virol 75:480–489 [CrossRef]
     [Google Scholar]
  12. Fleischli C., Verhaagh S., Havenga M., Sirena D., Schaffner W., Cattaneo R., Greber U. F., Hemmi S. 2005; The distal short consensus repeats 1 and 2 of the membrane cofactor protein CD46 and their distance from the cell membrane determine productive entry of species B adenovirus serotype 35. J Virol 79:10013–10022 [CrossRef]
     [Google Scholar]
  13. Fuerst T. R., Niles E. G., Studier F. W., Moss B. 1986; Eukaryotic transient-expression system based on recombinant vaccinia virus that synthesizes bacteriophage T7 RNA polymerase. Proc Natl Acad Sci U S A 83:8122–8126 [CrossRef]
     [Google Scholar]
  14. Gaggar A., Shayakhmetov D. M., Lieber A. 2003; CD46 is a cellular receptor for group B adenoviruses. Nat Med 9:1408–1412 [CrossRef]
     [Google Scholar]
  15. Gaggar A., Shayakhmetov D. M., Liszewski M. K., Atkinson J. P., Lieber A. 2005; Localization of regions in CD46 that interact with adenovirus. J Virol 79:7503–7513 [CrossRef]
     [Google Scholar]
  16. Gustafsson D. J., Segerman A., Lindman K., Mei Y. F., Wadell G. 2006; The Arg279Gln substitution in the adenovirus type 11p (Ad11p) fiber knob abolishes EDTA-resistant binding to A549 and CHO-CD46 cells, converting the phenotype to that of Ad7p. J Virol 80:1897–1905 [CrossRef]
     [Google Scholar]
  17. Holterman L., Vogels R., van der Vlugt R., Sieuwerts M., Grimbergen J., Kaspers J., Geelen E., van der Helm E., Lemckert A. other authors 2004; Novel replication-incompetent vector derived from adenovirus type 11 (Ad11) for vaccination and gene therapy: low seroprevalence and non-cross-reactivity with Ad5. J Virol 78:13207–13215 [CrossRef]
     [Google Scholar]
  18. Horwitz M. S. 2001; Adenoviruses. In Fields Virology . , 4th edn. pp 2301–2326 Edited by Knipe D. M., Howley P. M. Philadelphia, PA: Lippincott Williams & Wilkins;
  19. Koradi R., Billeter M., Wuthrich K. 1996; molmol: a program for display and analysis of macromolecular structures. J Mol Graph 14:51–55 [CrossRef]
     [Google Scholar]
  20. Law L. K., Davidson B. L. 2005; What does it take to bind CAR?. Mol Ther 12:599–609 [CrossRef]
     [Google Scholar]
  21. Leen A. M., Rooney C. M. 2005; Adenovirus as an emerging pathogen in immunocompromised patients. Br J Haematol 128:135–144 [CrossRef]
     [Google Scholar]
  22. Lemckert A. A., Grimbergen J., Smits S., Hartkoorn E., Holterman L., Berkhout B., Barouch D. H., Vogels R., Quax P. other authors 2006; Generation of a novel replication-incompetent adenoviral vector derived from human adenovirus type 49: manufacture on PER.C6 cells, tropism and immunogenicity. J Gen Virol 87:2891–2899 [CrossRef]
     [Google Scholar]
  23. Liszewski M. K., Post T. W., Atkinson J. P. 1991; Membrane cofactor protein (MCP or CD46): newest member of the regulators of complement activation gene cluster. Annu Rev Immunol 9:431–455 [CrossRef]
     [Google Scholar]
  24. Liszewski M. K., Leung M., Cui W., Subramanian V. B., Parkinson J., Barlow P. N., Manchester M., Atkinson J. P. 2000; Dissecting sites important for complement regulatory activity in membrane cofactor protein (MCP; CD46). J Biol Chem 275:37692–37701 [CrossRef]
     [Google Scholar]
  25. Maizel J. V. Jr, White D. O., Scharff M. D. 1968; The polypeptides of adenovirus. I. Evidence for multiple protein components in the virion and a comparison of types 2, 7A, and 12. Virology 36:115–125 [CrossRef]
     [Google Scholar]
  26. Manchester M., Gairin J. E., Patterson J. B., Alvarez J., Liszewski M. K., Eto D. S., Atkinson J. P., Oldstone M. B. 1997; Measles virus recognizes its receptor, CD46, via two distinct binding domains within SCR1-2. Virology 233:174–184 [CrossRef]
     [Google Scholar]
  27. Marttila M., Persson D., Gustafsson D., Liszewski M. K., Atkinson J. P., Wadell G., Arnberg N. 2005; CD46 is a cellular receptor for all species B adenoviruses except types 3 and 7. J Virol 79:14429–14436 [CrossRef]
     [Google Scholar]
  28. Meier O., Gastaldelli M., Boucke K., Hemmi S., Greber U. F. 2005; Early steps of clathrin-mediated endocytosis involved in phagosomal escape of Fc γ receptor-targeted adenovirus. J Virol 79:2604–2613 [CrossRef]
     [Google Scholar]
  29. Mumenthaler C., Schneider U., Buchholz C. J., Koller D., Braun W., Cattaneo R. 1997; A 3D model for the measles virus receptor CD46 based on homology modeling, Monte Carlo simulations, and hemagglutinin binding studies. Protein Sci 6:588–597
     [Google Scholar]
  30. Nagel H., Maag S., Tassis A., Nestle F. O., Greber U. F., Hemmi S. 2003; The α v β 5 integrin of hematopoietic and nonhematopoietic cells is a transduction receptor of RGD-4C fiber-modified adenoviruses. Gene Ther 10:1643–1653 [CrossRef]
     [Google Scholar]
  31. Persson B. D., Reiter D. M., Marttila M., Mei Y. F., Casasnovas J. M., Arnberg N., Stehle T. 2007; Adenovirus type 11 binding alters the conformation of its receptor CD46. Nat Struct Mol Biol 14:164–166 [CrossRef]
     [Google Scholar]
  32. Roelvink P. W., Lizonova A., Lee J. G., Li Y., Bergelson J. M., Finberg R. W., Brough D. E., Kovesdi I., Wickham T. J. 1998; The coxsackievirus-adenovirus receptor protein can function as a cellular attachment protein for adenovirus serotypes from subgroups A, C, D, E, and F. J Virol 72:7909–7915
     [Google Scholar]
  33. Sakurai F., Murakami S., Kawabata K., Okada N., Yamamoto A., Seya T., Hayakawa T., Mizuguchi H. 2006; The short consensus repeats 1 and 2, not the cytoplasmic domain, of human CD46 are crucial for infection of subgroup B adenovirus serotype 35. J Control Release 113:271–278 [CrossRef]
     [Google Scholar]
  34. Schmitz H., Wigand R., Heinrich W. 1983; Worldwide epidemiology of human adenovirus infections. Am J Epidemiol 117:455–466
     [Google Scholar]
  35. Segerman A., Arnberg N., Erikson A., Lindman K., Wadell G. 2003a; There are two different species B adenovirus receptors: sBAR, common to species B1 and B2 adenoviruses, and sB2AR, exclusively used by species B2 adenoviruses. J Virol 77:1157–1162 [CrossRef]
     [Google Scholar]
  36. Segerman A., Atkinson J. P., Marttila M., Dennerquist V., Wadell G., Arnberg N. 2003b; Adenovirus type 11 uses CD46 as a cellular receptor. J Virol 77:9183–9191 [CrossRef]
     [Google Scholar]
  37. Sirena D., Lilienfeld B., Eisenhut M., Kalin S., Boucke K., Beerli R. R., Vogt L., Ruedl C., Bachmann M. F. other authors 2004; The human membrane cofactor CD46 is a receptor for species B adenovirus serotype 3. J Virol 78:4454–4462 [CrossRef]
     [Google Scholar]
  38. Sirena D., Ruzsics Z., Schaffner W., Greber U. F., Hemmi S. 2005; The nucleotide sequence and a first generation gene transfer vector of species B human adenovirus serotype 3. Virology 343:283–298 [CrossRef]
     [Google Scholar]
  39. Stevenson S. C., Rollence M., White B., Weaver L., McClelland A. 1995; Human adenovirus serotypes 3 and 5 bind to two different cellular receptors via the fiber head domain. J Virol 69:2850–2857
     [Google Scholar]
  40. Tuve S., Wang H., Ware C., Liu Y., Gaggar A., Bernt K., Shayakhmetov D., Li Z., Strauss R. other authors 2006; A new group B adenovirus receptor is expressed at high levels on human stem and tumor cells. J Virol 80:12109–12120 [CrossRef]
     [Google Scholar]
  41. Wadell G. 2000; Adenoviruses. In Principles and Practice of Clinical Virology . , 4th edn. pp 307–327 Edited by Zuckerman A. J., Banatvala J. E., Pattison J. R. Chichester, UK: Wiley;
  42. Warming S., Costantino N., Court D. L., Jenkins N. A., Copeland N. G. 2005; Simple and highly efficient BAC recombineering using galK selection. Nucleic Acids Res 33:e36 [CrossRef]
     [Google Scholar]
  43. Wu E., Trauger S. A., Pache L., Mullen T. M., von Seggern D. J., Siuzdak G., Nemerow G. R. 2004; Membrane cofactor protein is a receptor for adenoviruses associated with epidemic keratoconjunctivitis. J Virol 78:3897–3905 [CrossRef]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.83142-0
Loading
Species B adenovirus serotypes 3, 7, 11 and 35 share similar binding sites on the membrane cofactor protein CD46 receptor
J. Gen. Virol. 88, 2925 (2007); https://doi.org/10.1099/vir.0.83142-0
/content/journal/jgv/10.1099/vir.0.83142-0
/content/journal/jgv/10.1099/vir.0.83142-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

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