Coagulation factors IX and X enhance binding and infection of adenovirus types 5 and 31 in human epithelial cells

Journal of Virology

Volumn 83, Issue 8, 2009, Pages 3816-3825

  Jonsson, Mari I ^a   Lenman, Annasara E ^a   Frängsmyr, Lars ^a   Nyberg, Cecilia ^a   Abdullahi, Mohamed ^a   Arnberg, Niklas ^a  

^a UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; BLOOD CLOTTING FACTOR 10; BLOOD CLOTTING FACTOR 9; HEPARAN SULFATE; HEPARIN; HEPARIN LYASE;

ADENOVIRUS; ADENOVIRUS 31; ADENOVIRUS 5; ADENOVIRUS INFECTION; ARTICLE; CIRCULATION; CONTROLLED STUDY; EPITHELIUM CELL; HUMAN; HUMAN CELL; LACRIMAL FLUID; LIVER; PLASMA; PRIMARY INFECTION; PRIORITY JOURNAL; SALIVA; SEROTYPE; TARGET CELL; VIRION; VIRUS ATTACHMENT; WILD TYPE; CLASSIFICATION; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE; VIROLOGY; VIRUS ENTRY;

ADENOVIRIDAE; HUMAN ADENOVIRUS TYPE 5;

ADENOVIRIDAE; CELL LINE, TUMOR; EPITHELIAL CELLS; FACTOR IX; FACTOR X; HUMANS; PLASMA; SALIVA; TEARS; VIRUS ATTACHMENT; VIRUS INTERNALIZATION;

EID: 64049086816     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02562-08     Document Type: Article

References (52)

1. Araki-Sasaki, K., K. Y. Ohasi, T. Sasabe, K. Hayashi, H. Watanabe, Y. Tano, and H. Handa. 1995. An SV-40-immortalized human corneal epithelial cell line and its characterization. Investig. Ophthalmol. 36:614-621.
2. Arnberg, N., K. Edlund, A. H. Kidd, and G. Wadell. 2000. Adenovirus type 37 uses sialic acid as a cellular receptor. J. Virol. 74:42-48. (Pubitemid 30002881)
3. v integrins. J. Virol. 74:7691-7693.
4. Arnberg, N., P. Pring-Akerblom, and G. Wadell. 2002. Adenovirus type 37 uses sialic acid as a cellular receptor on Chang C cells. J. Virol. 76:8834-8841.
5. Balakireva, L., G. Schoehn, E. Thouvenin, and J. Chroboczek. 2003. Binding of adenovirus capsid to dipalmitoyl phosphatidylcholine provides a novel pathway for virus entry. J. Virol. 77:4858-4866. (Pubitemid 36402835)
6. Belin, M. T., and P. Boulanger. 1993. Involvement of cellular adhesion sequences in the attachment of adenovirus to the HeLa cell surface. J. Gen. Virol. 74:1485-1497. (Pubitemid 23243158)
7. Bergelson, J. M., J. A. Cunningham, G. Droguett, E. A. Kurt-Jones, A. Krithivas, J. S. Hong, M. S. Horwitz, R. L. Crowell, and R. W. Finberg. 1997. Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 275:1320-1323.
8. Breidenbach, M., D. T. Rein, M. Wang, D. M. Nettelbeck, A. Hemminki, I. Ulasov, A. R. Rivera, M. Everts, R. D. Alvarez, J. T. Douglas, and D. T. Curiel. 2004. Genetic replacement of the adenovirus shaft fiber reduces liver tropism in ovarian cancer gene therapy. Hum. Gene Ther. 15:509-518. (Pubitemid 38639621)
9. Burmeister, W. P., D. Guilligay, S. Cusack, G. Wadell, and N. Arnberg. 2004. Crystal structure of species D adenovirus fiber knobs and their sialic acid binding sites. J. Virol. 78:7727-7736. (Pubitemid 38915919)
10. Chen, Z., M. Ahonen, H. Hamalainen, J. M. Bergelson, V. M. Kahari, and R. Lahesmaa. 2002. High-efficiency gene transfer to primary T lymphocytes by recombinant adenovirus vectors. J. Immunol. Methods 260:79-89. (Pubitemid 34132874)
11. Chu, Y., D. Heistad, M. I. Cybulsky, and B. L. Davidson. 2001. Vascular cell adhesion molecule-1 augments adenovirus-mediated gene transfer. Arterioscler. Thromb. Vasc. Biol. 21:238-242. (Pubitemid 32125372)
12. Coyne, C. B., and J. M. Bergelson. 2005. CAR: a virus receptor within the tight junction. Adv. Drug Deliv. Rev. 57:869-882.
13. Dechecchi, M. C., P. Melotti, A. Bonizzato, M. Santacatterina, M. Chilosi, and G. Cabrini. 2001. Heparan sulfate glycosaminoglycans are receptors sufficient to mediate initial binding of adenovirus types 2 and 5. J. Virol. 75:8772-8780. (Pubitemid 32768981)
14. Gaggar, A., D. M. Shayakhmetov, and A. Lieber. 2003. CD46 is a cellular receptor for group B adenoviruses. Nat. Med. 9:1408-1412. (Pubitemid 37466191)
15. Garnett, C. T., D. Erdman, W. Xu, and L. R. Gooding. 2002. Prevalence and quantitation of species C adenovirus DNA in human mucosal lymphocytes. J. Virol. 76:10608-10616. (Pubitemid 35176177)
16. Hierholzer, J. C. 1992. Adenoviruses in the immunocompromised host. Clin. Microbiol. Rev. 5:262-274.
17. Hong, S. S., L. Karayan, J. Tournier, D. T. Curiel, and P. A. Boulanger. 1997. Adenovirus type 5 fiber knob binds to MHC class I alpha2 domain at the surface of human epithelial and B lymphoblastoid cells. EMBO J. 16:2294-2306. (Pubitemid 27258631)
18. Jandik, K. A., K. Gu, and R. J. Linhardt. 1994. Action pattern of polysaccharide lyases on glycosaminoglycans. Glycobiology 4:289-296.
19. Johansson, C., M. Jonsson, M. Marttila, D. Persson, X. L. Fan, J. Skog, L. Frangsmyr, G. Wadell, and N. Arnberg. 2007. Adenoviruses use lactoferrin as a bridge for CAR-independent binding to and infection of epithelial cells. J. Virol. 81:954-963. (Pubitemid 46067920)
20. Johansson, S. M., E. C. Nilsson, M. Elofsson, N. Ahlskog, J. Kihlberg, and N. Arnberg. 2007. Multivalent sialic acid conjugates inhibit adenovirus type 37 from binding to and infecting human corneal epithelial cells. Antivir. Res. 73:92-100. (Pubitemid 46135767)
21. Kalyuzhniy, O., N. C. Di Paolo, M. Silvestry, S. E. Hofherr, M. A. Barry, P. L. Stewart, and D. M. Shayakhmetov. 2008. Adenovirus serotype 5 hexon is critical for virus infection of hepatocytes in vivo. Proc. Natl. Acad. Sci. USA 105:5483-5488.
22. Koizumi, N., K. Kawabata, F. Sakurai, Y. Watanabe, T. Hayakawa, and H. Mizuguchi. 2006. Modified adenoviral vectors ablated for coxsackievirus- adenovirus receptor, alphav integrin, and heparan sulfate binding reduce in vivo tissue transduction and toxicity. Hum. Gene Ther. 17:264-279.
23. Kritz, A. B., C. G. Nicol, K. L. Dishart, R. Nelson, S. Holbeck, D. J. Von Seggern, L. M. Work, J. H. McVey, S. A. Nicklin, and A. H. Baker. 2007. Adenovirus 5 fibers mutated at the putative HSPG-binding site show restricted retargeting with targeting peptides in the HI loop. Mol. Ther. 15:741-749. (Pubitemid 46431994)
24. 1 is an adenovirus coreceptor. J. Virol. 75:5405-5409.
25. Martin, K., A. Brie, P. Saulnier, M. Perricaudet, P. Yeh, and E. Vigne. 2003. Simultaneous CAR- and alpha V integrin-binding ablation fails to reduce Ad5 liver tropism. Mol. Ther. 8:485-494. (Pubitemid 37161470)
26. Marttila, M., D. Persson, D. Gustafsson, M. K. Liszewski, J. P. Atkinson, G. Wadell, and N. Arnberg. 2005. CD46 is a cellular receptor for all species B adenoviruses except types 3 and 7. J. Virol. 79:14429-14436. (Pubitemid 41552740)
27. Mertens, G., B. Van der Schueren, H. van den Berghe, and G. David. 1996. Heparan sulfate expression in polarized epithelial cells: the apical sorting of glypican (GPI-anchored proteoglycan) is inversely related to its heparan sulfate content. J. Cell Biol. 132:487-497.
28. Nicol, C. G., D. Graham, W. H. Miller, S. J. White, T. A. Smith, S. A. Nicklin, S. C. Stevenson, and A. H. Baker. 2004. Effect of adenovirus serotype 5 fiber and penton modifications on in vivo tropism in rats. Mol. Ther. 10:344-354. (Pubitemid 39117879)
29. Nilsson, E. C., F. Jamshidi, S. M. Johansson, M. S. Oberste, and N. Arnberg. 2008. Sialic acid is a cellular receptor for coxsackievirus a24 variant, an emerging virus with pandemic potential. J. Virol. 82:3061-3068.
30. Osterud, B., B. N. Bouma, and J. H. Griffin. 1978. Human blood coagulation factor IX. Purification, properties, and mechanism of activation by activated factor XI. J. Biol. Chem. 253:5946-5951.
31. Parker, A. L., J. H. McVey, J. H. Doctor, O. Lopez-Franco, S. N. Waddington, M. J. Havenga, S. A. Nicklin, and A. H. Baker. 2007. Influence of coagulation factor zymogens on the infectivity of adenoviruses pseudotyped with fibers from subgroup D. J. Virol. 81:3627-3631. (Pubitemid 46456671)
32. Parker, A. L., S. N. Waddington, C. G. Nicol, D. M. Shayakhmetov, S. M. Buckley, L. Denby, G. Kemball-Cook, S. Ni, A. Lieber, J. H. McVey, S. A. Nicklin, and A. H. Baker. 2006. Multiple vitamin K-dependent coagulation zymogens promote adenovirus-mediated gene delivery to hepatocytes. Blood 108:2554-2561.
33. Perrio, M. J., D. Ewen, M. A. Trevethick, G. P. Salmon, and J. K. Shute. 2007. Fibrin formation by wounded bronchial epithelial cell layers in vitro is essential for normal epithelial repair and independent of plasma proteins. Clin. Exp. Allergy 37:1688-1700.
34. Persson, C. G., I. Erjefält, U. Alkner, C. Baumgarten, L. Greiff, B. Gustafsson, A. P. Luts, U. Pipkorn, F. Sundler, C. Svensson, and P. Wollmer. 1991. Plasma exudation as a first line respiratory mucosal defence. Clin. Exp. Allergy 21:17-24.
35. Rao, L. V., and S. I. Rapaport. 1988. Activation of factor VII bound to tissue factor: a key early step in the tissue factor pathway of blood coagulation. Proc. Natl. Acad. Sci. USA 85:6687-6691.
36. Roelvink, P. W., A. Lizonova, J. G. Lee, Y. Li, J. M. Bergelson, R. W. Finberg, D. E. Brough, I. Kovesdi, and T. J. Wickham. 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.
37. Segerman, A., J. P. Atkinson, M. Marttila, V. Dennerquist, G. Wadell, and N. Arnberg. 2003. Adenovirus type 11 uses CD46 as a cellular receptor. J. Virol. 77:9183-9191. (Pubitemid 37011015)
38. Shayakhmetov, D. M., A. Gaggar, S. Ni, Z.-Y. Li, and A. Lieber. 2005. Adenovirus binding to blood factors results in liver cell infection and hepatotoxicity. J. Virol. 79:7478-7491. (Pubitemid 40756784)
39. Smith, T., N. Idamakanti, H. Kylefjord, M. Rollence, L. King, M. Kaloss, M. Kaleko, and S. C. Stevenson. 2002. In vivo hepatic adenoviral gene delivery occurs independently of the coxsackievirus-adenovirus receptor. Mol. Ther. 5:770-779.
40. Smith, T. A., N. Idamakanti, M. L. Rollence, J. Marshall-Neff, J. Kim, K. Mulgrew, G. R. Nemerow, M. Kaleko, and S. C. Stevenson. 2003. Adenovirus serotype 5 fiber shaft influences in vivo gene transfer in mice. Hum. Gene Ther. 14:777-787. (Pubitemid 36623514)
41. Tomko, R. P., R. Xu, and L. Philipson. 1997. HCAR and MCAR: the human and mouse cellular receptors for subgroup C adenoviruses and group B coxsackieviruses. Proc. Natl. Acad. Sci. USA 94:3352-3356.
42. Waddington, S. N., J. H. McVey, D. Bhella, A. L. Parker, K. Barker, H. Atoda, R. Pink, S. M. Buckley, J. A. Greig, L. Denby, J. Custers, T. Morita, I. M. Francischetti, R. Q. Monteiro, D. H. Barouch, N. van Rooijen, C. Napoli, M. J. Havenga, S. A. Nicklin, and A. H. Baker. 2008. Adenovirus serotype 5 hexon mediates liver gene transfer. Cell 132:397-409.
43. Waddington, S. N., A. L. Parker, M. Havenga, S. A. Nicklin, S. M. Buckley, J. H. McVey, and A. H. Baker. 2007. Targeting of adenovirus serotype 5 (Ad5) and 5/47 pseudotyped vectors in vivo: a fundamental involvement of coagulation factors and redundancy of CAR binding by Ad5. J. Virol. 81:9568-9571.
44. Wadell, G. 2000. Adenoviruses, p. 308-327. In A. J. Zuckerman, J. E. Banatvala, and J. R. Pattison (ed.), Principles and practice of clinical virology, 4 ed. John Wiley & Sons, New York, NY.
45. Wadell, G., A. Allard, and J. C. Hierholzer. 1999. Adenoviruses, p. 970-982. In P. R. Murray, E. J. Baron, M. A. Pfaller, F. C. Tenover, and R. H. Yolken (ed.), Manual of clinical microbiology, 7th ed. ASM Press, Washington, DC.
46. Walters, R. W., P. Freimuth, T. O. Moninger, I. Ganske, J. Zabner, and M. J. Welsh. 2002. Adenovirus fiber disrupts CAR-mediated intercellular adhesion allowing virus escape. Cell 110:789-799.
47. Walters, R. W., T. Grunst, J. M. Bergelson, R. W. Finberg, M. J. Welsh, and J. Zabner. 1999. Basolateral localization of fiber receptors limits adenovirus infection from the apical surface of airway epithelia. J. Biol. Chem. 274:10219-10226. (Pubitemid 129518312)
48. Wickham, T. J., P. Mathias, D. A. Cheresh, and G. R. Nemerow. 1993. Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment. Cell 73:309-319.
49. Vogels, R., D. Zuijdgeest, R. van Rijnsoever, E. Hartkoorn, I. Damen, M. P. de Bethune, S. Kostense, G. Penders, N. Helmus, W. Koudstaal, M. Cecchini, A. Wetterwald, M. Sprangers, A. Lemckert, O. Ophorst, B. Koel, M. van Meerendonk, P. Quax, L. Panitti, J. Grimbergen, A. Bout, J. Goudsmit, and M. Havenga. 2003. Replication-deficient human adenovirus type 35 vectors for gene transfer and vaccination: efficient human cell infection and bypass of preexisting adenovirus immunity. J. Virol. 77:8263-8271.
50. Wold, W. S. M., and M. S. Horwitz. 2007. Adenoviruses, p. 2395-2436. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 5th ed., vol. 2. Lippincott Williams & Wilkins, Philadelphia, PA.
51. Xu, Z., J. Tian, J. S. Smith, and A. P. Byrnes. 2008. Clearance of adenovirus by Kupffer cells is mediated by scavenger receptors, natural antibodies, and complement. J. Virol. 82:11705-11713.
52. Yun, C. O., A. R. Yoon, J. Y. Yoo, H. Kim, M. Kim, T. Ha, G. E. Kim, H. Kim, and J. H. Kim. 2005. Coxsackie and adenovirus receptor binding ablation reduces adenovirus liver tropism and toxicity. Hum. Gene Ther. 16:248-261. (Pubitemid 40344216)