Human erythrocytes bind and inactivate type 5 adenovirus by presenting Coxsackie virus-adenovirus receptor and complement receptor 1

Blood

Volumn 113, Issue 9, 2009, Pages 1909-1918

  Carlisle, Robert C ^a   Di, Ying ^a   Cerny, Anna M ^b   Sonnen, Andreas F P ^c   Sim, Robert B ^a   Green, Nicola K ^d   Subr, Vladimir ^e   Ulbrich, Karel ^e   Gilbert, Robert J C ^c   Fisher, Kerry D ^a   Finberg, Robert W ^b   Seymour, Leonard W ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d Cherwell Innovation Centre   (United Kingdom)

^e INSTITUTE OF MACROMOLECULAR CHEMISTRY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C3B RECEPTOR; COXSACKIE VIRUS AND ADENOVIRUS RECEPTOR; COXSACKIE VIRUS AND ADENOVIRUS RECEPTOR 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIVIRAL ACTIVITY; ARTICLE; CELL TRANSFER; COMPLEMENT FIXATION; CRYOELECTRON MICROSCOPY; ERYTHROCYTE ADHESIVENESS; ERYTHROCYTE MEMBRANE; FEMALE; HEPATITIS; HUMAN; HUMAN ADENOVIRUS 5; HUMAN CELL; INFECTION PREVENTION; MOUSE; NONHUMAN; PERIPHERAL CIRCULATION; PRIORITY JOURNAL; SCID MOUSE; TRANSGENIC MOUSE; VIRAL GENE DELIVERY SYSTEM; VIRUS ATTACHMENT; VIRUS INACTIVATION; XENOGRAFT;

EID: 61849089262     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-09-178459     Document Type: Article

References (42)

1. Hayashi S, Hogg JC. Adenovirus infections and lung disease. Curr Opin Pharmacol. 2007;7:237-243.
2. Parker AL, Waddington SN, Nicol CG, et al. Multiple vitamin K-dependent coagulation zymogens promote adenovirus-mediated gene delivery to hepatocytes. Blood. 2006;108:2554-2561.
3. Kalyuzhniy O, Di Paolo NC, Silvestry M, et al. Adenovirus serotype 5 hexon is critical for virus infection of hepatocytes in vivo. Proc Natl Acad Sci U S A. 2008;105:5483-5488.
4. Waddington SN, McVey JH, Bhella D, et al. Adenovirus serotype 5 hexon mediates liver gene transfer. Cell. 2008;132:397-409.
5. Peng Z. Current status of gendicine in China: recombinant human Ad-p53 agent for treatment of cancers. Hum Gene Ther. 2005;16:1016-1027.
6. Nakano MY, Boucke K, Suomalainen M, Stidwill RP, Greber UF. The first step of adenovirus type 2 disassembly occurs at the cell surface, independently of endocytosis and escape to the cytosol. J Virol. 2000;74:7085-7095.
7. Carlisle RC, Bettinger T, Ogris M, Hale S, Mautner V, Seymour LW. Adenovirus hexon protein enhances nuclear delivery and increases transgene expression of polyethylenimine/plasmid DNA vectors. Mol Ther. 2001;4:473-483.
8. Tomko RP, Xu R, Philipson L. HCAR and MCAR: the human and mouse cellular receptors for subgroup C adenoviruses and group B coxsackieviruses. Proc Natl Acad Sci U S A. 1997;94:3352-3356.
9. Green NK, Herbert CW, Hale SJ, et al. Extended plasma circulation time and decreased toxicity of polymer-coated adenovirus. Gene Ther. 2004;11:1256-1263.
10. Asher DR, Cerny AM, Finberg RW. The erythrocyte viral trap: transgenic expression of viral receptor on erythrocytes attenuates coxsackievirus B infection. Proc Natl Acad Sci U S A. 2005;102:12897-12902.
11. Repik A, Pincus SE, Ghiran I, et al. A transgenic mouse model for studying the clearance of blood-borne pathogens via human complement receptor 1 (CR1). Clin Exp Immunol. 2005;140:230-240.
12. Subr V, Kostka L, Selby-Milic T, et al. Coating of adenovirus type 5 with polymers containing quaternary amines prevents binding to blood components. J Control Release. 2009 (in press). DOI: 10.1016/j.jconrel.2008.12.009.
13. Carlisle RC, Benjamin R, Briggs SS, et al. Coating of adeno-associated virus with reactive polymers can ablate virus tropism, enable retargeting and provide resistance to neutralising antisera. J Gene Med. 2008;10:400-411.
14. Othman M, Labelle A, Mazzetti I, Elbatarny HS, Lillicrap D. Adenovirus-induced thrombocytopenia: the role of von Willebrand factor and P-selectin in mediating accelerated platelet clearance. Blood. 2007;109:2832-2839.
15. Jasin HE. Human heat labile opsonins: evidence for their mediation via the alternate pathway of complement activation. J Immunol. 1972;109:26-31.
16. Sahu A, Lambris JD. Structure and biology of complement protein C3, a connecting link between innate and acquired immunity. Immunol Rev. 2001;180:35-48.
17. Homicsko K, LukashevA, Iggo RD. RAD001 (everolimus) improves the efficacy of replicating adenoviruses that target colon cancer. Cancer Res. 2005;65:6882-6890.
18. Xu Z, Smith JS, Tian J, Brynes AP. Clearance of adenovirus by Kupffer cells is mediated by natural antibodies, complement and scavenger receptors. Mol Ther. 2008;16[suppl]:S93.
19. Cornacoff JB, Hebert LA, Smead WL, VanAman ME, Birmingham DJ, Waxman FJ. Primate erythrocyte-immune complex-clearing mechanism. J Clin Invest. 1983;71:236-247.
20. Wu E, Pache L, Von Seggern DJ, et al. Flexibility of the adenovirus fiber is required for efficient receptor interaction. J Virol. 2003;77:7225-7235.
21. Fabry CM, Rosa-Calatrava M, Conway JF, et al. A quasi-atomic model of human adenovirus type 5 capsid. EMBO J. 2005;24:1645-1654.
22. Cusack S. Adenovirus complex structures. Curr Opin Struct Biol. 2005;15:237-243.
23. Fender P, Schoehn G, Perron-Sierra F, Tucker GC, Lortat-Jacob H. Adenovirus dodecahedron cell attachment and entry are mediated by heparan sulfate and integrins and vary along the cell cycle. Virology. 2008;371:155-164.
24. Fisher KD, Stallwood Y, Green NK, Ulbrich K, Mautner V, Seymour LW. Polymer-coated adenovirus permits efficient retargeting and evades neutralising antibodies. Gene Ther. 2001;8:341-348.
25. Morrison J, Briggs SS, Green N, et al. Virotherapy of ovarian cancer with polymer-cloaked adenovirus retargeted to the epidermal growth factor receptor. Mol Ther. 2008;16:244-251.
26. Cohen CJ, Shieh JT, Pickles RJ, Okegawa T, Hsieh JT, Bergelson JM. The coxsackievirus and adenovirus receptor is a transmembrane component of the tight junction. Proc Natl Acad Sci U S A. 2001;98:15191-15196.
27. Honda T, Saitoh H, Masuko M, et al. The coxsackievirus-adenovirus receptor protein as a cell adhesion molecule in the developing mouse brain. Brain Res Mol Brain Res. 2000;77:19-28.
28. Coyne CB, Voelker T, Pichla SL, Bergelson JM. The coxsackievirus and adenovirus receptor interacts with the multi-PDZ domain protein-1 (MUPP-1) within the tight junction. J Biol Chem. 2004;279:48079-48084.
29. Raschperger E, Thyberg J, Pettersson S, Philipson L, Fuxe J, Pettersson RF. The coxsackie-and adenovirus receptor (CAR) is an in vivo marker for epithelial tight junctions, with a potential role in regulating permeability and tissue homeostasis. Exp Cell Res. 2006;312:1566-1580.
30. Yamashita M, InoA, Kawabata K, Sakurai F, Mizuguchi H. Expression of coxsackie and adenovirus receptor reduces the lung metastatic potential of murine tumor cells. Int J Cancer. 2007;121:1690-1696.
31. Martin TA, Watkins G, Jiang WG. The Coxsackie-adenovirus receptor has elevated expression in human breast cancer. Clin Exp Med. 2005;5:122-128.
32. Bergelson JM, Cunningham JA, Droguett G, et al. Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science. 1997;275:1320-1323.
33. Cichon G, Boeckh-Herwig S, Schmidt HH, et al. Complement activation by recombinant adenoviruses. Gene Ther. 2001;8:1794-1800.
34. Jiang H, Wang Z, Serra D, Frank MM, Amalfitano A. Recombinant adenovirus vectors activate the alternative complement pathway, leading to the binding of human complement protein C3 independent of anti-ad antibodies. Mol Ther. 2004;10:1140-1142.
35. Chen JW, Ghosh R, Finberg RW, Bergelson JM. Structure and chromosomal localization of the murine coxsackievirus and adenovirus receptor gene. DNA Cell Biol. 2003;22:253-259.
36. Neofytos D, Ojha A, Mookerjee B, et al. Treatment of adenovirus disease in stem cell transplant recipients with cidofovir. Biol Blood Marrow Transplant. 2007;13:74-81.
37. Seidemann K, Heim A, Pfister ED, et al. Monitoring of adenovirus infection in pediatric transplant recipients by quantitative PCR: report of six cases and review of the literature. Am J Transplant. 2004;4:2102-2108.
38. Lion T, Baumgartinger R, Watzinger F, et al. Molecular monitoring of adenovirus in peripheral blood after allogeneic bone marrow transplantation permits early diagnosis of disseminated disease. Blood. 2003;102:1114-1120.
39. Au T, Thorne S, Korn WM, Sze D, Kirn D, Reid TR. Minimal hepatic toxicity of Onyx-015: spatial restriction of coxsackie-adenoviral receptor in normal liver. Cancer Gene Ther. 2007;14:139-150.
40. Gaspar HB, Parsley KL, Howe S, et al. Gene therapy of X-linked severe combined immunodeficiency by use of a pseudotyped gammaretroviral vector. Lancet. 2004;364:2181-2187.
41. Bainbridge JW, Smith AJ, Barker SS, et al. Effect of gene therapy on visual function in Leber's congenital amaurosis. N Engl J Med. 2008;358:2231-2239.
42. Liu TC, Galanis E, Kirn D. Clinical trial results with oncolytic virotherapy: a century of promise, a decade of progress. Nat Clin Pract Oncol. 2007;4:101-117.