Assessment of a novel, capsid-modified adenovirus with an improved vascular gene transfer profile

Journal of Cardiothoracic Surgery

Volumn 8, Issue 1, 2013, Pages

  White, Katie M ^a   Alba, Raul ^a,b   Parker, Alan L ^a,c   Wright, Audrey F ^a   Bradshaw, Angela C ^a   Delles, Christian ^a   McDonald, Robert A ^a   Baker, Andrew H ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b Nanotherapix SL   (Spain)

^c CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Adenovirus; TIMP 3; Vascular gene therapy; Vein graft failure

Indexed keywords

BETA GALACTOSIDASE; TISSUE INHIBITOR OF METALLOPROTEINASE 3;

ADENOVIRUS; ARTICLE; CELL CULTURE; COMPARATIVE STUDY; GENE TRANSFER; GENE VECTOR; GENETIC TRANSDUCTION; GENETICS; HUMAN; SAPHENOUS VEIN; VIRUS CAPSID;

ADENOVIRIDAE; BETA-GALACTOSIDASE; CAPSID; CELLS, CULTURED; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; HUMANS; SAPHENOUS VEIN; TISSUE INHIBITOR OF METALLOPROTEINASE-3; TRANSDUCTION, GENETIC;

EID: 84881163929     PISSN: None     EISSN: 17498090     Source Type: Journal    
DOI: 10.1186/1749-8090-8-183     Document Type: Article

References (40)

1. George SJ, Wan S, Hu J, MacDonald R, Johnson JL, Baker AH. Sustained reduction of vein graft neointima formation by ex vivo TIMP-3 gene therapy. Circulation 2011, 124:S135-S142. 10.1161/CIRCULATIONAHA.110.012732, 21911803.
2. Johnson TW, Wu YX, Herdeg C, Baumbach A, Newby AC, Karsch KR, Oberhoff M. Stent-based delivery of Tissue Inhibitor of Metalloproteinase-3 adenovirus inhibits neointimal formation in porcine coronary arteries. Arterioscler Thromb Vasc Biol 2005, 25:754-759. 10.1161/01.ATV.0000157582.33180.a9, 15681295.
3. Ishii S, Koyama H, Miyata T, Nishikage S, Hamada H, Miyatake S-I, Shigematsu H. Appropriate control of ex vivo gene therapy delivering basic fibroblast growth factor promotes successful and safe development of collateral vessels in rabbit model of hind limb ischemia. J Vasc Surg 2004, 39:629-638. 10.1016/j.jvs.2003.09.016, 14981459.
4. Hedman M, Hartikainen J, Syvänne M, Stjernvall J, Hedman A, Kivelä A, Vanninen E, Mussalo H, Kauppila E, Simula S, et al. Safety and feasibility of catheter-based local intracoronary vascular endothelial growth factor gene transfer in the prevention of postangioplasty and in-stent restenosis and in the treatment of chronic myocardial ischemia. Circulation 2003, 107:2677-2683. 10.1161/01.CIR.0000070540.80780.92, 12742981.
5. Lopes RD, Williams JB, Mehta RH, Reyes EM, Hafley GE, Allen KB, Mack MJ, Peterson ED, Harrington RA, Gibson CM, et al. Edifoligide and long-term outcomes after coronary artery bypass grafting: PRoject of Ex-vivo Vein graft ENgineering via Transfection IV (PREVENT IV) 5-year results. Am Heart J 2012, 164:379-386. e371, 10.1016/j.ahj.2012.05.019, 22980305.
6. Henry TD, Grines CL, Watkins MW, Dib N, Barbeau G, Moreadith R, Andrasfay T, Engler RL. Effects of Ad5FGF-4 in patients with angina: An analysis of pooled data from the AGENT-3 and AGENT-4 trials. J Am Coll Cardiol 2007, 50:1038-1046. 10.1016/j.jacc.2007.06.010, 17825712.
7. Hedman M, Muona K, Hedman A, Kivela A, Syvanne M, Eranen J, Rantala A, Stjernvall J, Nieminen MS, Hartikainen J, Yla-Herttuala S. Eight-year safety follow-up of coronary artery disease patients after local intracoronary VEGF gene transfer. Gene Ther 2009, 16:629-634. 10.1038/gt.2009.4, 19212427.
8. Jessup M, Greenberg B, Mancini D, Cappola T, Pauly DF, Jaski B, Yaroshinsky A, Zsebo KM, Dittrich H, Hajjar RJ. Calcium upregulation by percutaneous administration of gene therapy in cardiac disease (CUPID): A phase 2 trial of intracoronary gene therapy of sarcoplasmic reticulum Ca 2 + -ATPase in patients with advanced heart failure. Circulation 2011, 124:304-313. 10.1161/CIRCULATIONAHA.111.022889, 21709064.
9. Lemarchand P, Jones M, Yamada I, Crystal RG. In vivo gene transfer and expression in normal uninjured blood vessels using replication-deficient recombinant adenovirus vectors. Circ Res 1993, 72:1132-1138. 10.1161/01.RES.72.5.1132, 8477524.
10. Merrick AF, Shewring LD, Sawyer GJ, Gustafsson KT, Fabre JW. Comparison of adenovirus gene transfer to vascular endothelial cells in cell culture, organ culture, and in vivo. Transplantation 1996, 62:1085-1089. 10.1097/00007890-199610270-00011, 8900307.
11. Rekhter MD, Simari RD, Work CW, Nabel GJ, Nabel EG, Gordon D. Gene transfer into normal and atherosclerotic human blood vessels. Circ Res 1998, 82:1243-1252. 10.1161/01.RES.82.12.1243, 9648720.
12. Parker AL, Laver CA, Rabhan ZS, White K, Custers J, Waddington SN, Baker AH. Pseudotyping the adenovirus serotype 5 capsid with both the fiber and penton of serotype 35 enhances vascular smooth muscle cell transduction. Gene Ther 2013, In press.
13. Carson SD, Hobbs JT, Tracy SM, Chapman NM. Expression of the coxsackievirus and adenovirus receptor in cultured human umbilical vein endothelial cells: Regulation in response to cell density. J Virol 1999, 73:7077-7079. 112800, 10400813.
14. Zanone MM, Favaro E, Ferioli E, Huang GC, Klein NJ, Perin PC, Peakman M, Conaldi PG, Camussi G. Human pancreatic islet endothelial cells express coxsackievirus and adenovirus receptor and are activated by coxsackie B virus infection. FASEB J 2007, 21:3308-3317. 10.1096/fj.06-7905com, 17494992.
15. Vigl B, Zgraggen C, Rehman N, Banziger-Tobler NE, Detmar M, Halin C. Coxsackie- and adenovirus receptor (CAR) is expressed in lymphatic vessels in human skin and affects lymphatic endothelial cell function in vitro. Exp Cell Res 2009, 315:336-347. 10.1016/j.yexcr.2008.10.020, 19007771.
16. Havenga MJE, Lemckert AAC, Grimbergen JM, Vogels R, Huisman LGM, Valerio D, Bout A, Quax PHA. Improved adenovirus vectors for infection of cardiovascular tissues. J Virol 2001, 75:3335-3342. 10.1128/JVI.75.7.3335-3342.2001, 114126, 11238859.
17. Vogels R, Zuijdgeest D, Van Rijnsoever R, Hartkoorn E, Damen I, De Béthune M-P, Kostense S, Penders G, Helmus N, Koudstaal W, et al. Replication-deficient human adenovirus type 35 vectors for gene transfer and vaccination: efficient human cell infection and bypass of preexisting adenovirus immunity. J Virol 2003, 77:8263-8271. 10.1128/JVI.77.15.8263-8271.2003, 165227, 12857895.
18. Sumida SM, Truitt DM, Lemckert AAC, Vogels R, Custers JHHV, Addo MM, Lockman S, Peter T, Peyerl FW, Kishko MG, et al. Neutralizing antibodies to adenovirus serotype 5 vaccine vectors are directed primarily against the adenovirus hexon protein. J Immunol 2005, 174:7179-7185.
19. Kuriyama S, Tominaga K, Kikukawa M, Nakatani M, Tsujinoue H, Yamazaki S, Nagao S, Toyokawa Y, Mitoro A, Fukio H. Inhibitory effects of human sera on adenovirus-mediated gene transfer into rat liver. Anticancer Res 1998, 18:2345-2351.
20. Roberts DM, Nanda A, Havenga MJE, Abbink P, Lynch DM, Ewald BA, Liu J, Thorner AR, Swanson PE, Gorgone DA, et al. Hexon-chimaeric adenovirus serotype 5 vectors circumvent pre-existing anti-vector immunity. Nature 2006, 441:239-243. 10.1038/nature04721, 16625206.
21. Parker AL, Waddington SN, Buckley SM, Custers J, Havenga MJ, Van Rooijen N, Goudsmit J, McVey JH, Nicklin SA, Baker AH. Effect of neutralizing sera on factor x-mediated adenovirus serotype 5 gene transfer. J Virol 2009, 83:479-483. 10.1128/JVI.01878-08, 2612319, 18945780.
22. Hilutnen MO, Turenen MP, Turenen A-M, Rissanen T, Laitinen M, Kosma V-M, Yla-Herttuala S. Biodistribution of adenoviral vector to nontarget tissues after local in vivo gene transfer to arterial wall using intravascular and periadventitial gene delivery methods. FASEB J 2000, 14:2230-2236. 10.1096/fj.00-0145com, 11053244.
23. Waddington SN, McVey JH, Bhella D, Parker AL, Barker K, Atoda H, Pink R, Buckley SM, Greig JA, Denby L, et al. Adenovirus serotype 5 hexon mediates liver gene transfer. Cell 2008, 132:397-409. 10.1016/j.cell.2008.01.016, 18267072.
24. Kalyuzhniy O, Di Paolo NC, Silvestry M, Hofherr SE, Barry MA, Stewart PL, Shayakhmetov DM. Adenovirus serotype 5 hexon is critical for virus infection of hepatocytes in vivo. Proc Nat Acad Sci 2008, 105:5483-5488. 10.1073/pnas.0711757105, 2291105, 18391209.
25. Bradshaw AC, Parker AL, Duffy MR, Coughlan L, Van Rooijen N, Kähäri V-M, Nicklin SA, Baker AH. Requirements for receptor engagement during infection by adenovirus complexed with blood coagulation Factor X. PLoS Pathog 2010, 6:e1001142. 10.1371/journal.ppat.1001142, 2951380, 20949078.
26. Alba R, Bradshaw AC, Coughlan L, Denby L, McDonald RA, Waddington SN, Buckley SMK, Greig JA, Parker AL, Miller AM, et al. Biodistribution and retargeting of FX-binding ablated adenovirus serotype 5 vectors. Blood 2010, 116:2656-2664. 10.1182/blood-2009-12-260026, 2974579, 20610817.
27. Bradshaw AC, Coughlan L, Miller AM, Alba R, Van Rooijen N, Nicklin SA, Baker AH. Biodistribution and inflammatory profiles of novel penton and hexon double-mutant serotype 5 adenoviruses. J Control Release 2012, 164:394-402. 10.1016/j.jconrel.2012.05.025, 3520007, 22626939.
28. Vigant F, Descamps D, Jullienne B, Esselin S, Connault E, Opolon P, Tordjmann T, Vigne E, Perricaudet M, Benihoud K. Substitution of hexon hypervariable region 5 of adenovirus serotype 5 abrogates blood factor binding and limits gene transfer to liver. Mol Ther 2008, 16:1474-1480. 10.1038/mt.2008.132, 18560416.
29. Nicklin SA, Baker AH. Development of targeted viral vectors for cardiovascular gene therapy. Genet Eng (N Y) 2003, 25:15-49.
30. Alba R, Bradshaw AC, Parker AL, Bhella D, Waddington SN, Nicklin SA, van Rooijen N, Custers J, Goudsmit J, Barouch DH, et al. Identification of coagulation factor (F)X binding sites on the adenovirus serotype 5 hexon: effect of mutagenesis on FX interactions and gene transfer. Blood 2009, 114:965-971. 10.1182/blood-2009-03-208835, 2721791, 19429866.
31. Sprangers MC, Lakhai W, Koudstaal W, Verhoeven M, Koel BF, Vogels R, Goudsmit J, Havenga MJE, Kostense S. Quantifying Adenovirus-Neutralizing Antibodies by Luciferase Transgene Detection: Addressing Preexisting Immunity to Vaccine and Gene Therapy Vectors. J Clin Microbiol 2003, 41:5046-5052. 10.1128/JCM.41.11.5046-5052.2003, 262545, 14605137.
32. Liang C-C, Park AY, Guan J-L. In vitro scratch assay: a convenient and inexpensive method for analysis of cell migration in vitro. Nat Protocols 2007, 2:329-333.
33. George SJ, Lloyd CT, Angelini GD, Newby AC, Baker AH. Inhibition of late vein graft neointima formation in human and porcine models by adenovirus-mediated overexpression of tissue inhibitor of metalloproteinase-3. Circulation 2000, 101:296-304. 10.1161/01.CIR.101.3.296, 10645926.
34. Baker AH, Zaltsman AB, George SJ, Newby AC. Divergent effects of tissue inhibitor of metalloproteinase-1, -2, or -3 overexpression on rat vascular smooth muscle cell invasion, proliferation, and death in vitro. TIMP-3 promotes apoptosis. J Clin Invest 1998, 101:1478-1487. 10.1172/JCI1584, 508704, 9502791.
35. Newman KD, Dunn PF, Owens JW, Schulick AH, Virmani R, Sukhova G, Libby P, Dichek DA. Adenovirus-mediated gene transfer into normal rabbit arteries results in prolonged vascular cell activation, inflammation, and neointimal hyperplasia. J Clin Invest 1995, 96:2955-2965. 10.1172/JCI118367, 186007, 8675667.
36. Doronin K, Flatt JW, Di Paolo NC, Khare R, Kalyuzhniy O, Acchione M, Sumida JP, Ohto U, Shimizu T, Akashi-Takamura S, et al. Coagulation Factor X activates innate immunity to human species C Adenovirus. Science 2012, 338:795-798. 10.1126/science.1226625, 23019612.
37. Bradley RR, Lynch DM, Iampietro MJ, Borducchi EN, Barouch DH. Adenovirus serotype 5 neutralizing antibodies target both hexon and fiber following vaccination and natural infection. J Virol 2012, 86:625-629. 10.1128/JVI.06254-11, 3255879, 22072776.
38. Inoue N, Ikawa M, Nakanishi T, Matsumoto M, Nomura M, Seya T, Okabe M. Disruption of mouse CD46 causes an accelerated spontaneous acrosome reaction in sperm. Mol Cell Biol 2003, 23:2614-2622. 10.1128/MCB.23.7.2614-2622.2003, 150730, 12640142.
39. Sakurai F. Development and evaluation of a novel gene delivery vehicle composed of adenovirus serotype 35. Biol Pharm Bull 2008, 31:1819-1825. 10.1248/bpb.31.1819, 18827334.
40. Soyombo AA, Angelini GD, Bryan AJ, Jasani B, Newby AC. Intimal proliferation in an organ culture of human saphenous vein. Am J Pathol 1990, 137:1401-1410. 1877721, 2260628.