Retargeting of gene expression using endothelium specific hexon modified adenoviral vector

Virology

Volumn 447, Issue 1-2, 2013, Pages 312-325

  Kaliberov, Sergey A ^a   Kaliberova, Lyudmila N ^a   Hong Lu, Zhi ^a   Preuss, Meredith A ^b   Barnes, Justin A ^c   Stockard, Cecil R ^c   Grizzle, William E ^c   Arbeit, Jeffrey M ^a   Curiel, David T ^a  

^a WASHINGTON UNIVERSITY   (United States)

^b University of Alabama at Birmingham   (United States)

^c University of Alabama at Birmingham   (United States)

Author keywords

Adenovirus; Endothelium; Hexon; Roundabout 4 promoter; Targeting

Indexed keywords

ADENOVIRUS VECTOR; BLOOD CLOTTING FACTOR 10; CAPSID PROTEIN; HEXON PROTEIN; ROUNDABOUT 4 RECEPTOR; ROUNDABOUT RECEPTOR; UNCLASSIFIED DRUG;

ADENOVIRUS 5; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOMEGALOVIRUS; DNA MODIFICATION; ENDOTHELIUM; ENHANCER REGION; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO GENE TRANSFER; IN VIVO GENE TRANSFER; LIVER; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; QUANTITATIVE ANALYSIS; THERMOSTABILITY; TISSUE DISTRIBUTION; TRANSGENIC MOUSE; VIRAL TROPISM; VIRUS REPLICATION;

ADENOVIRUS; ENDOTHELIUM; HEXON; ROUNDABOUT 4 PROMOTER; TARGETING;

ADENOVIRUSES, HUMAN; ANIMALS; CAPSID PROTEINS; CELL LINE; ENDOTHELIUM; FEMALE; GENE EXPRESSION REGULATION, VIRAL; GENETIC VECTORS; HUMANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; TRANSDUCTION, GENETIC; VIRAL TROPISM;

EID: 84885805591     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.09.020     Document Type: Article

References (54)

1. Aird W.C. Endothelial cell heterogeneity. Critical Care Medicine 2003, 31(4 Suppl):S221-S230.
2. Alba R., Bradshaw A.C., Coughlan L., Denby L., McDonald R.A., Waddington S.N., Buckley S.M., Greig J.A., Parker A.L., Miller A.M., Wang H., Lieber A., van Rooijen N., McVey J.H., Nicklin S.A., Baker A.H. Biodistribution and retargeting of FX-binding ablated adenovirus serotype 5 vectors. Blood 2010, 116(15):2656-2664.
3. Alba R., Bradshaw A.C., Parker A.L., Bhella D., Waddington S.N., Nicklin S.A., van Rooijen N., Custers J., Goudsmit J., Barouch D.H., McVey J.H., Baker A.H. 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(5):965-971.
4. Bachtarzi H., Stevenson M., Subr V., Ulbrich K., Seymour L.W., Fisher K.D. Targeting adenovirus gene delivery to activated tumour-associated vasculature via endothelial selectins. Journal of Controlled Release 2011, 150(2):196-203.
5. Baker A.H., Kritz A., Work L.M., Nicklin S.A. Cell-selective viral gene delivery vectors for the vasculature. Experimental Physiology 2005, 90(1):27-31.
6. Bedell V.M., Yeo S.Y., Park K.W., Chung J., Seth P., Shivalingappa V., Zhao J., Obara T., Sukhatme V.P., Drummond I.A., Li D.Y., Ramchandran R. Roundabout4 is essential for angiogenesis in vivo. Proceedings of the National Academy of Sciences of the United States of America 2005, 102(18):6373-6378.
7. Bergelson J.M., Krithivas A., Celi L., Droguett G., Horwitz M.S., Wickham T., Crowell R.L., Finberg R.W. The murine CAR homolog is a receptor for coxsackie B viruses and adenoviruses. Journal of Virology 1998, 72(1):415-419.
8. Cefai D., Simeoni E., Ludunge K.M., Driscoll R., von Segesser L.K., Kappenberger L., Vassalli G. Multiply attenuated, self-inactivating lentiviral vectors efficiently transduce human coronary artery cells in vitro and rat arteries in vivo. Journal of Molecular and Cellular Cardiology 2005, 38(2):333-344.
9. Dong Z., Nor J.E. Transcriptional targeting of tumor endothelial cells for gene therapy. Advanced Drug Delivery Reviews 2009, 61(7-8):542-553.
10. Doronin K., Flatt J.W., Di Paolo N.C., Khare R., Kalyuzhniy O., Acchione M., Sumida J.P., Ohto U., Shimizu T., Akashi-Takamura S., Miyake K., MacDonald J.W., Bammler T.K., Beyer R.P., Farin F.M., Stewart P.L., Shayakhmetov D.M. Coagulation factor X activates innate immunity to human species C adenovirus. Science 2012, 338(6108):795-798.
11. Edgar A.J., Chacon M.R., Bishop A.E., Yacoub M.H., Polak J.M. Upregulated genes in sporadic, idiopathic pulmonary arterial hypertension. Respiratory Research 2006, 7:1.
12. Everts M., Kim-Park S.A., Preuss M.A., Passineau M.J., Glasgow J.N., Pereboev A.V., Mahasreshti P.J., Grizzle W.E., Reynolds P.N., Curiel D.T. Selective induction of tumor-associated antigens in murine pulmonary vasculature using double-targeted adenoviral vectors. Gene Therapy 2005, 12(13):1042-1048.
13. Glasgow J.N., Everts M., Curiel D.T. Transductional targeting of adenovirus vectors for gene therapy. Cancer Gene Therapy 2006, 13(9):830-844.
14. Gorn M., Anige M., Burkholder I., Muller B., Scheffler A., Edler L., Boeters I., Panse J., Schuch G., Hossfeld D.K., Laack E. Serum levels of Magic Roundabout protein in patients with advanced non-small cell lung cancer (NSCLC). Lung Cancer 2005, 49(1):71-76.
15. Greenberger S., Shaish A., Varda-Bloom N., Levanon K., Breitbart E., Goldberg I., Barshack I., Hodish I., Yaacov N., Bangio L., Goncharov T., Wallach D., Harats D. Transcription-controlled gene therapy against tumor angiogenesis. Journal of Clinical Investigation 2004, 113(7):1017-1024.
16. Grone J., Doebler O., Loddenkemper C., Hotz B., Buhr H.J., Bhargava S. Robo1/Robo4: differential expression of angiogenic markers in colorectal cancer. Oncology Reports 2006, 15(6):1437-1443.
17. He T.C., Zhou S., da Costa L.T., Yu J., Kinzler K.W., Vogelstein B. A simplified system for generating recombinant adenoviruses. Proceedings of the National Academy of Sciences of the United States of America 1998, 95(5):2509-2514.
18. Huminiecki L., Gorn M., Suchting S., Poulsom R., Bicknell R. Magic roundabout is a new member of the roundabout receptor family that is endothelial specific and expressed at sites of active angiogenesis. Genomics 2002, 79(4):547-552.
19. Jones C.A., London N.R., Chen H., Park K.W., Sauvaget D., Stockton R.A., Wythe J.D., Suh W., Larrieu-Lahargue F., Mukouyama Y.S., Lindblom P., Seth P., Frias A., Nishiya N., Ginsberg M.H., Gerhardt H., Zhang K., Li D.Y. Robo4 stabilizes the vascular network by inhibiting pathologic angiogenesis and endothelial hyperpermeability. Nature Medicine 2008, 14(4):448-453.
20. Jones C.A., Nishiya N., London N.R., Zhu W., Sorensen L.K., Chan A.C., Lim C.J., Chen H., Zhang Q., Schultz P.G., Hayallah A.M., Thomas K.R., Famulok M., Zhang K., Ginsberg M.H., Li D.Y. Slit2-Robo4 signalling promotes vascular stability by blocking Arf6 activity. Nature Cell Biology 2009, 11(11):1325-1331.
21. Kalyuzhniy O., Di Paolo N.C., Silvestry M., Hofherr S.E., Barry M.A., Stewart P.L., Shayakhmetov D.M. Adenovirus serotype 5 hexon is critical for virus infection of hepatocytes in vivo. Proceedings of the National Academy of Sciences of the United States of America 2008, 105(14):5483-5488.
22. Kaur S., Castellone M.D., Bedell V.M., Konar M., Gutkind J.S., Ramchandran R. Robo4 signaling in endothelial cells implies attraction guidance mechanisms. Journal of Biological Chemistry 2006, 281(16):11347-11356.
23. Kim J., Nam H.Y., Kim T.I., Kim P.H., Ryu J., Yun C.O., Kim S.W. Active targeting of RGD-conjugated bioreducible polymer for delivery of oncolytic adenovirus expressing shRNA against IL-8mRNA. Biomaterials 2011, 32(22):5158-5166.
24. Koch A.W., Mathivet T., Larrivee B., Tong R.K., Kowalski J., Pibouin-Fragner L., Bouvree K., Stawicki S., Nicholes K., Rathore N., Scales S.J., Luis E., del Toro R., Freitas C., Breant C., Michaud A., Corvol P., Thomas J.L., Wu Y., Peale F., Watts R.J., Tessier-Lavigne M., Bagri A., Eichmann A. Robo4 maintains vessel integrity and inhibits angiogenesis by interacting with UNC5B. Developmental Cell 2011, 20(1):33-46.
25. Koski A., Rajecki M., Guse K., Kanerva A., Ristimaki A., Pesonen S., Escutenaire S., Hemminki A. Systemic adenoviral gene delivery to orthotopic murine breast tumors with ablation of coagulation factors, thrombocytes and Kupffer cells. Journal of Gene Medicine 2009, 11(11):966-977.
26. Legg J.A., Herbert J.M., Clissold P., Bicknell R. Slits and Roundabouts in cancer, tumour angiogenesis and endothelial cell migration. Angiogenesis 2008, 11(1):13-21.
27. Marlow R., Binnewies M., Sorensen L.K., Monica S.D., Strickland P., Forsberg E.C., Li D.Y., Hinck L. Vascular Robo4 restricts proangiogenic VEGF signaling in breast. Proceedings of the National Academy of Sciences of the United States of America 2010, 107(23):10520-10525.
28. Okada Y., Yano K., Jin E., Funahashi N., Kitayama M., Doi T., Spokes K., Beeler D.L., Shih S.C., Okada H., Danilov T.A., Maynard E., Minami T., Oettgen P., Aird W.C. A three-kilobase fragment of the human Robo4 promoter directs cell type-specific expression in endothelium. Circulation Research 2007, 100(12):1712-1722.
29. Park K.W., Morrison C.M., Sorensen L.K., Jones C.A., Rao Y., Chien C.B., Wu J.Y., Urness L.D., Li D.Y. Robo4 is a vascular-specific receptor that inhibits endothelial migration. Developmental Biology 2003, 261(1):251-267.
30. Parker A.L., McVey J.H., Doctor J.H., Lopez-Franco O., Waddington S.N., Havenga M.J., Nicklin S.A., Baker A.H. Influence of coagulation factor zymogens on the infectivity of adenoviruses pseudotyped with fibers from subgroup D. Journal of Virology 2007, 81(7):3627-3631.
31. Parker A.L., Waddington S.N., Nicol C.G., Shayakhmetov D.M., Buckley S.M., Denby L., Kemball-Cook G., Ni S., Lieber A., McVey J.H., Nicklin S.A., Baker A.H. Multiple vitamin K-dependent coagulation zymogens promote adenovirus-mediated gene delivery to hepatocytes. Blood 2006, 108(8):2554-2561.
32. Preuss M.A., Glasgow J.N., Everts M., Stoff-Khalili M.A., Wu H., Curiel D.T. Enhanced Gene Delivery to Human Primary Endothelial Cells Using Tropism-Modified Adenovirus Vectors. Open Gene Therapy Journal 2008, 1:7-11.
33. Reynolds P.N., Nicklin S.A., Kaliberova L., Boatman B.G., Grizzle W.E., Balyasnikova I.V., Baker A.H., Danilov S.M., Curiel D.T. Combined transductional and transcriptional targeting improves the specificity of transgene expression in vivo. Nature Biotechnology 2001, 19(9):838-842.
34. Savontaus M.J., Sauter B.V., Huang T.G., Woo S.L. Transcriptional targeting of conditionally replicating adenovirus to dividing endothelial cells. Gene Therapy 2002, 9(14):972-979.
35. Seth P., Lin Y., Hanai J., Shivalingappa V., Duyao M.P., Sukhatme V.P. Magic roundabout, a tumor endothelial marker: expression and signaling. Biochemical and Biophysical Research Communications 2005, 332(2):533-541.
36. Sharma A., Bangari D.S., Tandon M., Hogenesch H., Mittal S.K. Evaluation of innate immunity and vector toxicity following inoculation of bovine, porcine or human adenoviral vectors in a mouse model. Virus Research 2010, 153(1):134-142.
37. Shashkova E.V., Doronin K., Senac J.S., Barry M.A. Macrophage depletion combined with anticoagulant therapy increases therapeutic window of systemic treatment with oncolytic adenovirus. Cancer Research 2008, 68(14):5896-5904.
38. Shayakhmetov D.M., Gaggar A., Ni S., Li Z.Y., Lieber A. Adenovirus binding to blood factors results in liver cell infection and hepatotoxicity. Journal of Virology 2005, 79(12):7478-7491.
39. Shinozaki K., Suominen E., Carrick F., Sauter B., Kahari V.M., Lieber A., Woo S.L., Savontaus M. Efficient infection of tumor endothelial cells by a capsid-modified adenovirus. Gene Therapy 2006, 13(1):52-59.
40. Short J.J., Rivera A.A., Wu H., Walter M.R., Yamamoto M., Mathis J.M., Curiel D.T. Substitution of adenovirus serotype 3 hexon onto a serotype 5 oncolytic adenovirus reduces factor X binding, decreases liver tropism, and improves antitumor efficacy. Molecular Cancer Therapeutics 2010, 9(9):2536-2544.
41. Smith-Berdan S., Nguyen A., Hassanein D., Zimmer M., Ugarte F., Ciriza J., Li D., Garcia-Ojeda M.E., Hinck L., Forsberg E.C. Robo4 cooperates with CXCR4 to specify hematopoietic stem cell localization to bone marrow niches. Cell Stem Cell 2011, 8(1):72-83.
42. Song W., Sun Q., Dong Z., Spencer D.M., Nunez G., Nor J.E. Antiangiogenic gene therapy: disruption of neovascular networks mediated by inducible caspase-9 delivered with a transcriptionally targeted adenoviral vector. Gene Therapy 2005, 12(4):320-329.
43. Takayama K., Reynolds P.N., Adachi Y., Kaliberova L., Uchino J., Nakanishi Y., Curiel D.T. Vascular endothelial growth factor promoter-based conditionally replicative adenoviruses for pan-carcinoma application. Cancer Gene Therapy 2007, 14(1):105-116.
44. Tallone T., Malin S., Samuelsson A., Wilbertz J., Miyahara M., Okamoto K., Poellinger L., Philipson L., Pettersson S. A mouse model for adenovirus gene delivery. Proceedings of the National Academy of Sciences of the United States of America 2001, 98(14):7910-7915.
45. Waddington S.N., McVey J.H., Bhella D., Parker A.L., Barker K., Atoda H., Pink R., Buckley S.M., Greig J.A., Denby L., Custers J., Morita T., Francischetti I.M., Monteiro R.Q., Barouch D.H., van Rooijen N., Napoli C., Havenga M.J., Nicklin S.A., Baker A.H. Adenovirus serotype 5 hexon mediates liver gene transfer. Cell 2008, 132(3):397-409.
46. Wickham T.J., Mathias P., Cheresh D.A., Nemerow G.R. Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment. Cell 1993, 73(2):309-319.
47. Work L.M., Buning H., Hunt E., Nicklin S.A., Denby L., Britton N., Leike K., Odenthal M., Drebber U., Hallek M., Baker A.H. Vascular bed-targeted in vivo gene delivery using tropism-modified adeno-associated viruses. Molecular Therapy 2006, 13(4):683-693.
48. Wu H., Dmitriev I., Kashentseva E., Seki T., Wang M., Curiel D.T. Construction and characterization of adenovirus serotype 5 packaged by serotype 3 hexon. Journal of Virology 2002, 76(24):12775-12782.
49. Wung B.S., Ni C.W., Wang D.L. ICAM-1 induction by TNFalpha and IL-6 is mediated by distinct pathways via Rac in endothelial cells. Journal of Biomedical Science 2005, 12(1):91-101.
50. Xu Z., Qiu Q., Tian J., Smith J.S., Conenello G.M., Morita T., Byrnes A.P. Coagulation factor X shields adenovirus type 5 from attack by natural antibodies and complement. Nature Medicine 2013, 19(4):452-457.
51. Yang W.Y., Huang Z.H., Lin L.J., Li Z., Yu J.L., Song H.J., Qian Y., Che X.Y. Kinase domain insert containing receptor promoter controlled suicide gene system selectively kills human umbilical vein endothelial cells. World Journal of Gastroenterology 2006, 12(33):5331-5335.
52. Zhang X., Yu J., Kuzontkoski P.M., Zhu W., Li D.Y., Groopman J.E. Slit2/Robo4 signaling modulates HIV-1 gp120-induced lymphatic hyperpermeability. PLOS Pathogens 2012, 8(1):e1002461.
53. Zhuang X., Cross D., Heath V.L., Bicknell R. Shear stress, tip cells and regulators of endothelial migration. Biochemical Society Transactions 2011, 39(6):1571-1575.
54. Zinn K.R., Szalai A.J., Stargel A., Krasnykh V., Chaudhuri T.R. Bioluminescence imaging reveals a significant role for complement in liver transduction following intravenous delivery of adenovirus. Gene Therapy 2004, 11(19):1482-1486.