Adenoviruses with an αvβ integrin targeting moiety in the fiber shaft or the HI-loop increase tumor specificity without compromising antitumor efficacy in magnetic resonance imaging of colorectal cancer metastases

Journal of Translational Medicine

Volumn 8, Issue , 2010, Pages

  Lavilla Alonso, Sergio ^a,b   Bauerschmitz, Gerd ^c   Abo Ramadan, Usama ^b   Halavaara, Juha ^b   Escutenaire, Sophie ^a,b   Diaconu, Iulia ^a,b   Tatlisumak, Turgut ^b   Kanerva, Anna ^a,b   Hemminki, Akseli ^a,b   Pesonen, Sari ^a,b  

^a UNIVERSITY OF HELSINKI   (Finland)

^b HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^c HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHAVBETA INTEGRIN; ARGINYLGLYCYLASPARTIC ACID; CONDITIONALLY REPLICATING ADENOVIRUS; INTEGRIN; UNCLASSIFIED DRUG; ARGINYL-GLYCYL-ASPARTIC ACID; INTEGRIN ALPHAVBETA1; OLIGOPEPTIDE; VITRONECTIN RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; COLORECTAL CANCER; CONTROLLED STUDY; DRUG EFFICACY; DRUG POTENCY; DRUG SAFETY; DRUG SPECIFICITY; DRUG TARGETING; FEMALE; HUMAN; HUMAN CELL; LIVER METASTASIS; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; ONCOLYTIC VIROTHERAPY; SYSTEMIC THERAPY; VIRAL GENE DELIVERY SYSTEM; ADENOVIRUS; ANIMAL; ANTIBODY SPECIFICITY; CHEMISTRY; COLORECTAL TUMOR; CYTOTOXICITY; DRUG SCREENING; GENE TRANSFER; GENE VECTOR; GENETICS; LIVER TUMOR; METABOLISM; METASTASIS; PATHOLOGY; PHYSIOLOGY; SPLEEN TUMOR; TISSUE DISTRIBUTION; TUMOR CELL LINE; VIRUS CAPSID; VIRUS REPLICATION;

ADENOVIRIDAE; ANIMALS; CAPSID; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; CYTOTOXICITY, IMMUNOLOGIC; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; HUMANS; LIVER NEOPLASMS; MAGNETIC RESONANCE IMAGING; MICE; NEOPLASM METASTASIS; OLIGOPEPTIDES; ORGAN SPECIFICITY; RECEPTORS, VITRONECTIN; SPLENIC NEOPLASMS; TISSUE DISTRIBUTION; VIRUS REPLICATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 77955830323     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/1479-5876-8-80     Document Type: Article

References (43)

1. Center MM, Jemal A, Ward E. International trends in colorectal cancer incidence rates. Cancer Epidemiol Biomarkers Prev 2009, 18:1688-1694. 10.1158/1055-9965.EPI-09-0090, 19505900.
2. Coleman MP, Quaresma M, Berrino F, Lutz JM, De Angelis R, Capocaccia R, Baili P, Rachet B, Gatta G, Hakulinen T, et al. Cancer survival in five continents: a worldwide population-based study (CONCORD). Lancet Oncol 2008, 9:730-756. 10.1016/S1470-2045(08)70179-7, 18639491.
3. Reid T, Galanis E, Abbruzzese J, Sze D, Andrews J, Romel L, Hatfield M, Rubin J, Kirn D. Intra-arterial administration of a replication-selective adenovirus (dl1520) in patients with colorectal carcinoma metastatic to the liver: a phase I trial. Gene Ther 2001, 8:1618-1626. 10.1038/sj.gt.3301512, 11895000.
4. Nemunaitis J, Cunningham C, Buchanan A, Blackburn A, Edelman G, Maples P, Netto G, Tong A, Randlev B, Olson S, Kirn D. Intravenous infusion of a replication-selective adenovirus (ONYX-015) in cancer patients: safety, feasibility and biological activity. Gene Ther 2001, 8:746-759. 10.1038/sj.gt.3301424, 11420638.
5. Sangro B, Mazzolini G, Ruiz J, Herraiz M, Quiroga J, Herrero I, Benito A, Larrache J, Pueyo J, Subtil JC, et al. Phase I trial of intratumoral injection of an adenovirus encoding interleukin-12 for advanced digestive tumors. J Clin Oncol 2004, 22:1389-1397. 10.1200/JCO.2004.04.059, 15084613.
6. 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. 10.1038/sj.cgt.7700988, 17139321.
7. Nemunaitis J, Tong AW, Nemunaitis M, Senzer N, Phadke AP, Bedell C, Adams N, Zhang YA, Maples PB, Chen S, et al. A Phase I Study of Telomerase-specific Replication Competent Oncolytic Adenovirus (Telomelysin) for Various Solid Tumors. Mol Ther 2009, 18(2):429-34. 10.1038/mt.2009.262, 19935775.
8. Li JL, Liu HL, Zhang XR, Xu JP, Hu WK, Liang M, Chen SY, Hu F, Chu DT. A phase I trial of intratumoral administration of recombinant oncolytic adenovirus overexpressing HSP70 in advanced solid tumor patients. Gene Ther 2009, 16:376-382. 10.1038/gt.2008.179, 19092859.
9. Reid TR, Freeman S, Post L, McCormick F, Sze DY. Effects of Onyx-015 among metastatic colorectal cancer patients that have failed prior treatment with 5-FU/leucovorin. Cancer Gene Ther 2005, 12:673-681. 10.1038/sj.cgt.7700819, 15803147.
10. Reid T, Galanis E, Abbruzzese J, Sze D, Wein LM, Andrews J, Randlev B, Heise C, Uprichard M, Hatfield M, et al. Hepatic arterial infusion of a replication-selective oncolytic adenovirus (dl1520): phase II viral, immunologic, and clinical endpoints. Cancer Res 2002, 62:6070-6079.
11. Tolcher AW, Hao D, de Bono J, Miller A, Patnaik A, Hammond LA, Smetzer L, Van Wart Hood J, Merritt J, Rowinsky EK, et al. Phase I, pharmacokinetic, and pharmacodynamic study of intravenously administered Ad5CMV-p53, an adenoviral vector containing the wild-type p53 gene, in patients with advanced cancer. J Clin Oncol 2006, 24:2052-2058. 10.1200/JCO.2005.03.6756, 16648505.
12. Small EJ, Carducci MA, Burke JM, Rodriguez R, Fong L, van Ummersen L, Yu DC, Aimi J, Ando D, Working P, et al. A phase I trial of intravenous CG7870, a replication-selective, prostate-specific antigen-targeted oncolytic adenovirus, for the treatment of hormone-refractory, metastatic prostate cancer. Mol Ther 2006, 14:107-117. 10.1016/j.ymthe.2006.02.011, 16690359.
13. Worgall S, Wolff G, Falck-Pedersen E, Crystal RG. Innate immune mechanisms dominate elimination of adenoviral vectors following in vivo administration. Hum Gene Ther 1997, 8:37-44. 10.1089/hum.1997.8.1-37, 8989993.
14. Shayakhmetov DM, Gaggar A, Ni S, Li ZY, Lieber A. Adenovirus binding to blood factors results in liver cell infection and hepatotoxicity. J Virol 2005, 79:7478-7491. 10.1128/JVI.79.12.7478-7491.2005, 1143681, 15919903.
15. Parker AL, Waddington SN, Nicol CG, Shayakhmetov DM, Buckley SM, Denby L, Kemball-Cook G, Ni S, Lieber A, McVey JH, et al. Multiple vitamin K-dependent coagulation zymogens promote adenovirus-mediated gene delivery to hepatocytes. Blood 2006, 108:2554-2561. 10.1182/blood-2006-04-008532, 16788098.
16. Parker AL, McVey JH, Doctor JH, Lopez-Franco O, Waddington SN, Havenga MJ, Nicklin SA, Baker AH. Influence of coagulation factor zymogens on the infectivity of adenoviruses pseudotyped with fibers from subgroup D. J Virol 2007, 81:3627-3631. 10.1128/JVI.02786-06, 1866077, 17251290.
17. Baker AH, McVey JH, Waddington SN, Di Paolo NC, Shayakhmetov DM. The influence of blood on in vivo adenovirus bio-distribution and transduction. Mol Ther 2007, 15:1410-1416. 10.1038/sj.mt.6300206, 17505469.
18. 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 Natl Acad Sci USA 2008, 105:5483-5488. 10.1073/pnas.0711757105, 2291105, 18391209.
19. 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.
20. 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.
21. Alemany R, Curiel DT. CAR-binding ablation does not change biodistribution and toxicity of adenoviral vectors. Gene Ther 2001, 8:1347-1353. 10.1038/sj.gt.3301515, 11571572.
22. Bergelson JM, Cunningham JA, Droguett G, Kurt-Jones EA, Krithivas A, Hong JS, Horwitz MS, Crowell RL, Finberg RW. Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 1997, 275:1320-1323. 10.1126/science.275.5304.1320, 9036860.
23. Wickham TJ, Mathias P, Cheresh DA, Nemerow GR. Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment. Cell 1993, 73:309-319. 10.1016/0092-8674(93)90231-E, 8477447.
24. Einfeld DA, Schroeder R, Roelvink PW, Lizonova A, King CR, Kovesdi I, Wickham TJ. Reducing the native tropism of adenovirus vectors requires removal of both CAR and integrin interactions. J Virol 2001, 75:11284-11291. 10.1128/JVI.75.23.11284-11291.2001, 114713, 11689608.
25. Martin K, Brie A, Saulnier P, Perricaudet M, Yeh P, Vigne E. Simultaneous CAR- and alpha V integrin-binding ablation fails to reduce Ad5 liver tropism. Mol Ther 2003, 8:485-494. 10.1016/S1525-0016(03)00182-5, 12946322.
26. Smith TA, Idamakanti N, Rollence ML, Marshall-Neff J, Kim J, Mulgrew K, Nemerow GR, Kaleko M, Stevenson SC. Adenovirus serotype 5 fiber shaft influences in vivo gene transfer in mice. Hum Gene Ther 2003, 14:777-787. 10.1089/104303403765255165, 12804140.
27. Bayo-Puxan N, Cascallo M, Gros A, Huch M, Fillat C, Alemany R. Role of the putative heparan sulfate glycosaminoglycan-binding site of the adenovirus type 5 fiber shaft on liver detargeting and knob-mediated retargeting. J Gen Virol 2006, 87:2487-2495. 10.1099/vir.0.81889-0, 16894186.
28. Smith T, Idamakanti N, Kylefjord H, Rollence M, King L, Kaloss M, Kaleko M, Stevenson SC. In vivo hepatic adenoviral gene delivery occurs independently of the coxsackievirus-adenovirus receptor. Mol Ther 2002, 5:770-779. 10.1006/mthe.2002.0613, 12027562.
29. Smith TA, Idamakanti N, Marshall-Neff J, Rollence ML, Wright P, Kaloss M, King L, Mech C, Dinges L, Iverson WO, et al. Receptor interactions involved in adenoviral-mediated gene delivery after systemic administration in non-human primates. Hum Gene Ther 2003, 14:1595-1604. 10.1089/104303403322542248, 14633402.
30. Bayo-Puxan N, Gimenez-Alejandre M, Lavilla-Alonso S, Gros A, Cascallo M, Hemminki A, Alemany R. Replacement of adenovirus type 5 fiber shaft heparan sulfate proteoglycan-binding domain with RGD for improved tumor infectivity and targeting. Hum Gene Ther 2009, 20:1214-1221. 10.1089/hum.2009.038, 19537946.
31. Yu HK, Kim JS, Lee HJ, Ahn JH, Lee SK, Hong SW, Yoon Y. Suppression of colorectal cancer liver metastasis and extension of survival by expression of apolipoprotein(a) kringles. Cancer Res 2004, 64:7092-7098. 10.1158/0008-5472.CAN-04-0364, 15466205.
32. 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. J Gene Med 2009, 11:966-977. 10.1002/jgm.1373, 19670332.
33. Conti JA, Kendall TJ, Bateman A, Armstrong TA, Papa-Adams A, Xu Q, Packham G, Primrose JN, Benyon RC, Iredale JP. The desmoplastic reaction surrounding hepatic colorectal adenocarcinoma metastases aids tumor growth and survival via alphav integrin ligation. Clin Cancer Res 2008, 14:6405-6413. 10.1158/1078-0432.CCR-08-0816, 2590496, 18927279.
34. McCarty JH. Alphav integrins lead the way for colorectal metastases. Clin Cancer Res 2008, 14:6351-6353. 10.1158/1078-0432.CCR-08-1847, 2688736, 18927272.
35. Fujita S, Watanabe M, Kubota T, Teramoto T, Kitajima M. Alteration of expression in integrin beta 1-subunit correlates with invasion and metastasis in colorectal cancer. Cancer Lett 1995, 91:145-149. 10.1016/0304-3835(95)03735-F, 7538447.
36. Logunov DY, Zubkova OV, Karyagina-Zhulina AS, Shuvalova EA, Karpov AP, Shmarov MM, Tutykhina IL, Alyapkina YS, Grezina NM, Zinovieva NA, et al. Identification of HI-like loop in CELO adenovirus fiber for incorporation of receptor binding motifs. J Virol 2007, 81:9641-9652. 10.1128/JVI.00534-07, 2045437, 17596306.
37. Kimball KJ NT, Barnes MN, Makhija S, Wang M, Siegal GP, Harris R, Aurigemma R, Alvarez RD. A phase I study of a tropism modified conditionally replicative adenovirus (CRAd) for recurrent ovarian cancer. Mol Ther 2008, 16(Supplement 1):S113.
38. Gros SJ, Dohrmann T, Peldschus K, Schurr PG, Kaifi JT, Kalinina T, Reichelt U, Mann O, Strate TG, Adam G, et al. Complementary use of fluorescence and MR imaging of metastatic esophageal cancer in a novel orthotopic mouse model. Int J Cancer 2009, 126(11):2671-81.
39. Rajput A, Dominguez San Martin I, Rose R, Beko A, Levea C, Sharratt E, Mazurchuk R, Hoffman RM, Brattain MG, Wang J. Characterization of HCT116 human colon cancer cells in an orthotopic model. J Surg Res 2008, 147:276-281. 10.1016/j.jss.2007.04.021, 17961596.
40. Fechner H, Haack A, Wang H, Wang X, Eizema K, Pauschinger M, Schoemaker R, Veghel R, Houtsmuller A, Schultheiss HP, et al. Expression of coxsackie adenovirus receptor and alphav-integrin does not correlate with adenovector targeting in vivo indicating anatomical vector barriers. Gene Ther 1999, 6:1520-1535. 10.1038/sj.gt.3301030, 10490761.
41. Nettelbeck DM, Rivera AA, Kupsch J, Dieckmann D, Douglas JT, Kontermann RE, Alemany R, Curiel DT. Retargeting of adenoviral infection to melanoma: combining genetic ablation of native tropism with a recombinant bispecific single-chain diabody (scDb) adapter that binds to fiber knob and HMWMAA. Int J Cancer 2004, 108:136-145. 10.1002/ijc.11563, 14618628.
42. Wu H, Seki T, Dmitriev I, Uil T, Kashentseva E, Han T, Curiel DT. Double modification of adenovirus fiber with RGD and polylysine motifs improves coxsackievirus-adenovirus receptor-independent gene transfer efficiency. Hum Gene Ther 2002, 13:1647-1653. 10.1089/10430340260201734, 12228019.
43. Cascallo M, Alonso MM, Rojas JJ, Perez-Gimenez A, Fueyo J, Alemany R. Systemic toxicity-efficacy profile of ICOVIR-5, a potent and selective oncolytic adenovirus based on the pRB pathway. Mol Ther 2007, 15:1607-1615. 10.1038/sj.mt.6300239, 17579575.