Skip to main content
Top
Published in: Virology Journal 1/2011

Open Access 01-12-2011 | Research

Truncating the i-leader open reading frame enhances release of human adenovirus type 5 in glioma cells

Authors: Sanne K van den Hengel, Jeroen de Vrij, Taco G Uil, Martine L Lamfers, Peter AE Sillevis Smitt, Rob C Hoeben

Published in: Virology Journal | Issue 1/2011

Login to get access

Abstract

Background

The survival of glioma patients with the current treatments is poor. Early clinical trails with replicating adenoviruses demonstrated the feasibility and safety of the use of adenoviruses as oncolytic agents. Antitumor efficacy has been moderate due to inefficient virus replication and spread. Previous studies have shown that truncation of the adenovirus i-leader open reading frame enhanced cytopathic activity of HAdV-5 in several tumor cell lines. Here we report the effect of an i-leader mutation on the cytopathic activity in glioma cell lines and in primary high-grade glioma cell cultures.

Results

A mutation truncating the i-leader open reading frame was created in a molecular clone of replication-competent wild-type HAdV-5 by site-directed mutagenesis. We analyzed the cytopathic activity of this RL-07 mutant virus. A cell-viability assay showed increased cytopathic activity of the RL-07 mutant virus on U251 and SNB19 glioma cell lines. The plaque sizes of RL-07 on U251 monolayers were seven times larger than those of isogenic control viruses. Similarly, the cytopathic activity of the RL-07 viruses was strongly increased in six primary high-grade glioma cell cultures. In glioma cell lines the RL-07 virus was found to be released earlier into the culture medium. This was not due to enhanced viral protein synthesis, as was evident from equivalent E1A, Fiber and Adenovirus Death Protein amounts, nor to higher virus yields.

Conclusion

The cytopathic activity of replicating adenovirus in glioblastoma cells is increased by truncating the i-leader open reading frame. Such mutations may help enhancing the antitumor cytopathic efficacy of oncolytic adenoviruses in the treatment of glioblastoma.
Appendix
Available only for authorised users
Literature
1.
go back to reference Chiocca EA, Abbed KM, Tatter S, Louis DN, Hochberg FH, Barker F, et al.: A phase I open-label, dose-escalation, multi-institutional trial of injection with an E1B-Attenuated adenovirus, ONYX-015, into the peritumoral region of recurrent malignant gliomas, in the adjuvant setting. Mol Ther 2004, 10: 585-598. 10.1016/j.ymthe.2004.07.021CrossRef Chiocca EA, Abbed KM, Tatter S, Louis DN, Hochberg FH, Barker F, et al.: A phase I open-label, dose-escalation, multi-institutional trial of injection with an E1B-Attenuated adenovirus, ONYX-015, into the peritumoral region of recurrent malignant gliomas, in the adjuvant setting. Mol Ther 2004, 10: 585-598. 10.1016/j.ymthe.2004.07.021CrossRef
2.
go back to reference Forsyth P, Roldan G, George D, Wallace C, Palmer CA, Morris D, et al.: A phase I trial of intratumoral administration of reovirus in patients with histologically confirmed recurrent malignant gliomas. Mol Ther 2008, 16: 627-632. 10.1038/sj.mt.6300403CrossRefPubMed Forsyth P, Roldan G, George D, Wallace C, Palmer CA, Morris D, et al.: A phase I trial of intratumoral administration of reovirus in patients with histologically confirmed recurrent malignant gliomas. Mol Ther 2008, 16: 627-632. 10.1038/sj.mt.6300403CrossRefPubMed
3.
go back to reference Markert JM, Medlock MD, Rabkin SD, Gillespie GY, Todo T, Hunter WD, et al.: Conditionally replicating herpes simplex virus mutant, G207 for the treatment of malignant glioma: results of a phase I trial. Gene Ther 2000, 7: 867-874. 10.1038/sj.gt.3301205CrossRefPubMed Markert JM, Medlock MD, Rabkin SD, Gillespie GY, Todo T, Hunter WD, et al.: Conditionally replicating herpes simplex virus mutant, G207 for the treatment of malignant glioma: results of a phase I trial. Gene Ther 2000, 7: 867-874. 10.1038/sj.gt.3301205CrossRefPubMed
4.
go back to reference Pulkkanen KJ, Yla-Herttuala S: Gene therapy for malignant glioma: current clinical status. Mol Ther 2005, 12: 585-598. 10.1016/j.ymthe.2005.07.357CrossRefPubMed Pulkkanen KJ, Yla-Herttuala S: Gene therapy for malignant glioma: current clinical status. Mol Ther 2005, 12: 585-598. 10.1016/j.ymthe.2005.07.357CrossRefPubMed
5.
go back to reference Sonabend AM, Ulasov IV, Lesniak MS: Conditionally replicative adenoviral vectors for malignant glioma. Rev Med Virol 2006, 16: 99-115. 10.1002/rmv.490CrossRefPubMed Sonabend AM, Ulasov IV, Lesniak MS: Conditionally replicative adenoviral vectors for malignant glioma. Rev Med Virol 2006, 16: 99-115. 10.1002/rmv.490CrossRefPubMed
6.
go back to reference Glasgow JN, Everts M, Curiel DT: Transductional targeting of adenovirus vectors for gene therapy. Cancer Gene Ther 2006, 13: 830-844. 10.1038/sj.cgt.7700928PubMedCentralCrossRefPubMed Glasgow JN, Everts M, Curiel DT: Transductional targeting of adenovirus vectors for gene therapy. Cancer Gene Ther 2006, 13: 830-844. 10.1038/sj.cgt.7700928PubMedCentralCrossRefPubMed
7.
go back to reference De Vrij J, Uil TG, van den Hengel SK, Cramer SJ, Koppers-Lalic D, Verweij MC, et al.: Adenovirus targeting to HLA-A1/MAGE-A1-positive tumor cells by fusing a single-chain T-cell receptor with minor capsid protein IX. Gene Ther 2008, 15: 978-989. 10.1038/gt.2008.26CrossRefPubMed De Vrij J, Uil TG, van den Hengel SK, Cramer SJ, Koppers-Lalic D, Verweij MC, et al.: Adenovirus targeting to HLA-A1/MAGE-A1-positive tumor cells by fusing a single-chain T-cell receptor with minor capsid protein IX. Gene Ther 2008, 15: 978-989. 10.1038/gt.2008.26CrossRefPubMed
8.
go back to reference Van Houdt WJ, Wu H, Glasgow JN, Lamfers ML, Dirven CM, Gillespie GY, et al.: Gene delivery into malignant glioma by infectivity-enhanced adenovirus: in vivo versus in vitro models. Neuro Oncol 2007, 9: 280-290. 10.1215/15228517-2007-017PubMedCentralCrossRefPubMed Van Houdt WJ, Wu H, Glasgow JN, Lamfers ML, Dirven CM, Gillespie GY, et al.: Gene delivery into malignant glioma by infectivity-enhanced adenovirus: in vivo versus in vitro models. Neuro Oncol 2007, 9: 280-290. 10.1215/15228517-2007-017PubMedCentralCrossRefPubMed
9.
go back to reference Brouwer E, Havenga MJ, Ophorst O, de Leeuw B, Gijsbers L, Gillissen G, et al.: Human adenovirus type 35 vector for gene therapy of brain cancer: improved transduction and bypass of pre-existing anti-vector immunity in cancer patients. Cancer Gene Ther 2007, 14: 211-219. 10.1038/sj.cgt.7701010CrossRefPubMed Brouwer E, Havenga MJ, Ophorst O, de Leeuw B, Gijsbers L, Gillissen G, et al.: Human adenovirus type 35 vector for gene therapy of brain cancer: improved transduction and bypass of pre-existing anti-vector immunity in cancer patients. Cancer Gene Ther 2007, 14: 211-219. 10.1038/sj.cgt.7701010CrossRefPubMed
10.
go back to reference Nandi S, Ulasov IV, Rolle CE, Han Y, Lesniak MS: A chimeric adenovirus with an Ad 3 fiber knob modification augments glioma virotherapy. J Gene Med 2009, 11: 1005-1011. 10.1002/jgm.1385PubMedCentralCrossRefPubMed Nandi S, Ulasov IV, Rolle CE, Han Y, Lesniak MS: A chimeric adenovirus with an Ad 3 fiber knob modification augments glioma virotherapy. J Gene Med 2009, 11: 1005-1011. 10.1002/jgm.1385PubMedCentralCrossRefPubMed
11.
go back to reference Zheng S, Ulasov IV, Han Y, Tyler MA, Zhu ZB, Lesniak MS: Fiber-knob modifications enhance adenoviral tropism and gene transfer in malignant glioma. J Gene Med 2007, 9: 151-160. 10.1002/jgm.1008CrossRefPubMed Zheng S, Ulasov IV, Han Y, Tyler MA, Zhu ZB, Lesniak MS: Fiber-knob modifications enhance adenoviral tropism and gene transfer in malignant glioma. J Gene Med 2007, 9: 151-160. 10.1002/jgm.1008CrossRefPubMed
12.
go back to reference Bischoff JR, Kirn DH, Williams A, Heise C, Horn S, Muna M, et al.: An adenovirus mutant that replicates selectively in p53-deficient human tumor cells. Science 1996, 274: 373-376. 10.1126/science.274.5286.373CrossRefPubMed Bischoff JR, Kirn DH, Williams A, Heise C, Horn S, Muna M, et al.: An adenovirus mutant that replicates selectively in p53-deficient human tumor cells. Science 1996, 274: 373-376. 10.1126/science.274.5286.373CrossRefPubMed
13.
go back to reference Edwards SJ, Dix BR, Myers CJ, Dobson-Le D, Huschtscha L, Hibma M, et al.: Evidence that Replication of the Antitumor Adenovirus ONYX-015 Is Not Controlled by the p53 and p14ARF Tumor Suppressor Genes. J Virol 2002, 76: 437-445. Edwards SJ, Dix BR, Myers CJ, Dobson-Le D, Huschtscha L, Hibma M, et al.: Evidence that Replication of the Antitumor Adenovirus ONYX-015 Is Not Controlled by the p53 and p14ARF Tumor Suppressor Genes. J Virol 2002, 76: 437-445.
14.
go back to reference Subramanian T, Vijayalingam S, Chinnadurai G: Genetic identification of adenovirus type 5 genes that influence viral spread. J Virol 2006, 80: 2000-2012. 10.1128/JVI.80.4.2000-2012.2006PubMedCentralCrossRefPubMed Subramanian T, Vijayalingam S, Chinnadurai G: Genetic identification of adenovirus type 5 genes that influence viral spread. J Virol 2006, 80: 2000-2012. 10.1128/JVI.80.4.2000-2012.2006PubMedCentralCrossRefPubMed
15.
go back to reference Yan W, Kitzes G, Dormishian F, Hawkins L, Sampson-Johannes A, Watanabe J, et al.: Developing novel oncolytic adenoviruses through bioselection. J Virol 2003, 77: 2640-2650. 10.1128/JVI.77.4.2640-2650.2003PubMedCentralCrossRefPubMed Yan W, Kitzes G, Dormishian F, Hawkins L, Sampson-Johannes A, Watanabe J, et al.: Developing novel oncolytic adenoviruses through bioselection. J Virol 2003, 77: 2640-2650. 10.1128/JVI.77.4.2640-2650.2003PubMedCentralCrossRefPubMed
16.
go back to reference Symington JS, Lucher LA, Brackmann KH, Virtanen A, Pettersson U, Green M: Biosynthesis of adenovirus type 2 i-leader protein. J Virol 1986, 57: 848-856.PubMedCentralPubMed Symington JS, Lucher LA, Brackmann KH, Virtanen A, Pettersson U, Green M: Biosynthesis of adenovirus type 2 i-leader protein. J Virol 1986, 57: 848-856.PubMedCentralPubMed
17.
go back to reference Soloway PD, Shenk T: The adenovirus type 5 i-leader open reading frame functions in cis to reduce the half-life of L1 mRNAs. J Virol 1990, 64: 551-558.PubMedCentralPubMed Soloway PD, Shenk T: The adenovirus type 5 i-leader open reading frame functions in cis to reduce the half-life of L1 mRNAs. J Virol 1990, 64: 551-558.PubMedCentralPubMed
18.
go back to reference de Leeuw B, Su M, ter Horst M, Iwata S, Rodijk M, Hoeben RC, et al.: Increased glia-specific transgene expression with glial fibrillary acidic protein promoters containing multiple enhancer elements. J Neurosci Res 2006, 83: 744-753. 10.1002/jnr.20776CrossRefPubMed de Leeuw B, Su M, ter Horst M, Iwata S, Rodijk M, Hoeben RC, et al.: Increased glia-specific transgene expression with glial fibrillary acidic protein promoters containing multiple enhancer elements. J Neurosci Res 2006, 83: 744-753. 10.1002/jnr.20776CrossRefPubMed
19.
go back to reference Chartier C, Degryse E, Gantzer M, Dieterle A, Pavirani A, Mehtali M: Efficient generation of recombinant adenovirus vectors by homologous recombination in Escherichia coli. J Virol 1996, 70: 4805-4810.PubMedCentralPubMed Chartier C, Degryse E, Gantzer M, Dieterle A, Pavirani A, Mehtali M: Efficient generation of recombinant adenovirus vectors by homologous recombination in Escherichia coli. J Virol 1996, 70: 4805-4810.PubMedCentralPubMed
20.
go back to reference Fallaux FJ, Kranenburg O, Cramer SJ, Houweling A, Van Ormondt H, Hoeben RC, et al.: Characterization of 911: a new helper cell line for the titration and propagation of early region 1-deleted adenoviral vectors. Hum Gene Ther 1996, 7: 215-222. 10.1089/hum.1996.7.2-215CrossRefPubMed Fallaux FJ, Kranenburg O, Cramer SJ, Houweling A, Van Ormondt H, Hoeben RC, et al.: Characterization of 911: a new helper cell line for the titration and propagation of early region 1-deleted adenoviral vectors. Hum Gene Ther 1996, 7: 215-222. 10.1089/hum.1996.7.2-215CrossRefPubMed
21.
go back to reference Murakami P, McCaman MT: Quantitation of adenovirus DNA and virus particles with the PicoGreen fluorescent Dye. Anal Biochem 1999, 274: 283-288. 10.1006/abio.1999.4282CrossRefPubMed Murakami P, McCaman MT: Quantitation of adenovirus DNA and virus particles with the PicoGreen fluorescent Dye. Anal Biochem 1999, 274: 283-288. 10.1006/abio.1999.4282CrossRefPubMed
22.
go back to reference Hong JS, Engler JA: The amino terminus of the adenovirus fiber protein encodes the nuclear localization signal. Virology 1991, 185: 758-767. 10.1016/0042-6822(91)90547-OCrossRefPubMed Hong JS, Engler JA: The amino terminus of the adenovirus fiber protein encodes the nuclear localization signal. Virology 1991, 185: 758-767. 10.1016/0042-6822(91)90547-OCrossRefPubMed
23.
go back to reference Harlow E, Franza BR, Schley C: Monoclonal antibodies specific for adenovirus early region 1A proteins: extensive heterogeneity in early region 1A products. J Virol 1985, 55: 533-546.PubMedCentralPubMed Harlow E, Franza BR, Schley C: Monoclonal antibodies specific for adenovirus early region 1A proteins: extensive heterogeneity in early region 1A products. J Virol 1985, 55: 533-546.PubMedCentralPubMed
24.
go back to reference Tollefson AE, Scaria A, Saha SK, Wold WS: The 11,600-MW protein encoded by region E3 of adenovirus is expressed early but is greatly amplified at late stages of infection. J Virol 1992, 66: 3633-3642.PubMedCentralPubMed Tollefson AE, Scaria A, Saha SK, Wold WS: The 11,600-MW protein encoded by region E3 of adenovirus is expressed early but is greatly amplified at late stages of infection. J Virol 1992, 66: 3633-3642.PubMedCentralPubMed
25.
go back to reference Tollefson AE, Scaria A, Hermiston TW, Ryerse JS, Wold LJ, Wold WS: The adenovirus death protein (E3-11.6K) is required at very late stages of infection for efficient cell lysis and release of adenovirus from infected cells. J Virol 1996, 70: 2296-2306.PubMedCentralPubMed Tollefson AE, Scaria A, Hermiston TW, Ryerse JS, Wold LJ, Wold WS: The adenovirus death protein (E3-11.6K) is required at very late stages of infection for efficient cell lysis and release of adenovirus from infected cells. J Virol 1996, 70: 2296-2306.PubMedCentralPubMed
26.
go back to reference Driesse MJ, Vincent AJPE, Smitt PS, Kros JM, Hoogerbrugge PM, Avezaat CJJ, et al.: Intracerebral injection of adenovirus harboring the HSVtk gene combined with ganciclovir administration: toxicity study in nonhuman primates. Gene Ther 1998, 5: 1122-1129. 10.1038/sj.gt.3300695CrossRefPubMed Driesse MJ, Vincent AJPE, Smitt PS, Kros JM, Hoogerbrugge PM, Avezaat CJJ, et al.: Intracerebral injection of adenovirus harboring the HSVtk gene combined with ganciclovir administration: toxicity study in nonhuman primates. Gene Ther 1998, 5: 1122-1129. 10.1038/sj.gt.3300695CrossRefPubMed
27.
go back to reference Driesse MJ, Esandi MC, Kros JM, Avezaat CJJ, Vecht C, Zurcher C, et al.: Intra-CSF administered recombinant adenovirus causes an immune response-mediated toxicity. Gene Ther 2000, 7: 1401-1409. 10.1038/sj.gt.3301250CrossRefPubMed Driesse MJ, Esandi MC, Kros JM, Avezaat CJJ, Vecht C, Zurcher C, et al.: Intra-CSF administered recombinant adenovirus causes an immune response-mediated toxicity. Gene Ther 2000, 7: 1401-1409. 10.1038/sj.gt.3301250CrossRefPubMed
28.
go back to reference Horst M, Brouwer E, Verwijnen S, Rodijk M, De JM, Hoeben R, et al.: Targeting malignant gliomas with a glial fibrillary acidic protein (GFAP)-selective oncolytic adenovirus. J Gene Med 2007, 9: 1071-1079. 10.1002/jgm.1110CrossRefPubMed Horst M, Brouwer E, Verwijnen S, Rodijk M, De JM, Hoeben R, et al.: Targeting malignant gliomas with a glial fibrillary acidic protein (GFAP)-selective oncolytic adenovirus. J Gene Med 2007, 9: 1071-1079. 10.1002/jgm.1110CrossRefPubMed
29.
go back to reference Sillevis Smitt P, Driesse M, Wolbers J, Kros M, Avezaat C: Treatment of relapsed malignant glioma with an adenoviral vector containing the herpes simplex thymidine kinase gene followed by ganciclovir. Mol Ther 2003, 7: 851-858. 10.1016/S1525-0016(03)00100-XCrossRef Sillevis Smitt P, Driesse M, Wolbers J, Kros M, Avezaat C: Treatment of relapsed malignant glioma with an adenoviral vector containing the herpes simplex thymidine kinase gene followed by ganciclovir. Mol Ther 2003, 7: 851-858. 10.1016/S1525-0016(03)00100-XCrossRef
30.
go back to reference Vincent AJ, Esandi MC, Avezaat CJ, Vecht CJ, Sillevis Smitt P, van Bekkum DW, et al.: Preclinical testing of recombinant adenoviral herpes simplex virus-thymidine kinase gene therapy for central nervous system malignancies. Neurosurgery 1997, 41: 451-452. 10.1097/00006123-199708000-00023CrossRef Vincent AJ, Esandi MC, Avezaat CJ, Vecht CJ, Sillevis Smitt P, van Bekkum DW, et al.: Preclinical testing of recombinant adenoviral herpes simplex virus-thymidine kinase gene therapy for central nervous system malignancies. Neurosurgery 1997, 41: 451-452. 10.1097/00006123-199708000-00023CrossRef
Metadata
Title
Truncating the i-leader open reading frame enhances release of human adenovirus type 5 in glioma cells
Authors
Sanne K van den Hengel
Jeroen de Vrij
Taco G Uil
Martine L Lamfers
Peter AE Sillevis Smitt
Rob C Hoeben
Publication date
01-12-2011
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2011
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/1743-422X-8-162

Other articles of this Issue 1/2011

Virology Journal 1/2011 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine