Influence of vector design and host cell on the mechanism of recombination and emergence of mutant subpopulations of replicating retroviral vectors

BMC Molecular Biology

Volumn 10, Issue , 2009, Pages

  Paar, Matthias ^a,b   Klein, Dieter ^a   Salmons, Brian ^c   Günzburg, Walter H ^a,b   Renner, Matthias ^a   Portsmouth, Daniel ^a,b  

^a UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^b INSTITUTE FOR MICROELECTRONICS   (Austria)

^c Austrianova Singapore Pte Ltd   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

RETROVIRUS VECTOR; RNA;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL CULTURE; CONTROLLED STUDY; DNA SEQUENCE; HOST CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOLONEY LEUKEMIA ONCOVIRUS; MOUSE; MURINE LEUKEMIA VIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN MOTIF; PROTEIN SECONDARY STRUCTURE; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOLID TUMOR; TRANSGENE; VIRAL GENE DELIVERY SYSTEM; VIRUS GENOME; VIRUS MUTANT; VIRUS RECOMBINATION; VIRUS REPLICATION; VIRUS STRAIN; ANIMAL; CELL LINE; CELL STRAIN 3T3; GENE DELETION; GENE VECTOR; GENETIC RECOMBINATION; GENETICS; METABOLISM; MOLECULAR GENETICS; NUDE MOUSE; RETROVIRUS; TUMOR CELL LINE;

MURINAE;

ANIMALS; BASE SEQUENCE; CELL LINE; CELL LINE, TUMOR; GENETIC VECTORS; HUMANS; MALE; MICE; MICE, NUDE; MOLECULAR SEQUENCE DATA; NIH 3T3 CELLS; RECOMBINATION, GENETIC; RETROVIRIDAE; SEQUENCE DELETION; VIRUS REPLICATION;

EID: 61449212911     PISSN: None     EISSN: 14712199     Source Type: Journal    
DOI: 10.1186/1471-2199-10-8     Document Type: Article

References (73)

1. Hu WS Rhodes T Dang Q Pathak V Retroviral recombination: Review of genetic analyses Front Biosci 2003, 8:d143-155. 12456341
2. Negroni M Buc H Mechanisms of retroviral recombination Annual review of genetics 2001, 35:275-302. 11700285
3. Negroni M Buc H Retroviral recombination: What drives the switch? Nature reviews 2001, 2(2):151-155. 11252957
4. Svarovskaia ES Cheslock SR Zhang WH Hu WS Pathak VK Retroviral mutation rates and reverse transcriptase fidelity Front Biosci 2003, 8:d117-134. 12456349
5. Preston BD Dougherty JP Mechanisms of retroviral mutation Trends in microbiology 1996, 4(1):16-21. 8824790
6. Zhang J Tang LY Li T Ma Y Sapp CM Most retroviral recombinations occur during minus-strand DNA synthesis J Virol 2000, 74(5):2313-2322. 111713 10666262
7. Zhang J Host RNA polymerase II makes minimal contributions to retroviral frame-shift mutations The Journal of general virology 2004, 85(Pt 8):2389-2395. 15269381
8. Menendez-Arias L Molecular basis of fidelity of DNA synthesis and nucleotide specificity of retroviral reverse transcriptases Prog Nucleic Acid Res Mol Biol 2002, 71:91-147. 12102562
9. Zhang J Ma Y Evidence for retroviral intramolecular recombinations Journal of virology 2001, 75(14):6348-6358. 114357 11413301
10. Zhang J Sapp CM Recombination between two identical sequences within the same retroviral RNA molecule Journal of virology 1999, 73(7):5912-5917. 112652 10364343
11. Li T Zhang J Intramolecular recombinations of Moloney murine leukemia virus occur during minus-strand DNA synthesis Journal of virology 2002, 76(19):9614-9623. 136483 12208940
12. Hu WS Temin HM Retroviral recombination and reverse transcription Science 1990, 250(4985):1227-1233. 1700865
13. Stuhlmann H Berg P Homologous recombination of copackaged retrovirus RNAs during reverse transcription Journal of virology 1992, 66(4):2378-2388. 289033 1372369
14. Hu WS Temin HM Genetic consequences of packaging two RNA genomes in one retroviral particle: Pseudodiploidy and high rate of genetic recombination Proceedings of the National Academy of Sciences of the United States of America 1990, 87(4):1556-1560. 53514 2304918
15. Yu H Jetzt AE Ron Y Preston BD Dougherty JP The nature of human immunodeficiency virus type 1 strand transfers The Journal of biological chemistry 1998, 273(43):28384-28391. 9774465
16. Edelstein ML Abedi MR Wixon J Edelstein RM Gene therapy clinical trials worldwide 1989-2004-an overview The journal of gene medicine 2004, 6(6):597-602. 15170730
17. Vile RG Tuszynski A Castleden S Retroviral vectors. From laboratory tools to molecular medicine Molecular biotechnology 1996, 5(2):139-158. 8734426
18. Rainov NG A phase III clinical evaluation of herpes simplex virus type 1 thymidine kinase and ganciclovir gene therapy as an adjuvant to surgical resection and radiation in adults with previously untreated glioblastoma multiforme Human gene therapy 2000, 11(17):2389-2401. 11096443
19. Rainov NG Ren H Clinical trials with retrovirus mediated gene therapy - what have we learned? Journal of neuro-oncology 2003, 65(3):227-236. 14682373
20. Finger C Sun Y Sanz L Alvarez-Vallina L Buchholz CJ Cichutek K Replicating retroviral vectors mediating continuous production and secretion of therapeutic gene products from cancer cells Cancer gene therapy 2005, 12(5):464-474. 15692609
21. Jespersen T Duch M Carrasco ML Warming S Pedersen FS Expression of heterologous genes from an IRES translational cassette in replication competent murine leukemia virus vectors Gene 1999, 239(2):227-235. 10548723
22. Logg CR Logg A Matusik RJ Bochner BH Kasahara N Tissue-specific transcriptional targeting of a replication-competent retroviral vector Journal of virology 2002, 76(24):12783-12791. 136666 12438603
23. Logg CR Tai CK Logg A Anderson WF Kasahara N A uniquely stable replication-competent retrovirus vector achieves efficient gene delivery in vitro and in solid tumors Hum Gene Ther 2001, 12(8):921-932. 11387057
24. Metzl C Mischek D Salmons B Gunzburg WH Renner M Portsmouth D Tissue- and tumor-specific targeting of murine leukemia virus-based replication-competent retroviral vectors J Virol 2006, 80(14):7070-7078. 1489065 16809312
25. Sliva K Schnierle BS Stable integration of a functional shRNA expression cassette into the murine leukemia virus genome Virology 2006, 351(1):218-225. 16631223
26. Solly SK Trajcevski S Frisen C Holzer GW Nelson E Clerc B Abordo-Adesida E Castro M Lowenstein P Klatzmann D Replicative retroviral vectors for cancer gene therapy Cancer gene therapy 2003, 10(1):30-39. 12489026
27. Hiraoka K Kimura T Logg CR Kasahara N Tumor-selective gene expression in a hepatic metastasis model after locoregional delivery of a replication-competent retrovirus vector Clin Cancer Res 2006, 12(23):7108-7116. 17145835
28. Hiraoka K Kimura T Logg CR Tai CK Haga K Lawson GW Kasahara N Therapeutic efficacy of replication-competent retrovirus vector-mediated suicide gene therapy in a multifocal colorectal cancer metastasis model Cancer Res 2007, 67(11):5345-5353. 17545615
29. Kikuchi E Menendez S Ozu C Ohori M Cordon-Cardo C Logg CR Kasahara N Bochner BH Delivery of replication-competent retrovirus expressing Escherichia coli purine nucleoside phosphorylase increases the metabolism of the prodrug, fludarabine phosphate and suppresses the growth of bladder tumor xenografts Cancer Gene Ther 2007, 14(3):279-286. 17218950
30. Sun Y Finger C Alvarez-Vallina L Cichutek K Buchholz CJ Chronic gene delivery of interferon-inducible protein 10 through replication-competent retrovirus vectors suppresses tumor growth Cancer Gene Ther 2005, 12(11):900-912. 15905858
31. Tai CK Wang WJ Chen TC Kasahara N Single-shot, multicycle suicide gene therapy by replication-competent retrovirus vectors achieves long-term survival benefit in experimental glioma Mol Ther 2005, 12(5):842-851. 16257382
32. Wang WJ Tai CK Kasahara N Chen TC Highly efficient and tumor-restricted gene transfer to malignant gliomas by replication-competent retroviral vectors Hum Gene Ther 2003, 14(2):117-127. 12614563
33. Shin NH Hartigan-O'Connor D Pfeiffer JK Telesnitsky A Replication of lengthened Moloney murine leukemia virus genomes is impaired at multiple stages Journal of virology 2000, 74(6):2694-2702. 111759 10684285
34. Nethe M Berkhout B Kuyl van der AC Retroviral superinfection resistance Retrovirology 2005, 2:52. 1224871 16107223
35. Paar M Schwab S Rosenfellner D Salmons B Gunzburg WH Renner M Portsmouth D Effects of viral strain, transgene position, and target cell type on replication kinetics, genomic stability, and transgene expression of replication-competent murine leukemia virus-based vectors Journal of virology 2007, 81(13):6973-6983. 1933297 17442710
36. An W Telesnitsky A Effects of varying sequence similarity on the frequency of repeat deletion during reverse transcription of a human immunodeficiency virus type 1 vector Journal of virology 2002, 76(15):7897-7902. 136404 12097604
37. Pfeiffer JK Telesnitsky A Effects of limiting homology at the site of intermolecular recombinogenic template switching during Moloney murine leukemia virus replication Journal of virology 2001, 75(23):11263-11274. 114711 11689606
38. Hanson MN Balakrishnan M Roques BP Bambara RA Effects of donor and acceptor RNA structures on the mechanism of strand transfer by HIV-1 reverse transcriptase Journal of molecular biology 2005, 353(4):772-787. 16216274
39. Moumen A Polomack L Unge T Veron M Buc H Negroni M Evidence for a mechanism of recombination during reverse transcription dependent on the structure of the acceptor RNA The Journal of biological chemistry 2003, 278(18):15973-15982. 12595540
40. Roda RH Balakrishnan M Kim JK Roques BP Fay PJ Bambara RA Strand transfer occurs in retroviruses by a pause-initiated two-step mechanism The Journal of biological chemistry 2002, 277(49):46900-46911. 12370183
41. Laimins LA Khoury G Gorman C Howard B Gruss P Host-specific activation of transcription by tandem repeats from simian virus 40 and Moloney murine sarcoma virus Proceedings of the National Academy of Sciences of the United States of America 1982, 79(21):6453-6457. 347144 6292901
42. Robson ND Telesnitsky A Selection of optimal polypurine tract region sequences during Moloney murine leukemia virus replication Journal of virology 2000, 74(22):10293-10303. 110903 11044073
43. Jang SK Wimmer E Cap-independent translation of encephalomyocarditis virus RNA: Structural elements of the internal ribosomal entry site and involvement of a cellular 57-kD RNA-binding protein Genes Dev 1990, 4(9):1560-1572. 2174810
44. Pilipenko EV Blinov VM Chernov BK Dmitrieva TM Agol VI Conservation of the secondary structure elements of the 5′-untranslated region of cardio- and aphthovirus RNAs Nucleic Acids Res 1989, 17(14):5701-5711. 318190 2548167
45. Dalba C Klatzmann D Logg CR Kasahara N Beyond oncolytic virotherapy: replication-competent retrovirus vectors for selective and stable transduction of tumors Current gene therapy 2005, 5(6):655-667. 16457654
46. Logg CR Logg A Tai CK Cannon PM Kasahara N Genomic stability of murine leukemia viruses containing insertions at the Env-3' untranslated region boundary Journal of virology 2001, 75(15):6989-6998. 114427 11435579
47. O'Neill RR Hartley JW Repaske R Kozak CA Amphotropic proviral envelope sequences are absent from the Mus germ line J Virol 1987, 61(7):2225-2231. 283686 3035222
48. Bakhanashvili M Hizi A Fidelity of the RNA-dependent DNA synthesis exhibited by the reverse transcriptases of human immunodeficiency virus types 1 and 2 and of murine leukemia virus: Mispair extension frequencies Biochemistry 1992, 31(39):9393-9398. 1382590
49. Negroni M Buc H Recombination during reverse transcription: An evaluation of the role of the nucleocapsid protein Journal of molecular biology 1999, 286(1):15-31. 9931246
50. Onafuwa A An W Robson ND Telesnitsky A Human immunodeficiency virus type 1 genetic recombination is more frequent than that of Moloney murine leukemia virus despite similar template switching rates Journal of virology 2003, 77(8):4577-4587. 152108 12663764
51. Roda RH Balakrishnan M Hanson MN Wohrl BM Le Grice SF Roques BP Gorelick RJ Bambara RA Role of the Reverse Transcriptase, Nucleocapsid Protein, and Template Structure in the Two-step Transfer Mechanism in Retroviral Recombination The Journal of biological chemistry 2003, 278(34):31536-31546. 12801926
52. Bakhanashvili M p53 enhances the fidelity of DNA synthesis by human immunodeficiency virus type 1 reverse transcriptase Oncogene 2001, 20(52):7635-7644. 11753641
53. Bakhanashvili M Exonucleolytic proofreading by p53 protein European journal of biochemistry/FEBS 2001, 268(7):2047-2054. 11277927
54. Bakhanashvili M Novitsky E Lilling G Rahav G P53 in cytoplasm may enhance the accuracy of DNA synthesis by human immunodeficiency virus type 1 reverse transcriptase Oncogene 2004, 23(41):6890-6899. 15286711
55. Franca R Spadari S Maga G APOBEC deaminases as cellular antiviral factors: A novel natural host defense mechanism Med Sci Monit 2006, 12(5):RA92-98. 16641889
56. Holmes RK Malim MH Bishop KN APOBEC-mediated viral restriction: Not simply editing? Trends in biochemical sciences 2007, 32(3):118-128. 17303427
57. Towers GJ Control of viral infectivity by tripartite motif proteins Human gene therapy 2005, 16(10):1125-1132. 16218773
58. Towers GJ The control of viral infection by tripartite motif proteins and cyclophilin A Retrovirology 2007, 4:40. 1906832 17565686
59. Chimploy K Tassotto ML Mathews CK Ribonucleotide reductase, a possible agent in deoxyribonucleotide pool asymmetries induced by hypoxia The Journal of biological chemistry 2000, 275(50):39267-39271. 11006282
60. Julias JG Pathak VK Deoxyribonucleoside triphosphate pool imbalances in vivo are associated with an increased retroviral mutation rate Journal of virology 1998, 72(10):7941-7949. 110126 9733832
61. Pfeiffer JK Topping RS Shin NH Telesnitsky A Altering the intracellular environment increases the frequency of tandem repeat deletion during Moloney murine leukemia virus reverse transcription Journal of virology 1999, 73(10):8441-8447. 112863 10482596
62. Li T Zhang J Retroviral recombination is temperature dependent The Journal of general virology 2001, 82(Pt 6):1359-1364. 11369880
63. Malboeuf CM Isaacs SJ Tran NH Kim B Thermal effects on reverse transcription: Improvement of accuracy and processivity in cDNA synthesis BioTechniques 2001, 30(5):1074-1078. 11355343
64. Harrison GP Mayo MS Hunter E Lever AM Pausing of reverse transcriptase on retroviral RNA templates is influenced by secondary structures both 5' and 3' of the catalytic site Nucleic acids research 1998, 26(14):3433-3442. 147721 9649630
65. Klarmann GJ Schauber CA Preston BD Template-directed pausing of DNA synthesis by HIV-1 reverse transcriptase during polymerization of HIV-1 sequences in vitro The Journal of biological chemistry 1993, 268(13):9793-9802. 7683663
66. Lanciault C Champoux JJ Pausing during reverse transcription increases the rate of retroviral recombination Journal of virology 2006, 80(5):2483-2494. 1369041 16474155
67. Duch M Carrasco ML Jespersen T Aagaard L Pedersen FS An RNA secondary structure bias for non-homologous reverse transcriptase-mediated deletions in vivo Nucleic acids research 2004, 32(6):2039-2048. 390364 15069126
68. Duch M Carrasco ML Jespersen T Hansen BD Pedersen FS Transgene stability for three replication-competent murine leukemia virus vectors Gene 2004, 329:61-69. 15033529
69. Hilberg F Stocking C Ostertag W Grez M Functional analysis of a retroviral host-range mutant: Altered long terminal repeat sequences allow expression in embryonal carcinoma cells Proceedings of the National Academy of Sciences of the United States of America 1987, 84(15):5232-5236. 298829 3037539
70. Januszeski MM Cannon PM Chen D Rozenberg Y Anderson WF Functional analysis of the cytoplasmic tail of Moloney murine leukemia virus envelope protein Journal of virology 1997, 71(5):3613-3619. 191509 9094634
71. Yang C Compans RW Analysis of the murine leukemia virus R peptide: delineation of the molecular determinants which are important for its fusion inhibition activity Journal of virology 1997, 71(11):8490-8496. 192312 9343206
72. Olson P Temin HM Dornburg R Unusually high frequency of reconstitution of long terminal repeats in U3-minus retrovirus vectors by DNA recombination or gene conversion Journal of virology 1992, 66(3):1336-1343. 240855 1310753
73. Klein D Bugl B Gunzburg WH Salmons B Accurate estimation of transduction efficiency necessitates a multiplex real-time PCR Gene therapy 2000, 7(6):458-463. 10757018