Mathematical model of the rate-limiting steps for retrovirus-mediated gene transfer into mammalian cells

Biotechnology and Bioengineering

Volumn 105, Issue 1, 2010, Pages 195-209

  Tayi, Venkata S ^a,b   Bowen, Bruce D ^b   Piret, James M ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Gene therapy; Integrated virus copy number; Kinetic and mass transport modeling; Retroviral transduction; Spinoculation; Transduction efficiency

Indexed keywords

CELL CYTOPLASM; CELL NUCLEUS; CELL SURFACES; COPY NUMBER; CYTOSOLS; DESIGN AND OPTIMIZATION; EXPERIMENTAL DATA; INTERMEDIATE COMPLEX; K562 CELLS; MAMMALIAN CELLS; MASS TRANSPORT; MODEL PREDICTION; NUCLEAR IMPORT; RATE LIMITING; RATE-LIMITING STEPS; RETROVIRAL TRANSDUCTION; RETROVIRAL VECTORS; REVERSE TRANSCRIPTION; TARGET CELLS; TIME-SCALES; TRANSDUCTION EFFICIENCY; VIRAL VECTORS; VIRUS POPULATION;

BACTERIOPHAGES; CELL MEMBRANES; CENTRIFUGATION; COMPUTER SIMULATION; CYTOLOGY; DNA; GENE THERAPY; GENE TRANSFER; MAMMALS; MASS TRANSFER; POPULATION STATISTICS; RNA; TRANSCRIPTION; VECTORS;

MATHEMATICAL MODELS;

VIRUS VECTOR;

ARTICLE; CELL NUCLEUS; CELL STRAIN K 562; CELL SURFACE; CYTOPLASM; DIFFUSION; GENE THERAPY; GENE TRANSFER; GIBBON LEUKEMIA VIRUS; MAMMAL CELL; MATHEMATICAL MODEL; NONHUMAN; NUCLEAR IMPORT; RETROVIRUS; REVERSE TRANSCRIPTION; VIRUS ATTACHMENT;

ANIMALS; CELL LINE, TUMOR; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; HUMANS; MODELS, THEORETICAL; RETROVIRIDAE; TRANSDUCTION, GENETIC;

GIBBON APE LEUKEMIA VIRUS; HUMAN SPUMARETROVIRUS; MAMMALIA;

EID: 73949161044     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.22515     Document Type: Article

References (58)

1. Andreadis ST, Palsson BO. 1996. Kinetics of retrovirus mediated gene transfer: The importance of intracellular half-life of retroviruses. J Theor Biol 182(1):1-20.
2. Andreadis ST, Brott D, Fuller AO, Palsson BO. 1997. Moloney murine leukemia virus-derived retroviral vectors decay intracellularly with a half-life in the range of 5.5-7.5 h. J Virol 71(10):7541-7548.
3. Andreadis S, Lavery T, Davis HE, Le Doux JM, Yarmush ML, Morgan JR. 2000. Toward a more accurate quantitation of the activity of recombinant retroviruses: Alternatives to titer and multiplicity of infection. J Virol 74(7):3431-3439.
4. Arai T, Takada M, Ui M, Iba H. 1999. Dose-dependent transduction of vesicular stomatitis virus G protein-pseudotyped retrovirus vector into human solid tumor cell lines and murine fibroblasts. Virology 260(1): 109-115.
5. Bahnson AB, Dunigan JT, Baysal BE, Mohney T, Atchison RW, Nimgaonkar MT, Ball ED, Barranger JA. 1995. Centrifugal enhancement of retroviral mediated gene-transfer. J Virol Methods 54(2-3):131-143.
6. Barbosa P, Charneau P, Dumey N, Clavel F. 1994. Kinetic analysis of HIV-1 early replicative steps in a coculture system. AIDS Res Hum Retro-viruses 10(1):53-59.
7. Baum C, Dullmann J, Li ZX, Fehse B, Meyer J, Williams DA, von Kalle C. 2003. Side effects of retroviral gene transfer into hematopoietic stem cells. Blood 101(6):2099-2114.
8. Bell P, Montaner LJ, Maul GG. 2001. Accumulation and intranuclear distribution of unintegrated human immunodeficiency virus type 1 DNA. J Virol 75(16):7683-7691.
9. Berg HC, Purcell EM. 1977. Physics of chemoreception. Biophys J 20(2):193-219.
10. Chen ISY, Temin HM. 1982. Establishment of infection by spleen necrosis virus: Inhibition in stationary cells and the role of secondary infection. J Virol 41(1):183-191.
11. Chuck AS, Palsson BO. 1996. Consistent and high rates of gene transfer can be obtained using flow-through transduction over a wide range of retroviral titers. Hum Gene Ther 7(6):743-750.
12. Chuck AS, Clarke MF, Palsson BO. 1996. Retroviral infection is limited by Brownian motion. Hum Gene Ther 7(13):1527-1534.
13. Coelen RJ, Jose DG, May JT. 1983. The effect of hexadimethrine bromide (polybrene) on the infection of the primate retroviruses SSV1/SSAV1 and BAEV. Arch Virol 75(4):307-311.
14. Coffin JM, Hughes SH, Varmus HE. 1997. Retroviruses. New York: Cold Spring Harbor Laboratory Press. p. 843.
15. Cornetta K, Anderson WF. 1989. Protamine sulfate as an effective alternative to polybrene in retroviral-mediated gene-transfer - Implications for human-gene therapy. J Virol Methods 23(2):187-194.
16. Coroadinha AS, Silva AC, Pires E, Coelho A, Alves PM, Carrondo MJT. 2006. Effect of osmotic pressure on the production of retroviral vectors: Enhancement in vector stability. Biotechnol Bioeng 94(2):322-329.
17. Davis HE, Rosinski M, Morgan JR, Yarmush ML. 2004. Charged polymers modulate retrovirus transduction via membrane charge neutralization and virus aggregation. Biophys J 86(2):1234-1242.
18. Dee KU, Shuler ML. 1997. Mathematical model of the trafficking of acid-dependent enveloped viruses: Application to the binding, uptake, and nuclear accumulation of baculovirus. Biotechnol Bioeng 54(5):468-490.
19. Dee KU, Hammer DA, Shuler ML. 1995. A model of the binding, entry, uncoating, and RNA-synthesis of semliki-forest-virus in baby hamster-kidney (BHK-21) cells. Biotechnol Bioeng 46(5):485-496.
20. Edelstein ML, Abedi MR, Wixon J. 2007. Gene therapy clinical trials worldwide to 2007 - An update. J Gene Med 9(10):833-842.
21. Fassati A, Goff SP. 1999. Characterization of intracellular reverse transcription complexes of Moloney murine leukemia virus. J Virol 73(11): 8919-8925.
22. Fields BN, Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE. 2007. Fields virology. Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins. p. 3177.
23. Fritsch EF, Temin HM. 1977. Inhibition of viral-DNA synthesis in stationary chicken-embryo fibroblasts infected with avian retroviruses. J Virol 24(2):461-469.
24. Goulaouic H, Subra F, Mouscadet JF, Carteau S, Auclair C. 1994. Exogenous nucleosides promote the completion of MoMLV DNA-synthesis in G0-arrested BALB-C/3T3 fibroblasts. Virology 200(1):87-97.
25. Hanenberg H, Xiao XL, Dilloo D, Hashino K, Kato I, Williams DA. 1996. Colocalization of retrovirus and target cells on specific fibronectin fragments increases genetic transduction of mammalian cells. Nat Med 2(8):876-882.
26. Harel J, Rassart E, Jolicoeur P. 1981. Cell-cycle dependence of synthesis of unintegrated viral-DNA in mouse cells newly infected with murine leukemia virus. Virology 110(1):202-207.
27. Hennemann B, Conneally E, Pawliuk R, Leboulch P, Rose-John S, Reid D, Chuo JY, Humphries RK, Eaves CJ. 1999. Optimization of retroviral-mediated gene transfer to human NOD SCID mouse repopulating cord blood cells through a systematic analysis of protocol variables. Exp Hematol 27(5):817-825.
28. Hu WS, Temin HM. 1990. Retroviral recombination and reverse transcription. Science 250(4985):1227-1233.
29. Jones JS, Allan RW, Temin HM. 1994. One retroviral RNA is sufficient for synthesis of viral-DNA. J Virol 68(1):207-216.
30. Kaptein LCM, Greijer AE, Valerio D, vanBeusechem VW. 1997. Optimized conditions for the production of recombinant amphotropic retroviral vector preparations. Gene Therapy 4(2):172-176.
31. Kolokoltsov AA, Davey RA. 2004. Rapid and sensitive detection of retro-virus entry by using a novel luciferase-based content-mixing assay. J Virol 78(10):5124-5132.
32. Kotani H, Newton PB, Zhang SY, Chiang YWL, Otto E, Weaver L, Blaese RM, Anderson WF, Mcgarrity GJ. 1994. Improved methods of retroviral vector transduction and production for gene-therapy. Hum Gene Ther 5(1):19-28.
33. Kustikova OS, Wahlers A, Kuhicke K, Stahle B, Zander AR, Baum C, Fehse B. 2003. Dose finding with retroviral vectors: Correlation of retroviral vector copy numbers in single cells with gene transfer efficiency in a cell population. Blood 102(12):3934-3937.
34. Kwon YJ, Peng CA. 2002. Transduction rate constant as more reliable index quantifying efficiency of retroviral gene delivery. Biotechnol Bioeng 77(6):668-677.
35. Kwon YJ, Hung G, Anderson WF, Peng CA, Yu H. 2003. Determination of infectious retrovirus concentration from colony-forming assay with quantitative analysis. J Virol 77(10):5712-5720.
36. Le Doux JM. 1998. Analysis of retrovirus production and transduction. New Brunswick, NJ: Rutgers University. 234 p.
37. Le Doux JM, Davis HE, Morgan JR, Yarmush ML. 1999. Kinetics of retrovirus production and decay. Biotechnol Bioeng 63(6):654-662.
38. Lee YMH, Coffin JM. 1991. Relationship of avian retrovirus DNA-synthesis to integration invitro. Mol Cell Biol 11(3):1419-1430.
39. Lewis PF, Emerman M. 1994. Passage through mitosis is required for oncoretroviruses but not for the human immunodeficiency virus. J Virol 68(1):510-516.
40. Lim KI, Narayan S, Young JAT, Yin J. 2004. Effects of lipid rafts on dynamics of retroviral entry and trafficking: Quantitative analysis. Biotechnol Bioeng 86(6):650-660.
41. McDonald D, Vodicka MA, Lucero G, Svitkina TM, Borisy GG, Emerman M, Hope TJ. 2002. Visualization of the intracellular behavior of HIV in living cells. J Cell Biol 159(3):441-452.
42. Miller AD, Garcia JV, Vonsuhr N, Lynch CM, Wilson C, Eiden MV. 1991. Construction and properties of retrovirus packaging cells based on gibbon ape leukemia virus. J Virol 65(5):2220-2224.
43. Moolten FL, Cupples LA. 1992. A model for predicting the risk of cancer consequent to retroviral gene therapy. Hum Gene Ther 3(5):479-486.
44. Narayan S, Barnard RJO, Young JAT. 2003. Two retroviral entry pathways distinguished by lipid raft association of the viral receptor and differences in viral infectivity. J Virol 77(3):1977-1983.
45. O'Brien WA, Namazi A, Kalhor H, Mao SH, Zack JA, Chen ISY. 1994. Kinetics of human-immunodeficiency-virus type-1 reverse transcription in blood mononuclear phagocytes are slowed by limitations of nucleotide precursors. J Virol 68(2):1258-1263.
46. O'Doherty U, Swiggard WJ, Malim MH. 2000. Human immunodeficiency virus type 1 spinoculation enhances infection through virus binding. J Virol 74(21):10074-10080.
47. Panganiban AT, Fiore D. 1988. Ordered interstrand and intrastrand DNA transfer during reverse transcription. Science 241(4869):1064-1069.
48. Patankar SV. 1980. Numerical heat transfer and fluid flow. New York: McGraw-Hill. 218 p.
49. Quintas-Cardama A, Yeh RK, Hollyman D, Stefanski J, Taylor C, Nikhamin Y, Imperato G, Sadelain M, Riviere I, Brentjens RJ. 2007. Multifactorial optimization of gammaretroviral gene transfer into human T lymphocytes for clinical application. Hum Gene Ther 18(12):1253-1260.
50. Rethwilm A. 2007. Foamy virus vectors: An awaited alternative to gammaretro-and lentiviral vectors. Curr Gene Ther 7(4):261-271.
51. Roe T, Reynolds TC, Yu G, Brown PO. 1993. Integration of murine leukemia virus DNA depends on mitosis. EMBO J 12(5):2099-2108.
52. Roe T, Chow SA, Brown PO. 1997. 30-end processing and kinetics of 5′-end joining during retroviral integration in vivo. J Virol 71(2):1334-1340.
53. Scherer F, Anton M, Schillinger U, Henkel J, Bergemann C, Kruger A, Gansbacher B, Plank C. 2002. Magnetofection: Enhancing and targeting gene delivery by magnetic force in vitro and in vivo. Gene Ther 9(2): 102-109.
54. Smoluchowski Mv. 1917. Versuch einer mathematischen theorie der koagulationskinetik kolloidaler lösungen. Z Phys Chem 92(2):129-168.
55. Springett GM, Moen RC, Anderson S, Blaese RM, Anderson WF. 1989. Infection efficiency of T-lymphocytes with amphotropic retroviral vectors is cell-cycle dependent. J Virol 63(9):3865-3869.
56. Varmus HE, Padgett T, Heasley S, Simon G, Bishop JM. 1977. Cellular functions are required for synthesis and integration of avian sarcoma virus specific DNA. Cell 11(2):307-319.
57. Wahlers A, Schwieger M, Li Z, Meier-Tackmann D, Lindemann C, Eckert HG, von Laer D, Baum C. 2001. Influence of multiplicity of infection and protein stability on retroviral vector-mediated gene expression in hematopoietic cells. Gene Ther 8(6):477-486.
58. Wolf D, Goff SP. 2008. Host restriction factors blocking retroviral replication. Annu Rev Genet 42:143-163.