Ocular gene delivery using lentiviral vectors

Gene Therapy

Volumn 19, Issue 2, 2012, Pages 145-153

  Balaggan, K S ^a,b   Ali, R R ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b MOORFIELDS EYE HOSPITAL   (United Kingdom)

Author keywords

choroidal neovascularization; glaucoma; lentivirus; ocular; retinal degeneration

Indexed keywords

ANGIOSTATIN; BETA GLUCURONIDASE; CILIARY NEUROTROPHIC FACTOR; CYCLOOXYGENASE 2; ENDOSTATIN; FIBROBLAST GROWTH FACTOR 2; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 10; LENTIVIRUS VECTOR; MYOCILIN; PHOSPHODIESTERASE; PIGMENT EPITHELIUM DERIVED FACTOR; PROSTAGLANDIN F RECEPTOR; PROSTAGLANDIN RECEPTOR; PROSTAGLANDIN SYNTHASE; PROTEIN; PROTEIN ABCA4; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 1;

BIOENGINEERING; BIOSAFETY; DRUG SAFETY; EYE DISEASE; GENE EXPRESSION; GENE TARGETING; GENE TRANSFER; HUMAN; NONHUMAN; PRIMATE; PRIORITY JOURNAL; REVIEW; VIRAL GENE DELIVERY SYSTEM;

ANIMALS; CHOROIDAL NEOVASCULARIZATION; DISEASE MODELS, ANIMAL; GENE EXPRESSION; GENE THERAPY; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; GLAUCOMA; HUMANS; LENTIVIRUS; RETINAL DEGENERATION;

ANIMALIA; LENTIVIRUS; PRIMATES;

EID: 84856966481     PISSN: 09697128     EISSN: 14765462     Source Type: Journal    
DOI: 10.1038/gt.2011.153     Document Type: Review

References (89)

1. Lever AM, Strappe PM, Zhao J. Lentiviral vectors. J Biomed Sci 2004; 11: 439-449. (Pubitemid 38721027)
2. Martin-Rendon E, Azzouz M, Mazarakis ND. Lentiviral vectors for the treatment of neurodegenerative diseases. Curr Opin Mol Ther 2001; 3: 476-481. (Pubitemid 32999000)
3. Azzouz M, Kingsman SM, Mazarakis ND. Lentiviral vectors for treating and modeling human CNS disorders. J Gene Med 2004; 6: 951-962. (Pubitemid 40228110)
4. Maury W. Regulation of equine infectious anemia virus expression. J Biomed Sci 1998; 5: 11-23. (Pubitemid 28150194)
5. Srinivasakumar N. HIV-1 vector systems. Somat Cell Mol Genet 2001; 26: 51-81. (Pubitemid 35332979)
6. Olsen JC. EIAV, CAEV and other lentivirus vector systems. Somat Cell Mol Genet 2001; 26: 131-145. (Pubitemid 35332982)
7. Miyoshi H, Takahashi M, Gage FH, Verma IM. Stable and efficient gene transfer into the retina using an HIV-based lentiviral vector. Proc Natl Acad Sci USA 1997; 94: 10319-10323. (Pubitemid 27407039)
8. Bainbridge JW, Stephens C, Parsley K, Demaison C, Halfyard A, Thrasher AJ et al. In vivo gene transfer to the mouse eye using an HIV-based lentiviral vector; efficient longterm transduction of corneal endothelium and retinal pigment epithelium. Gene Therapy 2001; 8: 1665-1668. (Pubitemid 33085588)
9. Harvey AR, Kamphuis W, Eggers R, Symons NA, Blits B, Niclou S et al. Intravitreal injection of adeno-associated viral vectors results in the transduction of different types of retinal neurons in neonatal and adult rats: a comparison with lentiviral vectors. Mol Cell Neurosci 2002; 21: 141-157. (Pubitemid 35178505)
10. Kostic C, Chiodini F, Salmon P, Wiznerowicz M, Deglon N, Hornfeld D et al. Activity analysis of housekeeping promoters using self-inactivating lentiviral vector delivery into the mouse retina. Gene Therapy 2003; 10: 818-821. (Pubitemid 36621827)
11. Auricchio A, Kobinger G, Anand V, Hildinger M, O'Connor E, Maguire AM et al. Exchange of surface proteins impacts on viral vector cellular specificity and transduction characteristics: the retina as a model. Hum Mol Genet 2001; 10: 3075-3081. (Pubitemid 34083493)
12. Galileo DS, Hunter K, Smith SB. Stable and efficient gene transfer into the mutant retinal pigment epithelial cells of the Mitf(vit) mouse using a lentiviral vector. Curr Eye Res 1999; 18: 135-142. (Pubitemid 29137571)
13. Bemelmans AP, Bonnel S, Houhou L, Dufour N, Nandrot E, Helmlinger D et al. Retinal cell type expression specificity of HIV-1-derived gene transfer vectors upon subretinal injection in the adult rat: influence of pseudotyping and promoter. J Gene Med 2005; 7: 1367-1374. (Pubitemid 41555442)
14. Challa P, Luna C, Liton PB, Chamblin B, Wakefield J, Ramabhadran R et al. Lentiviral mediated gene delivery to the anterior chamber of rodent eyes. Mol Vis 2005; 11: 425-430. (Pubitemid 41410237)
15. Trittibach P, Barker SE, Broderick CA, Natkunarajah M, Duran Y, Robbie SJ et al. Lentiviral-vector-mediated expression of murine IL-1 receptor antagonist or IL-10 reduces the severity of endotoxin-induced uveitis. Gene Therapy 2008; 15: 1478-1488.
16. Greenberg KP, Geller SF, Schaffer DV, Flannery JG. Targeted transgene expression in Muller glia of normal and diseased retinas using lentiviral vectors. Invest Ophthalmol Vis Sci 2007; 48: 1844-1852. (Pubitemid 351261374)
17. Bemelmans AP, Kostic C, Crippa SV, Hauswirth WW, Lem J, Munier FL et al. Lentiviral gene transfer of RPE65 rescues survival and function of cones in a mouse model of Leber congenital amaurosis. PLoS Med 2006; 3: e347.
18. Yanez-Munoz RJ, Balaggan KS, MacNeil A, Howe SJ, Schmidt M, Smith AJ et al. Effective gene therapy with nonintegrating lentiviral vectors. Nat Med 2006; 12: 348-353. (Pubitemid 43355085)
19. Parker DG, Kaufmann C, Brereton HM, Anson DS, Francis-Staite L, Jessup CF et al. Lentivirus-mediated gene transfer to the rat, ovine and human cornea. Gene Therapy 2007; 14: 760-767. (Pubitemid 46585657)
20. Wang X, Appukuttan B, Ott S, Patel R, Irvine J, Song J et al. Efficient and sustained transgene expression in human corneal cells mediated by a lentiviral vector. Gene Therapy 2000; 7: 196-200. (Pubitemid 30113767)
21. Beutelspacher SC, Ardjomand N, Tan PH, Patton GS, Larkin DF, George AJ et al. Comparison of HIV-1 and EIAV-based lentiviral vectors in corneal transduction. Exp Eye Res 2005; 80: 787-794. (Pubitemid 40798043)
22. Parker DG, Brereton HM, Klebe S, Coster DJ, Williams KA. A steroid-inducible promoter for the cornea. Br J Ophthalmol 2009; 93: 1255-1259.
23. Bemelmans AP, Arsenijevic Y, Majo F. Efficient lentiviral gene transfer into corneal stroma cells using a femtosecond laser. Gene Therapy 2009; 16: 933-938.
24. Loewen N, Fautsch MP, Peretz M, Bahler CK, Cameron JD, Johnson DH et al. Genetic modification of human trabecular meshwork with lentiviral vectors. Hum Gene Ther 2001; 12: 2109-2119. (Pubitemid 34053494)
25. Cheng L, Chaidhawangul S, Wong-Staal F, Gilbert J, Poeschla E, Toyoguchi M et al. Human immunodeficiency virus type 2 (HIV-2) vector-mediated in vivo gene transfer into adult rabbit retina. Curr Eye Res 2002; 24: 196-201. (Pubitemid 35216129)
26. Ikeda Y, Goto Y, Yonemitsu Y, Miyazaki M, Sakamoto T, Ishibashi T et al. Simian immunodeficiency virus-based lentivirus vector for retinal gene transfer: a preclinical safety study in adult rats. Gene Therapy 2003; 10: 1161-1169. (Pubitemid 36896591)
27. Ikeda Y, Yonemitsu Y, Miyazaki M, Kohno Ri, Murakami Y, Murata T et al. Stable retinal gene expression in nonhuman primates via subretinal injection of SIVagm-based lentiviral vectors. Hum Gene Ther 2009; 20: 573-579.
28. Duisit G, Conrath H, Saleun S, Folliot S, Provost N, Cosset FL et al. Five recombinant simian immunodeficiency virus pseudotypes lead to exclusive transduction of retinal pigmented epithelium in rat. Mol Ther 2002; 6: 446-454. (Pubitemid 35214865)
29. Murakami Y, Ikeda Y, Yonemitsu Y, Miyazaki M, Inoue M, Hasegawa M et al. Inhibition of choroidal neovascularization via brief subretinal exposure to a newly developed lentiviral vector pseudotyped with Sendai viral envelope proteins. Hum Gene Ther 2010; 21: 199-209.
30. Balaggan KS, Binley K, Esapa M, Iqball S, Askham Z, Kan O et al. Stable and efficient intraocular gene transfer using pseudotyped EIAV lentiviral vectors. J Gene Med 2006; 8: 275-285.
31. Kachi S, Binley K, Yokoi K, Umeda N, Akiyama H, Muramatu D et al. Equine infectious anemia viral vector-mediated codelivery of endostatin and angiostatin driven by retinal pigmented epithelium-specific VMD2 promoter inhibits choroidal neovascularization. Hum Gene Ther 2009; 20: 31-39.
32. Widdowson P, Hamirally S, Binley K, Nork M, Miller P, Bantseev V et al. Toleration of subretinal delivered EIAV-based RetinoStat(R) in the rodent, rabbit and nonhuman primate. Invest Ophthalmol Vis Sci 2009; 50: 3027.
33. Nicoud M, Kong J, Iqball S, Kan O, Naylor S, Gouras P et al. Development of photoreceptor-specific promoters and their utility to investigate EIAV lentiviral vector mediated gene transfer to photoreceptors. J Gene Med 2007; 9: 1015-1023. (Pubitemid 350286406)
34. Kong J, Kim SR, Binley K, Pata I, Doi K, Mannik J et al. Correction of the disease phenotype in the mouse model of Stargardt disease by lentiviral gene therapy. Gene Therapy 2008; 15: 1311-1320.
35. Hamirally S, Fernandes A, Wong P, Yan J, Gao W, Aaberg Sr T et al. Effective photoreceptor and RPE transduction using EIAV-based lentiviral vector expressing GFP following ocular delivery in the nonhuman primate model. Invest Ophthalmol Vis Sci 2009; 50: 3026.
36. Lotery AJ, Derksen TA, Russell SR, Mullins RF, Sauter S, Affatigato LM et al. Gene transfer to the nonhuman primate retina with recombinant feline immunodeficiency virus vectors. Hum Gene Ther 2002; 13: 689-696. (Pubitemid 34280483)
37. Barraza RA, Rasmussen CA, Loewen N, Cameron JD, Gabelt BT, Teo WL et al. Prolonged transgene expression with lentiviral vectors in the aqueous humor outflow pathway of nonhuman primates. Hum Gene Ther 2009; 20: 191-200.
38. Derksen TA, Sauter SL, Davidson BL. Feline immunodeficiency virus vectors. Gene transfer to mouse retina following intravitreal injection. J Gene Med 2002; 4: 463-469. (Pubitemid 40268371)
39. Loewen N, Leske DA, Cameron JD, Chen Y, Whitwam T, Simari RD et al. Long-term retinal transgene expression with FIV versus adenoviral vectors. Mol Vis 2004; 10: 272-280. (Pubitemid 38628951)
40. Loewen N, Leske DA, Chen Y, Teo WL, Saenz DT, Peretz M et al. Comparison of wildtype and class I integrase mutant-FIV vectors in retina demonstrates sustained expression of integrated transgenes in retinal pigment epithelium. J Gene Med 2003; 5: 1009-1017. (Pubitemid 40310425)
41. Loewen N, Fautsch MP, Teo WL, Bahler CK, Johnson DH, Poeschla EM. Long-term, targeted genetic modification of the aqueous humor outflow tract coupled with noninvasive imaging of gene expression in vivo. Invest Ophthalmol Vis Sci 2004; 45: 3091-3098. (Pubitemid 39121840)
42. Cheng L, Toyoguchi M, Looney DJ, Lee J, Davidson MC, Freeman WR. Efficient gene transfer to retinal pigment epithelium cells with long-term expression. Retina 2005; 25: 193-201. (Pubitemid 40365944)
43. Loewen N, Bahler C, Teo WL, Whitwam T, Peretz M, Xu R et al. Preservation of aqueous outflow facility after second-generation FIV vector-mediated expression of marker genes in anterior segments of human eyes. Invest Ophthalmol Vis Sci 2002; 43: 3686-3690. (Pubitemid 35470605)
44. Takahashi K, Luo T, Saishin Y, Saishin Y, Sung J, Hackett S et al. Sustained transduction of ocular cells with a bovine immunodeficiency viral vector. Hum Gene Ther 2002; 13: 1305-1316. (Pubitemid 35034510)
45. Molina RP, Ye HQ, Brady J, Zhang J, Zimmerman H, Kaleko M et al. A synthetic Revindependent bovine immunodeficiency virus-based packaging construct. Hum Gene Ther 2004; 15: 865-877. (Pubitemid 39244841)
46. Rolling F. Recombinant AAV-mediated gene transfer to the retina: gene therapy perspectives. Gene Therapy 2004; 11(Suppl 1): S26-S32. (Pubitemid 39359444)
47. Sastry L, Xu Y, Duffy L, Koop S, Jasti A, Roehl H et al. Product-enhanced reverse transcriptase assay for replication-competent retrovirus and lentivirus detection. Hum Gene Ther 2005; 16: 1227-1236. (Pubitemid 41443715)
48. Kronenberg S, Kleinschmidt JA, Bottcher B. Electron cryo-microscopy and image reconstruction of adeno-associated virus type 2 empty capsids. EMBO Rep 2001; 2: 997-1002. (Pubitemid 33130605)
49. Sastry L, Miller C, Johnson T, Jasti A, Gattone V, Cornetta K. 494. Assessing lentiviral vector quality using transmission electron microscopy. Mol Ther 2005; 11 (S1): S191-S192.
50. Gruter O, Kostic C, Crippa SV, Perez M-TR, Zografos L, Schorderet DF et al. Lentiviral vector-mediated gene transfer in adult mouse photoreceptors is impaired by the presence of a physical barrier. Gene Therapy 2005; 12: 942-947. (Pubitemid 40852213)
51. Cashman SM, McCullough L, Kumar-Singh R. Improved retinal transduction in vivo and photoreceptor-specific transgene expression using adenovirus vectors with modified penton base. Mol Ther 2007; 15: 1640-1646. (Pubitemid 47289007)
52. Murthy RC, McFarland TJ, Yoken J, Chen S, Barone C, Burke D et al. Corneal transduction to inhibit angiogenesis and graft failure. Invest Ophthalmol Vis Sci 2003; 44: 1837-1842. (Pubitemid 36520270)
53. Parker DG, Coster DJ, Brereton HM, Hart PH, Koldej R, Anson DS et al. Lentivirusmediated gene transfer of interleukin 10 to the ovine and human cornea. Clin Exp Ophthalmol 2010; 38: 405-413.
54. Beutelspacher SC, Pillai R, Watson MP, Tan PH, Tsang J, McClure MO et al. Function of indoleamine 2,3-dioxygenase in corneal allograft rejection and prolongation of allograft survival by over-expression. Eur J Immunol 2006; 36: 690-700.
55. Barraza RA, McLaren JW, Poeschla EM. Prostaglandin pathway gene therapy for sustained reduction of intraocular pressure. Mol Ther 2010; 18: 491-501.
56. Khare PD, Loewen N, Teo W, Barraza RA, Saenz DT, Johnson DH et al. Durable, safe, multi-gene lentiviral vector expression in feline trabecular meshwork. Mol Ther 2008; 16: 97-106.
57. van Adel BA, Kostic C, Deglon N, Ball AK, Arsenijevic Y. Delivery of ciliary neurotrophic factor via lentiviral-mediated transfer protects axotomized retinal ganglion cells for an extended period of time. Hum Gene Ther 2003; 14: 103-115. (Pubitemid 36418815)
58. Igarashi T, Miyake K, Kato K, Watanabe A, Ishizaki M, Ohara K et al. Lentivirusmediated expression of angiostatin efficiently inhibits neovascularization in a murine proliferative retinopathy model. Gene Therapy 2003; 10: 219-226. (Pubitemid 36204410)
59. Min Z, Qiang W, Benwen S, Bin L, Xinhua D. Lentivirus-mediated sFlt-1 gene fragment transfer suppresses retinal neovascularization. Curr Eye Res 2009; 34: 401-410.
60. Balaggan KS, Binley K, Esapa M, Maclaren RE, Iqball S, Duran Y et al. EIAV vectormediated delivery of endostatin or angiostatin inhibits angiogenesis and vascular hyperpermeability in experimental CNV. Gene Therapy 2006; 13: 1153-1165. (Pubitemid 44084074)
61. Takahashi M, Miyoshi H, Verma IM, Gage FH. Rescue from photoreceptor degeneration in the rd mouse by human immunodeficiency virus vector-mediated gene transfer. J Virol 1999; 73: 7812-7816. (Pubitemid 29383266)
62. Tschernutter M, Schlichtenbrede FC, Howe S, Balaggan KS, Munro PM, Bainbridge JW et al. Long-term preservation of retinal function in the RCS rat model of retinitis pigmentosa following lentivirus-mediated gene therapy. Gene Therapy 2005; 12: 694-701. (Pubitemid 40561508)
63. Miyazaki M, Ikeda Y, Yonemitsu Y, Goto Y, Sakamoto T, Tabata T et al. Simian lentiviral vector-mediated retinal gene transfer of pigment epithelium-derived factor protects retinal degeneration and electrical defect in Royal College of Surgeons rats. Gene Therapy 2003; 10: 1503-1511. (Pubitemid 36987144)
64. Miyazaki M, Ikeda Y, Yonemitsu Y, Goto Y, Kohno R, Murakami Y et al. Synergistic neuroprotective effect via simian lentiviral vector-mediated simultaneous gene transfer of human pigment epithelium-derived factor and human fibroblast growth factor-2 in rodent models of retinitis pigmentosa. J Gene Med 2008; 10: 1273-1281.
65. Klausner EA, Peer D, Chapman RL, Multack RF, Andurkar SV. Corneal gene therapy. J Control Release 2007; 124: 107-133. (Pubitemid 350101883)
66. Williams KA, Coster DJ. Gene therapy for diseases of the cornea-a review. Clin Exp Ophthalmol 2010; 38: 93-103.
67. Liu X, Rasmussen CA, Gabelt BT, Brandt CR, Kaufman PL. Gene therapy targeting glaucoma: where are we? Surv Ophthalmol 2009; 54: 472-486.
68. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1995; 1: 27-31.
69. Muether PS, Hermann MM, Koch K, Fauser S. Delay between medical indication to anti-VEGF treatment in age-related macular degeneration can result in a loss of visual acuity. Graefes Arch Clin Exp Ophthalmol 2011; 249: 633-637.
70. Curnow SJ, Murray PI. Inflammatory mediators of uveitis: cytokines and chemokines. Curr Opin Ophthalmol 2006; 17: 532-537. (Pubitemid 44655586)
71. Buch PK, Maclaren RE, Duran Y, Balaggan KS, MacNeil A, Schlichtenbrede FC et al. In contrast to AAV-mediated Cntf expression, AAV-mediated Gdnf expression enhances gene replacement therapy in rodent models of retinal degeneration. Mol Ther 2006; 14: 700-709. (Pubitemid 44480755)
72. Wanisch K, Yanez-Munoz RJ. Integration-deficient lentiviral vectors: a slow coming of age. Mol Ther 2009; 17: 1316-1332.
73. Manilla P, Rebello T, Afable C, Lu X, Slepushkin V, Humeau LM et al. Regulatory considerations for novel gene therapy products: a review of the process leading to the first clinical lentiviral vector. Hum Gene Ther 2005; 16: 17-25. (Pubitemid 40250328)
74. Romano G, Marino IR, Pentimalli F, Adamo V, Giordano A. Insertional mutagenesis and development of malignancies induced by integrating gene delivery systems: implications for the design of safer gene-based interventions in patients. Drug News Perspect 2009; 22: 185-196.
75. Sinn PL, Sauter SL, McCray Jr PB. Gene therapy progress and prospects: development of improved lentiviral and retroviral vectors-design, biosafety, and production. Gene Therapy 2005; 12: 1089-1098. (Pubitemid 41030614)
76. Hacker CV, Vink CA, Wardell TW, Lee S, Treasure P, Kingsman SM et al. The integration profile of EIAV-based vectors. Mol Ther 2006; 14: 536-545. (Pubitemid 44313460)
77. Mitchell RS, Beitzel BF, Schroder AR, Shinn P, Chen H, Berry CC et al. Retroviral DNA integration: ASLV, HIV, and MLV show distinct target site preferences. PLoS Biol 2004; 2: E234.
78. Schroder AR, Shinn P, Chen H, Berry C, Ecker JR, Bushman F. HIV-1 integration in the human genome favors active genes and local hotspots. Cell 2002; 110: 521-529. (Pubitemid 35232295)
79. Bartholomae CC, Arens A, Balaggan KS, Yanez-Munoz RJ, Montini E, Howe SJ et al. Lentiviral vector integration profiles differ in rodent postmitotic tissues. Mol Ther 2011; 19: 703-710.
80. Balaggan KS, Duran Y, Buch PK, MacNeil A, Robbie S, Barker SE et al. Absence of ocular malignant transformation after subretinal delivery of Raav2/2 or Hiv-1 vectors in P53 knockout mice. ARVO Meeting Abstracts 2011; 52: 4548.
81. Sadelain M. Insertional oncogenesis in gene therapy: how much of a risk? Gene Therapy 2004; 11: 569-573. (Pubitemid 38455974)
82. Philpott NJ, Thrasher AJ. Use of nonintegrating lentiviral vectors for gene therapy. Hum Gene Ther 2007; 18: 483-489. (Pubitemid 47036043)
83. Rahim AA, Wong AM, Howe SJ, Buckley SM, Acosta-Saltos AD, Elston KE et al. Efficient gene delivery to the adult and fetal CNS using pseudotyped non-integrating lentiviral vectors. Gene Therapy 2009; 16: 509-520.
84. Philippe S, Sarkis C, Barkats M, Mammeri H, Ladroue C, Petit C et al. Lentiviral vectors with a defective integrase allow efficient and sustained transgene expression in vitro and in vivo. Proc Natl Acad Sci USA 2006; 103: 17684-17689. (Pubitemid 44852220)
85. Apolonia L, Waddington SN, Fernandes C, Ward NJ, Bouma G, Blundell MP et al. Stable gene transfer to muscle using non-integrating lentiviral vectors. Mol Ther 2007; 15: 1947-1954. (Pubitemid 350011734)
86. Bayer M, Kantor B, Cockrell A, Ma H, Zeithaml B, Li X et al. A large U3 deletion causes increased in vivo expression from a nonintegrating lentiviral vector. Mol Ther 2008; 16: 1968-1976.
87. Michelini Z, Negri DR, Baroncelli S, Spada M, Leone P, Bona R et al. Development and use of SIV-based Integrase defective lentiviral vector for immunization. Vaccine 2009; 27: 4622-4629.
88. Kachi S, Binley K, Yokoi K, Umeda N, Akiyama H, Muramatu D et al. Equine infectious anemia viral vector-mediated codelivery of endostatin and angiostatin driven by retinal pigmented epithelium-specific VMD2 promoter inhibits choroidal neovascularization. Hum Gene Ther 2009; 20: 31-39.
89. Binley KM, Iqball S, Nork TM, Miller PE, Christian BJ, Kan O et al. Evaluation of EIAV based lentiviral vectors following ocular delivery in the nonhuman primate model: development of RetinoStat(R). ARVO Meeting Abstracts 2008; 49: 5340.