Lung gene therapy-How to capture illumination from the light already present in the tunnel

Genes and Diseases

Volumn 1, Issue 1, 2014, Pages 40-52

  Xia, Emily ^a,b   Munegowda, Manjunatha Ankathatti ^a,b   Cao, Huibi ^a,b   Hu, Jim ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Animal model; Cystic fibrosis; Gene therapy; Lung diseases; Vector delivery

Indexed keywords

AIRWAY; CYSTIC FIBROSIS; EXPRESSION VECTOR; GENE EXPRESSION; GENE THERAPY; HUMAN; IMMUNE RESPONSE; LUNG DISEASE; NONHUMAN; REVIEW;

ANIMALIA;

EID: 84943367147     PISSN: None     EISSN: 23523042     Source Type: Journal    
DOI: 10.1016/j.gendis.2014.06.001     Document Type: Review

References (142)

1. Maguire A.M., Simonelli F., Pierce E.A., et al. Safety and efficacy of gene transfer for Leber's congenital amaurosis. N Engl J Med May 22 2008, 358(21):2240-2248.
2. Bainbridge J.W., Smith A.J., Barker S.S., et al. Effect of gene therapy on visual function in Leber's congenital amaurosis. N Engl J Med May 22 2008, 358(21):2231-2239.
3. Cideciyan A.V., Aleman T.S., Boye S.L., et al. Human gene therapy for RPE65 isomerase deficiency activates the retinoid cycle of vision but with slow rod kinetics. Proc Natl Acad Sci U S A Sep 30 2008, 105(39):15112-15117.
4. Hanein S., Perrault I., Gerber S., et al. Leber congenital amaurosis: comprehensive survey of the genetic heterogeneity, refinement of the clinical definition, and genotype-phenotype correlations as a strategy for molecular diagnosis. Hum Mutat Apr 2004, 23(4):306-317.
5. Bennett J., Ashtari M., Wellman J., et al. AAV2 gene therapy readministration in three adults with congenital blindness. Sci Transl Med Feb 8 2012, 4(120):120ra115.
6. Maclaren R.E., Groppe M., Barnard A.R., et al. Retinal gene therapy in patients with choroideremia: initial findings from a phase 1/2 clinical trial. Lancet Jan 15 2014, 383(9923):1129-1137.
7. Bryant L.M., Christopher D.M., Giles A.R., et al. Lessons learned from the clinical development and market authorization of Glybera. Hum Gene Ther Clin Dev Jun 2013, 24(2):55-64.
8. Yla-Herttuala S. Endgame: glybera finally recommended for approval as the first gene therapy drug in the European Union. Mol Ther Oct 2012, 20(10):1831-1832.
9. Miller N. Glybera and the future of gene therapy in the European Union. Nat Rev Drug Discov May 2012, 11(5):419.
10. Cao H., Molday R.S., Hu J. Gene therapy: light is finally in the tunnel. Protein Cell Dec 2011, 2(12):973-989.
11. Griesenbach U., Alton E.W. Moving forward: cystic fibrosis gene therapy. Hum Mol Genet Oct 15 2013, 22(R1):R52-R58.
12. Prickett M., Jain M. Gene therapy in cystic fibrosis. Transl Res Apr 2013, 161(4):255-264.
13. Flotte T.R., Ng P., Dylla D.E., et al. Viral vector-mediated and cell-based therapies for treatment of cystic fibrosis. Mol Ther J Am Soc Gene Ther 2007, 15(2):229-241.
14. Rommens J.M., Iannuzzi M.C., Kerem B., et al. Identification of the cystic fibrosis gene: chromosome walking and jumping. Science Sep 8 1989, 245(4922):1059-1065.
15. Kerem B., Rommens J.M., Buchanan J.A., et al. Identification of the cystic fibrosis gene: genetic analysis. Science Sep 8 1989, 245(4922):1073-1080.
16. Rommens J.M., Zengerling-Lentes S., Kerem B., Melmer G., Buchwald M., Tsui L.C. Physical localization of two DNA markers closely linked to the cystic fibrosis locus by pulsed-field gel electrophoresis. Am J Hum Genet Dec 1989, 45(6):932-941.
17. Koehler D.R., Hitt M.M., Hu J. Challenges and strategies for cystic fibrosis lung gene therapy. Mol Ther J Am Soc Gene Ther 2001, 4(2):84-91.
18. Zabner J., Couture L.A., Gregory R.J., Graham S.M., Smith A.E., Welsh M.J. Adenovirus-mediated gene transfer transiently corrects the chloride transport defect in nasal epithelia of patients with cystic fibrosis. Cell Oct 22 1993, 75(2):207-216.
19. Grubb B.R., Pickles R.J., Ye H., et al. Inefficient gene transfer by adenovirus vector to cystic fibrosis airway epithelia of mice and humans. Nature Oct 27 1994, 371(6500):802-806.
20. Boucher R.C., Knowles M.R., Johnson L.G., et al. Gene therapy for cystic fibrosis using E1-deleted adenovirus: a phase I trial in the nasal cavity. Hum Gene Ther May 1994, 5(5):615-639. The University of North Carolina at Chapel Hill.
21. Knowles M.R., Hohneker K.W., Zhou Z., et al. A controlled study of adenoviral-vector-mediated gene transfer in the nasal epithelium of patients with cystic fibrosis. N Engl J Med Sep 28 1995, 333(13):823-831.
22. Crystal R.G., McElvaney N.G., Rosenfeld M.A., et al. Administration of an adenovirus containing the human CFTR cDNA to the respiratory tract of individuals with cystic fibrosis. Nat Genet Sep 1994, 8(1):42-51.
23. Bellon G., Michel-Calemard L., Thouvenot D., et al. Aerosol administration of a recombinant adenovirus expressing CFTR to cystic fibrosis patients: a phase I clinical trial. Hum Gene Ther Jan 1 1997, 8(1):15-25.
24. Harvey B.G., Leopold P.L., Hackett N.R., et al. Airway epithelial CFTR mRNA expression in cystic fibrosis patients after repetitive administration of a recombinant adenovirus. J Clin Invest Nov 1999, 104(9):1245-1255.
25. Joseph P.M., O'Sullivan B.P., Lapey A., et al. Aerosol and lobar administration of a recombinant adenovirus to individuals with cystic fibrosis. I. Methods, safety, and clinical implications. Hum Gene Ther Jul 20 2001, 12(11):1369-1382.
26. Perricone M.A., Morris J.E., Pavelka K., et al. Aerosol and lobar administration of a recombinant adenovirus to individuals with cystic fibrosis. II. Transfection efficiency in airway epithelium. Hum Gene Ther Jul 20 2001, 12(11):1383-1394.
27. Wagner J.A., Messner A.H., Moran M.L., et al. Safety and biological efficacy of an adeno-associated virus vector-cystic fibrosis transmembrane regulator (AAV-CFTR) in the cystic fibrosis maxillary sinus. Laryngoscope Feb 1999, 109(2 Pt 1):266-274.
28. Moss R.B., Rodman D., Spencer L.T., et al. Repeated adeno-associated virus serotype 2 aerosol-mediated cystic fibrosis transmembrane regulator gene transfer to the lungs of patients with cystic fibrosis: a multicenter, double-blind, placebo-controlled trial. Chest Feb 2004, 125(2):509-521.
29. Caplen N.J., Alton E.W., Middleton P.G., et al. Liposome-mediated CFTR gene transfer to the nasal epithelium of patients with cystic fibrosis. Nat Med Jan 1995, 1(1):39-46.
30. Gill D.R., Southern K.W., Mofford K.A., et al. A placebo-controlled study of liposome-mediated gene transfer to the nasal epithelium of patients with cystic fibrosis. Gene Ther Mar 1997, 4(3):199-209.
31. Porteous D.J., Dorin J.R., McLachlan G., et al. Evidence for safety and efficacy of DOTAP cationic liposome mediated CFTR gene transfer to the nasal epithelium of patients with cystic fibrosis. Gene Ther Mar 1997, 4(3):210-218.
32. Zabner J., Cheng S.H., Meeker D., et al. Comparison of DNA-lipid complexes and DNA alone for gene transfer to cystic fibrosis airway epithelia invivo. J Clin Invest Sep 15 1997, 100(6):1529-1537.
33. Noone P.G., Hohneker K.W., Zhou Z., et al. Safety and biological efficacy of a lipid-CFTR complex for gene transfer in the nasal epithelium of adult patients with cystic fibrosis. Mol Ther Jan 2000, 1(1):105-114.
34. Alton E.W., Stern M., Farley R., et al. Cationic lipid-mediated CFTR gene transfer to the lungs and nose of patients with cystic fibrosis: a double-blind placebo-controlled trial. Lancet Mar 20 1999, 353(9157):947-954.
35. Ruiz F.E., Clancy J.P., Perricone M.A., et al. A clinical inflammatory syndrome attributable to aerosolized lipid-DNA administration in cystic fibrosis. Hum Gene Ther May 1 2001, 12(7):751-761.
36. Cao H., Koehler D.R., Hu J. Adenoviral vectors for gene replacement therapy. Viral Immunol 2004, 17(3):327-333.
37. Kojaoghlanian T., Flomenberg P., Horwitz M.S. The impact of adenovirus infection on the immunocompromised host. Rev Med Virol May-Jun 2003, 13(3):155-171.
38. Moss R.B., Milla C., Colombo J., et al. Repeated aerosolized AAV-CFTR for treatment of cystic fibrosis: a randomized placebo-controlled phase 2B trial. Hum Gene Ther 2007, 18(8):726-732.
39. Wagner J.A., Nepomuceno I.B., Messner A.H., et al. A phase II, double-blind, randomized, placebo-controlled clinical trial of tgAAVCF using maxillary sinus delivery in patients with cystic fibrosis with antrostomies. Hum Gene Ther 2002, 13(11):1349-1359.
40. Berns K.I., Giraud C. Biology of adeno-associated virus. Curr Top Microbiol Immunol 1996, 218:1-23.
41. Gao X., Huang L. Cationic liposome-mediated gene transfer. Gene Ther 1995, 2(10):710-722.
42. Shimizu K., Sakurai F., Machitani M., Katayama K., Mizuguchi H. Quantitative analysis of the leaky expression of adenovirus genes in cells transduced with a replication-incompetent adenovirus vector. Mol Pharm 2011, 8(4):1430-1435.
43. Wivel N.A., Gao P.-G., Wilson J.M. Adenovirus vectors. The Development of Human Gene Therapy 1999, Cold Spring Harbor Laboratory Press, San Diego, CA.
44. Parks R.J. Improvements in adenoviral vector technology: overcoming barriers for gene therapy. Clin Genet 2000, 58(1):1-11.
45. Seiler M.P., Cerullo V., Lee B. Immune response to helper dependent adenoviral mediated liver gene therapy: challenges and prospects. Curr Gene Ther 2007, 7(5):297-305.
46. Kim I.H., Jozkowicz A., Piedra P.A., Oka K., Chan L. Lifetime correction of genetic deficiency in mice with a single injection of helper-dependent adenoviral vector. Proc Natl Acad Sci U S A 2001, 98(23):13282-13287.
47. Toietta G., Koehler D.R., Finegold M.J., Lee B., Hu J., Beaudet A.L. Reduced inflammation and improved airway expression using helper-dependent adenoviral vectors with a K18 promoter. Mol Ther J Am Soc Gene Ther 2003, 7(5 Pt 1):649-658.
48. Koehler D.R., Sajjan U., Chow Y.H., et al. Protection of Cftr knockout mice from acute lung infection by a helper-dependent adenoviral vector expressing Cftr in airway epithelia. Proc Natl Acad Sci U S A 2003, 100(26):15364-15369.
49. Koehler D.R., Frndova H., Leung K., et al. Aerosol delivery of an enhanced helper-dependent adenovirus formulation to rabbit lung using an intratracheal catheter. J Gene Med 2005, 7(11):1409-1420.
50. Cao H., Machuca T.N., Yeung J.C., et al. Efficient gene delivery to pig airway epithelia and submucosal glands using helper-dependent adenoviral vectors. Mol Ther Nucleic Acids 2013, 2:e127.
51. Afione S.A., Conrad C.K., Kearns W.G., et al. Invivo model of adeno-associated virus vector persistence and rescue. J Virol 1996, 70(5):3235-3241.
52. Conrad C.K., Allen S.S., Afione S.A., et al. Safety of single-dose administration of an adeno-associated virus (AAV)-CFTR vector in the primate lung. Gene Ther 1996, 3(8):658-668.
53. Allocca M., Doria M., Petrillo M., et al. Serotype-dependent packaging of large genes in adeno-associated viral vectors results in effective gene delivery in mice. J Clin Invest 2008, 118(5):1955-1964.
54. Lai Y., Yue Y., Duan D. Evidence for the failure of adeno-associated virus serotype 5 to package a viral genome > or = 8.2kb. Mol Ther 2010, 18(1):75-79.
55. Gruntman A.M., Mueller C., Flotte T.R., Gao G. Gene transfer in the lung using recombinant adeno-associated virus. Curr Protoc Microbiol 2012, Chapter 14:Unit14D 12.
56. Duan D., Yue Y., Engelhardt J.F. Expanding AAV packaging capacity with trans-splicing or overlapping vectors: a quantitative comparison. Mol Ther 2001, 4(4):383-391.
57. Yan Z., Zhang Y., Duan D., Engelhardt J.F. Trans-splicing vectors expand the utility of adeno-associated virus for gene therapy. Proc Natl Acad Sci U S A 2000, 97(12):6716-6721.
58. White A.F., Mazur M., Sorscher E.J., Zinn K.R., Ponnazhagan S. Genetic modification of adeno-associated viral vector type 2 capsid enhances gene transfer efficiency in polarized human airway epithelial cells. Hum Gene Ther 2008, 19(12):1407-1414.
59. Li W., Zhang L., Johnson J.S., et al. Generation of novel AAV variants by directed evolution for improved CFTR delivery to human ciliated airway epithelium. Mol Ther 2009, 17(12):2067-2077.
60. Pozzi D., Marchini C., Cardarelli F., et al. Mechanistic evaluation of the transfection barriers involved in lipid-mediated gene delivery: interplay between nanostructure and composition. Biochim Biophys Acta 2014, 1838(3):957-967.
61. Bienenstock J. The lung as an immunologic organ. Annu Rev Med 1984, 35:49-62.
62. Dai Y., Schwarz E.M., Gu D., Zhang W.W., Sarvetnick N., Verma I.M. Cellular and humoral immune responses to adenoviral vectors containing factor IX gene: tolerization of factor IX and vector antigens allows for long-term expression. Proc Natl Acad Sci U S A 1995, 92(5):1401-1405.
63. Yang Y., Li Q., Ertl H.C., Wilson J.M. Cellular and humoral immune responses to viral antigens create barriers to lung-directed gene therapy with recombinant adenoviruses. J Virol 1995, 69(4):2004-2015.
64. Kay M.A., Holterman A.X., Meuse L., et al. Long-term hepatic adenovirus-mediated gene expression in mice following CTLA4Ig administration. Nat Genet 1995, 11(2):191-197.
65. Yang Y., Nunes F.A., Berencsi K., Furth E.E., Gonczol E., Wilson J.M. Cellular immunity to viral antigens limits E1-deleted adenoviruses for gene therapy. Proc Natl Acad Sci U S A 1994, 91(10):4407-4411.
66. Raper S.E., Chirmule N., Lee F.S., et al. Fatal systemic inflammatory response syndrome in a ornithine transcarbamylase deficient patient following adenoviral gene transfer. Mol Genet Metab 2003, 80(1-2):148-158.
67. Lee B.H., Kushwah R., Wu J., et al. Adenoviral vectors stimulate innate immune responses in macrophages through cross-talk with epithelial cells. Immunol Lett 2010, 134(1):93-102.
68. Sinn P.L., Burnight E.R., McCray P.B. Progress and prospects: prospects of repeated pulmonary administration of viral vectors. Gene Ther 2009, 16(9):1059-1065.
69. Zsengeller Z., Otake K., Hossain S.A., Berclaz P.Y., Trapnell B.C. Internalization of adenovirus by alveolar macrophages initiates early proinflammatory signaling during acute respiratory tract infection. J Virol 2000, 74(20):9655-9667.
70. Baldwin A.S. The NF-kappa B and I kappa B proteins: new discoveries and insights. Annu Rev Immunol 1996, 14:649-683.
71. Cao H.B., Wang A., Martin B., et al. Down-regulation of IL-8 expression in human airway epithelial cells through helper-dependent adenoviral-mediated RNA interference. Cell Res 2005, 15(2):111-119.
72. Matsushima K., Morishita K., Yoshimura T., et al. Molecular cloning of a human monocyte-derived neutrophil chemotactic factor (MDNCF) and the induction of MDNCF mRNA by interleukin 1 and tumor necrosis factor. J Exp Med 1988, 167(6):1883-1893.
73. Sun L., Wu J., Du F., Chen X., Chen Z.J. Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type Iinterferon pathway. Science 2013, 339(6121):786-791.
74. Mays L.E., Wilson J.M. The complex and evolving story of T cell activation to AAV vector-encoded transgene products. Mol Ther 2011, 19(1):16-27.
75. Fearon D.T., Locksley R.M. The instructive role of innate immunity in the acquired immune response. Science 1996, 272(5258):50-53.
76. Scaria A., St George J.A., Gregory R.J., et al. Antibody to CD40 ligand inhibits both humoral and cellular immune responses to adenoviral vectors and facilitates repeated administration to mouse airway. Gene Ther 1997, 4(6):611-617.
77. Wilson C.B., Embree L.J., Schowalter D., et al. Transient inhibition of CD28 and CD40 ligand interactions prolongs adenovirus-mediated transgene expression in the lung and facilitates expression after secondary vector administration. J Virol 1998, 72(9):7542-7550.
78. Jiang Z., Feingold E., Kochanek S., Clemens P.R. Systemic delivery of a high-capacity adenoviral vector expressing mouse CTLA4Ig improves skeletal muscle gene therapy. Mol Ther 2002, 6(3):369-376.
79. Yamashita K., Masunaga T., Yanagida N., et al. Long-term acceptance of rat cardiac allografts on the basis of adenovirus mediated CD40Ig plus CTLA4Ig gene therapies. Transplantation 2003, 76(7):1089-1096.
80. Mastrangeli A., Harvey B.G., Yao J., et al. "Sero-switch" adenovirus-mediated invivo gene transfer: circumvention of anti-adenovirus humoral immune defenses against repeat adenovirus vector administration by changing the adenovirus serotype. Hum Gene Ther 1996, 7(1):79-87.
81. Sumner-Jones S.G., Gill D.R., Hyde S.C. Lack of repeat transduction by recombinant adeno-associated virus type 5/5 vectors in the mouse airway. J Virol 2007, 81(22):12360-12367.
82. Mack C.A., Song W.R., Carpenter H., et al. Circumvention of anti-adenovirus neutralizing immunity by administration of an adenoviral vector of an alternate serotype. Hum Gene Ther 1997, 8(1):99-109.
83. Kaplan J.M., Pennington S.E., St George J.A., et al. Potentiation of gene transfer to the mouse lung by complexes of adenovirus vector and polycations improves therapeutic potential. Hum Gene Ther 1998, 9(10):1469-1479.
84. Cao H., Yang T., Li X.F., et al. Readministration of helper-dependent adenoviral vectors to mouse airway mediated via transient immunosuppression. Gene Ther 2011, 18(2):173-181.
85. Pickles R.J., Fahrner J.A., Petrella J.M., Boucher R.C., Bergelson J.M. Retargeting the coxsackievirus and adenovirus receptor to the apical surface of polarized epithelial cells reveals the glycocalyx as a barrier to adenovirus-mediated gene transfer. J Virol 2000, 74(13):6050-6057.
86. Arcasoy S.M., Latoche J., Gondor M., et al. MUC1 and other sialoglycoconjugates inhibit adenovirus-mediated gene transfer to epithelial cells. Am J Respir Cell Mol Biol 1997, 17(4):422-435.
87. Bals R., Xiao W., Sang N., Weiner D.J., Meegalla R.L., Wilson J.M. Transduction of well-differentiated airway epithelium by recombinant adeno-associated virus is limited by vector entry. J Virol 1999, 73(7):6085-6088.
88. Worgall S., Leopold P.L., Wolff G., Ferris B., Van Roijen N., Crystal R.G. Role of alveolar macrophages in rapid elimination of adenovirus vectors administered to the epithelial surface of the respiratory tract. Hum Gene Ther 1997, 8(14):1675-1684.
89. Kushwah R., Oliver J.R., Cao H., Hu J. Nacystelyn enhances adenoviral vector-mediated gene delivery to mouse airways. Gene Ther 2007, 14(16):1243-1248.
90. Singh B., de la Concha-Bermejillo A. Gadolinium chloride removes pulmonary intravascular macrophages and curtails the degree of ovine lentivirus-induced lymphoid interstitial pneumonia. Int J Exp Pathol 1998, 79(3):151-162.
91. Thepen T., McMenamin C., Oliver J., Kraal G., Holt P.G. Regulation of immune response to inhaled antigen by alveolar macrophages: differential effects of invivo alveolar macrophage elimination on the induction of tolerance vs. immunity. Eur J Immunol 1991, 21(11):2845-2850.
92. Guzdek A., Turyna B., Allison A.C., Sladek K., Koj A. Rooperol, an inhibitor of cytokine synthesis, decreases the respiratory burst in human and rat leukocytes and macrophages. Mediators Inflamm 1997, 6(1):53-57.
93. Cai P., Kaphalia B.S., Ansari G.A. Methyl palmitate: inhibitor of phagocytosis in primary rat Kupffer cells. Toxicology 2005, 210(2-3):197-204.
94. Garcia D., Delgado R., Ubeira F.M., Leiro J. Modulation of rat macrophage function by the Mangifera indica L. extracts Vimang and mangiferin. Int Immunopharmacol 2002, 2(6):797-806.
95. Nakamura Y., Murai T., Ogawa Y. Effect of invitro and invivo administration of dexamethasone on rat macrophage functions: comparison between alveolar and peritoneal macrophages. Eur Respir J 1996, 9(2):301-306.
96. Chu Q., St George J.A., Lukason M., Cheng S.H., Scheule R.K., Eastman S.J. EGTA enhancement of adenovirus-mediated gene transfer to mouse tracheal epithelium invivo. Hum Gene Ther 2001, 12(5):455-467.
97. Limberis M., Anson D.S., Fuller M., Parsons D.W. Recovery of airway cystic fibrosis transmembrane conductance regulator function in mice with cystic fibrosis after single-dose lentivirus-mediated gene transfer. Hum Gene Ther 2002, 13(16):1961-1970.
98. Rawlins E.L., Hogan B.L. Ciliated epithelial cell lifespan in the mouse trachea and lung. Am J Physiol Lung Cell Mol Physiol 2008, 295(1):L231-L234.
99. Hacein-Bey-Abina S., Von Kalle C., Schmidt M., et al. LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 2003, 302(5644):415-419.
100. Hacein-Bey-Abina S., Hauer J., Lim A., et al. Efficacy of gene therapy for X-linked severe combined immunodeficiency. N Engl J Med 2010, 363(4):355-364.
101. Xu L., Zhao P., Mariano A., Han R. Targeted myostatin gene editing in multiple mammalian species directed by a single pair of TALE nucleases. Mol Ther Nucleic Acids 2013, 2:e112.
102. Li H., Haurigot V., Doyon Y., et al. Invivo genome editing restores haemostasis in a mouse model of haemophilia. Nature 2011, 475(7355):217-221.
103. Joung J.K., Sander J.D. TALENs: a widely applicable technology for targeted genome editing. Nat Rev Mol Cell Biol 2013, 14(1):49-55.
104. Urnov F.D., Rebar E.J., Holmes M.C., Zhang H.S., Gregory P.D. Genome editing with engineered zinc finger nucleases. Nat Rev Genet 2010, 11(9):636-646.
105. High K.A. Gene therapy: the moving finger. Nature 2005, 435(7042):577-579.
106. Moehle E.A., Rock J.M., Lee Y.L., et al. Targeted gene addition into a specified location in the human genome using designed zinc finger nucleases. Proc Natl Acad Sci U S A 2007, 104(9):3055-3060.
107. Mussolino C., Morbitzer R., Lutge F., Dannemann N., Lahaye T., Cathomen T. A novel TALE nuclease scaffold enables high genome editing activity in combination with low toxicity. Nucleic Acids Res 2011, 39(21):9283-9293.
108. Li T., Huang S., Zhao X., et al. Modularly assembled designer TAL effector nucleases for targeted gene knockout and gene replacement in eukaryotes. Nucleic Acids Res 2011, 39(14):6315-6325.
109. Hockemeyer D., Wang H., Kiani S., et al. Genetic engineering of human pluripotent cells using TALE nucleases. Nat Biotechnol 2011, 29(8):731-734.
110. Cermak T., Doyle E.L., Christian M., et al. Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res 2011, 39(12):e82.
111. Bhaya D., Davison M., Barrangou R. CRISPR-Cas systems in bacteria and archaea: versatile small RNAs for adaptive defense and regulation. Annu Rev Genet 2011, 45:273-297.
112. Terns M.P., Terns R.M. CRISPR-based adaptive immune systems. Curr Opin Microbiol 2011, 14(3):321-327.
113. Wiedenheft B., Sternberg S.H., Doudna J.A. RNA-guided genetic silencing systems in bacteria and archaea. Nature 2012, 482(7385):331-338.
114. Jinek M., Chylinski K., Fonfara I., Hauer M., Doudna J.A., Charpentier E. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 2012, 337(6096):816-821.
115. Deltcheva E., Chylinski K., Sharma C.M., et al. CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 2011, 471(7340):602-607.
116. Jinek M., East A., Cheng A., Lin S., Ma E., Doudna J. RNA-programmed genome editing in human cells. Elife 2013, 2:e00471.
117. Yang H., Wang H., Shivalila C.S., Cheng A.W., Shi L., Jaenisch R. One-step generation of mice carrying reporter and conditional alleles by CRISPR/Cas-mediated genome engineering. Cell 2013, 154(6):1370-1379.
118. Cradick T.J., Fine E.J., Antico C.J., Bao G. CRISPR/Cas9 systems targeting beta-globin and CCR5 genes have substantial off-target activity. Nucleic Acids Res 2013, 41(20):9584-9592.
119. Hsu P.D., Scott D.A., Weinstein J.A., et al. DNA targeting specificity of RNA-guided Cas9 nucleases. Nat Biotechnol 2013, 31(9):827-832.
120. Vandenberghe L.H., Auricchio A. Novel adeno-associated viral vectors for retinal gene therapy. Gene Ther 2012, 19(2):162-168.
121. Hamel C.P., Tsilou E., Pfeffer B.A., Hooks J.J., Detrick B., Redmond T.M. Molecular cloning and expression of RPE65, a novel retinal pigment epithelium-specific microsomal protein that is post-transcriptionally regulated invitro. J Biol Chem 1993, 268(21):15751-15757.
122. Streilein J.W. Ocular immune privilege: the eye takes a dim but practical view of immunity and inflammation. J Leukoc Biol 2003, 74(2):179-185.
123. Petrs-Silva H., Linden R. Advances in gene therapy technologies to treat retinitis pigmentosa. Clin Ophthalmol 2014, 8:127-136.
124. Wu L., Lam S., Cao H., et al. Subretinal gene delivery using helper-dependent adenoviral vectors. Cell Biosci 2011, 1(1):15.
125. Buch P.K., Bainbridge J.W., Ali R.R. AAV-mediated gene therapy for retinal disorders: from mouse to man. Gene Ther 2008, 15(11):849-857.
126. Wang X., Zhang Y., Amberson A., Engelhardt J.F. New models of the tracheal airway define the glandular contribution to airway surface fluid and electrolyte composition. Am J Respir Cell Mol Biol 2001, 24(2):195-202.
127. Pack R.J., Al-Ugaily L.H., Morris G., Widdicombe J.G. The distribution and structure of cells in the tracheal epithelium of the mouse. Cell Tissue Res 1980, 208(1):65-84.
128. Plopper C.G., Mariassy A.T., Lollini L.O. Structure as revealed by airway dissection. A comparison of mammalian lungs. Am Rev Respir Dis 1983, 128(2 Pt 2):S4-7.
129. Mercer R.R., Russell M.L., Roggli V.L., Crapo J.D. Cell number and distribution in human and rat airways. Am J Respir Cell Mol Biol 1994, 10(6):613-624.
130. Rogers C.S., Abraham W.M., Brogden K.A., et al. The porcine lung as a potential model for cystic fibrosis. Am J Physiol Lung Cell Mol Physiol 2008, 295(2):L240-L263.
131. Sun X., Yan Z., Yi Y., et al. Adeno-associated virus-targeted disruption of the CFTR gene in cloned ferrets. J Clin Invest 2008, 118(4):1578-1583.
132. Rogers C.S., Stoltz D.A., Meyerholz D.K., et al. Disruption of the CFTR gene produces a model of cystic fibrosis in newborn pigs. Science 2008, 321(5897):1837-1841.
133. Sauter C., Wolfensberger C. Interferon in human serum after injection of endotoxin. Lancet 1980, 2(8199):852-853.
134. Taveira da Silva A.M., Kaulbach H.C., Chuidian F.S., Lambert D.R., Suffredini A.F., Danner R.L. Brief report: shock and multiple-organ dysfunction after self-administration ofSalmonella endotoxin. N Engl J Med 1993, 328(20):1457-1460.
135. Acland G.M., Aguirre G.D., Bennett J., et al. Long-term restoration of rod and cone vision by single dose rAAV-mediated gene transfer to the retina in a canine model of childhood blindness. Mol Ther 2005, 12(6):1072-1082.
136. Acland G.M., Aguirre G.D., Ray J., et al. Gene therapy restores vision in a canine model of childhood blindness. Nat Genet 2001, 28(1):92-95.
137. Jacobson S.G., Acland G.M., Aguirre G.D., et al. Safety of recombinant adeno-associated virus type 2-RPE65 vector delivered by ocular subretinal injection. Mol Ther 2006, 13(6):1074-1084.
138. Narfstrom K., Katz M.L., Bragadottir R., et al. Functional and structural recovery of the retina after gene therapy in the RPE65 null mutation dog. Invest Ophthalmol Vis Sci 2003, 44(4):1663-1672.
139. Narfstrom K., Katz M.L., Ford M., Redmond T.M., Rakoczy E., Bragadottir R. Invivo gene therapy in young and adult RPE65-/- dogs produces long-term visual improvement. J Hered 2003, 94(1):31-37.
140. Dejneka N.S., Surace E.M., Aleman T.S., et al. In utero gene therapy rescues vision in a murine model of congenital blindness. Mol Ther 2004, 9(2):182-188.
141. Brandenburg B., Zhuang X. Virus trafficking - learning from single-virus tracking. Nat Rev Microbiol 2007, 5(3):197-208.
142. Pelkmans L., Puntener D., Helenius A. Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae. Science 2002, 296(5567):535-539.