AAV-mediated transduction and targeting of retinal bipolar cells with improved mGluR6 promoters in rodents and primates

Gene Therapy

Volumn 23, Issue 8-9, 2016, Pages 680-689

  Lu, Q ^a   Ganjawala, T H ^a   Ivanova, E ^b   Cheng, J G ^c   Troilo, D ^d   Pan, Z H ^a,e  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d STATE UNIVERSITY OF NEW YORK   (United States)

^e WAYNE STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

METABOTROPIC RECEPTOR 6; PARVOVIRUS VECTOR; GLUK2 KAINATE RECEPTOR; KAINIC ACID RECEPTOR;

ADENO ASSOCIATED VIRUS; ANIMAL CELL; ARTICLE; CALLITHRIX JACCHUS; CONTROLLED STUDY; GENE TARGETING; GENETIC MANIPULATION; GENETIC TRANSDUCTION; INTRON; MOUSE; NONHUMAN; PRIMATE; PRIORITY JOURNAL; PROMOTER REGION; RAT; REGULATORY SEQUENCE; RETINA BIPOLAR GANGLION CELL; ANIMAL; C57BL MOUSE; CALLITHRIX; DEPENDOPARVOVIRUS; ENHANCER REGION; FEMALE; GENE THERAPY; GENETICS; MALE; METABOLISM; PROCEDURES; SIMIAN VIRUS 40;

ANIMALS; CALLITHRIX; DEPENDOVIRUS; ENHANCER ELEMENTS, GENETIC; FEMALE; GENE TARGETING; GENETIC THERAPY; MALE; MICE; MICE, INBRED C57BL; PROMOTER REGIONS, GENETIC; RECEPTORS, KAINIC ACID; RETINAL BIPOLAR CELLS; SIMIAN VIRUS 40;

EID: 84966470704     PISSN: 09697128     EISSN: 14765462     Source Type: Journal    
DOI: 10.1038/gt.2016.42     Document Type: Article

References (50)

1. Zhu Y, Xu J, Hauswirth WW, DeVries SH. Genetically targeted binary labeling of retinal neurons. J Neurosci 2014; 34: 7845-7861.
2. Maguire AM, Simonelli F, Pierce EA, Pugh Jr EN, Mingozzi F, Bennicelli J et al. Safety and efficacy of gene transfer for Leber's congenital amaurosis. N Engl J Med 2008; 358: 2240-2248.
3. Boye SE, Boye SL, Lewin AS, Hauswirth WW. A comprehensive review of retinal gene therapy. Mol Ther 2013; 21: 509-519.
4. Trapani I, Puppo A, Auricchio A. Vector platforms for gene therapy of inherited retinopathies. Prog Retin Eye Res 2014; 43: 108-128.
5. Vandenberghe LH, Auricchio A. Novel adeno-associated viral vectors for retinal gene therapy. Gene Therapy 2012; 19: 162-168.
6. Euler T, Haverkamp S, Schubert T, Baden T. Retinal bipolar cells: elementary building blocks of vision. Nat Rev Neurosci 2014; 15: 507-519.
7. Bi A, Cui J, Ma YP, Olshevskaya E, Pu M, Dizhoor AM et al. Ectopic expression of a microbial-type rhodopsin restores visual responses in mice with photoreceptor degeneration. Neuron 2006; 50: 23-33.
8. Lagali PS, Balya D, Awatramani GB, Munch TA, Kim DS, Busskamp V et al. Light-activated channels targeted to ON bipolar cells restore visual function in retinal degeneration. Nat Neurosci 2008; 11: 667-675.
9. Busskamp V, Picaud S, Sahel JA, Roska B. Optogenetic therapy for retinitis pigmentosa. Gene Therapy 2012; 19: 169-175.
10. Pan Z-H, Lu Q, Bi A, Dizhoor AM, Abrams GW. Optogenetic approaches to restoring vision. Annu Rev Vis Sci 2015; 1: 185-210.
11. Ueda Y, Iwakabe H, Masu M, Suzuki M, Nakanishi S. The mGluR6 5' upstream transgene sequence directs a cell-specific and developmentally regulated expression in retinal rod and ON-type cone bipolar cells. J Neurosci 1997; 17: 3014-3023.
12. Morgan JL, Dhingra A, Vardi N, Wong RO. Axons and dendrites originate from neuroepithelial-like processes of retinal bipolar cells. Nat Neurosci 2006; 9: 85-92.
13. Dhingra A, Sulaiman P, Xu Y, Fina ME, Veh RW, Vardi N. Probing neurochemical structure and function of retinal ON bipolar cells with a transgenic mouse. J Comp Neurol 2008; 510: 484-496.
14. Kim DS, Matsuda T, Cepko CL. A core paired-type and POU homeodomaincontaining transcription factor program drives retinal bipolar cell gene expression. J Neurosci 2008; 28: 7748-7764.
15. Doroudchi MM, Greenberg KP, Liu J, Silka KA, Boyden ES, Lockridge JA et al. Virally delivered channelrhodopsin-2 safely and effectively restores visual function in multiple mouse models of blindness. Mol Ther 2011; 19: 1220-1229.
16. Cronin T, Vandenberghe LH, Hantz P, Juttner J, Reimann A, Kacsó AE et al. Efficient transduction and optogenetic stimulation of retinal bipolar cells by a synthetic adeno-associated virus capsid and promoter. EMBO Mol Med 2014; 6: 1175-1190.
17. Mace E, Caplette R, Marre O, Sengupta A, Chaffiol A, Barbe P et al. Targeting channelrhodopsin-2 to ON-bipolar cells with vitreally administered AAV restores ON and OFF visual responses in blind mice. Mol Ther 2015; 23: 7-16.
18. Dalkara D, Kolstad KD, Caporale N, Visel M, Klimczak RR, Schaffer DV et al. Inner limiting membrane barriers to AAV-mediated retinal transduction from the vitreous. Mol Ther 2009; 17: 2096-2102.
19. Petrs-Silva H, Dinculescu A, Li Q, Deng WT, Pang JJ, Min SH et al. Novel properties of tyrosine-mutant AAV2 vectors in the mouse retina. Mol Ther 2011; 19: 293-301.
20. Lu Q, Ivanova E, Ganjawala HT, Pan Z-H. Cre-mediated recombination efficiency and transgene expression patterns of three retinal bipolar cell-expressing Cre transgenic mouse lines. Mol Vis 2013; 19: 1310-1320.
21. Butler JE, Kadonaga JT. The RNA polymerase II core promoter: a key component in the regulation of gene expression. Genes Dev 2002; 16: 2583-2592.
22. Papadakis ED, Nicklin SA, Baker AH, White SJ. Promoters and control elements: designing expression cassettes for gene therapy. Curr Gene Ther 2004; 4: 89-113.
23. Pennacchio LA, Bickmore W, Dean A, Nobrega MA, Bejerano G. Enhancers: five essential questions. Nat Rev Genet 2013; 14: 288-295.
24. Visel A, Blow MJ, Li Z, Zhang T, Akiyama JA, Holt A et al. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 2009; 457: 854-858.
25. Petrs-Silva H, Dinculescu A, Li Q, Min SH, Chiodo V, Pang JJ et al. High-efficiency transduction of the mouse retina by tyrosine-mutant AAV serotype vectors. Mol Ther 2009; 17: 463-471.
26. Greferath U, Grünert U, Wässle H. Rod bipolar cells in the mammalian retina show protein kinase C-like immunoreactivity. J Comp Neurol 1990; 301: 433-442.
27. Dalkara D, Byrne LC, Klimczak RR, Visel M, Yin L, Merigan WH et al. In vivo-directed evolution of a new adeno-associated virus for therapeutic outer retinal gene delivery from the vitreous. Sci Transl Med 2013; 5: 189ra76.
28. Huang L, Max M, Margolskee RF, Su H, Masland RH, Euler T. G protein subunit Gγ13 is coexpressed with Gαo, Gβ3, and Gβ4 in retinal ON bipolar cells. J Comp Neurol 2003; 455: 1-10.
29. Chan TL, Martin PR, Clunas N, Grünert U. Bipolar cell diversity in the primate retina: morphologic and immunocytochemical analysis of a new world monkey, the marmoset Callithrix jacchus. J Comp Neurol 2001; 437: 219-239.
30. Weltzien F, Percival KA, Martin PR, Grünert U. Analysis of bipolar and amacrine populations in marmoset retina. J Comp Neurol 2015; 523: 313-334.
31. Surace EM, Auricchio A. Versatility of AAV vectors for retinal gene transfer. Vis Res 2008; 48: 353-359.
32. de Leeuw CN, Dyka FM, Boye SL, Laprise S, Zhou M, Chou AY et al. Targeted CNS delivery using human MiniPromoters and demonstrated compatibility with adeno-associated viral vectors. Mol Ther Methods Clin Dev 2014; 1: 5.
33. Scalabrino ML, Boye SL, Fransen KM, Noel JM, Dyka FM, Min SH et al. Intravitreal delivery of a novel AAV vector targets ON bipolar cells and restores visual function in a mouse model of complete congenital stationary night blindness. Hum Mol Genet 2015; 24: 6229-6239.
34. Wässle H, Puller C, Müller F, Haverkamp S. Cone contacts, mosaics, and territories of bipolar cells in the mouse retina. J Neurosci 2009; 29: 106-117.
35. Strettoi E, Pignatelli V. Modifications of retinal neurons in a mouse model of retinitis pigmentosa. Proc Natl Acad Sci USA 2000; 97: 11020-11025.
36. Hibino H, Tani K, Ikebuchi K, Wu MS, Sugiyama H, Nakazaki Y et al. The common marmoset as a target preclinical primate model for cytokine and gene therapy studies. Blood 1999; 93: 2839-2848.
37. t'Hart BA, Vervoordeldonk M, Heeney JL, Tak PP. Gene therapy in nonhuman primate models of human autoimmune disease. Gene Therapy 2003; 10: 890-901.
38. Ivanova E, Hwang GS, Pan ZH, Troilo D. Evaluation of AAV-mediated expression of Chop2-GFP in the marmoset retina. Investig Ophthalmol Vis Sci 2010; 51: 5288-5296.
39. Baba Y, Satoh S, Otsu M, Sasaki E, Okada T, Watanabe S. In vitro cell subtypespecific transduction of adeno-associated virus in mouse and marmoset retinal explant culture. Biochimie 2012; 94: 2716-2822.
40. Troilo D, Howland HC, Judge SJ. Visual optics and retinal cone topography in the common marmoset (Callithrix jacchus). Vision Res 1993; 33: 1301-1310.
41. Goodchild AK, Ghosh KK, Martin PR. Comparison of photoreceptor spatial density and ganglion cell morphology in the retina of human, macaque monkey, cat, and the marmoset Callithrix jacchus. J Comp Neurol 1996; 366: 55-75.
42. Wilder HD, Grunert U, Lee BB, Martin PR. Topography of ganglion cells and photoreceptors in the retina of a New World monkey: the marmoset Callithrix jacchus. Vis Neurosci 1996; 13: 335-352.
43. Hendrickson A, Troilo D, Djajadi H, Possin D, Springer A. Expression of synaptic and phototransduction markers during photoreceptor development in the marmoset monkey Callithrix jacchus. J Comp Neurol 2009; 512: 218-231.
44. Hendrickson A, Troilo D, Possin D, Springer A. Development of the neural retina and its vasculature in the marmoset Callithrix jacchus. J Comp Neurol 2006; 497: 270-286.
45. Cehajic-Kapetanovic J, Eleftheriou C, Allen AE, Milosavljevic N, Pienaar A, Bedford R et al. Restoration of vision with ectopic expression of human rod opsin. Curr Biol 2015; 25: 2111-2122.
46. Gaub BM, Berry MH, Holt AE, Reiner A, Kienzler MA, Dolgova N et al. Restoration of visual function by expression of a light-gated mammalian ion channel in retinal ganglion cells or ON-bipolar cells. Proc Natl Acad Sci USA 2014; 111: E5574-E5583.
47. Gaub BM, Berry MH, Holt AE, Isacoff EY, Flannery JG. Optogenetic vision restoration using rhodopsin for enhanced sensitivity. Mol Ther 2015; 23: 1562-1571.
48. Yin L, Greenberg K, Hunter JJ, Dalkara D, Kolstad KD, Masella BD et al. Intravitreal injection of AAV2 transduces macaque inner retina. Investig Ophthalmol Vis Sci 2011; 52: 2775-2783.
49. Kay CN, Ryals RC, Aslanidi GV, Min SH, Ruan Q, Sun J et al. Targeting photoreceptors via intravitreal delivery using novel, capsid-mutated AAV vectors. PLoS One 2013; 8: e62097.
50. Aslanidi GV, Rivers AE, Ortiz L, Song L, Ling C, Govindasamy L et al. Optimization of the capsid of recombinant adeno-associated virus 2 (AAV2) vectors: the final threshold? PLoS One 2013; 8: e59142.