Use of Adeno-Associated and Herpes Simplex Viral Vectors for In Vivo Neuronal Expression in Mice

Current Protocols in Neuroscience

Volumn 73, Issue 1, 2015, Pages 4.37.1-4.37.31

  Penrod, Rachel D ^a   Wells, Audrey M ^a   Carlezon, William A ^a   Cowan, Christopher W ^a  

^a MCLEAN HOSPITAL   (United States)

Author keywords

adeno associated virus; brain; herpes simplex virus; in vivo; mouse

Indexed keywords

ADENO ASSOCIATED VIRUS VECTOR; HERPES SIMPLEX VIRUS VECTOR; UNCLASSIFIED DRUG; VIRUS VECTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; CONTROLLED STUDY; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; SEROTYPE; STEREOTAXIC SURGERY; VIRAL GENE DELIVERY SYSTEM; WESTERN BLOTTING; ANIMAL; CYTOLOGY; DEPENDOPARVOVIRUS; GENE TRANSFER; GENE VECTOR; GENETICS; METABOLISM; NERVE CELL; PHYSIOLOGY; SIMPLEXVIRUS; STEREOTACTIC PROCEDURE;

ANIMALS; BRAIN; DEPENDOVIRUS; GENE EXPRESSION; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; MICE; NEURONS; SIMPLEXVIRUS; STEREOTAXIC TECHNIQUES;

EID: 85009300132     PISSN: 19348584     EISSN: 19348576     Source Type: Journal    
DOI: 10.1002/0471142301.ns0437s73     Document Type: Article

References (103)

1. Aschauer, D.F, Kreuz, S, and Rumpel, S. 2013. Analysis of transduction efficiency, tropism and axonal transport of AAV serotypes 1, 2, 5, 6, 8 and 9 in the mouse brain. PLoS One 8:e76310. doi: 10.1371/journal.pone.0076310.
2. Atasoy, D, Aponte, Y, Su, H.H, and Sternson, S.M. 2008. A FLEX switch targets Channelrhodopsin-2 to multiple cell types for imaging and long-range circuit mapping. J. Neurosci. 28:7025-7030. doi: 10.1523/JNEUROSCI.1954-08.2008.
3. Berns, K.I. and Giraud, C. 1996. Biology of adeno-associated virus. Curr. Top. Microbiol. Immunol. 218:1-23.
4. Cai, D, Cohen, K.B, Luo, T, Lichtman, J.W, and Sanes, J.R. 2013. Improved tools for the Brainbow toolbox. Nat. Methods 10:540-547. doi: 10.1038/nmeth.2450.
5. Carlezon, W.A. Jr, Boundy, V.A, Haile, C.N, Lane, S.B, Kalb, R.G, Neve, R.L, and Nestler, E.J. 1997. Sensitization to morphine induced by viral-mediated gene transfer. Science 277:812-814.
6. Carlezon, W.A. Jr, Haile, C.N, Coppersmith, R, Hayashi, Y, Malinow, R, Neve, R.L, and Nestler, E.J. 2000. Distinct sites of opiate reward and aversion within the midbrain identified using a herpes simplex virus vector expressing GluR1. J. Neurosci. 20:RC62.
7. Carlezon, W.A. Jr, Thome, J, Olson, V.G, Lane-Ladd, S.B, Brodkin, E.S, Hiroi, N, Duman, R.S, Neve, R.L, and Nestler, E.J. 1998. Regulation of cocaine reward by CREB. Science 282:2272-2275.
8. Castle, M.J, Gershenson, Z.T, Giles, A.R, Holzbaur, E.L.F, and Wolfe, J.H. 2014. Adeno-associated virus serotypes 1, 8, and 9 share conserved mechanisms for anterograde and retrograde axonal transport. Hum. Gene Ther. 25:705-720.
9. Cearley, C.N. and Wolfe, J. 2006. Transduction characteristics of adeno-associated virus vectors expressing cap serotypes 7, 8, 9, and Rh10 in the mouse brain. Mol. Ther. 13:528-537.
10. Cearley, C.N, Vandenberghe, L.H, Parente, M.K, Carnish, E.R, Wilson, J.M, and Wolfe, J.H. 2008. Expanded repertoire of AAV vector serotypes mediate unique patterns of transduction in mouse brain. Mol. Ther. 16:1710-1718.
11. Cho, J-H, Deisseroth, K, and Bolshakov, V.Y. 2013. Synaptic encoding of fear extinction in mPFC-amygdala circuits. Neuron 80:1491-1507.
12. Choi, J.-H, Yu, N.-K, Baek, G.-C, Bakes, J, Seo, D, Nam, H.J, Baek, S.H, Lim, C.-S, Lee, Y.-S, and Kaang, B.-K. 2014. Optimization of AAV expression cassettes to improve packaging capacity and transgene expression in neurons. Molecular Brain 7:17.
13. Christoffel, D.J, Golden, S.A, Dumitriu, D, Robison, A.J, Janssen, W.G, Ahn, H.F, Krishnan, V, Reyes, C.M, Han, M.-H, Ables, J.L, Eisch, A.J, Dietz, D.M, Ferguson, D, Neve, R.L, Greengard, P, Kim, Y, Morrison, J.H, and Russo, S.J. 2011. IκB kinase regulates social defeat stress-induced synaptic and behavioral plasticity. J. Neurosci. 31:314-321.
14. Costantini, L.C, Jacoby, D.R, Wang, S, Fraefel, C, Breakefield, X.O, and Isacson, O. 1999. Gene transfer to the nigrostriatal system by hybrid herpes simplex virus/adeno-associated virus amplicon vectors. Hum. Gene Ther. 10:2481-2494.
15. Covington, H.E, Lobo, M.K, Maze, I, Vialou, V, Hyman, J.M, Zaman, S, LaPlant, Q, Mouzon, E, Ghose, S, Tamminga, C.A, Neve, R.L, Deisseroth, K, and Nestler, E.J. 2010. Antidepressant effect of optogenetic stimulation of the medial prefrontal cortex. J. Neurosci. 30:16082-16090.
16. Crock, L.W, Kolber, B.J, Morgan, C.D, Sadler, K.E, Vogt, S.K, Bruchas, M.R, and Gereau, R.W. 2012. Central amygdala metabotropic glutamate receptor 5 in the modulation of visceral pain. J. Neurosci. 32:14217-14226.
17. Cuchet, D, Potel, C, Thomas, J, and Epstein, A.L. 2007. HSV-1 amplicon vectors. Expert Opin. Biol. Ther. 7:975-995.
18. Davidson, B.L, Stein, C.S, Heth, J.A, Martins, I, Kotin, R.M, Derksen, T.A, Zabner, J, Ghodsi, A, and Chiorini, J.A. 2000. Recombinant adeno-associated virus type 2, 4, and 5 vectors: Transduction of variant cell types and regions in the mammalian central nervous system. Proc. Natl. Acad. Sci. U.S.A. 97:3428-3432.
19. Dong, J.Y, Fan, P.D, and Frizzell, R.A. 1996. Quantitative analysis of the packaging capacity of recombinant adeno-associated virus. Hum. Gene Ther. 7:2101-2112.
20. Fagoe, N.D, Eggers, R, Verhaagen, J, and Mason, M.R.J. 2014. A compact dual promoter adeno-associated viral vector for efficient delivery of two genes to dorsal root ganglion neurons. Gene Ther. 21:242-252.
21. Fenno, L.E, Mattis, J, Ramakrishnan, C, Hyun, M, Lee, S.Y, He, M, Tucciarone, J, Selimbeyoglu, A, Berndt, A, Grosenick, L, Zalocusky, K.A, Bernstein, H, Perry, C, Diester, I, Boyce, F.M, Bass, C.E, Neve, R, Huang, Z.J, and Deisseroth, K. 2014. Targeting cells with single vectors using multiple-feature Boolean logic. Nat. Methods 11:763-772.
22. Ferguson, S.M, Eskenazi, D, Ishikawa, M, Wanat, M.J, Phillips, P.E.M, Dong, Y, Roth, B.L, and Neumaier, J.F. 2011. Transient neuronal inhibition reveals opposing roles of indirect and direct pathways in sensitization. Nat. Publ. Group 14:22-24.
23. Fink, D.J, DeLuca, N.A, Goins, W.F, and Glorioso, J.C. 1996. Gene transfer to neurons using herpes simplex virus-based vectors. Annu. Rev. Neurosci. 19:265-287.
24. Flotte, T.R, Afione, S.A, and Zeitlin, P.L. 1994. Adeno-associated virus vector gene expression occurs in nondividing cells in the absence of vector DNA integration. Am. J. Respir. Cell Mol. Biol. 11:517-521.
25. Fraefel, C, Song, S, Lim, F, Lang, P, Yu, L, Wang, Y, Wild, P, and Geller, A.I. 1996. Helper virus-free transfer of herpes simplex virus type 1 plasmid vectors into neural cells. J. Virol. 70:7190-7197.
26. Frenkel, N. 2006. The history of the hsv amplicon: From naturally occurring defective genomes to engineered amplicon vectors. Curr. Gene Ther. 6:277-299.
27. Gallagher, S, Winston, S.E, Fuller, S.A, and Hurrell, J.G.R. 2011. Immunoblotting and Immunodetection. Curr. Protoc. Cell Biol. 52:6.2.1-6.2.28.
28. Ghosh, A, Yue, Y, and Duan, D. 2011. Efficient transgene reconstitution with hybrid dual AAV vectors carrying the minimized bridging sequences. Hum. Gene Ther. 22:77-83.
29. Goins, W.F, Wolfe, D, Krisky, D.M, Bai, Q, Burton, E.A, Fink, D.J, and Glorioso, J.C. 2004. Delivery using herpes simplex virus: An overview. Methods Mol. Biol. 246:257-299.
30. Gradinaru, V, Zhang, F, Ramakrishnan, C, Mattis, J, Prakash, R, Diester, I, Goshen, I, Thompson, K.R, and Deisseroth, K. 2010. Molecular and cellular approaches for diversifying and extending optogenetics. Cell 141:154-165.
31. Gräff, J, Joseph, N.F, Horn, M.E, Samiei, A, Meng, J, Seo, J, Rei, D, Bero, A.W, Phan, T.X, Wagner, F, Holson, E, Xu, J, Sun, J, Neve, R.L, Mach, R.H, Haggarty, S.J, and Tsai, L-H. 2014. Epigenetic priming of memory updating during reconsolidation to attenuate remote fear memories. Cell 156:261-276.
32. Han, J.H, Yiu, A.P, Cole, C.J, Hsiang, H.L, Neve, R.L, and Josselyn, S.A. 2008. Increasing CREB in the auditory thalamus enhances memory and generalization of auditory conditioned fear. Learn. Mem. 15:443-453.
33. Han, J.H, Kushner, S.A, Yiu, A.P, Cole, C.J, Matynia, A, Brown, R.A, Neve, R.L, Guzowski, J.F, Silva, A.J, and Josselyn, S.A. 2007. Neuronal competition and selection during memory formation. Science 316:457-460.
34. Hofman F.M. and Taylor, C.R. 2013. Immunohistochemistry. Curr. Protoc. Immunol. 103:21.4.1-21.4.26.
35. Hong, C.-S, Goins, W.F, Goss, J.R, Burton, E.A, and Glorioso, J.C. 2006. Herpes simplex virus RNAi and neprilysin gene transfer vectors reduce accumulation of Alzheimer's disease-related amyloid-β peptide in vivo. Gene Ther. 13:1068-1079.
36. Hooks, B.M, Mao, T, Gutinsky, D.A, Yamawaki, N, Svoboda, K, and Shepherd, G.M. 2013. Organization of cortical and thalamic input to pyramidal neurons in mouse motor cortex. J. Neurosci. 33:748-760.
37. Horsburgh, B.C, Hubinette, M.M, Qiang, D, MacDonald, M.L, and Tufaro, F. 1999. Allele replacement: An application that permits rapid manipulation of herpes simplex virus type 1 genomes. Gene Ther. 6:922-930.
38. Husain, T, Passini, M.A, Parente, M.K, Fraser, N.W, and Wolfe, J.H. 2009. Long-term AAV vector gene and protein expression in mouse brain from a small pan-cellular promoter is similar to neural cell promoters. Gene Ther. 16:927-932.
39. Jennings, J.H, Sparta, D.R, Stamatakis, A.M, Ung, R.L, Pleil, K.E, Kash, T.L, and Stuber, G.D. 2013. Distinct extended amygdala circuits for divergent motivational states. Nature 496:224-228.
40. Jerusalinsky, D. and Epstein, A. 2006. Amplicon vectors as outstanding tools to study and modify cognitive functions. Curr. Gene. Ther. 6:351-360.
41. Jerusalinsky, D, Baez, M.V, and Epstein, A.L. 2012. Herpes simplex virus type 1-based amplicon vectors for fundamental research in neurosciences and gene therapy of neurological diseases. J. Physiol. 106:2-11.
42. Jin, B.K, Belloni, M, Conti, B, Federoff, H.J, Starr, R, Son, J.H, Baker, H, and Joh, T.H. 1996. Prolonged in vivo gene expression driven by a tyrosine hydroxylase promoter in a defective herpes simplex virus amplicon vector. Hum. Gene Ther. 7:2015-2024.
43. Johnston, K.M, Jacoby, D, Pechan, P.A, Fraefel, C, Borghesani, P, Schuback, D, Dunn, R.J, Smith, F.I, and Breakefield, X.O. 1997. HSV/AAV hybrid amplicon vectors extend transgene expression in human glioma cells. Hum. Gene Ther. 8:359-370.
44. Kaplitt, M.G, Leone, P, Samulski, R.J, Xiao, X, Pfaff, D.W, O'Malley, K.L, and During, M.J. 1994. Long-term gene expression and phenotypic correction using adeno-associated virus vectors in the mammalian brain. Nat. Genet. 8:148-154.
45. Kelz, M.B, Chen, J, Carlezon, W.A, Whisler, K, Gilden, L, Beckmann, A.M, Steffen, C, Zhang, Y.J, Marotti, L, Self, D.W, Tkatch, T, Baranauskas, G, Surmeier, D.J, Neve, R.L, Duman, R.S, Picciotto, M.R, and Nestler, E.J. 1999. Expression of the transcription factor deltaFosB in the brain controls sensitivity to cocaine. Nature 401:272-276.
46. Krisky, D.M, Wolfe, D, Goins, W.F, Marconi, P.C, Ramakrishnan, R, Mata, M, Rouse, R.J, Fink, D.J, and Glorioso, J.C. 1998. Deletion of multiple immediate-early genes from herpes simplex virus reduces cytotoxicity and permits long-term gene expression in neurons. Gene Ther. 5:1593-1603.
47. Kügler, S, Lingor, P, Schöll, U, Zolotukhin, S, and Bähr, M. 2003. Differential transgene expression in brain cells in vivo and in vitro from AAV-2 vectors with small transcriptional control units. Virology 311:89-95.
48. Kupferschmidt, D.A, Cody, P.A, Lovinger, D.M, and Davis, M.I. 2015. Brain BLAQ: Post-hoc thick-section histochemistry for localizing optogenetic constructs in neurons and their distal terminals. Front. Neuroanat. 9:6.
49. Le Guiner, C, Stieger, K, Toromanoff, A, Guilbaud, M, Mendes-Madeira, A, Devaux, M, Guigand, L, Cherel, Y, Moullier, P, Rolling, F, and Adjali, O. 2014. Transgene regulation using the tetracycline-inducible TetR-KRAB system after AAV-mediated gene transfer in rodents and nonhuman primates. PLoS One 9:e102538.
50. Lim, F. 2013. HSV-1 as a Model for emerging gene delivery vehicles. ISRN Virology 2013;Article ID 397243, 12 pages. doi: 10.5402/2013/397243.
51. Lim, F, Hartley, D, Starr, P, Lang, P, Song, S, Yu, L, Wang, Y, and Geller, A.I. 1996. Generation of high-titer defective HSV-1 vectors using an IE 2 deletion mutant and quantitative study of expression in cultured cortical cells. BioTechniques 20:460-469.
52. Liu, B, Wang, S, Brenner, M, Paton, J.F.R, and Kasparov, S. 2008. Enhancement of cell-specific transgene expression from a Tet-Off regulatory system using a transcriptional amplification strategy in the rat brain. J. Gene Med. 10:583-592.
53. Logvinoff, C. and Epstein, A.L. 2000. Genetic engineering of herpes simplex virus and vector genomes carrying loxP sites in cells expressing Cre recombinase. Virology 267:102-110.
54. Loweth, J.A, Li, D, Cortright, J.J, Wilke, G, Jeyifous, O, Neve, R.L, Bayer, K.U, and Vezina, P. 2013. Persistent reversal of enhanced amphetamine intake by transient CaMKII inhibition. J. Neurosci. 33:1411-1416.
55. Marconi, P, Fraefel, C, and Epstein, A.L. 2015. Herpes simplex virus type 1 (HSV-1)-derived recombinant vectors for gene transfer and gene therapy. Methods Mol. Biol. 1254:269-293.
56. Mata, M, Glorioso, J.C, and Fink, D.J. 2002. Targeted gene delivery to the nervous system using herpes simplex virus vectors. Physiol. Behav. 77:483-488.
57. McCown, T.J, Xiao, X, Li, J, Breese, G.R, and Jude Samulski, R. 1996. Differential and persistent expression patterns of CNS gene transfer by an adeno-associated virus (AAV) vector. Brain Res. 713:99-107.
58. Michaelides, M, Anderson, S.A.R, Ananth, M, Smirnov, D, Thanos, P.K, Neumaier, J.F, Wang, G.-J, Volkow, N.D, and Hurd, Y.L. 2013. Whole-brain circuit dissection in free-moving animals reveals cell-specific mesocorticolimbic networks. J. Clin. Invest. 123:5342-5350.
59. Muschamp, J.W. and Carlezon, W.A. 2013. Roles of Nucleus Accumbens CREB and Dynorphin in Dysregulation of Motivation. Cold Spring Harb. Perspect. Med. 3:a012005-a012005.
60. Muzumdar, M.D, Tasic, B, Miyamichi, K, Li, L, and Luo, L. 2007. A global double-fluorescent Cre reporter mouse. Genesis 45:593-605.
61. Neve, R.L. and Lim, F. 2013. Generation of high-titer defective HSV-1 vectors. Curr. Protoc. Neurosci. 62:4.13.1-4.13.15.
62. Neve, R.L, Neve, K.A, Nestler, E.J, and Carlezon, W.A. 2005. Use of herpes virus amplicon vectors to study brain disorders. BioTechniques 39:381-391.
63. Norgren, R.B. and Lehman, M.N. 1998. Herpes simplex virus as a transneuronal tracer. Neurosci. Biobehav. Rev. 22:695-708.
64. Palfi, A, Chadderton, N, McKee, A.G, Blanco Fernandez, A, Humphries, P, Kenna, P.F, and Farrar, G.J. 2012. Efficacy of codelivery of dual AAV2/5 vectors in the murine retina and hippocampus. Hum. Gene Ther. 23:847-858.
65. Pascoli, V, Turiault, M, and Luscher, C. 2012. Reversal of cocaine-evoked synaptic potentiation resets drug-induced adaptive behavior. Nature 481:71-75.
66. Pliakas, A.M, Carlson, R.R, Neve, R.L, Konradi, C, Nestler, E.J, and Carlezon, W.A. Jr. 2001. Altered responsiveness to cocaine and increased immobility in the forced swim test associated with elevated cAMP response element-binding protein expression in nucleus accumbens. J. Neurosci. 21:7397-7403.
67. Podsakoff, G, Wong, K.K, and Chatterjee, S. 1994. Efficient gene transfer into nondividing cells by adeno-associated virus-based vectors. J. Virol. 68:5656-5666.
68. Pulipparacharuvil, S, Renthal, W, Hale, C.F, Taniguchi, M, Xiao, G, Kumar, A, Russo, S.J, Sikder, D, Dewey, C.M, Davis, M.M, Greengard, P, Nairn, A.C, Nestler, E.J, and Cowan, C.W. 2008. Cocaine regulates MEF2 to control synaptic and behavioral plasticity. Neuron 59:621-633.
69. Rabinowitz, J.E, Rolling, F, Li, C, Conrath, H, Xiao, W, Xiao, X, and Samulski, R.J. 2002. Cross-packaging of a single adeno-associated virus (AAV) Type 2 vector genome into multiple AAV serotypes enables transduction with broad specificity. J. Virol. 76:791-801.
70. Rothermel, M, Brunert, D, Zabawa, C, Diaz-Quesada, M, and Wachowiak, M. 2013. Transgene expression in target-defined neuron populations mediated by retrograde infection with adeno-associated viral vectors. J. Neurosci. 33:15195-15206.
71. Rumpel, S, LeDoux, J, Zador, A, and Malinow, R. 2005. Postsynaptic receptor trafficking underlying a form of associative learning. Science 308:83-88.
72. Saeki, Y, Fraefel, C, Ichikawa, T, Breakefield, X.O, and Chiocca, E.A. 2001. Improved helper virus-free packaging system for HSV amplicon vectors using an ICP27-deleted, oversized HSV-1 DNA in a bacterial artificial chromosome. Mol. Ther. 3:591-601.
73. Saeki, Y, Ichikawa, T, Saeki, A, Chiocca, E.A, Tobler, K, Ackermann, M, Breakefield, X.O, and Fraefel, C. 1998. Herpes simplex virus type 1 DNA amplified as bacterial artificial chromosome in Escherichia coli: Rescue of replication-competent virus progeny and packaging of amplicon vectors. Hum. Gene Ther. 9:2787-2794.
74. Salegio, E.A, Samaranch, L, Kells, A.P, Mittermeyer, G, San Sebastian, W, Zhou, S, Beyer, J, Forsayeth, J, and Bankiewicz, K.S. 2013. Axonal transport of adeno-associated viral vectors is serotype-dependent. Gene Ther. 20:348-352.
75. Schnepp, B.C, Clark, K.R, Klemanski, D.L, Pacak, C.A, and Johnson, P.R. 2003. Genetic fate of recombinant adeno-associated virus vector genomes in muscle. J. Virol. 77:3495-3504.
76. Scobie, K.N, Damez-Werno, D, Sun, H, Shao, N, Gancarz, A, Panganiban, C.H, Dias, C, Koo, J, Caiafa, P, Kaufman, L, Neve, R.L, Dietz, D.M, Shen, L, and Nestler, E.J. 2014. Essential role of poly(ADP-ribosyl)ation in cocaine action. Proc. Natl. Acad. Sci. U.S.A. 111:2005-2010.
77. Senn, V, Wolff, S.B.E, Herry, C, Grenier, F, Ehrlich, I, Gründemann, J, Fadok, J.P, Müller, C, Letzkus, J.J, and Lüthi, A. 2014. Long-range connectivity defines behavioral specificity of amygdala neurons. Neuron 81:428-437.
78. Simonato, M, Manservigi, R, Marconi, P, and Glorioso, J. 2000. Gene transfer into neurones for the molecular analysis of behaviour: Focus on herpes simplex vectors. Trends Neurosci. 23:183-190.
79. Smith, L.N, Jedynak, J.P, Fontenot, M.R, Hale, C.F, Dietz, K.C, Taniguchi, M, Thomas, F.S, Zirlin, B.C, Birnbaum, S.G, Huber, K.M, and Cowan, C.W. 2014. Fragile X mental retardation protein regulates synaptic and behavioral plasticity to repeated cocaine administration. Neuron 82:645-658.
80. Spaete, R.R. and Frenkel, N. 1982. The herpes simplex virus amplicon: A new eukaryotic defective-virus cloning-amplifying vector. Cell 30:295-304.
81. Spaete, R.R. and Frenkel, N. 1985. The herpes simplex virus amplicon: Analyses of cis-acting replication functions. Proc. Natl. Acad. Sci. U.S.A. 82:694-698.
82. Stamatakis, A.M. and Stuber, G.D. 2012. Activation of lateral habenula inputs to the ventral midbrain promotes behavioral avoidance. Nat. Neurosci. 15:1105-1107.
83. Stamatakis, A.M, Jennings, J.H, Ung, R.L, Blair, G.A, Weinberg, R.J, Neve, R.L, Boyce, F, Mattis, J, Ramakrishnan, C, Deisseroth, K, and Stuber, G.D. 2013. A unique population of ventral tegmental area neurons inhibits the lateral habenula to promote reward. Neuron 80:1039-1053.
84. Stavropoulos, T.A. and Strathdee, C.A. 1998. An enhanced packaging system for helper-dependent herpes simplex virus vectors. J. Virol. 72:7137-7143.
85. Swiech, L, Heidenreich, M, Banerjee, A, Habib, N, Li, Y, Trombetta, J, Sur, M, and Zhang, F. 2015. In vivo interrogation of gene function in the mammalian brain using CRISPR-Cas9. Nat. Biotechnol. 33:102-106.
86. Taymans, J.-M, Vandenberghe, L.H, Haute, C.V.D, Thiry, I, Deroose, C.M, Mortelmans, L, Wilson, J.M, Debyser, Z, and Baekelandt, V. 2007. Comparative analysis of adeno-associated viral vector serotypes 1, 2, 5, 7, and 8 in mouse brain. Hum. Gene Ther. 18:195-206.
87. Todtenkopf, M.S, Parsegian, A, Naydenov, A, Neve, R.L, Conradi, C, and Carlezon, W.A. Jr. 2006. Brain reward regulated by AMPA receptor subunits in nucleus accumbens shell. J. Neurosci. 6:11665-11669.
88. Vetere, G, Restivo, L, Cole, C.J, Ross, P.J, Ammassari-Teule, M, Josselyn, S.A, and Frankland, P.W. 2011. Spine growth in the anterior cingulate cortex is necessary for the consolidation of contextual fear memory. PNAS. 108:8456-8460.
89. Wang, C, Wang, C.-M, Clark, K.R, and Sferra, T.J. 2003. Recombinant AAV serotype 1 transduction efficiency and tropism in the murine brain. Gene Ther. 10:1528-1534.
90. Wang, Q, Henry, A.M, Harris, J.A, Oh, S.W, Joines, K.M, Nyhus, J, Hirokawa, K.E, Dee, N, Mortrud, M, and Parry, S. 2014. Systematic comparison of adeno-associated virus and biotinylated dextran amine reveals equivalent sensitivity between tracers and novel projection targets in the mouse brain - Wang - 2014 - Journal of Comparative Neurology - Wiley Online Library. J. Comp. Neurol. 522:1989-2012. Available at: http://www-ncbi-nlm-nih-gov.ezp-prod1.hul.harvard.edu/pubmed/24639291.
91. Watakabe, A, Ohtsuka, M, Kinoshita, M, Takaji, M, Isa, K, Mizukami, H, Ozawa, K, Isa, T, and Yamamori, T. 2014a. Comparative analyses of adeno-associated viral vector serotypes 1, 2, 5, 8 and 9 in marmoset, mouse and macaque cerebral cortex. Neurosci. Res. 93:144-157.
92. Watakabe, A, Takaji, M, Kato, S, Kobayashi, K, Mizukami, H, Ozawa, K, Ohsawa, S, Matsui, R, Watanabe, D, and Yamamori, T. 2014b. Simultaneous visualization of extrinsic and intrinsic axon collaterals in Golgi-like detail for mouse corticothalamic and corticocortical cells: A double viral infection method. Front. Neural Circuits 8:110. doi: 10.3389/fncir.2014.00110.
93. Wouterlood, F.G, Bloem, B, Mansvelder, H.D, Luchicchi, A, and Deisseroth, K. 2014. A fourth generation of neuroanatomical tracing techniques: Exploiting the offspring of genetic engineering. J. Neurosci. Methods 235:331-348.
94. Wu, N, Watkins, S.C, Schaffer, P.A, and DeLuca, N.A. 1996. Prolonged gene expression and cell survival after infection by a herpes simplex virus mutant defective in the immediate-early genes encoding ICP4, ICP27, and ICP22. J. Virol. 70:6358-6369.
95. Xiao, X, Li, J, McCown, T.J, and Samulski, R.J. 1997. Gene transfer by adeno-associated virus vectors into the central nervous system. Exp. Neurol. 144:113-124.
96. Xu, J, Ma, C, Bass, C, and Terwilliger, E.F. 2005. A combination of mutations enhances the neurotropism of AAV-2. Virology 341:203-214.
97. Yang, A.R.S.T, Liu, J, Yi, H.S, Warnock, K.T, Wang, M, June, H.L, Puche, A.C, Elnabawi, A, Sieghart, W, Aurelian, L, and June, H.L. 2011. Binge drinking: In search of its molecular target via the GABA(A) receptor. Front. Neurosci. 5:123.
98. Yizhar, O, Fenno, L.E, Davidson, T.J, Mogri, M, and Deisseroth, K. 2011. Optogenetics in neural systems. Neuron 71:9-34.
99. Yonehara, K, Farrow, K, Ghanem, A, Hillier, D, Balint, K, Teixeira, M, Jüttner, J, Noda, M, Neve, R.L, Conzelmann, K.-K, and Roska, B. 2013. The first stage of cardinal direction selectivity is localized to the dendrites of retinal ganglion cells. Neuron 79:1078-1085.
100. Zaupa, C, Revol-Guyot, V, and Epstein, A.L. 2003. Improved packaging system for generation of high-level noncytotoxic HSV-1 amplicon vectors using cre-loxp site-specific recombination to delete the packaging signals of defective helper genomes. Hum. Gene Ther. 14:1049-1063.
101. Zhang, G.-R, Zhao, H, Abdul-Muneer, P.M, Cao, H, Li, X, and Geller, A.I. 2015. Neurons can be labeled with unique hues by helper virus-free HSV-1 vectors expressing Brainbow. J. Neurosci. Methods 240:77-88.
102. Zhu, P, Narita, Y, Bundschuh, S.T, Fajardo, O, Schärer, Y.-P.Z, Chattopadhyaya, B, Bouldoires, E.A, Stepien, A.E, Deisseroth, K, Arber, S, Sprengel, R, Rijli, F.M, and Friedrich, R.W. 2009. Optogenetic dissection of neuronal circuits in zebrafish using viral gene transfer and the tet system. Front. Neural Circuits 3:21.
103. Zou, M, De Koninck, P, Neve, R.L, and Friedrich, R.W. 2014. Fast gene transfer into the adult zebrafish brain by herpes simplex virus 1 (HSV-1) and electroporation: Methods and optogenetic applications. Front. Neural Circuits 8:41.