A Designer AAV Variant Permits Efficient Retrograde Access to Projection Neurons

Neuron

Volumn 92, Issue 2, 2016, Pages 372-382

  Tervo, D Gowanlock R ^a   Hwang, Bum Yeol ^b   Viswanathan, Sarada ^a   Gaj, Thomas ^b   Lavzin, Maria ^a,c   Ritola, Kimberly D ^a   Lindo, Sarah ^a   Michael, Susan ^a   Kuleshova, Elena ^a,e   Ojala, David ^b   Huang, Cheng Chiu ^a   Gerfen, Charles R ^a,d   Schiller, Jackie ^a,c   Dudman, Joshua T ^a   Hantman, Adam W ^a   Looger, Loren L ^a   Schaffer, David V ^b   Karpova, Alla Y ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b University of California   (United States)

^c TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^d NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^e INSTITUTE OF HIGHER NERVOUS ACTIVITY AND NEUROPHYSIOLOGY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

PARVOVIRUS VECTOR; TRACER;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONNECTOME; CONTROLLED STUDY; DIRECTED MOLECULAR EVOLUTION; GENE EXPRESSION; GENETIC MANIPULATION; GENETIC VARIABILITY; IN VIVO STUDY; MONITORING; MOUSE; NERVE PROJECTION; NONHUMAN; PRIORITY JOURNAL; RAT; TRANSGENE; VIRAL GENE DELIVERY SYSTEM; VIRUS CAPSID; ANIMAL; CEREBELLUM; CYTOLOGY; DEPENDOPARVOVIRUS; FEMALE; GENE EDITING; GENE TRANSFER; GENE VECTOR; MALE; METABOLISM; NERVE CELL; PROCEDURES;

ANIMALS; CAPSID; CEREBELLUM; DEPENDOVIRUS; FEMALE; GENE EDITING; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; MALE; MICE; NEURONS; RATS;

EID: 84992036288     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2016.09.021     Document Type: Article

References (65)

1. Arnett, A.L., Beutler, L.R., Quintana, A., Allen, J., Finn, E., Palmiter, R.D., Chamberlain, J.S., Heparin-binding correlates with increased efficiency of AAV1- and AAV6-mediated transduction of striated muscle, but negatively impacts CNS transduction. Gene Ther. 20 (2013), 497–503.
2. Baer, G.M., Shanthaveerappa, T.R., Bourne, G.H., Studies on the pathogenesis of fixed rabies virus in rats. Bull. World Health Organ. 33 (1965), 783–794.
3. Braak, H., Braak, E., Development of Alzheimer-related neurofibrillary changes in the neocortex inversely recapitulates cortical myelogenesis. Acta Neuropathol. 92 (1996), 197–201.
4. Braak, H., Rüb, U., Gai, W.P., Del Tredici, K., Idiopathic Parkinson's disease: possible routes by which vulnerable neuronal types may be subject to neuroinvasion by an unknown pathogen. J Neural Transm (Vienna) 110 (2003), 517–536.
5. Brettschneider, J., Del Tredici, K., Lee, V.M.-Y., Trojanowski, J.Q., Spreading of pathology in neurodegenerative diseases: a focus on human studies. Nat. Rev. Neurosci. 16 (2015), 109–120.
6. Brodal, P., Bjaalie, J.G., Organization of the pontine nuclei. Neurosci. Res. 13 (1992), 83–118.
7. Brown, S.P., Hestrin, S., Intracortical circuits of pyramidal neurons reflect their long-range axonal targets. Nature 457 (2009), 1133–1136.
8. Callaway, E.M., Luo, L., Monosynaptic circuit tracing with glycoprotein-deleted rabies viruses. J. Neurosci. 35 (2015), 8979–8985.
9. Castle, M.J., Gershenson, Z.T., Giles, A.R., Holzbaur, E.L., Wolfe, J.H., Adeno-associated virus serotypes 1, 8, and 9 share conserved mechanisms for anterograde and retrograde axonal transport. Hum. Gene Ther. 25 (2014), 705–720.
10. Chen, T.-W., Wardill, T.J., Sun, Y., Pulver, S.R., Renninger, S.L., Baohan, A., Schreiter, E.R., Kerr, R.A., Orger, M.B., Jayaraman, V., et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499 (2013), 295–300.
11. Cong, L., Ran, F.A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P.D., Wu, X., Jiang, W., Marraffini, L.A., Zhang, F., Multiplex genome engineering using CRISPR/Cas systems. Science 339 (2013), 819–823.
12. Coulon, P., Derbin, C., Kucera, P., Lafay, F., Prehaud, C., Flamand, A., Invasion of the peripheral nervous systems of adult mice by the CVS strain of rabies virus and its avirulent derivative AvO1. J. Virol. 63 (1989), 3550–3554.
13. Dalkara, D., Byrne, L.C., Klimczak, R.R., Visel, M., Yin, L., Merigan, W.H., Flannery, J.G., Schaffer, D.V., In vivo-directed evolution of a new adeno-associated virus for therapeutic outer retinal gene delivery from the vitreous. Sci. Transl. Med., 5, 2013, 189ra76.
14. Enquist, L.W., Husak, P.J., Banfield, B.W., Smith, G.A., Infection and spread of alphaherpesviruses in the nervous system. Adv. Virus Res. 51 (1998), 237–347.
15. Fusi, S., Miller, E.K., Rigotti, M., Why neurons mix: high dimensionality for higher cognition. Curr. Opin. Neurobiol. 37 (2016), 66–74.
16. Gaudet, D., de Wal, J., Tremblay, K., Déry, S., van Deventer, S., Freidig, A., Brisson, D., Méthot, J., Review of the clinical development of alipogene tiparvovec gene therapy for lipoprotein lipase deficiency. Atheroscler. Suppl. 11 (2010), 55–60.
17. Gerfen, C.R., The neostriatal mosaic: striatal patch-matrix organization is related to cortical lamination. Science 246 (1989), 385–388.
18. Gerfen, C.R., Paletzki, R., Heintz, N., GENSAT BAC cre-recombinase driver lines to study the functional organization of cerebral cortical and basal ganglia circuits. Neuron 80 (2013), 1368–1383.
19. Gregoire, S., Zhang, S., Costanzo, J., Wilson, K., Fernandez, E.J., Kwon, I., Cis-suppression to arrest protein aggregation in mammalian cells. Biotechnol. Bioeng. 111 (2014), 462–474.
20. Guo, J.L., Lee, V.M., Cell-to-cell transmission of pathogenic proteins in neurodegenerative diseases. Nat. Med. 20 (2014), 130–138.
21. Guo, J.-Z., Graves, A.R., Guo, W.W., Zheng, J., Lee, A., Rodríguez-González, J., Li, N., Macklin, J.J., Phillips, J.W., Mensh, B.D., et al. Cortex commands the performance of skilled movement. eLife, 4, 2015, e10774.
22. He, M., Liu, Y., Wang, X., Zhang, M.Q., Hannon, G.J., Huang, Z.J., Cell-type-based analysis of microRNA profiles in the mouse brain. Neuron 73 (2012), 35–48.
23. Hollis, E.R. 2nd, Kadoya, K., Hirsch, M., Samulski, R.J., Tuszynski, M.H., Efficient retrograde neuronal transduction utilizing self-complementary AAV1. Mol. Ther. 16 (2008), 296–301.
24. Jackrel, M.E., DeSantis, M.E., Martinez, B.A., Castellano, L.M., Stewart, R.M., Caldwell, K.A., Caldwell, G.A., Shorter, J., Potentiated Hsp104 variants antagonize diverse proteotoxic misfolding events. Cell 156 (2014), 170–182.
25. Junyent, F., Kremer, E.J., CAV-2–why a canine virus is a neurobiologist's best friend. Curr. Opin. Pharmacol. 24 (2015), 86–93.
26. Kaplitt, M.G., Feigin, A., Tang, C., Fitzsimons, H.L., Mattis, P., Lawlor, P.A., Bland, R.J., Young, D., Strybing, K., Eidelberg, D., During, M.J., Safety and tolerability of gene therapy with an adeno-associated virus (AAV) borne GAD gene for Parkinson's disease: an open label, phase I trial. Lancet 369 (2007), 2097–2105.
27. Kaspar, B.K., Erickson, D., Schaffer, D., Hinh, L., Gage, F.H., Peterson, D.A., Targeted retrograde gene delivery for neuronal protection. Mol. Ther. 5 (2002), 50–56.
28. Kaspar, B.K., Lladó, J., Sherkat, N., Rothstein, J.D., Gage, F.H., Retrograde viral delivery of IGF-1 prolongs survival in a mouse ALS model. Science 301 (2003), 839–842.
29. Kato, S., Kobayashi, K., Inoue, K., Kuramochi, M., Okada, T., Yaginuma, H., Morimoto, K., Shimada, T., Takada, M., Kobayashi, K., A lentiviral strategy for highly efficient retrograde gene transfer by pseudotyping with fusion envelope glycoprotein. Hum. Gene Ther. 22 (2011), 197–206.
30. Kelly, R.M., Strick, P.L., Rabies as a transneuronal tracer of circuits in the central nervous system. J. Neurosci. Methods 103 (2000), 63–71.
31. Kern, A., Schmidt, K., Leder, C., Müller, O.J., Wobus, C.E., Bettinger, K., Von der Lieth, C.W., King, J.A., Kleinschmidt, J.A., Identification of a heparin-binding motif on adeno-associated virus type 2 capsids. J. Virol. 77 (2003), 11072–11081.
32. Koerber, J.T., Maheshri, N., Kaspar, B.K., Schaffer, D.V., Construction of diverse adeno-associated viral libraries for directed evolution of enhanced gene delivery vehicles. Nat. Protoc. 1 (2006), 701–706.
33. Koerber, J.T., Jang, J.-H., Schaffer, D.V., DNA shuffling of adeno-associated virus yields functionally diverse viral progeny. Mol. Ther. 16 (2008), 1703–1709.
34. Koerber, J.T., Klimczak, R., Jang, J.-H., Dalkara, D., Flannery, J.G., Schaffer, D.V., Molecular evolution of adeno-associated virus for enhanced glial gene delivery. Mol. Ther. 17 (2009), 2088–2095.
35. Kotterman, M.A., Schaffer, D.V., Engineering adeno-associated viruses for clinical gene therapy. Nat. Rev. Genet. 15 (2014), 445–451.
36. Kremer, E.J., Boutin, S., Chillon, M., Danos, O., Canine adenovirus vectors: an alternative for adenovirus-mediated gene transfer. J. Virol. 74 (2000), 505–512.
37. Kuan, L., Li, Y., Lau, C., Feng, D., Bernard, A., Sunkin, S.M., Zeng, H., Dang, C., Hawrylycz, M., Ng, L., Neuroinformatics of the allen mouse brain connectivity atlas. Methods 73 (2015), 4–17.
38. Legg, C.R., Mercier, B., Glickstein, M., Corticopontine projection in the rat: the distribution of labelled cortical cells after large injections of horseradish peroxidase in the pontine nuclei. J. Comp. Neurol. 286 (1989), 427–441.
39. Li, N., Chen, T.-W., Guo, Z.V., Gerfen, C.R., Svoboda, K., A motor cortex circuit for motor planning and movement. Nature 519 (2015), 51–56.
40. Maheshri, N., Koerber, J.T., Kaspar, B.K., Schaffer, D.V., Directed evolution of adeno-associated virus yields enhanced gene delivery vectors. Nat. Biotechnol. 24 (2006), 198–204.
41. Miller, M.W., Vogt, B.A., Direct connections of rat visual cortex with sensory, motor, and association cortices. J. Comp. Neurol. 226 (1984), 184–202.
42. Müller, O.J., Kaul, F., Weitzman, M.D., Pasqualini, R., Arap, W., Kleinschmidt, J.A., Trepel, M., Random peptide libraries displayed on adeno-associated virus to select for targeted gene therapy vectors. Nat. Biotechnol. 21 (2003), 1040–1046.
43. Murlidharan, G., Samulski, R.J., Asokan, A., Biology of adeno-associated viral vectors in the central nervous system. Front. Mol. Neurosci., 7, 2014, 76.
44. Nagy, A., Cre recombinase: the universal reagent for genome tailoring. Genesis 26 (2000), 99–109.
45. Ohka, S., Yang, W.-X., Terada, E., Iwasaki, K., Nomoto, A., Retrograde transport of intact poliovirus through the axon via the fast transport system. Virology 250 (1998), 67–75.
46. Ojala, D.S., Amara, D.P., Schaffer, D.V., Adeno-associated virus vectors and neurological gene therapy. Neuroscientist 21 (2015), 84–98.
47. Osborne, J.E., Dudman, J.T., RIVETS: a mechanical system for in vivo and in vitro electrophysiology and imaging. PLoS ONE, 9, 2014, e89007.
48. Pan, W.X., Mao, T., Dudman, J.T., Inputs to the dorsal striatum of the mouse reflect the parallel circuit architecture of the forebrain. Front. Neuroanat., 4, 2010, 147.
49. Piersanti, S., Astrologo, L., Licursi, V., Costa, R., Roncaglia, E., Gennetier, A., Ibanes, S., Chillon, M., Negri, R., Tagliafico, E., et al. Differentiated neuroprogenitor cells incubated with human or canine adenovirus, or lentiviral vectors have distinct transcriptome profiles. PLoS ONE, 8, 2013, e69808.
50. Pillay, S., Meyer, N.L., Puschnik, A.S., Davulcu, O., Diep, J., Ishikawa, Y., Jae, L.T., Wosen, J.E., Nagamine, C.M., Chapman, M.S., Carette, J.E., An essential receptor for adeno-associated virus infection. Nature 530 (2016), 108–112.
51. Ramón y Cajal, S., Histologie du Système Nerveux de l'homme et des Vertébrés. 1911, Maloine.
52. Reardon, T.R., Murray, A.J., Turi, G.F., Wirblich, C., Croce, K.R., Schnell, M.J., Jessell, T.M., Losonczy, A., Rabies virus CVS-N2c(ΔG) strain enhances retrograde synaptic transfer and neuronal viability. Neuron 89 (2016), 711–724.
53. Rothermel, M., Brunert, D., Zabawa, C., Díaz-Quesada, M., Wachowiak, M., Transgene expression in target-defined neuron populations mediated by retrograde infection with adeno-associated viral vectors. J. Neurosci. 33 (2013), 15195–15206.
54. Saunders, A., Johnson, C.A., Sabatini, B.L., Novel recombinant adeno-associated viruses for Cre activated and inactivated transgene expression in neurons. Front. Neural Circuits, 6, 2012, 47.
55. Schmued, L.C., Fallon, J.H., Fluoro-Gold: a new fluorescent retrograde axonal tracer with numerous unique properties. Brain Res. 377 (1986), 147–154.
56. Schnell, M.J., McGettigan, J.P., Wirblich, C., Papaneri, A., The cell biology of rabies virus: using stealth to reach the brain. Nat. Rev. Microbiol. 8 (2010), 51–61.
57. Seeley, W.W., Crawford, R.K., Zhou, J., Miller, B.L., Greicius, M.D., Neurodegenerative diseases target large-scale human brain networks. Neuron 62 (2009), 42–52.
58. Simão, D., Pinto, C., Fernandes, P., Peddie, C.J., Piersanti, S., Collinson, L.M., Salinas, S., Saggio, I., Schiavo, G., Kremer, E.J., et al. Evaluation of helper-dependent canine adenovirus vectors in a 3D human CNS model. Gene Ther. 23 (2016), 86–94.
59. Slaymaker, I.M., Gao, L., Zetsche, B., Scott, D.A., Yan, W.X., Zhang, F., Rationally engineered Cas9 nucleases with improved specificity. Science 351 (2016), 84–88.
60. Soudais, C., Laplace-Builhe, C., Kissa, K., Kremer, E.J., Preferential transduction of neurons by canine adenovirus vectors and their efficient retrograde transport in vivo. FASEB J. 15 (2001), 2283–2285.
61. Taymans, J.-M., Vandenberghe, L.H., Haute, C.V.D., Thiry, I., Deroose, C.M., Mortelmans, L., Wilson, J.M., Debyser, Z., Baekelandt, V., Comparative analysis of adeno-associated viral vector serotypes 1, 2, 5, 7, and 8 in mouse brain. Hum. Gene Ther. 18 (2007), 195–206.
62. Tomioka, R., Okamoto, K., Furuta, T., Fujiyama, F., Iwasato, T., Yanagawa, Y., Obata, K., Kaneko, T., Tamamaki, N., Demonstration of long-range GABAergic connections distributed throughout the mouse neocortex. Eur. J. Neurosci. 21 (2005), 1587–1600.
63. Towne, C., Schneider, B.L., Kieran, D., Redmond, D.E. Jr., Aebischer, P., Efficient transduction of non-human primate motor neurons after intramuscular delivery of recombinant AAV serotype 6. Gene Ther. 17 (2010), 141–146.
64. Ugolini, G., Kuypers, H.G., Simmons, A., Retrograde transneuronal transfer of herpes simplex virus type 1 (HSV 1) from motoneurones. Brain Res. 422 (1987), 242–256.
65. Wickersham, I.R., Finke, S., Conzelmann, K.K., Callaway, E.M., Retrograde neuronal tracing with a deletion-mutant rabies virus. Nat. Methods 4 (2007), 47–49.