Avian Adeno-Associated Virus Vector Efficiently Transduces Neurons in the Embryonic and Post-Embryonic Chicken Brain

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Matsui, Ryosuke ^a   Tanabe, Yasuto ^b   Watanabe, Dai ^a  

^a KYOTO UNIVERSITY   (Japan)

^b OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PARVOVIRUS VECTOR; TETRACYCLINE;

ANIMAL TISSUE; ARTICLE; AUDITORY SYSTEM; AUDITORY SYSTEM PARAMETERS; BRAIN FUNCTION; BRAIN NERVE CELL; BRAIN STEM; BRAIN TISSUE; CHICKEN; DEVELOPMENTAL STAGE; EMBRYO; GENE EXPRESSION SYSTEM; GENE INDUCTION; GENETIC MANIPULATION; GENETIC TRANSDUCTION; GENOME IMPRINTING; HUMAN; HUMAN CELL; INFORMATION PROCESSING; INTERAURAL TIME DISCRIMINATION; INTRACELLULAR SIGNALING; MAGNOCELLULAR NUCLEUS; MATHEMATICAL COMPUTING; MEMORY; NERVE CELL MEMBRANE POTENTIAL; NEURAL TUBE; NONHUMAN; PERINATAL PERIOD; THALAMUS INTRALAMINAR NUCLEUS; VIRAL GENE DELIVERY SYSTEM;

ANIMALS; BRAIN; CHICK EMBRYO; CHICKENS; DEPENDOVIRUS; GENE EXPRESSION PROFILING; GENETIC VECTORS; NEURONS; TRANSDUCTION, GENETIC;

AVIAN ADENO-ASSOCIATED VIRUS; LENTIVIRUS;

EID: 84868705066     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0048730     Document Type: Article

References (71)

1. Muir GD, (2000) Early ontogeny of locomotor behaviour: a comparison between altricial and precocial animals. Brain Res Bull 53: 719-726.
2. Mezey S, Krivokuca D, Bálint E, Adorján A, Zachar G, et al. (2012) Postnatal changes in the distribution and density of neuronal nuclei and doublecortin antigens in domestic chicks (Gallus domesticus). J Comp Neurol 520: 100-116 doi:10.1002/cne.22696.
3. Horn G, (2004) Pathways of the past: the imprint of memory. Nat Rev Neurosci 5: 108-120 doi:10.1038/nrn1324.
4. Horn G, McCabe B, (1984) Predispositions and Preferences- Effects on Imprinting of Lesions to the Chick Brain. Anim Behav 32: 288-292.
5. Johnson M, Bolhuis J, Horn G, (1985) Interaction Between Acquired Preferences and Developing Predispositions During Imprinting. Anim Behav 33: 1000-1006.
6. Bolhuis JJ, (1999) Early learning and the development of filial preferences in the chick. Behav Brain Res 98: 245-252.
7. Funahashi J, Okafuji T, Ohuchi H, Noji S, Tanaka H, et al. (1999) Role of Pax-5 in the regulation of a mid-hindbrain organizer's activity. Dev Growth Differ 41: 59-72.
8. Hughes SH, Greenhouse JJ, Petropoulos CJ, Sutrave P, (1987) Adaptor plasmids simplify the insertion of foreign DNA into helper-independent retroviral vectors. J Virol 61: 3004-3012.
9. Yamaguchi S, Katagiri S, Hirose N, Fujimoto Y, Mori M, et al. (2007) In-vivo gene transfer into newly hatched chick brain by electroporation. Neuroreport 18: 735-739 doi:10.1097/WNR.0b013e3280bef990.
10. Coleman JE, Huentelman MJ, Kasparov S, Metcalfe BL, Paton JFR, et al. (2003) Efficient large-scale production and concentration of HIV-1-based lentiviral vectors for use in vivo. Physiol Genomics 12: 221-228 doi:10.1152/physiolgenomics.00135.2002.
11. Muramatsu T, Mizutani Y, Ohmori Y, Okumura J, (1997) Comparison of three nonviral transfection methods for foreign gene expression in early chicken embryos in ovo. Biochem Biophys Res Commun 230: 376-380.
12. Momose T, Tonegawa A, Takeuchi J, Ogawa H, Umesono K, et al. (1999) Efficient targeting of gene expression in chick embryos by microelectroporation. Dev Growth Differ 41: 335-344.
13. Tenenbaum L, Chtarto A, Lehtonen E, Velu T, Brotchi J, et al. (2004) Recombinant AAV-mediated gene delivery to the central nervous system. J Gene Med 6 (Suppl 1): S212-S222 doi:10.1002/jgm.506.
14. Burger C, Nash K, Mandel RJ, (2005) Recombinant adeno-associated viral vectors in the nervous system. Hum Gene Ther 16: 781-791 doi:10.1089/hum.2005.16.781.
15. Mueller C, Flotte TR, (2008) Clinical gene therapy using recombinant adeno-associated virus vectors. Gene Ther 15: 858-863 doi:10.1038/gt.2008.68.
16. Kaplitt MG, Leone P, Samulski RJ, Xiao X, Pfaff DW, et al. (1994) Long-term gene expression and phenotypic correction using adeno-associated virus vectors in the mammalian brain. Nat Genet 8: 148-154 doi:10.1038/ng1094-148.
17. Buller RM, Janik JE, Sebring ED, Rose JA, (1981) Herpes simplex virus types 1 and 2 completely help adenovirus-associated virus replication. J Virol 40: 241-247.
18. Srivastava A, Lusby EW, Berns KI, (1983) Nucleotide sequence and organization of the adeno-associated virus 2 genome. J Virol 45: 555-564.
19. Wistuba A, Weger S, Kern A, Kleinschmidt JA, (1995) Intermediates of adeno-associated virus type 2 assembly: identification of soluble complexes containing Rep and Cap proteins. J Virol 69: 5311-5319.
20. Musatov S, Roberts J, Pfaff D, Kaplitt M, (2002) A cis-acting element that directs circular adeno-associated virus replication and packaging. J Virol 76: 12792-12802.
21. Samulski RJ, Chang LS, Shenk T, (1989) Helper-free stocks of recombinant adeno-associated viruses: normal integration does not require viral gene expression. J Virol 63: 3822-3828.
22. McCown TJ, Xiao X, Li J, Breese GR, Samulski RJ, (1996) Differential and persistent expression patterns of CNS gene transfer by an adeno-associated virus (AAV) vector. Brain Res 713: 99-107.
23. Wu Z, Asokan A, Samulski RJ, (2006) Adeno-associated virus serotypes: vector toolkit for human gene therapy. Mol Ther 14: 316-327 doi:10.1016/j.ymthe.2006.05.009.
24. Xu R, Janson CG, Mastakov M, Lawlor P, Young D, et al. (2001) Quantitative comparison of expression with adeno-associated virus (AAV-2) brain-specific gene cassettes. Gene Ther 8: 1323-1332 doi:10.1038/sj.gt.3301529.
25. Shevtsova Z, Malik JMI, Michel U, Bähr M, Kügler S, (2005) Promoters and serotypes: targeting of adeno-associated virus vectors for gene transfer in the rat central nervous system in vitro and in vivo. Exp Physiol 90: 53-59 doi:10.1113/expphysiol.2004.028159.
26. Oh MS, Hong SJ, Huh Y, Kim K-S, (2009) Expression of transgenes in midbrain dopamine neurons using the tyrosine hydroxylase promoter. Gene Ther 16: 437-440 doi:10.1038/gt.2008.148.
27. Nathanson JL, Jappelli R, Scheeff ED, Manning G, Obata K, et al. (2009) Short Promoters in Viral Vectors Drive Selective Expression in Mammalian Inhibitory Neurons, but do not Restrict Activity to Specific Inhibitory Cell-Types. Front Neural Circuits 3: 19 doi:10.3389/neuro.04.019.2009.
28. Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K, (2005) Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 8: 1263-1268 doi:10.1038/nn1525.
29. Tian L, Hires SA, Mao T, Huber D, Chiappe ME, et al. (2009) Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat Methods 6: 875-881 doi:10.1038/nmeth.1398.
30. Bossis I, Chiorini JA, (2003) Cloning of an avian adeno-associated virus (AAAV) and generation of recombinant AAAV particles. J Virol 77: 6799-6810.
31. Estevez C, Villegas P, (2004) Sequence analysis, viral rescue from infectious clones and generation of recombinant virions of the avian adeno-associated virus. Virus Res 105: 195-208 doi:10.1016/j.virusres.2004.05.010.
32. Wang J, Zhu L, Zhu J, Sun H, Zhu G, (2011) Molecular characterization and phylogenetic analysis of an avian adeno-associated virus originating from a chicken in China. Arch Virol 156: 71-77 doi:10.1007/s00705-010-0822-x.
33. Bartashunas C, Suboski MD, (1984) Effects of age of chick on social transmission of pecking preferences from hen to chicks. Developmental psychobiology 17: 121-127 doi:10.1002/dev.420170203.
34. Zhou X, Vink M, Klaver B, Berkhout B, Das AT, (2006) Optimization of the Tet-On system for regulated gene expression through viral evolution. Gene Ther 13: 1382-1390 doi:10.1038/sj.gt.3302780.
35. Carr CE, Konishi M, (1990) A circuit for detection of interaural time differences in the brain stem of the barn owl. J Neurosci 10: 3227-3246.
36. Jackson H, Hackett JT, Rubel EW, (1982) Organization and development of brain stem auditory nuclei in the chick: ontogeny of postsynaptic responses. J Comp Neurol 210: 80-86 doi:10.1002/cne.902100109.
37. Young SR, Rubel EW, (1983) Frequency-specific projections of individual neurons in chick brainstem auditory nuclei. J Neurosci 3: 1373-1378.
38. Luo L, Flanagan JG, (2007) Development of continuous and discrete neural maps. Neuron 56: 284-300 doi:10.1016/j.neuron.2007.10.014.
39. Lippe W, Rubel EW, (1985) Ontogeny of tonotopic organization of brain stem auditory nuclei in the chicken: implications for development of the place principle. J Comp Neurol 237: 273-289 doi:10.1002/cne.902370211.
40. Bartlett JS, Samulski RJ, McCown TJ, (1998) Selective and rapid uptake of adeno-associated virus type 2 in brain. Hum Gene Ther 9: 1181-1186 doi:10.1089/hum.1998.9.8-1181.
41. Naldini L, Blömer U, Gallay P, Ory D, Mulligan R, et al. (1996) In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272: 263-267.
42. Nicol AU, Brown MW, Horn G, (1995) Neurophysiological investigations of a recognition memory system for imprinting in the domestic chick. Eur J Neurosci 7: 766-776.
43. Carr CE, Boudreau RE, (1993) Organization of the nucleus magnocellularis and the nucleus laminaris in the barn owl: encoding and measuring interaural time differences. J Comp Neurol 334: 337-355 doi:10.1002/cne.903340302.
44. Urlinger S, Baron U, Thellmann M, Hasan MT, Bujard H, et al. (2000) Exploring the sequence space for tetracycline-dependent transcriptional activators: novel mutations yield expanded range and sensitivity. Proc Natl Acad Sci USA 97: 7963-7968 doi:10.1073/pnas.130192197.
45. Gossen M, Bujard H, (1992) Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc Natl Acad Sci USA 89: 5547-5551.
46. Qing K, Mah C, Hansen J, Zhou S, Dwarki V, et al. (1999) Human fibroblast growth factor receptor 1 is a co-receptor for infection by adeno-associated virus 2. Nat Med 5: 71-77 doi:10.1038/4758.
47. Summerford C, Samulski RJ, (1998) Membrane-associated heparan sulfate proteoglycan is a receptor for adeno-associated virus type 2 virions. J Virol 72: 1438-1445.
48. Summerford C, Bartlett JS, Samulski RJ, (1999) AlphaVbeta5 integrin: a co-receptor for adeno-associated virus type 2 infection. Nat Med 5: 78-82 doi:10.1038/4768.
49. Gorman CM, Merlino GT, Willingham MC, Pastan I, Howard BH, (1982) The Rous sarcoma virus long terminal repeat is a strong promoter when introduced into a variety of eukaryotic cells by DNA-mediated transfection. Proc Natl Acad Sci USA 79: 6777-6781.
50. Nathanson JL, Yanagawa Y, Obata K, Callaway EM, (2009) Preferential labeling of inhibitory and excitatory cortical neurons by endogenous tropism of adeno-associated virus and lentivirus vectors. Neuroscience 161: 441-450 doi:10.1016/j.neuroscience.2009.03.032.
51. McCarty DM, Young SM Jr, Samulski RJ, (2004) Integration of adeno-associated virus (AAV) and recombinant AAV vectors. Annu Rev Genet 38: 819-845 doi:10.1146/annurev.genet.37.110801.143717.
52. Cramer KS, Fraser SE, Rubel EW, (2000) Embryonic origins of auditory brain-stem nuclei in the chick hindbrain. Dev Biol 224: 138-151 doi:10.1006/dbio.2000.9779.
53. Seidl AH, Rubel EW, Harris DM, (2010) Mechanisms for adjusting interaural time differences to achieve binaural coincidence detection. J Neurosci 30: 70-80 doi:10.1523/JNEUROSCI.3464-09.2010.
54. Szulc J, Wiznerowicz M, Sauvain M-O, Trono D, Aebischer P, (2006) A versatile tool for conditional gene expression and knockdown. Nat Methods 3: 109-116 doi:10.1038/nmeth846.
55. Lerchner W, Xiao C, Nashmi R, Slimko EM, van Trigt L, et al. (2007) Reversible silencing of neuronal excitability in behaving mice by a genetically targeted, ivermectin-gated Cl- channel. Neuron 54: 35-49 doi:10.1016/j.neuron.2007.02.030.
56. Tye KM, Prakash R, Kim S-Y, Fenno LE, Grosenick L, et al. (2011) Amygdala circuitry mediating reversible and bidirectional control of anxiety. Nature 471: 358-362 doi:10.1038/nature09820.
57. Hikida T, Kimura K, Wada N, Funabiki K, Nakanishi S, (2010) Distinct roles of synaptic transmission in direct and indirect striatal pathways to reward and aversive behavior. Neuron 66: 896-907 doi:10.1016/j.neuron.2010.05.011.
58. Huber D, Gutnisky DA, Peron S, O'Connor DH, Wiegert JS, et al. (2012) Multiple dynamic representations in the motor cortex during sensorimotor learning. Nature 484: 473-478 doi:10.1038/nature11039.
59. Pettmann B, Louis JC, Sensenbrenner M, (1979) Morphological and biochemical maturation of neurones cultured in the absence of glial cells. Nature 281: 378-380.
60. Schlinger BA, Amur-Umarjee S, Shen P, Campagnoni AT, Arnold AP, (1994) Neuronal and non-neuronal aromatase in primary cultures of developing zebra finch telencephalon. J Neurosci 14: 7541-7552.
61. Shaner NC, Campbell RE, Steinbach PA, Giepmans BNG, Palmer AE, et al. (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22: 1567-1572 doi:10.1038/nbt1037.
62. Zolotukhin S, Byrne BJ, Mason E, Zolotukhin I, Potter M, et al. (1999) Recombinant adeno-associated virus purification using novel methods improves infectious titer and yield. Gene Ther 6: 973-985 doi:10.1038/sj.gt.3300938.
63. Lock M, McGorray S, Auricchio A, Ayuso E, Beecham EJ, et al. (2010) Characterization of a recombinant adeno-associated virus type 2 Reference Standard Material. Hum Gene Ther 21: 1273-1285 doi:10.1089/hum.2009.223.
64. Rohr U-P, Wulf M-A, Stahn S, Steidl U, Haas R, et al. (2002) Fast and reliable titration of recombinant adeno-associated virus type-2 using quantitative real-time PCR. J Virol Methods 106: 81-88.
65. Geraerts M, Willems S, Baekelandt V, Debyser Z, Gijsbers R, (2006) Comparison of lentiviral vector titration methods. BMC Biotechnol 6: 34 doi:10.1186/1472-6750-6-34.
66. Sastry L, Johnson T, Hobson MJ, Smucker B, Cornetta K, (2002) Titering lentiviral vectors: comparison of DNA, RNA and marker expression methods. Gene Ther 9: 1155-1162 doi:10.1038/sj.gt.3301731.
67. Tiscornia G, Singer O, Verma IM, (2006) Production and purification of lentiviral vectors. Nat Protoc 1: 241-245 doi:10.1038/nprot.2006.37.
68. Lois C, Hong EJ, Pease S, Brown EJ, Baltimore D, (2002) Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 295: 868-872 doi:10.1126/science.1067081.
69. Schneider CA, Rasband WS, Eliceiri KW, (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671-675 doi:10.1038/nmeth.2089.
70. Hamburger V, Hamilton HL, (1951) A series of normal stages in the development of the chick embryo. J Morphol 88: 49-92 doi:10.1002/jmor.1050880104.
71. Puelles L (2007) The chick brain in stereotaxic coordinates. 1st ed. Waltham, MA, USA: Academic Pr. pp.