pUNISHER: A high-level expression cassette for use with recombinant viral vectors for rapid and long term in vivo neuronal expression in the CNS

Journal of Neurophysiology

Volumn 106, Issue 6, 2011, Pages 3230-3244

  Montesinos, Monica S ^a   Chen, Zuxin ^a,b   Young Jr , Samuel M ^a  

^a MAX PLANCK FLORIDA INSTITUTE FOR NEUROSCIENCE   (United States)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Adenovirus; Calyx of held; In vivo transduction; Viral vectors

Indexed keywords

ADENOVIRUS VECTOR; CALCIUM ION; GREEN FLUORESCENT PROTEIN; MAGNESIUM ION; SYNAPSIN;

3' UNTRANSLATED REGION; ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN STEM; CALCIUM CURRENT; CELL SPECIFICITY; CELL STRAIN; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DEPOLARIZATION; GENE CASSETTE; GENE DOSAGE; GENE EXPRESSION; GENETIC TRANSDUCTION; HELD SYNAPSE; HIPPOCAMPUS; IN VITRO STUDY; IN VIVO STUDY; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROMOTER REGION; PUNISHER CASSETTE; RAT; SYNAPSE; SYNAPTIC TRANSMISSION; TRANSGENE; VIRAL GENE DELIVERY SYSTEM;

ADENOVIRIDAE; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; CELL LINE, TRANSFORMED; CENTRAL NERVOUS SYSTEM; CYTOMEGALOVIRUS; EXCITATORY POSTSYNAPTIC POTENTIALS; GENE EXPRESSION REGULATION; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; HUMANS; MEMBRANE POTENTIALS; MICE; NEURONS; PATCH-CLAMP TECHNIQUES; PHOSPHOPYRUVATE HYDRATASE; PROMOTER REGIONS, GENETIC; RATS; RATS, WISTAR; REGULATORY SEQUENCES, NUCLEIC ACID; RNA PROCESSING, POST-TRANSCRIPTIONAL; SHAW POTASSIUM CHANNELS; SYNAPSES; SYNAPSINS; SYNAPTIC TRANSMISSION; TIME FACTORS; TRANSFECTION;

EID: 83055165915     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00713.2011     Document Type: Article

References (82)

1. Aronov S, Marx R, Ginzburg I. Identification of 3=UTR region implicated in tau mRNA stabilization in neuronal cells. J Mol Neurosci 12: 131-145, 1999.
2. Borst JG, Helmchen F, Sakmann B. Pre-and postsynaptic whole-cell recordings in the medial nucleus of the trapezoid body of the rat. J Physiol 489: 825-840, 1995.
3. Brun S, Faucon-Biguet N, Mallet J. Optimization of transgene expression at the posttranscriptional level in neural cells: implications for gene therapy. Mol Ther 7: 782-789, 2003.
4. Chillon M, Bosch A, Zabner J, Law L, Armentano D, Welsh MJ, Davidson BL. Group D adenoviruses infect primary central nervous system cells more efficiently than those from group C. J Virol 73: 2537-2540, 1999.
5. Cockrell AS, Kafri T. Gene delivery by lentivirus vectors. Mol Biotechnol 36: 184-204, 2007.
6. Croyle MA, Roessler BJ, Davidson BL, Hilfinger JM, Amidon GL. Factors that influence stability of recombinant adenoviral preparations for human gene therapy. Pharm Dev Technol 3: 373-383, 1998.
7. Daly C, Ziff EB. Post-transcriptional regulation of synaptic vesicle protein expression and the developmental control of synaptic vesicle formation. J Neurosci 17: 2365-2375, 1997.
8. Danthinne X, Imperiale MJ. Production of first generation adenovirus vectors: a review. Gene Ther 7: 1707-1714, 2000.
9. Davidson BL, Allen ED, Kozarsky KF, Wilson JM, Roessler BJ. A model system for in vivo gene transfer into the central nervous system using an adenoviral vector. Nat Genet 3: 219-223, 1993.
10. Donello JE, Loeb JE, Hope TJ. Woodchuck hepatitis virus contains a tripartite posttranscriptional regulatory element. J Virol 72: 5085-5092, 1998.
11. Duale H, Kasparov S, Paton JF, Teschemacher AG. Differences in transductional tropism of adenoviral and lentiviral vectors in the rat brainstem. Exp Physiol 90: 71-78, 2005.
12. Dusonchet J, Kochubey O, Stafa K, Young SM Jr, Zufferey R, Moore DJ, Schneider BL, Aebischer P. A rat model of progressive nigral neurodegeneration induced by the Parkinson's disease-associated G2019S mutation in LRRK2. J Neurosci 31: 907-912, 2011.
13. Ferrari FK, Samulski T, Shenk T, Samulski RJ. Second-strand synthesis is a rate-limiting step for efficient transduction by recombinant adeno-associated virus vectors. J Virol 70: 3227-3234, 1996.
14. Forsythe ID. Direct patch recording from identified presynaptic terminals mediating glutamatergic EPSCs in the rat CNS, in vitro. J Physiol 479: 381-387, 1994.
15. Gan L, Hahn SJ, Kaczmarek LK. Cell type-specific expression of the Kv3.1 gene is mediated by a negative element in the 5= untranslated region of the Kv31 promoter. J Neurochem 73: 1350-1362, 1999.
16. Gan L, Perney TM, Kaczmarek LK. Cloning and characterization of the promoter for a potassium channel expressed in high frequency firing neurons. J Biol Chem 271: 5859-5865, 1996.
17. Gascon S, Paez-Gomez JA, Diaz-Guerra M, Scheiffele P, Scholl FG. Dual-promoter lentiviral vectors for constitutive and regulated gene expression in neurons. J Neurosci Methods 168: 104-112, 2008.
18. Gerdes CA, Castro MG, Lowenstein PR. Strong promoters are the key to highly efficient, noninflammatory and noncytotoxic adenoviral-mediated transgene delivery into the brain in vivo. Mol Ther 2: 330-338, 2000.
19. Ghadge GD, Roos RP, Kang UJ, Wollmann R, Fishman PS, Kalynych AM, Barr E, Leiden JM. CNS gene delivery by retrograde transport of recombinant replication-defective adenoviruses. Gene Ther 2: 132-137, 1995.
20. Glover CP, Bienemann AS, Heywood DJ, Cosgrave AS, Uney JB. Adenoviral-mediated, high-level, cell-specific transgene expression: a SYN1-WPRE cassette mediates increased transgene expression with no loss of neuron specificity. Mol Ther 5: 509-516, 2002.
21. Goodwin EC, Rottman FM. The 3=-flanking sequence of the bovine growth hormone gene contains novel elements required for efficient and accurate polyadenylation. J Biol Chem 267: 16330-16334, 1992.
22. Gray SJ, Foti SB, Schwartz JW, Bachaboina L, Taylor-Blake B, Coleman J, Ehlers MD, Zylka MJ, McCown TJ, Samulski RJ. Optimizing promoters for recombinant adeno-associated virus-mediated gene expression in the peripheral and central nervous system using self-complementary vectors. Hum Gene Ther 22: 1143-1153, 2011.
23. Grieger JC, Samulski RJ. Adeno-associated virus as a gene therapy vector: vector development, production and clinical applications. Adv Biochem Eng Biotechnol 99: 119-145, 2005.
24. Hanganu-Opatz IL. Between molecules and experience: role of early patterns of coordinated activity for the development of cortical maps and sensory abilities. Brain Res Rev 64: 160-176, 2010.
25. Hermening S, Kugler S, Bahr M, Isenmann S. Improved high-capacity adenoviral vectors for high-level neuron-restricted gene transfer to the CNS. J Virol Methods 136: 30-37, 2006.
26. Hioki H, Kameda H, Nakamura H, Okunomiya T, Ohira K, Nakamura K, Kuroda M, Furuta T, Kaneko T. Efficient gene transduction of neurons by lentivirus with enhanced neuron-specific promoters. Gene Ther 14: 872-882, 2007.
27. Kissa K, Mordelet E, Soudais C, Kremer EJ, Demeneix BA, Brulet P, Coen L. In vivo neuronal tracing with GFP-TTC gene delivery. Mol Cell Neurosci 20: 627-637, 2002.
28. Klein RL, Hamby ME, Gong Y, Hirko AC, Wang S, Hughes JA, King MA, Meyer EM. Dose and promoter effects of adeno-associated viral vector for green fluorescent protein expression in the rat brain. Exp Neurol 176: 66-74, 2002.
29. Klein RL, Meyer EM, Peel AL, Zolotukhin S, Meyers C, Muzyczka N, King MA. Neuron-specific transduction in the rat septohippocampal or nigrostriatal pathway by recombinant adeno-associated virus vectors. Exp Neurol 150: 183-194, 1998.
30. Kopp-Scheinpflug C, Tong J, Steinert Young JR, Robinson SW, Forsythe ID. Kv2.2 currents decline rapidly after deprivation of afferent activity. Program No. 446.10. 2010 Neuroscience Meeting Planner. San Diego, CA: Society for Neuroscience, 2010. Online.
31. Kraner SD, Chong JA, Tsay HJ, Mandel G. Silencing the type II sodium channel gene: a model for neural-specific gene regulation. Neuron 9: 37-44, 1992.
32. Kremer EJ, Boutin S, Chillon M, Danos O. Canine adenovirus vectors: an alternative for adenovirus-mediated gene transfer. J Virol 74: 505-512, 2000.
33. Kugler S, Kilic E, Bahr M. Human synapsin 1 gene promoter confers highly neuron-specific long-term transgene expression from an adenoviral vector in the adult rat brain depending on the transduced area. Gene Ther 10: 337-347, 2003a.
34. Kugler S, Lingor P, Scholl U, Zolotukhin S, Bahr M. Differential transgene expression in brain cells in vivo and in vitro from AAV-2 vectors with small transcriptional control units. Virology 311: 89-95, 2003b.
35. Kugler S, Meyn L, Holzmuller H, Gerhardt E, Isenmann S, Schulz JB, Bahr M. Neuron-specific expression of therapeutic proteins: evaluation of different cellular promoters in recombinant adenoviral vectors. Mol Cell Neurosci 17: 78-96, 2001.
36. Kuo H, Ingram DK, Crystal RG, Mastrangeli A. Retrograde transfer of replication deficient recombinant adenovirus vector in the central nervous system for tracing studies. Brain Res 705: 31-38, 1995.
37. Kuroda H, Kutner RH, Bazan NG, Reiser J. A comparative analysis of constitutive and cell-specific promoters in the adult mouse hippocampus using lentivirus vector-mediated gene transfer. J Gene Med 10: 1163-1175, 2008.
38. Le Hir H, Nott A, Moore MJ. How introns influence and enhance eukaryotic gene expression. Trends Biochem Sci 28: 215-220, 2003.
39. Lin JY. A user's guide to channelrhodopsin variants: features, limitations and future developments. Exp Physiol 96: 19-25, 2011.
40. Liu BH, Wang X, Ma YX, Wang S. CMV enhancer/human PDGF-beta promoter for neuron-specific transgene expression. Gene Ther 11: 52-60, 2004.
41. Liu BH, Yang Y, Paton JF, Li F, Boulaire J, Kasparov S, Wang S. GAL4-NF-kappaB fusion protein augments transgene expression from neuronal promoters in the rat brain. Mol Ther 14: 872-882, 2006.
42. Loeb JE, Cordier WS, Harris ME, Weitzman MD, Hope TJ. Enhanced expression of transgenes from adeno-associated virus vectors with the woodchuck hepatitis virus posttranscriptional regulatory element: implications for gene therapy. Hum Gene Ther 10: 2295-2305, 1999.
43. Lowenstein PR, Castro MG. Inflammation and adaptive immune responses to adenoviral vectors injected into the brain: peculiarities, mechanisms, and consequences. Gene Ther 10: 946-954, 2003.
44. Lowenstein PR, Mandel RJ, Xiong WD, Kroeger K, Castro MG. Immune responses to adenovirus and adeno-associated vectors used for gene therapy of brain diseases: the role of immunological synapses in understanding the cell biology of neuroimmune interactions. Curr Gene Ther 7: 347-360, 2007.
45. Marconi P, Manservigi R, Epstein AL. HSV-1-derived helper-independent defective vectors, replicating vectors and amplicon vectors, for the treatment of brain diseases. Curr Opin Drug Discov Devel 13: 169-183, 2010.
46. Maskos U, Kissa K, St Cloment C, Brulet P. Retrograde trans-synaptic transfer of green fluorescent protein allows the genetic mapping of neuronalcircuits in transgenic mice. Proc Natl Acad Sci USA 99: 10120-10125, 2002.
47. McCarty DM, Monahan PE, Samulski RJ. Self-complementary recombinant adeno-associated virus (scAAV) vectors promote efficient transduction independently of DNA synthesis. Gene Ther 8: 1248-1254, 2001.
48. McCown TJ, Xiao X, Li J, Breese GR, Samulski RJ. Differential and persistent expression patterns of CNS gene transfer by an adeno-associated virus (AAV) vector. Brain Res 713: 99-107, 1996.
49. Mori N, Schoenherr C, Vandenbergh DJ, Anderson DJ. A common silencer element in the SCG10 and type II Na_ channel genes binds a factor present in nonneuronal cells but not in neuronal cells. Neuron 9: 45-54, 1992.
50. Muzyczka N. Use of adeno-associated virus as a general transduction vector for mammalian cells. Curr Top Microbiol Immunol 158: 97-129, 1992.
51. Ng P, Graham FL. Construction of first-generation adenoviral vectors. Methods Mol Med 69: 389-414, 2002.
52. Niwa H, Yamamura K, Miyazaki J. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108: 193-199, 1991.
53. Nott A, Meislin SH, Moore MJ. A quantitative analysis of intron effects on mammalian gene expression. RNA 9: 607-617, 2003.
54. Oral HB, Larkin DF, Fehervari Z, Byrnes AP, Rankin AM, Haskard DO, Wood MJ, Dallman MJ, George AJ. Ex vivo adenovirus-mediated gene transfer and immunomodulatory protein production in human cornea. Gene Ther 4: 639-647, 1997.
55. Palmer DJ, Ng P. Helper-dependent adenoviral vectors for gene therapy. Hum Gene Ther 16: 1-16, 2005.
56. Peel AL, Zolotukhin S, Schrimsher GW, Muzyczka N, Reier PJ. Efficient transduction of green fluorescent protein in spinal cord neurons using adeno-associated virus vectors containing cell type-specific promoters. Gene Ther 4: 16-24, 1997.
57. Peltekian E, Garcia L, Danos O. Neurotropism and retrograde axonal transport of a canine adenoviral vector: a tool for targeting key structures undergoing neurodegenerative processes. Mol Ther 5: 25-32, 2002.
58. Rogers JT, Leiter LM, McPhee J, Cahill CM, Zhan SS, Potter H, Nilsson LN. Translation of the Alzheimer amyloid precursor protein mRNA is up-regulated by interleukin-1 through 5=-untranslated region sequences. J Biol Chem 274: 6421-6431, 1999.
59. Sakaba T, Neher E. Calmodulin mediates rapid recruitment of fast-releasing synaptic vesicles at a calyx-type synapse. Neuron 32: 1119-1131, 2001a.
60. Sakaba T, Neher E. Quantitative relationship between transmitter release and calcium current at the calyx of held synapse. J Neurosci 21: 462-476, 2001b.
61. Schneggenburger R, Forsythe ID. The calyx of Held. Cell Tissue Res 326: 311-337, 2006.
62. Schneggenburger R, Meyer AC, Neher E. Released fraction and total size of a pool of immediately available transmitter quanta at a calyx synapse. Neuron 23: 399-409, 1999.
63. Schneider H, Groves M, Muhle C, Reynolds PN, Knight A, Themis M, Carvajal J, Scaravilli F, Curiel DT, Fairweather NF, Coutelle C. Retargeting of adenoviral vectors to neurons using the Hc fragment of tetanus toxin. Gene Ther 7: 1584-1592, 2000.
64. Scott BB, Lois C. Generation of tissue-specific transgenic birds with lentiviral vectors. Proc Natl Acad Sci USA 102: 16443-16447, 2005.
65. Shaw G, Morse S, Ararat M, Graham FL. Preferential transformation of human neuronal cells by human adenoviruses and the origin of HEK 293 cells. FASEB J 16: 869-871, 2002.
66. Smith RL, Traul DL, Schaack J, Clayton GH, Staley KJ, Wilcox CL. Characterization of promoter function and cell-type-specific expression from viral vectors in the nervous system. J Virol 74: 11254-11261, 2000.
67. Stilwell JL, McCarty DM, Negishi A, Superfine R, Samulski RJ. Development and characterization of novel empty adenovirus capsids and their impact on cellular gene expression. J Virol 77: 12881-12885, 2003.
68. Stilwell JL, Samulski RJ. Role of viral vectors and virion shells in cellular gene expression. Mol Ther 9: 337-346, 2004.
69. Thiel G, Greengard P, Sudhof TC. Characterization of tissue-specific transcription by the human synapsin I gene promoter. Proc Natl Acad Sci USA 88: 3431-3435, 1991.
70. Thomas CE, Birkett D, Anozie I, Castro MG, Lowenstein PR. Acute direct adenoviral vector cytotoxicity and chronic, but not acute, inflammatory responses correlate with decreased vector-mediated transgene expression in the brain. Mol Ther 3: 36-46, 2001.
71. Thomas CE, Schiedner G, Kochanek S, Castro MG, Lowenstein PR. Peripheral infection with adenovirus causes unexpected long-term brain inflammation in animals injected intracranially with first-generation, but not with high-capacity, adenovirus vectors: toward realistic long-term neurological gene therapy for chronic diseases. Proc Natl Acad Sci USA 97: 7482-7487, 2000.
72. Wimmer VC, Horstmann H, Groh A, Kuner T. Donut-like topology of synaptic vesicles with a central cluster of mitochondria wrapped into membrane protrusions: a novel structure-function module of the adult calyx of Held. J Neurosci 26: 109-116, 2006.
73. Wimmer VC, Nevian T, Kuner T. Targeted in vivo expression of proteins in the calyx of Held. Pflügers Arch 449: 319-333, 2004.
74. Wu Z, Asokan A, Samulski RJ. Adeno-associated virus serotypes: vector toolkit for human gene therapy. Mol Ther 14: 316-327, 2006.
75. Wu Z, Sun J, Zhang T, Yin C, Yin F, Van Dyke T, Samulski RJ, Monahan PE. Optimization of self-complementary AAV vectors for liver-directed expression results in sustained correction of hemophilia B at low vector dose. Mol Ther 16: 280-289, 2008.
76. Xu ZL, Mizuguchi H, Ishii-Watabe A, Uchida E, Mayumi T, Hayakawa T. Optimization of transcriptional regulatory elements for constructing plasmid vectors. Gene 272: 149-156, 2001.
77. Xu ZL, Mizuguchi H, Ishii-Watabe A, Uchida E, Mayumi T, Hayakawa T. Strength evaluation of transcriptional regulatory elements for transgene expression by adenovirus vector. J Control Release 81: 155-163, 2002.
78. Yoshihara Y, Mizuno T, Nakahira M, Kawasaki M, Watanabe Y, Kagamiyama H, Jishage K, Ueda O, Suzuki H, Tabuchi K, Sawamoto K, Okano H, Noda T, Mori K. A genetic approach to visualization of multisynaptic neural pathways using plant lectin transgene. Neuron 22: 33-41, 1999.
79. Young SM Jr. Proteolysis of SNARE proteins alters facilitation and depression in a specific way. Proc Natl Acad Sci USA 102: 2614-2619, 2005.
80. Young SM Jr, Neher E. Synaptotagmin has an essential function in synaptic vesicle positioning for synchronous release in addition to its role as a calcium sensor. Neuron 63: 482-496, 2009.
81. Zhou H, Beaudet AL. A new vector system with inducible E2a cell line for production of higher titer and safer adenoviral vectors. Virology 275: 348-357, 2000.
82. Zhou H, O'Neal W, Morral N, Beaudet AL. Development of a complementing cell line and a system for construction of adenovirus vectors with E1 and E2a deleted. J Virol 70: 7030-7038, 1996.