A versatile system for the neuronal subtype specific expression of lentiviral vectors

FASEB Journal

Volumn 24, Issue 3, 2010, Pages 723-730

  Tolu, Stefania ^a   Avale, M Elena ^a,f   Nakatani, Hiroko ^a,d   Pons, Stéphanie ^a   Parnaudeau, Sébastien ^b,g   Tronche, François ^b   Vogt, Angelika ^c   Monyer, Hannah ^c   Vogel, Roland ^d,e   De Chaumont, Fabrice ^b   Olivo Marin, Jean Christophe ^b   Changeux, Jean Pierre ^a   Maskos, Uwe ^a  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

^c Interdisciplinary Center for Neuroscience   (Germany)

^d PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^e SORBONNE UNIVERSITÉ   (France)

^f KING'S COLLEGE LONDON   (United Kingdom)

^g NewYork Presbyterian Hospital   (United States)

Author keywords

Cell type specific reexpression; Cre loxP recombination system; eGFP; Stereotactic injection; Ventral tegmental area; VTA

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; CRE RECOMBINASE; ENHANCED GREEN FLUORESCENT PROTEIN; GLUTAMATE DECARBOXYLASE 67; LENTIVIRUS VECTOR; PLATELET DERIVED GROWTH FACTOR; 4 AMINOBUTYRIC ACID; DOPAMINE; GREEN FLUORESCENT PROTEIN; INTEGRASE;

ANIMAL CELL; ARTICLE; CELL COUNT; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; EXPRESSION VECTOR; IMAGE ANALYSIS; IMMUNOHISTOCHEMISTRY; INTERNEURON; LOXP SITE; MOUSE; NERVE CELL CULTURE; NONHUMAN; PRIORITY JOURNAL; REPORTER GENE; TRANSGENE; TRANSGENIC MOUSE; VENTRAL TEGMENTUM; VIRAL GENE DELIVERY SYSTEM; ANIMAL; BIOLOGICAL MODEL; CELL CULTURE; CYTOLOGY; FLUORESCENCE MICROSCOPY; GENE VECTOR; GENETICS; HIPPOCAMPUS; LENTIVIRINAE; METABOLISM; NERVE CELL;

MAMMALIA; MUS MUSCULUS;

ANIMALS; CELLS, CULTURED; DOPAMINE; GAMMA-AMINOBUTYRIC ACID; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; INTEGRASES; LENTIVIRUS; MICE; MICROSCOPY, FLUORESCENCE; MODELS, GENETIC; NEURONS; VENTRAL TEGMENTAL AREA;

EID: 77952303358     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-139790     Document Type: Article

References (45)

1. Naldini, L., Blomer, U., Gallay, P., Ory, D., Mulligan, R., Gage, F. H., Verma, I. M., and Trono, D. (1996) In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272, 263-267 (Pubitemid 26119138)
2. Zufferey, R., Dull, T., Mandel, R. J., Bukovsky, A., Quiroz, D., Naldini, L., and Trono, D. (1998) Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J. Virol. 72, 9873-9880 (Pubitemid 28520853)
3. Galimi, F., and Verma, I. M. (2002) Opportunities for the use of lentiviral vectors in human gene therapy. Curr. Top. Microbiol. Immunol. 261, 245-254 (Pubitemid 34259347)
4. Ikawa, M., Tanaka, N., Kao, W. W., and Verma, I. M. (2003) Generation of transgenic mice using lentiviral vectors: a novel preclinical assessment of lentiviral vectors for gene therapy. Mol. Ther. 8, 666-673 (Pubitemid 37321696)
5. Wong, L. F., Goodhead, L., Prat, C., Mitrophanous, K. A., Kingsman, S. M., and Mazarakis, N. D. (2006) Lentivirus-mediated gene transfer to the central nervous system: therapeutic and research applications. Hum. Gene Ther. 17, 1-9 (Pubitemid 43102718)
6. Jakobsson, J., Ericson, C., Jansson, M., Bjork, E., and Lundberg, C. (2003) Targeted transgene expression in rat brain using lentiviral vectors. J. Neurosci. Res. 73, 876-885 (Pubitemid 37071743)
7. Kafri, T., van Praag, H., Ouyang, L., Gage, F. H., and Verma, I. M. (1999) A packaging cell line for lentivirus vectors. J. Virol. 73, 576-584 (Pubitemid 28565401)
8. Blomer, U., Naldini, L., Kafri, T., Trono, D., Verma, I. M., and Gage, F. H. (1997) Highly efficient and sustained gene transfer in adult neurons with a lentivirus vector. J. Virol. 71, 6641-6649 (Pubitemid 27355322)
9. Verma, I. M., and Weitzman, M. D. (2005) Gene therapy: twenty-first century medicine. Annu. Rev. Biochem. 74, 711-738
10. Nair-Roberts, R. G., Chatelain-Badie, S. D., Benson, E., White-Cooper, H., Bolam, J. P., and Ungless, M. A. (2008) Stereological estimates of dopaminergic, GABAergic and glutamatergic neurons in the ventral tegmental area, substantia nigra and retrorubral field in the rat. Neuroscience 152, 1024-1031
11. Oades, R. D., and Halliday, G. M. (1987) Ventral tegmental (A10) system: neurobiology. 1. Anatomy and connectivity. Brain Res. 434, 117-165
12. Swanson, L. W. (1982) The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res. Bull. 9, 321-353
13. Sternberg, N., and Hamilton, D. (1981) Bacteriophage P1 site-specific recombination. I. Recombination between loxP sites. J. Mol. Biol. 150, 467-486
14. Naldini, L., Blomer, U., Gage, F. H., Trono, D., and Verma, I. M. (1996) Efficient transfer, integration, and sustained long-term expression of the transgene in adult rat brains injected with a lentiviral vector. Proc. Natl. Acad. Sci. U. S. A. 93, 11382-11388 (Pubitemid 26347130)
15. Sirven, A., Ravet, E., Charneau, P., Zennou, V., Coulombel, L., Guetard, D., Pflumio, F., and Dubart-Kupperschmitt, A. (2001) Enhanced transgene expression in cord blood CD34(+)-derived hematopoietic cells, including developing T cells and NOD/SCID mouse repopulating cells, following transduction with modified trip lentiviral vectors. Mol. Ther. 3, 438-448 (Pubitemid 32509837)
16. Charneau, P., Alizon, M., and Clavel, F. (1992) A second origin of DNA plus-strand synthesis is required for optimal human immunodeficiency virus replication. J. Virol. 66, 2814-2820
17. Charneau, P., Mirambeau, G., Roux, P., Paulous, S., Buc, H., and Clavel, F. (1994) HIV-1 reverse transcription: a termination step at the center of the genome. J. Mol. Biol. 241, 651-662 (Pubitemid 24277435)
18. Zennou, V., Petit, C., Guetard, D., Nerhbass, U., Montagnier, L., and Charneau, P. (2000) HIV-1 genome nuclear import is mediated by a central DNA flap. Cell 101, 173-185 (Pubitemid 32004745)
19. Zufferey, R., Donello, J. E., Trono, D., and Hope, T. J. (1999) Woodchuck hepatitis virus posttranscriptional regulatory element enhances expression of transgenes delivered by retroviral vectors. J. Virol. 73, 2886-2892
20. Shaner, N. C., Campbell, R. E., Steinbach, P. A., Giepmans, B. N., Palmer, A. E., and Tsien, R. Y. (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 22, 1567-1572
21. Maskos, U., Molles, B. E., Pons, S., Besson, M., Guiard, B. P., Guilloux, J. P., Evrard, A., Cazala, P., Cormier, A., Mameli-Engvall, M., Dufour, N., Cloez-Tayarani, I., Bemelmans, A. P., Mallet, J., Gardier, A. M., David, V., Faure, P., Granon, S., and Changeux, J. P. (2005) Nicotine reinforcement and cognition restored by targeted expression of nicotinic receptors. Nature 436, 103-107
22. Goslin, K., and Banker, G. (1989) Experimental observations on the development of polarity by hippocampal neurons in culture. J. Cell Biol. 108, 1507-1516
23. Fuchs, E. C., Doheny, H., Faulkner, H., Caputi, A., Traub, R. D., Bibbig, A., Kopell, N., Whittington, M. A., and Monyer, H. (2001) Genetically altered AMPA-type glutamate receptor kinetics in interneurons disrupt long-range synchrony of gamma oscillation. Proc. Natl. Acad. Sci. U. S. A. 98, 3571-3576
24. Turiault, M., Parnaudeau, S., Milet, A., Parlato, R., Rouzeau, J. D., Lazar, M., and Tronche, F. (2007) Analysis of dopamine transporter gene expression pattern-generation of DAT-iCre transgenic mice. FEBS J. 274, 3568-3577
25. Cunningham, M. G., and McKay, R. D. (1993) A hypothermic miniaturized stereotaxic instrument for surgery in newborn rats. J. Neurosci. Methods 47, 105-114
26. Paxinos, G., and Franklin, K. (2001) The Mouse Brain in Stereotaxic Coordinates, Academic Press, San Diego, CA, USA
27. Kellendonk, C., Tronche, F., Casanova, E., Anlag, K., Opherk, C., and Schutz, G. (1999) Inducible site-specific recombination in the brain. J. Mol. Biol. 285, 175-182
28. Olivo-Marin, J.-C. (2002) Extraction of spots in biological images using multiscale products. Pattern Recognit. 35, 1989-1996
29. Deglon, N., Tseng, J. L., Bensadoun, J. C., Zurn, A. D., Arsenijevic, Y., Pereira de Almeida, L., Zufferey, R., Trono, D., and Aebischer, P. (2000) Self-inactivating lentiviral vectors with enhanced transgene expression as potential gene transfer system in Parkinson's disease. Hum. Gene Ther. 11, 179-190
30. Mitrophanous, K., Yoon, S., Rohll, J., Patil, D., Wilkes, F., Kim, V., Kingsman, S., Kingsman, A., and Mazarakis, N. (1999) Stable gene transfer to the nervous system using a non-primate lentiviral vector. Gene Ther. 6, 1808-1818
31. Baekelandt, V., Claeys, A., Eggermont, K., Lauwers, E., De Strooper, B., Nuttin, B., and Debyser, Z. (2002) Characterization of lentiviral vector-mediated gene transfer in adult mouse brain. Hum. Gene Ther. 13, 841-853
32. Dittgen, T., Nimmerjahn, A., Komai, S., Licznerski, P., Waters, J., Margrie, T. W., Helmchen, F., Denk, W., Brecht, M., and Osten, P. (2004) Lentivirus-based genetic manipulations of cortical neurons and their optical and electrophysiological monitoring in vivo. Proc. Natl. Acad. Sci. U. S. A. 101, 18206-18211
33. Carlsson, A. (1993) Thirty years of dopamine research. Adv. Neurol. 60, 1-10
34. Everitt, B. J., and Robbins, T. W. (2005) Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat. Neurosci. 8, 1481-1489
35. Goldman-Rakic, P. S. (1998) The cortical dopamine system: role in memory and cognition. Adv. Pharmacol. 42, 707-711
36. Kuhn, R., Schwenk, F., Aguet, M., and Rajewsky, K. (1995) Inducible gene targeting in mice. Science 269, 1427-1429
37. Lakso, M., Sauer, B., Mosinger, B., Jr., Lee, E. J., Manning, R. W., Yu, S. H., Mulder, K. L., and Westphal, H. (1992) Targeted oncogene activation by site-specific recombination in transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 89, 6232-6236
38. Orban, P. C., Chui, D., and Marth, J. D. (1992) Tissue- and site-specific DNA recombination in transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 89, 6861-6865
39. Sauer, B., and Henderson, N. (1988) Site-specific DNA recombination in mammalian cells by the Cre recombinase of bacteriophage P1. Proc. Natl. Acad. Sci. U. S. A. 85, 5166-5170
40. Kaczmarczyk, S. J., and Green, J. E. (2001) A single vector containing modified cre recombinase and LOX recombination sequences for inducible tissue-specific amplification of gene expression. Nucleic Acids Res. 29, E56-E56
41. Lobe, C. G., Koop, K. E., Kreppner, W., Lomeli, H., Gertsenstein, M., and Nagy, A. (1999) Z/AP, a double reporter for cre-mediated recombination. Dev. Biol. 208, 281-292
42. Jakobsson, J., and Lundberg, C. (2006) Lentiviral vectors for use in the central nervous system. Mol. Ther. 13, 484-493
43. Watson, D. J., Kobinger, G. P., Passini, M. A., Wilson, J. M., and Wolfe, J. H. (2002) Targeted transduction patterns in the mouse brain by lentivirus vectors pseudotyped with VSV, Ebola, Mokola, LCMV, or MuLV envelope proteins. Mol. Ther. 5, 528-537
44. Wong, L. F., Azzouz, M., Walmsley, L. E., Askham, Z., Wilkes, F. J., Mitrophanous, K. A., Kingsman, S. M., and Mazarakis, N. D. (2004) Transduction patterns of pseudotyped lentiviral vectors in the nervous system. Mol. Ther. 9, 101-111
45. Colin, A., Faideau, M., Dufour, N., Auregan, G., Hassig, R., Andrieu, T., Brouillet, E., Hantraye, P., Bonvento, G., and Deglon, N. (2009) Engineered lentiviral vector targeting astrocytes in vivo. Glia 57, 667-679