Optical control of retrogradely infected neurons using drug-regulated "TLoop" lentiviral vectors

Journal of Neurophysiology

Volumn 111, Issue 10, 2014, Pages 2150-2159

  Cetin, Ali ^a   Callaway, Edward M ^a,b  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Channelrhodopsin(H134R); Equine infectious anemia virus; Rabies glycoprotein; tTA

Indexed keywords

DOXYCYCLINE; LENTIVIRUS VECTOR; RABIES GLYCOPROTEIN; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN; BACTERIAL PROTEIN; CHANNELRHODOPSIN 2, MOUSE; GLYCOPROTEIN; PEPTIDE FRAGMENT; PHOTOPROTEIN; PROTEIN SYNTHESIS INHIBITOR; RABIES VIRUS GLYCOPROTEIN PEPTIDE; RHODOPSIN; TETRACYCLINE; VIRUS PROTEIN; YELLOW FLUORESCENT PROTEIN, BACTERIA;

ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN FUNCTION; BRAIN INFECTION; DNA SEQUENCE; EQUINE INFECTIOUS ANEMIA VIRUS; GENE EXPRESSION; HOST; INTRACELLULAR RECORDING; LONG TERM CARE; MOUSE; NERVE CELL; NERVE ENDING; NONHUMAN; OPTOGENETICS; PLASMID; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PSEUDOTYPING; RETINA GANGLION CELL; RETROGRADE INFECTION; SECONDARY SOMATOSENSORY CORTEX; SOMATOSENSORY CORTEX; SUPERIOR COLLICULUS; TRANSGENIC MOUSE; VIRAL GENE DELIVERY SYSTEM; WHOLE CELL PATCH CLAMP; ANIMAL; BRAIN; C57BL MOUSE; DRUG EFFECTS; FEEDBACK SYSTEM; GENE VECTOR; GENETICS; LENTIVIRINAE; METABOLISM; MICROELECTRODE; NERVE FIBER; PHYSIOLOGY; PROCEDURES; TISSUE CULTURE TECHNIQUE; TRANSCRIPTION INITIATION; VIROLOGY;

ANIMALS; AXONS; BACTERIAL PROTEINS; BRAIN; DOXYCYCLINE; FEEDBACK, PHYSIOLOGICAL; GENE EXPRESSION; GENETIC VECTORS; GLYCOPROTEINS; LENTIVIRUS; LUMINESCENT PROTEINS; MICE, INBRED C57BL; MICROELECTRODES; NEURONS; OPTOGENETICS; PEPTIDE FRAGMENTS; PROTEIN SYNTHESIS INHIBITORS; RHODOPSIN; TETRACYCLINE; TISSUE CULTURE TECHNIQUES; TRANSCRIPTIONAL ACTIVATION; VIRAL PROTEINS;

EID: 84900809338     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00495.2013     Document Type: Article

References (47)

1. Apicella AJ, Wickersham IR, Seung HS, Shepherd GM. Laminarly orthogonal excitation of fast-spiking and low-threshold-spiking interneurons in mouse motor cortex. J Neurosci 32: 7021-7033, 2012.
2. Aronoff R, Matyas F, Mateo C, Ciron C, Schneider B, Petersen CC. Long-range connectivity of mouse primary somatosensory barrel cortex. Eur J Neurosci 31: 2221-2233, 2010.
3. Atasoy D, Aponte Y, Su HH, Sternson SM. A FLEX switch targets Channelrhodopsin-2 to multiple cell types for imaging and long-range circuit mapping. J Neurosci 28: 7025-7030, 2008.
4. Azzouz M, Ralph GS, Storkebaum E, Walmsley LE, Mitrophanous KA, Kingsman SM, Carmeliet P, Mazarakis ND. VEGF delivery with retrogradely transported lentivector prolongs survival in a mouse ALS model. Nature 429: 413-417, 2004.
5. Baron U, Gossen M, Bujard H. Tetracycline-controlled transcription in eukaryotes: novel transactivators with graded transactivation potential. Nucleic Acids Res 25: 2723-2729, 1997.
6. Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K. Millisecondtimescale, genetically targeted optical control of neural activity. Nat Neurosci 8: 1263-1268, 2005.
7. Burger C, Gorbatyuk OS, Velardo MJ, Peden CS, Williams P, Zolotukhin S, Reier PJ, Mandel RJ, Muzyczka N. Recombinant AAV viral vectors pseudotyped with viral capsids from serotypes 1, 2, and 5 display differential efficiency and cell tropism after delivery to different regions of the central nervous system. Mol Ther 10: 302-317, 2004.
8. Cardin JA, Carlen M, Meletis K, Knoblich U, Zhang F, Deisseroth K, Tsai LH, Moore CI. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459: 663-667, 2009.
9. Cetin A, Komai S, Eliava M, Seeburg PH, Osten P. Stereotaxic gene delivery in the rodent brain. Nat Protoc 1: 3166-3173, 2006.
10. Chaudhury D, Walsh JJ, Friedman AK, Juarez B, Ku SM, Koo JW, Ferguson D, Tsai HC, Pomeranz L, Christoffel DJ, Nectow AR, Ekstrand M, Domingos A, Mazei-Robison MS, Mouzon E, Lobo MK, Neve RL, Friedman JM, Russo SJ, Deisseroth K, Nestler EJ, Han MH. Rapid regulation of depression-related behaviours by control of midbrain dopamine neurons. Nature 493: 532-536, 2013.
11. Chen JL, Carta S, Soldado-Magraner J, Schneider BL, Helmchen F. Behaviour-dependent recruitment of long-range projection neurons in somatosensory cortex. Nature 499: 336-340, 2013.
12. Chow BY, Han X, Dobry AS, Qian X, Chuong AS, Li M, Henninger MA, Belfort GM, Lin Y, Monahan PE, Boyden ES. High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature 463: 98-102, 2010.
13. Gossen M, Bujard H. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc Natl Acad Sci USA 89: 5547-5551, 1992.
14. Hollis ER 2nd, Jamshidi P, Lorenzana AO, Lee JK, Gray SJ, Samulski RJ, Zheng B, Tuszynski MH. Transient demyelination increases the efficiency of retrograde AAV transduction. Mol Ther 18: 1496-1500, 2010.
15. Kaspar BK, Llado J, Sherkat N, Rothstein JD, Gage FH. Retrograde viral delivery of IGF-1 prolongs survival in a mouse ALS model. Science 301: 839-842, 2003.
16. Kato S, Inoue K, Kobayashi K, Yasoshima Y, Miyachi S, Inoue S, Hanawa H, Shimada T, Takada M. Efficient gene transfer via retrograde transport in rodent and primate brains using a human immunodeficiency virus type 1-based vector pseudotyped with rabies virus glycoprotein. Hum Gene Ther 18: 1141-1151, 2007.
17. Kato S, Kobayashi K, Inoue K, Kuramochi M, Okada T, Yaginuma H, Morimoto K, Shimada T, Takada M. A lentiviral strategy for highly efficient retrograde gene transfer by pseudotyping with fusion envelope glycoprotein. Hum Gene Ther 22: 197-206, 2011.
18. Kinoshita M, Matsui R, Kato S, Hasegawa T, Kasahara H, Isa K, Watakabe A, Yamamori T, Nishimura Y, Alstermark B, Watanabe D, Kobayashi K, Isa T. Genetic dissection of the circuit for hand dexterity in primates. Nature 487: 235-238, 2012.
19. Kiritani T, Wickersham IR, Seung HS, Shepherd GM. Hierarchical connectivity and connection-specific dynamics in the corticospinal-corticostriatal microcircuit in mouse motor cortex. J Neurosci 32: 4992-5001, 2012.
20. Kress GJ, Yamawaki N, Wokosin DL, Wickersham IR, Shepherd GM, Surmeier DJ. Convergent cortical innervation of striatal projection neurons. Nat Neurosci 16: 665-667, 2013.
21. Kuhn B, Ozden I, Lampi Y, Hasan MT, Wang SS. An amplified promoter system for targeted expression of calcium indicator proteins in the cerebellar cortex. Front Neural Circuits 6: 49, 2012.
22. Lima SQ, Hromadka T, Znamenskiy P, Zador AM. PINP: a new method of tagging neuronal populations for identification during in vivo electrophysiological recording. PloS One 4: e6099, 2009.
23. Luo L, Callaway EM, Svoboda K. Genetic dissection of neural circuits. Neuron 57: 634-660, 2008.
24. Mazarakis ND, Azzouz M, Rohll JB, Ellard FM, Wilkes FJ, Olsen AL, Carter EE, Barber RD, Baban DF, Kingsman SM, Kingsman AJ, O'Malley K, Mitrophanous KA. Rabies virus glycoprotein pseudotyping of lentiviral vectors enables retrograde axonal transport and access to the nervous system after peripheral delivery. Hum Mol Genet 10: 2109-2121, 2001.
25. Nagel G, Brauner M, Liewald JF, Adeishvili N, Bamberg E, Gottschalk A. Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses. Curr Biol 15: 2279-2284, 2005.
26. Nagel G, Szellas T, Huhn W, Kateriya S, Adeishvili N, Berthold P, Ollig D, Hegemann P, Bamberg E. Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc Natl Acad Sci USA 100: 13940-13945, 2003.
27. Naldini L, Blomer U, Gallay P, Ory D, Mulligan R, Gage FH, Verma IM, Trono D. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272: 263-267, 1996.
28. Nathanson JL, Yanagawa Y, Obata K, Callaway EM. Preferential labeling of inhibitory and excitatory cortical neurons by endogenous tropism of adeno-associated virus and lentivirus vectors. Neuroscience 161: 441-450, 2009.
29. Olsen JC. Gene transfer vectors derived from equine infectious anemia virus. Gene Ther 5: 1481-1487, 1998.
30. Osakada F, Mori T, Cetin AH, Marshel JH, Virgen B, Callaway EM. New rabies virus variants for monitoring and manipulating activity and gene expression in defined neural circuits. Neuron 71: 617-631, 2011.
31. Schnutgen F, Doerflinger N, Calleja C, Wendling O, Chambon P, Ghyselinck NB. A directional strategy for monitoring Cre-mediated recombination at the cellular level in the mouse. Nat Biotechnol 21: 562-565, 2003.
32. Sena-Esteves M, Tebbets JC, Steffens S, Crombleholme T, Flake AW. Optimized large-scale production of high titer lentivirus vector pseudotypes. J Virol Methods 122: 131-139, 2004.
33. Sohal VS, Zhang F, Yizhar O, Deisseroth K. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459: 698-702, 2009.
34. Stepien AE, Tripodi M, Arber S. Monosynaptic rabies virus reveals premotor network organization and synaptic specificity of cholinergic partition cells. Neuron 68: 456-472, 2010.
35. Szymczak AL, Workman CJ, Wang Y, Vignali KM, Dilioglou S, Vanin EF, Vignali DA. Correction of multi-gene deficiency in vivo using a single "self-cleaving" 2A peptide-based retroviral vector. Nat Biotechnol 22: 589-594, 2004.
36. Tang W, Ehrlich I, Wolff SB, Michalski AM, Wolfl S, Hasan MT, Luthi A, Sprengel R. Faithful expression of multiple proteins via 2A-peptide selfprocessing: a versatile and reliable method for manipulating brain circuits. J Neurosci 29: 8621-8629, 2009.
37. Toniatti C, Bujard H, Cortese R, Ciliberto G. Gene therapy progress and prospects: transcription regulatory systems. Gene Ther 11: 649-657, 2004.
38. Towne C, Pertin M, Beggah AT, Aebischer P, Decosterd I. Recombinant adeno-associated virus serotype 6 (rAAV2/6)-mediated gene transfer to nociceptive neurons through different routes of delivery. Mol Pain 5: 52, 2009.
39. Wickersham IR, Callaway EM. Suitability of hCMV for viral gene expression in the brain-Wickersham and Callaway reply. Nat Methods 4: 379, 2007.
40. Wickersham IR, Finke S, Conzelmann KK, Callaway EM. Retrograde neuronal tracing with a deletion-mutant rabies virus. Nat Methods 4: 47-49, 2007.
41. Xu J, Ma C, Bass C, Terwilliger EF. A combination of mutations enhances the neurotropism of AAV-2. Virology 341: 203-214, 2005.
42. Yonehara K, Balint K, Noda M, Nagel G, Bamberg E, Roska B. Spatially asymmetric reorganization of inhibition establishes a motion-sensitive circuit. Nature 469: 407-410, 2011.
43. Yoshimura Y, Dantzker JL, Callaway EM. Excitatory cortical neurons form fine-scale functional networks. Nature 433: 868-873, 2005.
44. Zhang F, Wang LP, Brauner M, Liewald JF, Kay K, Watzke N, Wood PG, Bamberg E, Nagel G, Gottschalk A, Deisseroth K. Multimodal fast optical interrogation of neural circuitry. Nature 446: 633-639, 2007.
45. Zhang YP, Holbro N, Oertner TG. Optical induction of plasticity at single synapses reveals input-specific accumulation of alpha CaMKII. Proc Natl Acad Sci USA 105: 12039-12044, 2008.
46. Znamenskiy P, Zador AM. Corticostriatal neurons in auditory cortex drive decisions during auditory discrimination. Nature 497: 482-485, 2013.
47. Zufferey R, Donello JE, Trono D, Hope TJ. Woodchuck hepatitis virus posttranscriptional regulatory element enhances expression of transgenes delivered by retroviral vectors. J Virol 73: 2886-2892, 1999.