High-Throughput, High-Resolution Mapping of Protein Localization in Mammalian Brain by in Vivo Genome Editing

Cell

Volumn 165, Issue 7, 2016, Pages 1803-1817

  Mikuni, Takayasu ^a   Nishiyama, Jun ^a   Sun, Ye ^a,b   Kamasawa, Naomi ^a   Yasuda, Ryohei ^a  

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

^b FLORIDA ATLANTIC UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ACTIN; DOUBLECORTIN; FMRP PROTEIN; GUIDE RNA; OLIGODEOXYNUCLEOTIDE; PROTEIN; PROTEIN KINASE C ALPHA; RAB11A PROTEIN; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL; NERVE PROTEIN;

ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN; BRAIN CELL; BRAIN CORTEX; CELL LABELING; CELL MIGRATION; CELLS BY BODY ANATOMY; CELLULAR DISTRIBUTION; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; DENDRITIC SPINE; DNA END JOINING REPAIR; DNA SEQUENCE; DOUBLE STRANDED DNA BREAK; FEMALE; GENE SILENCING; GENOME; GENOME EDITING; HIGH THROUGHPUT SEQUENCING; HUMAN; IMMUNOELECTRON MICROSCOPY; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MALE; MICROFILAMENT; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PURKINJE CELL; PYRAMIDAL NERVE CELL; RETT SYNDROME; SCANNING ELECTRON MICROSCOPY; SINGLE CELL LABELING; START CODON; STEM CELL; STREPTOCOCCUS PYOGENES; SUBICULUM; TRANSPOSON; BRAIN CHEMISTRY; BRAIN MAPPING; CHEMISTRY; CRISPR CAS SYSTEM; EMBRYOLOGY; EVALUATION STUDY; GENETIC ENGINEERING; NERVE CELL; NEUROIMAGING; PROCEDURES; SINGLE CELL ANALYSIS;

BRAIN; BRAIN CHEMISTRY; BRAIN MAPPING; CRISPR-CAS SYSTEMS; GENETIC ENGINEERING; NERVE TISSUE PROTEINS; NEUROIMAGING; NEURONS; SINGLE-CELL ANALYSIS;

EID: 84966692476     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.04.044     Document Type: Article

References (61)

1. V. Borrell, Y. Yoshimura, and E.M. Callaway Targeted gene delivery to telencephalic inhibitory neurons by directional in utero electroporation J. Neurosci. Methods 143 2005 151 158
2. M. Bosch, J. Castro, T. Saneyoshi, H. Matsuno, M. Sur, and Y. Hayashi Structural and molecular remodeling of dendritic spine substructures during long-term potentiation Neuron 82 2014 444 459
3. F. Chen, and J. LoTurco A method for stable transgenesis of radial glia lineage in rat neocortex by piggyBac mediated transposition J. Neurosci. Methods 207 2012 172 180
4. R.Z. Chen, S. Akbarian, M. Tudor, and R. Jaenisch Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice Nat. Genet. 27 2001 327 331
5. V.T. Chu, T. Weber, B. Wefers, W. Wurst, S. Sander, K. Rajewsky, and R. Kühn Increasing the efficiency of homology-directed repair for CRISPR-Cas9-induced precise gene editing in mammalian cells Nat. Biotechnol. 33 2015 543 548
6. L. Cong, F.A. Ran, D. Cox, S. Lin, R. Barretto, N. Habib, P.D. Hsu, X. Wu, W. Jiang, L.A. Marraffini, and F. Zhang Multiplex genome engineering using CRISPR/Cas systems Science 339 2013 819 823
7. A. Contractor, V.A. Klyachko, and C. Portera-Cailliau Altered neuronal and circuit excitability in Fragile X syndrome Neuron 87 2015 699 715
8. D.B. Cox, R.J. Platt, and F. Zhang Therapeutic genome editing: prospects and challenges Nat. Med. 21 2015 121 131
9. J.A. Doudna, and E. Charpentier Genome editing. The new frontier of genome engineering with CRISPR-Cas9 Science 346 2014 1258096
10. D.A. Fortin, S.E. Tillo, G. Yang, J.C. Rah, J.B. Melander, S. Bai, O. Soler-Cedeño, M. Qin, B.V. Zemelman, C. Guo, and et al. Live imaging of endogenous PSD-95 using ENABLED: a conditional strategy to fluorescently label endogenous proteins J. Neurosci. 34 2014 16698 16712
11. M. Fukaya, and M. Watanabe Improved immunohistochemical detection of postsynaptically located PSD-95/SAP90 protein family by protease section pretreatment: a study in the adult mouse brain J. Comp. Neurol. 426 2000 572 586
12. J.G. Gleeson, P.T. Lin, L.A. Flanagan, and C.A. Walsh Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons Neuron 23 1999 257 271
13. V)1.2 encodes a transcription factor Cell 127 2006 591 606
14. G.G. Gross, J.A. Junge, R.J. Mora, H.B. Kwon, C.A. Olson, T.T. Takahashi, E.R. Liman, G.C. Ellis-Davies, A.W. McGee, B.L. Sabatini, and et al. Recombinant probes for visualizing endogenous synaptic proteins in living neurons Neuron 78 2013 971 985
15. K.M. Harris, F.E. Jensen, and B. Tsao Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation J. Neurosci. 12 1992 2685 2705
16. M. Heidenreich, and F. Zhang Applications of CRISPR-Cas systems in neuroscience Nat. Rev. Neurosci. 17 2016 36 44
17. J.W. Hell, R.E. Westenbroek, C. Warner, M.K. Ahlijanian, W. Prystay, M.M. Gilbert, T.P. Snutch, and W.A. Catterall Identification and differential subcellular localization of the neuronal class C and class D L-type calcium channel alpha 1 subunits J. Cell Biol. 123 1993 949 962
18. P.D. Hsu, E.S. Lander, and F. Zhang Development and applications of CRISPR-Cas9 for genome engineering Cell 157 2014 1262 1278
19. A.H. Hutagalung, and P.J. Novick Role of Rab GTPases in membrane traffic and cell physiology Physiol. Rev. 91 2011 119 149
20. F. Imamura, and C.A. Greer Segregated labeling of olfactory bulb projection neurons based on their birthdates Eur. J. Neurosci. 41 2015 147 156
21. S. Incontro, C.S. Asensio, R.H. Edwards, and R.A. Nicoll Efficient, complete deletion of synaptic proteins using CRISPR Neuron 83 2014 1051 1057
22. M. Jinek, K. Chylinski, I. Fonfara, M. Hauer, J.A. Doudna, and E. Charpentier A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity Science 337 2012 816 821
23. N. Kasthuri, K.J. Hayworth, D.R. Berger, R.L. Schalek, J.A. Conchello, S. Knowles-Barley, D. Lee, A. Vázquez-Reina, V. Kaynig, T.R. Jones, and et al. Saturated reconstruction of a volume of neocortex Cell 162 2015 648 661
24. S. Kim, D. Kim, S.W. Cho, J. Kim, and J.S. Kim Highly efficient RNA-guided genome editing in human cells via delivery of purified Cas9 ribonucleoproteins Genome Res. 24 2014 1012 1019
25. K. Kim, G. Lakhanpal, H.E. Lu, M. Khan, A. Suzuki, M.K. Hayashi, R. Narayanan, T.T. Luyben, T. Matsuda, T. Nagai, and et al. A temporary gating of actin remodeling during synaptic plasticity consists of the interplay between the kinase and structural functions of CaMKII Neuron 87 2015 813 826
26. A. Kitazawa, K. Kubo, K. Hayashi, Y. Matsunaga, K. Ishii, and K. Nakajima Hippocampal pyramidal neurons switch from a multipolar migration mode to a novel "climbing" migration mode during development J. Neurosci. 34 2014 1115 1126
27. B.P. Kleinstiver, V. Pattanayak, M.S. Prew, S.Q. Tsai, N.T. Nguyen, Z. Zheng, and J.K. Joung High-fidelity CRISPR-Cas9 nucleases with no detectable genome-wide off-target effects Nature 529 2016 490 495
28. E. Korb, C.L. Wilkinson, R.N. Delgado, K.L. Lovero, and S. Finkbeiner Arc in the nucleus regulates PML-dependent GluA1 transcription and homeostatic plasticity Nat. Neurosci. 16 2013 874 883
29. S.J. Lee, Y. Escobedo-Lozoya, E.M. Szatmari, and R. Yasuda Activation of CaMKII in single dendritic spines during long-term potentiation Nature 458 2009 299 304
30. S. Lin, B.T. Staahl, R.K. Alla, and J.A. Doudna Enhanced homology-directed human genome engineering by controlled timing of CRISPR/Cas9 delivery eLife 3 2014 e04766
31. J. Lisman, R. Yasuda, and S. Raghavachari Mechanisms of CaMKII action in long-term potentiation Nat. Rev. Neurosci. 13 2012 169 182
32. T. Maruyama, S.K. Dougan, M.C. Truttmann, A.M. Bilate, J.R. Ingram, and H.L. Ploegh Increasing the efficiency of precise genome editing with CRISPR-Cas9 by inhibition of nonhomologous end joining Nat. Biotechnol. 33 2015 538 542
33. J. Nishiyama, and R. Yasuda Biochemical computation for spine structural plasticity Neuron 87 2015 63 75
34. J. Nishiyama, Y. Hayashi, T. Nomura, E. Miura, W. Kakegawa, and M. Yuzaki Selective and regulated gene expression in murine Purkinje cells by in utero electroporation Eur. J. Neurosci. 36 2012 2867 2876
35. v)2.3 subunit of R-type calcium channel in mouse brain J. Neurosci. 32 2012 13555 13567
36. R.J. Platt, S. Chen, Y. Zhou, M.J. Yim, L. Swiech, H.R. Kempton, J.E. Dahlman, O. Parnas, T.M. Eisenhaure, M. Jovanovic, and et al. CRISPR-Cas9 knockin mice for genome editing and cancer modeling Cell 159 2014 440 455
37. F.A. Ran, P.D. Hsu, J. Wright, V. Agarwala, D.A. Scott, and F. Zhang Genome engineering using the CRISPR-Cas9 system Nat. Protoc. 8 2013 2281 2308
38. J. Riedl, A.H. Crevenna, K. Kessenbrock, J.H. Yu, D. Neukirchen, M. Bista, F. Bradke, D. Jenne, T.A. Holak, Z. Werb, and et al. Lifeact: a versatile marker to visualize F-actin Nat. Methods 5 2008 605 607
39. N. Saleh-Gohari, and T. Helleday Conservative homologous recombination preferentially repairs DNA double-strand breaks in the S phase of the cell cycle in human cells Nucleic Acids Res. 32 2004 3683 3688
40. J.D. Sander, and J.K. Joung CRISPR-Cas systems for editing, regulating and targeting genomes Nat. Biotechnol. 32 2014 347 355
41. R. Schalek, N. Kasthuri, K. Hayworth, D. Berger, J. Tapia, J. Morgan, S. Turaga, E. Fagerholm, H. Seung, and J. Lichtman Development of high-throughput, high-resolution 3D reconstruction of large-volume biological tissue using automated tape collection ultramicrotomy and scanning electron microscopy Microsc. Microanal. 17 2011 966 967
42. J.D. Shepherd, and M.F. Bear New views of Arc, a master regulator of synaptic plasticity Nat. Neurosci. 14 2011 279 284
43. I.M. Slaymaker, L. Gao, B. Zetsche, D.A. Scott, W.X. Yan, and F. Zhang Rationally engineered Cas9 nucleases with improved specificity Science 351 2016 84 88
44. M. Soma, H. Aizawa, Y. Ito, M. Maekawa, N. Osumi, E. Nakahira, H. Okamoto, K. Tanaka, and S. Yuasa Development of the mouse amygdala as revealed by enhanced green fluorescent protein gene transfer by means of in utero electroporation J. Comp. Neurol. 513 2009 113 128
45. S.F. Steinberg Structural basis of protein kinase C isoform function Physiol. Rev. 88 2008 1341 1378
46. L. Stoppini, P.A. Buchs, and D. Muller A simple method for organotypic cultures of nervous tissue J. Neurosci. Methods 37 1991 173 182
47. C. Straub, A.J. Granger, J.L. Saulnier, and B.L. Sabatini CRISPR/Cas9-mediated gene knock-down in post-mitotic neurons PLoS ONE 9 2014 e105584
48. L. Swiech, M. Heidenreich, A. Banerjee, N. Habib, Y. Li, J. Trombetta, M. Sur, and F. Zhang In vivo interrogation of gene function in the mammalian brain using CRISPR-Cas9 Nat. Biotechnol. 33 2015 102 106
49. H. Tabata, and K. Nakajima Efficient in utero gene transfer system to the developing mouse brain using electroporation: visualization of neuronal migration in the developing cortex Neuroscience 103 2001 865 872
50. K. Toyo-oka, T. Wachi, R.F. Hunt, S.C. Baraban, S. Taya, H. Ramshaw, K. Kaibuchi, Q.P. Schwarz, A.F. Lopez, and A. Wynshaw-Boris 14-3-3ϵ and ζ regulate neurogenesis and differentiation of neuronal progenitor cells in the developing brain J. Neurosci. 34 2014 12168 12181
51. S. Viswanathan, M.E. Williams, E.B. Bloss, T.J. Stasevich, C.M. Speer, A. Nern, B.D. Pfeiffer, B.M. Hooks, W.P. Li, B.P. English, and et al. High-performance probes for light and electron microscopy Nat. Methods 12 2015 568 576
52. H. Wang, H. Yang, C.S. Shivalila, M.M. Dawlaty, A.W. Cheng, F. Zhang, and R. Jaenisch One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering Cell 153 2013 910 918
53. W. Xue, S. Chen, H. Yin, T. Tammela, T. Papagiannakopoulos, N.S. Joshi, W. Cai, G. Yang, R. Bronson, D.G. Crowley, and et al. CRISPR-mediated direct mutation of cancer genes in the mouse liver Nature 514 2014 380 384
54. N. Yamamoto, T. Kurotani, and K. Toyama Neural connections between the lateral geniculate nucleus and visual cortex in vitro Science 245 1989 192 194
55. J. Yang, C.J. Siao, G. Nagappan, T. Marinic, D. Jing, K. McGrath, Z.Y. Chen, W. Mark, L. Tessarollo, F.S. Lee, and et al. Neuronal release of proBDNF Nat. Neurosci. 12 2009 113 115
56. H. Yang, H. Wang, C.S. Shivalila, A.W. Cheng, L. Shi, and R. Jaenisch One-step generation of mice carrying reporter and conditional alleles by CRISPR/Cas-mediated genome engineering Cell 154 2013 1370 1379
57. H. Yin, W. Xue, S. Chen, R.L. Bogorad, E. Benedetti, M. Grompe, V. Koteliansky, P.A. Sharp, T. Jacks, and D.G. Anderson Genome editing with Cas9 in adult mice corrects a disease mutation and phenotype Nat. Biotechnol. 32 2014 551 553
58. K. Yusa, L. Zhou, M.A. Li, A. Bradley, and N.L. Craig A hyperactive piggyBac transposase for mammalian applications Proc. Natl. Acad. Sci. USA 108 2011 1531 1536
59. R. Yuste, and T. Bonhoeffer Genesis of dendritic spines: insights from ultrastructural and imaging studies Nat. Rev. Neurosci. 5 2004 24 34
60. B. Zetsche, J.S. Gootenberg, O.O. Abudayyeh, I.M. Slaymaker, K.S. Makarova, P. Essletzbichler, S.E. Volz, J. Joung, J. van der Oost, A. Regev, and et al. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system Cell 163 2015 759 771
61. H. Zong, J.S. Espinosa, H.H. Su, M.D. Muzumdar, and L. Luo Mosaic analysis with double markers in mice Cell 121 2005 479 492