Whole-brain 3D mapping of human neural transplant innervation

Nature Communications

Volumn 8, Issue , 2017, Pages

  Doerr, Jonas ^a,b   Schwarz, Martin Karl ^a,b   Wiedermann, Dirk ^c   Leinhaas, Anke ^a   Jakobs, Alina ^a   Schloen, Florian ^a   Schwarz, Inna ^a   Diedenhofen, Michael ^c   Braun, Nils Christian ^a   Koch, Philipp ^a   Peterson, Daniel A ^d   Kubitscheck, Ulrich ^a   Hoehn, Mathias ^c   Brüstle, Oliver ^a,b  

^a UNIVERSITY OF BONN   (Germany)

^b Life and Brain Center   (Germany)

^c MAX PLANCK INSTITUTE FOR NEUROLOGICAL RESEARCH   (Germany)

^d ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANATOMY; BRAIN; CELLS AND CELL COMPONENTS; MAPPING METHOD; NEUROLOGY; PRECISION; RODENT; THREE-DIMENSIONAL MODELING;

ADULT; ANATOMICAL VARIATION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN MAPPING; BRAIN REGION; CELL POPULATION; CONTROLLED STUDY; DONOR-HOST CELL INTERACTION; EMBRYO; FEMALE; FLUORESCENCE MICROSCOPY; FUNCTIONAL CONNECTIVITY; HUMAN; HUMAN CELL; INNERVATION; MOUSE; NEURAL STEM CELL TRANSPLANTATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; THREE DIMENSIONAL IMAGING; ANIMAL; BRAIN; CELL DIFFERENTIATION; GENE VECTOR; INTERNEURON; NERVE CELL; NEURAL STEM CELL; PHYSIOLOGY; PROCEDURES; RABIES VIRUS; TRANSPLANTATION;

RABIES VIRUS;

ANIMALS; BRAIN; BRAIN MAPPING; CELL DIFFERENTIATION; GENETIC VECTORS; HUMANS; INTERNEURONS; MAGNETIC RESONANCE IMAGING; MICE; MICROSCOPY, FLUORESCENCE; NEURAL STEM CELLS; NEURONS; RABIES VIRUS;

EID: 85010383243     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms14162     Document Type: Article

References (47)

1. Thompson, L. H. & Björklund, A. Reconstruction of brain circuitry by neural transplants generated from pluripotent stem cells. Neurobiol. Dis. 79, 28-40 (2015).
2. Steinbeck, J. & Studer, L. Moving stem cells to the clinic: potential and limitations for brain repair. Neuron 86, 187-206 (2015).
3. Debanne, D. et al. Paired-recordings from synaptically coupled cortical and hippocampal neurons in acute and cultured brain slices. Nat. Protoc. 3, 1559-1568 (2008).
4. Svoboda, K., Denk, W., Kleinfeld, D. & Tank, D. W. In vivo dendritic calcium dynamics in neocortical pyramidal neurons. Nature 385, 161-165 (1997).
5. Antic, S. D., Empson, R. M. & Knopfel, T. Voltage imaging to understand connections and functions of neuronal circuits. J. Neurophysiol. 116, 135-152 (2016).
6. Wickersham, I. R. et al. Monosynaptic restriction of transsynaptic tracing from single, genetically targeted neurons. Neuron 53, 639-647 (2007).
7. Wickersham, I. R., Finke, S., Conzelmann, K. K. & Callaway, E. M. Retrograde neuronal tracing with a deletion-mutant rabies virus. Nat. Methods. 4, 47-49 (2007).
8. Dodt, H. U. et al. Ultramicroscopy: Three-dimensional visualization of neuronal networks in the whole mouse brain. Nat. Methods 4, 331-336 (2007).
9. Ertürk, A. et al. Three-dimensional imaging of the unsectioned adult spinal cord to assess axon regeneration and glial responses after injury. Nat. Med. 18, 166-171 (2011).
10. Hama, H. et al. Scale: A chemical approach for fluorescence imaging and reconstruction of transparent mouse brain. Nat. Neurosci. 14, 1481-1488 (2011).
11. Kuwajima, T. et al. ClearT: A detergent-And solvent-free clearing method for neuronal and non-neuronal tissue. Development 140, 1364-1368 (2013).
12. Ke, M. T., Fujimoto, S. & Imai, T. SeeDB: A simple and morphology-preserving optical clearing agent for neuronal circuit reconstruction. Nat. Neurosci. 16, 1154-1161 (2013).
13. Yang, B. et al. Single-cell phenotyping within transparent intact tissue through whole-body clearing. Cell 158, 945-958 (2014).
14. Susaki, E. A. et al. Whole-brain imaging with single-cell resolution using chemical cocktails and computational analysis. Cell 157, 726-739 (2014).
15. Schwarz, M. et al. Fluorescent-protein stabilization and high-resolution imaging of cleared, intact mouse brains. PLoS ONE 10, e0124650 (2015).
16. Koch, P., Opitz, T., Steinbeck, J. A., Ladewig, J. & Brüstle, O. A rosette-Type, self-renewing human ES cell-derived neural stem cell with potential for in vitro instruction and synaptic integration. Proc. Natl Acad. Sci. USA 106, 3225-3230 (2009).
17. Falk, A. et al. Capture of neuroepithelial-like stem cells from pluripotent stem cells provides a versatile system for in vitro production of human neurons. PLoS ONE 7, e29597 (2012).
18. Ladewig, J., Koch, P. & Brüstle, O. Auto-Attraction of neural precursors and their neuronal progeny impairs neuronal migration. Nat. Neurosci. 17, 24-26 (2014).
19. Mertens, J. et al. Embryonic stem cell-based modeling of tau pathology in human neurons. Am. J. Pathol. 182, 1769-1779 (2013).
20. Doerr, J. et al. Arylsulfatase A overexpressing human iPSC-derived neural cells reduce CNS sulfatide storage in a mouse model of metachromatic leukodystrophy. Mol. Ther. 23, 1519-1531 (2015).
21. Steinbeck, J. A., Koch, P., Derouiche, A. & Brüstle, O. Human embryonic stem cell-derived neurons establish region-specific, long-range projections in the adult brain. Cell. Mol. Life Sci. 69, 461-470 (2012).
22. Niedworok, C. et al. Charting monosynaptic connectivity maps by two-color light-sheet fluorescence microscopy. Cell Rep. 2, 1375-1386 (2012).
23. Shinkai, Y. et al. RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell 68, 855-867 (1992).
24. Grealish, S. et al. Monosynaptic tracing using modified rabies virus reveals early and extensive circuit integration of human embryonic stem cell-derived neurons. Stem Cell Rep. 4, p975-p983 (2015).
25. Koester, S. E. & O'Leary, D. D. Functional classes of cortical projection neurons develop dendritic distinctions by class-specific sculpting of an early common pattern. J. Neurosci. 12, 1382-1393 (1992).
26. Wall, N., De La Parra, M., Callaway, E. & Kreitzer, A. Differential innervation of direct-And indirect-pathway striatal projection neurons. Neuron 79, 347-360 (2013).
27. Reinhardt, P. et al. Derivation and expansion using only small molecules of human neural progenitors for neurodegenerative disease modeling. PLoS ONE 8, e59252 (2013).
28. Dorr, A. E., Lerch, J. P., Spring, S., Kabani, N. & Henkelman, R. M. High resolution three-dimensional brain atlas using an average magnetic resonance image of 40 adult C57Bl/6 J mice. NeuroImage 42, 60-69 (2008).
29. Ullmann, J. F., Watson, C., Janke, A. L., Kurniawan, N. D. & Reutens, D. C. A segmentation protocol and MRI atlas of the C57BL/6 J mouse neocortex. NeuroImage 78, 196-203 (2013).
30. Sun, Y. et al. Cell-Type-specific circuit connectivity of hippocampal CA1 revealed through Cre-dependent rabies tracing. Cell Rep. 7, 269-280 (2014).
31. Bachoud-Lévi, A. C. & Perrier, A. L. Regenerative medicine in Huntington's disease: current status on fetal grafts and prospects for the use of pluripotent stem cell. Rev. Neurol. (Paris). 170, 749-762 (2014).
32. Barker, R. A., Drouin-Ouellet, J. & Parmar, M. Cell-based therapies for Parkinson disease-past insights and future potential. Nat. Rev. Neurol. 11, 492-503 (2015).
33. Lindvall, O. Clinical translation of stem cell transplantation in Parkinson's disease. J. Intern. Med. 279, 30-40 (2016).
34. Takahashi, K. & Yamanaka, S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676 (2006).
35. Takahashi, K. et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861-872 (2007).
36. Masuda-Suzukake, M. et al. Pathological alpha-synuclein propagates through neural networks. Acta Neuropathol. Commun. 2, 88 (2014).
37. Pecho-Vrieseling, E. et al. Transneuronal propagation of mutant huntingtin contributes to non-cell autonomous pathology in neurons. Nat. Neurosci. 17, 1064-1072 (2014).
38. Rey, N. L., Petit, G. H., Bousset, L., Melki, R. & Brundin, P. Transfer of human a-synuclein from the olfactory bulb to interconnected brain regions in mice. Acta Neuropathol. 126, 555-573 (2013).
39. Vierbuchen, T. et al. Direct conversion of fibroblasts to functional neurons by defined factors. Nature 463, 1035-1041 (2010).
40. Pang, Z. P. et al. Induction of human neuronal cells by defined transcription factors. Nature 476, 220-223 (2011).
41. Giorgetti, A. et al. Cord blood-derived neuronal cells by ectopic expression of Sox2 and c-Myc. Proc. Natl Acad. Sci. USA 109, 12556-12561 (2012).
42. Mertens, J., Marchetto, M. C., Bardy, C. & Gage, F. Evaluating cell reprogramming, differentiation and conversion technologies in neuroscience. Nat. Rev. Neurosci. 17, 424-437 (2016).
43. Kutner, R. H., Zhang, X. Y. & Reiser, J. Production, concentration and titration of pseudotyped HIV-1-based lentiviral vectors. Nat. Protoc. 4, 495-505 (2009).
44. Jenkinson, M., Bannister, P., Brady, M. & Smith, S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage 17, 825-841 (2002).
45. Jenkinson, M. & Smith, S. A global optimisation method for robust affine registration of brain images. Med. Image Anal. 5, 143-156 (2001).
46. West, M. J. New stereological methods for counting neurons. Neurobiol. Aging 14, 275-285 (1993).
47. Peterson, D. A. in Fluorescence Microscopy (Academic Press, 2014).