Genetic strategies to investigate neuronal circuit properties using stem cell-derived neurons

Frontiers in Cellular Neuroscience

Volumn , Issue NOV, 2012, Pages

  Garcia, Isabella ^a   Kim, Cynthia ^a,b   Arenkiel, Benjamin R ^a,b  

^a TEXAS CHILDREN S HOSPITAL   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Circuit; Neuron; Optogenetic; Reprogramming; Stem cell; Synapse; Transsynaptic

Indexed keywords

CELL LINEAGE; CELL STRUCTURE; CELL TYPE; EMBRYONIC STEM CELL; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC ENGINEERING; HERPES SIMPLEX VIRUS 1; HUMAN; IN VITRO STUDY; NERVE CELL; NERVE CELL NETWORK; NERVE CONDUCTION; NEUROANATOMICAL TRACT TRACING; NONHUMAN; PLURIPOTENT STEM CELL; PSEUDORABIES HERPETOVIRUS; REVIEW; SOMATIC CELL; SYNAPSE;

EID: 84871357867     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2012.00059     Document Type: Review

References (157)

1. Ahmed, B., Anderson, J.C., Martin, K.A., and Nelson, J.C. (1997). Map of the synapses onto layer 4 basket cells of the primary visual cortex of the cat. J Comp Neurol 380, 230-242.
2. Akerboom, J., Chen, T.W., Wardill, T.J., Tian, L., Marvin, J.S., Mutlu, S., Calderon, N.C., Esposti, F., Borghuis, B.G., Sun, X.R., et al. (2012). Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging. J Neurosci 32, 13819-13840.
3. Alvarez Dolado, M., and Broccoli, V. (2011). GABAergic neuronal precursor grafting: implications in brain regeneration and plasticity. Neural Plast 2011, 384216.
4. Anderson, J.C., Douglas, R.J., Martin, K.A., and Nelson, J.C. (1994). Map of the synapses formed with the dendrites of spiny stellate neurons of cat visual cortex. J Comp Neurol 341, 25-38.
5. Angelucci, A., Clasca, F., and Sur, M. (1996). Anterograde axonal tracing with the subunit B of cholera toxin: a highly sensitive immunohistochemical protocol for revealing fine axonal morphology in adult and neonatal brains. J Neurosci Methods 65, 101-112.
6. Apps, R., and Ruigrok, T.J. (2007). A fluorescence-based double retrograde tracer strategy for charting central neuronal connections. Nat Protoc 2, 1862-1868.
7. Arenkiel, B.R. (2011). Genetic approaches to reveal the connectivity of adult-born neurons. Front Neurosci 5, 48.
8. Arenkiel, B.R., Hasegawa, H., Yi, J.J., Larsen, R.S., Wallace, M.L., Philpot, B.D., Wang, F., and Ehlers, M.D. (2011). Activity-induced remodeling of olfactory bulb microcircuits revealed by monosynaptic tracing. PLoS One 6, e29423.
9. Arenkiel, B.R., Klein, M.E., Davison, I.G., Katz, L.C., and Ehlers, M.D. (2008). Genetic control of neuronal activity in mice conditionally expressing TRPV1. Nat Methods 5, 299-302.
10. Arenkiel, B.R., Peca, J., Davison, I.G., Feliciano, C., Deisseroth, K., Augustine, G.J., Ehlers, M.D., and Feng, G. (2007). In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2. Neuron 54, 205-218.
11. Armbruster, B. N., Li, X., Pausch, M.H., Herlitze, S., and Roth, B.L. (2007). Evolving the lock to fit the key to create a family of G protein-couple receptors potently activated by an inert ligand, Proc Natl Acad Sci USA 104(12), 5163-5168.
12. Armstrong, R.J., Hurelbrink, C.B., Tyers, P., Ratcliffe, E.L., Richards, A., Dunnett, S.B., Rosser, A.E., and Barker, R.A. (2002). The potential for circuit reconstruction by expanded neural precursor cells explored through porcine xenografts in a rat model of Parkinson's disease. Exp Neurol 175, 98-111.
13. Babaei, P., Soltani Tehrani, B., and Alizadeh, A. (2012). Transplanted bone marrow mesenchymal stem cells improve memory in rat models of Alzheimer's disease. Stem Cells Int 2012, 369417.
14. rd (2012). Microtubule Stabilizing Agents as Potential Treatment for Alzheimer's Disease and Related Neurodegenerative Tauopathies. J Med Chem.
15. Bibel, M., Richter, J., Lacroix, E., and Barde, Y.A. (2007). Generation of a defined and uniform population of CNS progenitors and neurons from mouse embryonic stem cells. Nat Protoc 2, 1034-1043.
16. Birgul, N., Weise, C., Kreienkamp, H. J., and Richter, D. (1999). Reverse physiology in drosophila: identification of a novel allatostatin-like neuropeptide and its cognate receptor structurally related to the mammalian somatostatin/galanin/opiod receptor family. EMBO J 18 (21), 5892-900.
17. Bissonnette, C.J., Lyass, L., Bhattacharyya, B.J., Belmadani, A., Miller, R.J., and Kessler, J.A. (2011). The controlled generation of functional basal forebrain cholinergic neurons from human embryonic stem cells. Stem Cells 29, 802-811.
18. Bjorklund, L.M., Sanchez-Pernaute, R., Chung, S., Andersson, T., Chen, I.Y., McNaught, K.S., Brownell, A.L., Jenkins, B.G., Wahlestedt, C., Kim, K.S., et al. (2002). Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model. Proc Natl Acad Sci U S A 99, 2344-2349.
19. Briggman, K.L., and Denk, W. (2006). Towards neural circuit reconstruction with volume electron microscopy techniques. Curr Opin Neurobiol 16, 562-570.
20. Bruce, L.L., Christensen, M.A., and Fritzsch, B. (1997). Electron microscopic differentiation of directly and transneuronally transported DiI and applications for studies of synaptogenesis. J Neurosci Methods 73, 107-112.
21. Caiazzo, M., Dell'Anno, M.T., Dvoretskova, E., Lazarevic, D., Taverna, S., Leo, D., Sotnikova, T.D., Menegon, A., Roncaglia, P., Colciago, G., et al. (2011). Direct generation of functional dopaminergic neurons from mouse and human fibroblasts. Nature 476, 224-227.
22. Callaway, E.M. (2008). Transneuronal circuit tracing with neurotropic viruses. Curr Opin Neurobiol 18, 617-623.
23. Camnasio, S., Carri, A.D., Lombardo, A., Grad, I., Mariotti, C., Castucci, A., Rozell, B., Riso, P.L., Castiglioni, V., Zuccato, C., et al. (2012). The first reported generation of several induced pluripotent stem cell lines from homozygous and heterozygous Huntington's disease patients demonstrates mutation related enhanced lysosomal activity. Neurobiol Dis 46, 41-51.
24. Cao, L., Schrank, B.R., Rodriguez, S., Benz, E.G., Moulia, T.W., Rickenbacher, G.T., Gomez, A.C., Levites, Y., Edwards, S.R., Golde, T.E., et al. (2012). Abeta alters the connectivity of olfactory neurons in the absence of amyloid plaques in vivo. Nat Commun 3, 1009.
25. Capetian, P., Dobrossy, M., Winkler, C., Prinz, M., and Nikkhah, G. (2011). To be or not to be accepted: the role of immunogenicity of neural stem cells following transplantation into the brain in animal and human studies. Semin Immunopathol 33, 619-626.
26. Castillo, C.G., Mendoza-Trejo, S., Aguilar, M.B., Freed, W.J., and Giordano, M. (2008). Intranigral transplants of a GABAergic cell line produce long-term alleviation of established motor seizures. Behav Brain Res 193, 17-27.
27. Chang, Y.L., Chen, S.J., Kao, C.L., Hung, S.C., Ding, D.C., Yu, C.C., Chen, Y.J., Ku, H.H., Lin, C.P., Lee, K.H., et al. (2012). Docosahexaenoic acid promotes dopaminergic differentiation in induced pluripotent stem cells and inhibits teratoma formation in rats with Parkinson-like pathology. Cell Transplant 21, 313-332.
28. Chen Q., Cichon J., Wang W., Qiu L., Lee S.J., Campbell N.R., Destefino N., Goard M.J., Fu Z., Yasuda R., Looger L.L., Arenkiel B.R., Gan W.B., Feng G. (2012). Imaging neural activity using Thy1-GCaMP transgenic mice. Neuron 76(2), 297-308.
29. Chen, W.W., and Blurton-Jones, M. (2012). Concise Review: Can Stem Cells be Used to Treat or Model Alzheimer Disease? Stem Cells.
30. Chen, Z., Phillips, L.K., Gould, E., Campisi, J., Lee, S.W., Ormerod, B.K., Zwierzchoniewska, M., Martinez, O.M., and Palmer, T.D. (2011). MHC mismatch inhibits neurogenesis and neuron maturation in stem cell allografts. PLoS One 6, e14787.
31. Cho, E.G., Zaremba, J.D., McKercher, S.R., Talantova, M., Tu, S., Masliah, E., Chan, S.F., Nakanishi, N., Terskikh, A., and Lipton, S.A. (2011). MEF2C enhances dopaminergic neuron differentiation of human embryonic stem cells in a parkinsonian rat model. PLoS One 6, e24027.
32. Chow, B.Y., Han, X., Dobry, A.S., Qian, X., Chuong, A.S., Li, M., Henninger, M.A., Belfort, G.M., Lin, Y., Monahan, P.E., et al. (2010). High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature 463, 98-102.
33. Chung, S., Moon, J.I., Leung, A., Aldrich, D., Lukianov, S., Kitayama, Y., Park, S., Li, Y., Bolshakov, V.Y., Lamonerie, T., et al. (2011). ES cell-derived renewable and functional midbrain dopaminergic progenitors. Proc Natl Acad Sci U S A 108, 9703-9708.
34. Chow, B. Y., Han, X., Dobry, A. A., et al. (2010). High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature 463, 98-102.
35. Conklin, B.R., Hsiao, E.C., Claeysen, S., Dumuis, A., Srinivasan, S., Forsayeth, J.R., Guettier, J.M., Chang, W.C., Pei, Y., McCarthy, K.D., et al. (2008). Engineering GPCR signaling pathways with RASSLs. Nat Methods 5, 673-678.
36. Coward, P., Wada, H.G., Falk, M.S., Chan, S.D., Meng, F., Akil, H., and Conklin, B.R. (1998). Controlling signaling with a specifically designed Gi-coupled receptor. Proc Natl Acad Sci USA 95(1), 352-357.
37. Cunningham, J.J., Ulbright, T.M., Pera, M.F., and Looijenga, L.H. (2012). Lessons from human teratomas to guide development of safe stem cell therapies. Nat Biotechnol 30, 849-857.
38. Daadi, M.M., Li, Z., Arac, A., Grueter, B.A., Sofilos, M., Malenka, R.C., Wu, J.C., and Steinberg, G.K. (2009). Molecular and magnetic resonance imaging of human embryonic stem cell-derived neural stem cell grafts in ischemic rat brain. Mol Ther 17, 1282-1291.
39. Das, N., Dhanawat, M., and Shrivastava, S.K. (2012). An overview on antiepileptic drugs. Drug Discov Ther 6, 178-193.
40. Deacon, T., Dinsmore, J., Costantini, L.C., Ratliff, J., and Isacson, O. (1998). Blastula-stage stem cells can differentiate into dopaminergic and serotonergic neurons after transplantation. Exp Neurol 149, 28-41.
41. Deisseroth, K. (2010). Controlling the brain with light. Sci Am 303, 48-55.
42. Denham, M., and Dottori, M. (2011). Neural differentiation of induced pluripotent stem cells. Methods Mol Biol 793, 99-110.
43. Dhar, D., Dickson, J.L., Carby, M.R., Lyster, H.S., Hall, A.V., and Banner, N.R. (2012). Fungal infection in cardiothoracic transplant recipients: outcome without systemic amphotericin therapy. Transpl Int 25, 758-764.
44. Drenan, R.M., Grady, S.R., Whiteaker, P., McClure-Begley, T., McKinney, S., Miwa, J.M., Bupp, S., Heintz, N., McIntosh, J.M., Bencherif, M., et al. (2008). In vivo activation of midbrain dopamine neurons via sensitized, high-affinity alpha 6 nicotinic acetylcholine receptors. Neuron 60, 123-136.
45. Dyson, S.C., and Barker, R.A. (2011). Cell-based therapies for Parkinson's disease. Expert Rev Neurother 11, 831-844.
46. Enquist, L.W. (2002). Exploiting circuit-specific spread of pseudorabies virus in the central nervous system: insights to pathogenesis and circuit tracers. J Infect Dis 186 Suppl 2, S209-214.
47. Erdo, F., Trapp, T., Buhrle, C., Fleischmann, B., and Hossmann, K.A. (2004). [Embryonic stem cell therapy in experimental stroke: host-dependent malignant transformation]. Orv Hetil 145, 1307-1313.
48. Fainstein, N., Einstein, O., Cohen, M.E., Brill, L., Lavon, I., and Ben-Hur, T. (2012). Time limited immunomodulatory functions of transplanted neural precursor cells. Glia.
49. Fong, C.Y., Gauthaman, K., and Bongso, A. (2010). Teratomas from pluripotent stem cells: A clinical hurdle. J Cell Biochem 111, 769-781.
50. Freed, C.R., Zhou, W., and Breeze, R.E. (2011). Dopamine cell transplantation for Parkinson's disease: the importance of controlled clinical trials. Neurotherapeutics 8, 549-561.
51. Fridhandler, J.D., Coelho, F.M., Tai, P., Jette, N., and Andrade, D.M. (2012). A comparison of antiepileptic drug therapy in patients with severe intellectual disability and patients with normal intellect. Epilepsy Behav 25, 196-199.
52. Gancher, S.T., Woodward, W.R., and Nutt, J.G. (1996). Apomorphine tolerance in Parkinson's disease: lack of a dose effect. Clin Neuropharmacol 19, 59-64.
53. Garcia, I., Huang, L., Ung, K., and Arenkiel, B.R. (2012). Tracing Synaptic Connectivity onto Embryonic Stem Cell-derived Neurons. Stem Cells 30, 2140-2151.
54. Ghiglieri, V., Bagetta, V., Calabresi, P., and Picconi, B. (2012). Functional interactions within striatal microcircuit in animal models of Huntington's disease. Neuroscience 211, 165-184.
55. Gomez-Nieto, R., Rubio, M.E., and Lopez, D.E. (2008). Cholinergic input from the ventral nucleus of the trapezoid body to cochlear root neurons in rats. J Comp Neurol 506, 452-468.
56. Grienberger, C., Rochefort, N.L., Adelsberger, H., Henning, H.A., Hill, D.N., Reichwald, J., Staufenbiel, M., and Konnerth, A. (2012). Staged decline of neuronal function in vivo in an animal model of Alzheimer's disease. Nat Commun 3, 774.
57. Han, D.W., Tapia, N., Hermann, A., Hemmer, K., Hoing, S., Arauzo-Bravo, M.J., Zaehres, H., Wu, G., Frank, S., Moritz, S., et al. (2012). Direct reprogramming of fibroblasts into neural stem cells by defined factors. Cell Stem Cell 10, 465-472.
58. Hanna, J., Wernig, M., Markoulaki, S., Sun, C.W., Meissner, A., Cassady, J.P., Beard, C., Brambrink, T., Wu, L.C., Townes, T.M., et al. (2007). Treatment of sickle cell anemia mouse model with iPS cells generated from autologous skin. Science 318, 1920-1923.
59. Hattiangady, B., Shuai, B., Cai, J., Coksaygan, T., Rao, M.S., and Shetty, A.K. (2007). Increased dentate neurogenesis after grafting of glial restricted progenitors or neural stem cells in the aging hippocampus. Stem Cells 25, 2104-2117.
60. Hovakimyan, M., Muller, J., Wree, A., Ortinau, S., Rolfs, A., and Schmitt, O. (2012). Survival of transplanted human neural stem cell line (ReNcell VM) into the rat brain with and without immunosuppression. Ann Anat 194, 429-435.
61. Israel, M.A., Yuan, S.H., Bardy, C., Reyna, S.M., Mu, Y., Herrera, C., Hefferan, M.P., Van Gorp, S., Nazor, K.L., Boscolo, F.S., et al. (2012). Probing sporadic and familial Alzheimer's disease using induced pluripotent stem cells. Nature 482, 216-220.
62. Jing, Y., Machon, O., Hampl, A., Dvorak, P., Xing, Y., and Krauss, S. (2011). In vitro differentiation of mouse embryonic stem cells into neurons of the dorsal forebrain. Cell Mol Neurobiol 31, 715-727.
63. Juliandi, B., Abematsu, M., Sanosaka, T., Tsujimura, K., Smith, A., and Nakashima, K. (2012). Induction of superficial cortical layer neurons from mouse embryonic stem cells by valproic acid. Neurosci Res 72, 23-31.
64. Kasper, E.M., Bartek, J., Jr., Johnson, S., Kasper, B.S., Pavlakis, M., and Wong, M. (2011). Post-transplant aspergillosis and the role of combined neurosurgical and antifungal therapies under belatacept immunosuppression. Surg Neurol Int 2, 75.
65. Kauhausen, J., Thompson, L.H., and Parish, C.L. (2012). Cell intrinsic and extrinsic factors contribute to enhance neural circuit reconstruction following transplantation in Parkinsonian mice. J Physiol.
66. Kelly, C.M., Precious, S.V., Penketh, R., Amso, N., Dunnett, S.B., and Rosser, A.E. (2007). Striatal graft projections are influenced by donor cell type and not the immunogenic background. Brain 130, 1317-1329.
67. Kirkeby, A., Grealish, S., Wolf, D.A., Nelander, J., Wood, J., Lundblad, M., Lindvall, O., and Parmar, M. (2012). Generation of Regionally Specified Neural Progenitors and Functional Neurons from Human Embryonic Stem Cells under Defined Conditions. Cell Rep 1, 703-714.
68. Kraft, E., Loichinger, W., Diepers, M., Lule, D., Schwarz, J., Ludolph, A.C., and Storch, A. (2009). Levodopa-induced striatal activation in Parkinson's disease: a functional MRI study. Parkinsonism Relat Disord 15, 558-563.
69. Kriks, S., Shim, J.W., Piao, J., Ganat, Y.M., Wakeman, D.R., Xie, Z., Carrillo-Reid, L., Auyeung, G., Antonacci, C., Buch, A., et al. (2011). Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson's disease. Nature 480, 547-551.
70. Kuypers, H.G., and Ugolini, G. (1990). Viruses as transneuronal tracers. Trends Neurosci 13, 71-75.
71. Krystkowiak, P., Gaura, V., Labalette, M., Rialland, A., Remy, P., Peschanski, M., and Bachoud-Levi, A. C. (2007). Alloimmunisation to donor antigens and immune rejection following foetal neural grafts to the brain in patients with Huntington's disease. PLoS One 2, e166.
72. Lerchner, W., Xiao, C., Nashmi, R., Slimko, E.M., van Trigt, L., Lester, H.A., and Anderson, D.J. (2007). Reversible silencing of neuronal excitability in behaving mice by a genetically targeted, ivermectin-gated Cl- channel. Neuron 54, 35-49.
73. Lescaudron, L., Naveilhan, P., and Neveu, I. (2012). The use of stem cells in regenerative medicine for Parkinson's and Huntington's diseases. Curr Med Chem.
74. Leuner, B., Mendolia-Loffredo, S., Kozorovitskiy, Y., Samburg, D., Gould, E., and Shors, T.J. (2004). Learning enhances the survival of new neurons beyond the time when the hippocampus is required for memory. J Neurosci 24, 7477-7481.
75. Leveque, X., Cozzi, E., Naveilhan, P., and Neveu, I. (2011). Intracerebral xenotransplantation: recent findings and perspectives for local immunosuppression. Curr Opin Organ Transplant 16, 190-194.
76. Liemburg, E.J., van der Meer, L., Swart, M., Curcic-Blake, B., Bruggeman, R., Knegtering, H., and Aleman, A. (2012a). Reduced connectivity in the self-processing network of schizophrenia patients with poor insight. PLoS One 7, e42707.
77. Liemburg, E.J., Vercammen, A., Ter Horst, G.J., Curcic-Blake, B., Knegtering, H., and Aleman, A. (2012b). Abnormal connectivity between attentional, language and auditory networks in schizophrenia. Schizophr Res 135, 15-22.
78. Lilley, C.E., Branston, R.H., and Coffin, R.S. (2001). Herpes simplex virus vectors for the nervous system. Curr Gene Ther 1, 339-358.
79. Lindvall, O. (2012). Why is it taking so long to develop clinically competitive stem cell therapies for CNS disorders? Cell Stem Cell 10, 660-662.
80. Louis, G.W., Leinninger, G.M., Rhodes, C.J., and Myers, M.G., Jr. (2010). Direct innervation and modulation of orexin neurons by lateral hypothalamic LepRb neurons. J Neurosci 30, 11278-11287.
81. Ma, K., Fox, L., Shi, G., Shen, J., Liu, Q., Pappas, J.D., Cheng, J., and Qu, T. (2011). Generation of neural stem cell-like cells from bone marrow-derived human mesenchymal stem cells. Neurol Res 33, 1083-1093.
82. Madisen, L., Mao, T., Koch, H., Zhuo, J.M., Berenyi, A., Fujisawa, S., Hsu, Y.W., Garcia, A.J., 3rd, Gu, X., Zanella, S., et al. (2012). A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing. Nat Neurosci 15, 793-802.
83. Magnus, C.J., Lee, P.H., Atasoy, D., Su, H.H., Looger, L.L., and Sternson, S.M. (2011). Chemcial and genetic engineering of selective ion channel-ligand interactions. Science 333, 1292-1296.
84. Maisano, X., Carpentino, J., Becker, S., Lanza, R., Aaron, G., Grabel, L., and Naegele, J.R. (2009). Embryonic stem cell-derived neural precursor grafts for treatment of temporal lobe epilepsy. Neurotherapeutics 6, 263-277.
85. Makarenko, I.G., Ugrumov, M.V., Derer, P., and Calas, A. (2000). Projections from the hypothalamus to the posterior lobe in rats during ontogenesis: 1,1'-dioctadecyl-3,3,3', 3'-tetramethylindocarbocyanine perchlorate tracing study. J Comp Neurol 422, 327-337.
86. Mao, T., O'Connor, D.H., Scheuss, V., Nakai, J., and Svoboda, K. (2008). Characterization and subcellular targeting of GCaMP-type genetically-encoded calcium indicators. PLoS One 3, e1796.
87. Maroof, A.M., Brown, K., Shi, S.H., Studer, L., and Anderson, S.A. (2010). Prospective isolation of cortical interneuron precursors from mouse embryonic stem cells. J Neurosci 30, 4667-4675.
88. Mazzocchi-Jones, D., Dobrossy, M., and Dunnett, S.B. (2009). Embryonic striatal grafts restore bi-directional synaptic plasticity in a rodent model of Huntington's disease. Eur J Neurosci 30, 2134-2142.
89. Micheva, K.D., and Smith, S.J. (2007). Array tomography: a new tool for imaging the molecular architecture and ultrastructure of neural circuits. Neuron 55, 25-36.
90. Miller, B.R., Walker, A.G., Barton, S.J., and Rebec, G.V. (2011). Dysregulated Neuronal Activity Patterns Implicate Corticostriatal Circuit Dysfunction in Multiple Rodent Models of Huntington's Disease. Front Syst Neurosci 5, 26.
91. Miyamichi, K., Amat, F., Moussavi, F., Wang, C., Wickersham, I., Wall, N.R., Taniguchi, H., Tasic, B., Huang, Z.J., He, Z., et al. (2011). Cortical representations of olfactory input by transsynaptic tracing. Nature 472, 191-196.
92. Miyashita, T., and Rockland, K.S. (2007). GABAergic projections from the hippocampus to the retrosplenial cortex in the rat. Eur J Neurosci 26, 1193-1204.
93. Moon, J.S., Lee, H.S., Kang, J., Park, J., Leung, A., Hong, S., Chung, S., and Kim, K.S. (2012). Stem cell grafting improves both motor and cognitive impairments in a genetic model of Parkinson's disease, the aphakia mouse. Cell Transplant.
94. Moviglia, G.A., Moviglia-Brandolino, M.T., Varela, G.S., Albanese, G., Piccone, S., Echegaray, G., Martinez, G., Blasseti, N., Farias, J., Farina, P., et al. (2012). Feasibility, safety, and preliminary proof of principles of autologous neural stem cell treatment combined with T-cell vaccination for ALS patients. Cell Transplant 21 Suppl 1, S57-S63.
95. Muller, U., Reuter, M., Hermann, W., and Gertz, H.J. (2002). [Levodopa dependency in Parkinson's disease: case report and review]. Nervenarzt 73, 887-891.
96. Muneton-Gomez, V.C., Doncel-Perez, E., Fernandez, A.P., Serrano, J., Pozo-Rodrigalvarez, A., Vellosillo-Huerta, L., Taylor, J.S., Cardona-Gomez, G.P., Nieto-Sampedro, M., and Martinez-Murillo, R. (2012). Neural differentiation of transplanted neural stem cells in a rat model of striatal lacunar infarction: light and electron microscopic observations. Front Cell Neurosci 6, 30.
97. Nagai, N., Kawao, N., Okada, K., Okumoto, K., Teramura, T., Ueshima, S., Umemura, K., and Matsuo, O. (2010). Systemic transplantation of embryonic stem cells accelerates brain lesion decrease and angiogenesis. Neuroreport 21, 575-579.
98. Nagel, G., Szellas, T., Kateriya, S., Adeishvili, N., Hegemann, P., and Bamberg, E. (2005). Channelrhodopsins: directly light-gated cation channels. Biochem Soc Trans 33, 863-866.
99. Neely, M.D., Stanwood, G.D., and Deutch, A.Y. (2009). Combination of diOlistic labeling with retrograde tract tracing and immunohistochemistry. J Neurosci Methods 184, 332-336.
100. Niclis, J., Trounson, A.O., Dottori, M., Ellisdon, A., Bottomley, S.P., Verlinsky, Y., and Cram, D. (2009). Human embryonic stem cell models of Huntington disease. Reprod Biomed Online 19, 106-113.
101. Nilsson, M., Perfilieva, E., Johansson, U., Orwar, O., and Eriksson, P.S. (1999). Enriched environment increases neurogenesis in the adult rat dentate gyrus and improves spatial memory. J Neurobiol 39, 569-578.
102. Noebels, J.R., Avoli, M., Rogawski, M.A., Olsen, R.W., and Delgado-Escueta, A.V. (2012). Jasper's Basic Mechanism of the Epilepsies.
103. Nolte, M.W., Loscher, W., Herden, C., Freed, W.J., and Gernert, M. (2008). Benefits and risks of intranigral transplantation of GABA-producing cells subsequent to the establishment of kindlinginduced seizures. Neurobiol Dis 31, 342-354.
104. Noutel, J., Hong, Y.K., Leu, B., Kang, E., and Chen, C. (2011). Experience-dependent retinogeniculate synapse remodeling is abnormal in MeCP2-deficient mice. Neuron 70, 35-42.
105. Okita, K., Nakagawa, M., Hyenjong, H., Ichisaka, T., and Yamanaka, S. (2008). Generation of mouse induced pluripotent stem cells without viral vectors. Science 322, 949-953.
106. Ooi, L., Sidhu, K., Poljak, A., Sutherland, G., O'Connor, M.D., Sachdev, P., and Munch, G. (2012). Induced pluripotent stem cells as tools for disease modelling and drug discovery in Alzheimer's disease. J Neural Transm.
107. Parsons, X.H., Teng, Y.D., Parsons, J.F., Snyder, E.Y., Smotrich, D.B., and Moore, D.A. (2011). Efficient derivation of human cardiac precursors and cardiomyocytes from pluripotent human embryonic stem cells with small molecule induction. J Vis Exp, e3274.
108. Pedersen, S.W., Clausen, J., and Gregerslund, M.M. (2012). Practical Guidance on How to Handle Levodopa/Carbidopa Intestinal Gel Therapy of Advanced PD in a Movement Disorder Clinic. Open Neurol J 6, 37-50.
109. Petit, I., Kesner, N.S., Karry, R., Robicsek, O., Aberdam, E., Muller, F.J., Aberdam, D., and Ben-Shachar, D. (2012). Induced pluripotent stem cells from hair follicles as a cellular model for neurodevelopmental disorders. Stem Cell Res 8, 134-140.
110. Petreanu, L., Huber, D., Sobczyk, A., and Svoboda, K. (2007). Channelrhodopsin-2-assisted circuit mapping of long-range callosal projections. Nat Neurosci 10, 663-668.
111. Pfisterer, U., Kirkeby, A., Torper, O., Wood, J., Nelander, J., Dufour, A., Bjorklund, A., Lindvall, O., Jakobsson, J., and Parmar, M. (2011). Direct conversion of human fibroblasts to dopaminergic neurons. Proc Natl Acad Sci U S A 108, 10343-10348.
112. Pologruto, T.A., Yasuda, R., and Svoboda, K. (2004). Monitoring neural activity and [Ca2+] with genetically encoded Ca2+ indicators. J Neurosci 24, 9572-9579.
113. Pun, R.Y., Rolle, I.J., Lasarge, C.L., Hosford, B.E., Rosen, J.M., Uhl, J.D., Schmeltzer, S.N., Faulkner, C., Bronson, S.L., Murphy, B.L., et al. (2012). Excessive Activation of mTOR in Postnatally Generated Granule Cells Is Sufficient to Cause Epilepsy. Neuron 75, 1022-1034.
114. Pustavoitau, A., Bhardwaj, A., and Stevens, R. (2011). Neurological complications of transplantation. J Intensive Care Med 26, 209-222.
115. Ramamoorthi, K., and Lin, Y. (2011). The contribution of GABAergic dysfunction to neuro-developmental disorders. Trends Mol Med 17, 452-462.
116. Ring, K.L., Tong, L.M., Balestra, M.E., Javier, R., Andrews-Zwilling, Y., Li, G., Walker, D., Zhang, W.R., Kreitzer, A.C., and Huang, Y. (2012). Direct reprogramming of mouse and human fibroblasts into multipotent neural stem cells with a single factor. Cell Stem Cell 11, 100-109.
117. Rochefort, C., Gheusi, G., Vincent, J.D., and Lledo, P.M. (2002). Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J Neurosci 22, 2679-2689.
118. Rochefort, C., and Lledo, P.M. (2005). Short-term survival of newborn neurons in the adult olfactory bulb after exposure to a complex odor environment. Eur J Neurosci 22, 2863-2870.
119. Rochester, L., Yarnall, A.J., Baker, M.R., David, R.V., Lord, S., Galna, B., and Burn, D.J. (2012). Cholinergic dysfunction contributes to gait disturbance in early Parkinson's disease. Brain 135, 2779-2788.
120. Rossetti, F., Rodrigues, M.C., Marroni, S.S., Fernandes, A., Foresti, M.L., Romcy-Pereira, R.N., de Araujo, D.B., and Garcia-Cairasco, N. (2012). Behavioral and EEG effects of GABAergic manipulation of the nigro-tectal pathway in the Wistar audiogenic rat (WAR) strain II: an EEG wavelet analysis and retrograde neuronal tracer approach. Epilepsy Behav 24, 391-398.
121. Salti, A., Nat, R., Neto, S., Puschban, Z., Wenning, G., and Dechant, G. (2012). Expression of Early Developmental Markers Predicts the Efficiency of Embryonic Stem Cell Differentiation into Midbrain Dopaminergic Neurons. Stem Cells Dev.
122. Seminatore, C., Polentes, J., Ellman, D., Kozubenko, N., Itier, V., Tine, S., Tritschler, L., Brenot, M., Guidou, E., Blondeau, J., et al. (2010). The postischemic environment differentially impacts teratoma or tumor formation after transplantation of human embryonic stem cell-derived neural progenitors. Stroke 41, 153-159.
123. Shehab, S., McGonigle, D., Hughes, D.I., Todd, A.J., and Redgrave, P. (2005). Anatomical evidence for an anticonvulsant relay in the rat ventromedial medulla. Eur J Neurosci 22, 1431-1444.
124. Slimko, E. M., McKinney, S., Anderson, D. J., Davidson, N., and Lester, H. A. (2002). Selective electrical silencing of mammalian neuron in vitro by the use of invertebrate ligand-gated chloride channels. J Neurosci 22(17), 7373-7379.
125. Soldner, F., Laganiere, J., Cheng, A.W., Hockemeyer, D., Gao, Q., Alagappan, R., Khurana, V., Golbe, L.I., Myers, R.H., Lindquist, S., et al. (2011). Generation of isogenic pluripotent stem cells differing exclusively at two early onset Parkinson point mutations. Cell 146, 318-331.
126. Song, J., Lee, S.T., Kang, W., Park, J.E., Chu, K., Lee, S.E., Hwang, T., Chung, H., and Kim, M. (2007). Human embryonic stem cell-derived neural precursor transplants attenuate apomorphine induced rotational behavior in rats with unilateral quinolinic acid lesions. Neurosci Lett 423, 58-61.
127. Steinbeck, J.A., Koch, P., Derouiche, A., and Brustle, O. (2012). Human embryonic stem cell derived neurons establish region-specific, long-range projections in the adult brain. Cell Mol Life Sci 69, 461-470.
128. Stevens, J.K., McGuire, B.A., and Sterling, P. (1980). Toward a functional architecture of the retina: serial reconstruction of adjacent ganglion cells. Science 207, 317-319.
129. Swartling, F.J., Savov, V., Persson, A.I., Chen, J., Hackett, C.S., Northcott, P.A., Grimmer, M.R., Lau, J., Chesler, L., Perry, A., et al. (2012). Distinct neural stem cell populations give rise to disparate brain tumors in response to N-MYC. Cancer Cell 21, 601-613.
130. Takahashi, K., Tanabe, K., Ohnuki, M., Narita, M., Ichisaka, T., Tomoda, K., and Yamanaka, S. (2007). Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861-872.
131. Takahashi, K., and Yamanaka, S. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676.
132. Tan, E.M., Yamaguchi, Y., Horwitz, G.D., Gosgnach, S., Lein, E.S., Goulding, M., Albright, T.D., and Callaway, E.M. (2006). Selective and quickly reversible inactivation of mammalian neurons in vivo using the Drosophila allatostatin receptor. Neuron 51, 157-170.
133. Tang, H.L., Sun, H.P., Wu, X., Sha, H.Y., Feng, X.Y., and Zhu, J.H. (2011). Detection of neural stem cells function in rats with traumatic brain injury by manganese-enhanced magnetic resonance imaging. Chin Med J (Engl) 124, 1848-1853.
134. Thier, M., Worsdorfer, P., Lakes, Y.B., Gorris, R., Herms, S., Opitz, T., Seiferling, D., Quandel, T., Hoffmann, P., Nothen, M.M., et al. (2012). Direct conversion of fibroblasts into stably expandable neural stem cells. Cell Stem Cell 10, 473-479.
135. Tian, L., Hires, S.A., Mao, T., Huber, D., Chiappe, M.E., Chalasani, S.H., Petreanu, L., Akerboom, J., McKinney, S.A., Schreiter, E.R., et al. (2009). Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat Methods 6, 875-881.
136. Tonnesen, J., Parish, C.L., Sorensen, A.T., Andersson, A., Lundberg, C., Deisseroth, K., Arenas, E., Lindvall, O., and Kokaia, M. (2011). Functional integration of grafted neural stem cell derived dopaminergic neurons monitored by optogenetics in an in vitro Parkinson model. PLoS One 6, e17560.
137. Ugolini, G. (2010). Advances in viral transneuronal tracing. J Neurosci Methods 194, 2-20.
138. Ugolini, G. (2011). Rabies virus as a transneuronal tracer of neuronal connections. Adv Virus Res 79, 165-202.
139. van Praag, H., Christie, B.R., Sejnowski, T.J., and Gage, F.H. (1999). Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci U S A 96, 13427-13431.
140. Vierbuchen, T., Ostermeier, A., Pang, Z.P., Kokubu, Y., Sudhof, T.C., and Wernig, M. (2010). Direct conversion of fibroblasts to functional neurons by defined factors. Nature 463, 1035-1041.
141. Wang, T.Y., Forsythe, J.S., Nisbet, D.R., and Parish, C.L. (2012). Promoting engraftment of transplanted neural stem cells/progenitors using biofunctionalised electrospun scaffolds. Biomaterials.
142. Wang, Z., Maia, T.V., Marsh, R., Colibazzi, T., Gerber, A., and Peterson, B.S. (2011). The neural circuits that generate tics in Tourette's syndrome. Am J Psychiatry 168, 1326-1337.
143. Weaver, F.M., Stroupe, K.T., Cao, L., Holloway, R.G., Vickrey, B.G., Simuni, T., Hendricks, A., and Ippolito, D. (2012). Parkinson's disease medication use and costs following deep brain stimulation. Mov Disord 27, 1398-1403.
144. Wehr, M., Hostick, U., Kyweriga, M., Tan, A., Weible, A.P., Wu, H., Wu, W., Callaway, E.M., and Kentros, C. (2009). Transgenic silencing of neurons in the mammalian brain by expression of the allatostatin receptor (AlstR). J Neurophysiol 102, 2554-2562.
145. Wesson, D.W., Nixon, R.A., Levy, E., and Wilson, D.A. (2011). Mechanisms of neural and behavioral dysfunction in Alzheimer's disease. Mol Neurobiol 43, 163-179.
146. Wickersham, I.R., Finke, S., Conzelmann, K.K., and Callaway, E.M. (2007a). Retrograde neuronal tracing with a deletion-mutant rabies virus. Nat Methods 4, 47-49.
147. Wickersham, I.R., Lyon, D.C., Barnard, R.J., Mori, T., Finke, S., Conzelmann, K.K., Young, J.A., and Callaway, E.M. (2007b). Monosynaptic restriction of transsynaptic tracing from single, genetically targeted neurons. Neuron 53, 639-647.
148. Wulff, P., and Arenkiel, B.R. (2012). Chemical genetics: receptor-ligand pairs for rapid manipulation of neuronal activity. Curr Opin Neurobiol 22, 54-60.
149. Yagi, T., Kosakai, A., Ito, D., Okada, Y., Akamatsu, W., Nihei, Y., Nabetani, A., Ishikawa, F., Arai, Y., Hirose, N., et al. (2012). Establishment of induced pluripotent stem cells from centenarians for neurodegenerative disease research. PLoS One 7, e41572.
150. Yamaguchi, M., and Mori, K. (2005). Critical period for sensory experience-dependent survival of newly generated granule cells in the adult mouse olfactory bulb. Proc Natl Acad Sci U S A 102, 9697-9702.
151. Yamanaka, S. (2009). A fresh look at iPS cells. Cell 137, 13-17.
152. Yang, D., Zhang, Z.J., Oldenburg, M., Ayala, M., and Zhang, S.C. (2008). Human embryonic stem cell-derived dopaminergic neurons reverse functional deficit in parkinsonian rats. Stem Cells 26, 55-63.
153. Yusa, K., Rashid, S.T., Strick-Marchand, H., Varela, I., Liu, P.Q., Paschon, D.E., Miranda, E., Ordonez, A., Hannan, N.R., Rouhani, F.J., et al. (2011). Targeted gene correction of alpha1-antitrypsin deficiency in induced pluripotent stem cells. Nature 478, 391-394.
154. Zhang, F., Aravanis, A.M., Adamantidis, A., de Lecea, L., and Deisseroth, K. (2007a). Circuitbreakers: optical technologies for probing neural signals and systems. Nat Rev Neurosci 8, 577-581.
155. Zhang, F., Wang, L.P., Brauner, M., Liewald, J.F., Kay, K., Watzke, N., Wood, P.G., Bamberg, E., Nagel, G., Gottschalk, A., et al. (2007b). Multimodal fast optical interrogation of neural circuitry. Nature 446, 633-639.
156. Zhang, J., Giesert, F., Kloos, K., Vogt Weisenhorn, D.M., Aigner, L., Wurst, W., and Couillard-Despres, S. (2010). A powerful transgenic tool for fate mapping and functional analysis of newly generated neurons. BMC Neurosci 11, 158.
157. Zhu, J.M., Zhao, Y.Y., Chen, S.D., Zhang, W.H., Lou, L., and Jin, X. (2011). Functional recovery after transplantation of neural stem cells modified by brain-derived neurotrophic factor in rats with cerebral ischaemia. J Int Med Res 39, 488-498.