Dysregulation of astrocyte extracellular signaling in Costello syndrome

Science Translational Medicine

Volumn 7, Issue 286, 2015, Pages

  Krencik, Robert ^a   Hokanson, Kenton C ^b   Narayan, Aditi R ^a   Dvornik, Jill ^a   Rooney, Gemma E ^a   Rauen, Katherine A ^c   Weiss, Lauren A ^b   Rowitch, David H ^a   Ullian, Erik M ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN FARNESYLTRANSFERASE INHIBITOR; PROTEOGLYCAN; RAS PROTEIN; TRANSCRIPTION FACTOR SLUG; SNAI2 PROTEIN, HUMAN; SNAI2 PROTEIN, MOUSE; SNAI2 PROTEIN, RAT; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SNAIL;

ARTICLE; ASTROCYTE; CELL MATURATION; CONTROLLED STUDY; COSTELLO SYNDROME; EXTRACELLULAR MATRIX; EXTRACELLULAR SPACE; HUMAN; HUMAN CELL; HYPERPLASIA; IN VITRO STUDY; INTELLECTUAL IMPAIRMENT; INTERNEURON; NERVE CELL DIFFERENTIATION; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; WILD TYPE; ANIMAL; CELL DIFFERENTIATION; CELL LINE; CYTOLOGY; DNA MICROARRAY; GENE EXPRESSION REGULATION; GENETICS; GENOTYPE; HIPPOCAMPUS; INDUCED PLURIPOTENT STEM CELL; MASS SPECTROMETRY; METABOLISM; MOUSE; MUTATION; NERVE CELL; NERVE CELL PLASTICITY; ONCOGENE RAS; PHENOTYPE; TRANSGENIC MOUSE;

ANIMALS; ASTROCYTES; CELL DIFFERENTIATION; CELL LINE; COSTELLO SYNDROME; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; GENES, RAS; GENOTYPE; HIPPOCAMPUS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MASS SPECTROMETRY; MICE; MICE, TRANSGENIC; MUTATION; NEURONAL PLASTICITY; NEURONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; PROTEOGLYCANS; RAS PROTEINS; SIGNAL TRANSDUCTION; SNAIL FAMILY TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS;

EID: 84928974662     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aaa5645     Document Type: Article

References (84)

1. G. Perea, M. Sur, A. Araque, Neuron-glia networks: Integral gear of brain function. Front. Cell. Neurosci. 8, 378 (2014).
2. N. J. Allen, Astrocyte regulation of synaptic behavior. Annu. Rev. Cell Dev. Biol. 30, 439-463 (2014).
3. A. V. Molofsky, R. Krencik, E. M. Ullian, H.-H. Tsai, B. Deneen, W. D. Richardson, B. A. Barres, D. H. Rowitch, Astrocytes and disease: A neurodevelopmental perspective. Genes Dev. 26, 891-907 (2012).
4. A. Verkhratsky, M. V. Sofroniew, A. Messing, N. C. deLanerolle, D. Rempe, J. J. Rodríguez, M. Nedergaard, Neurological diseases as primary gliopathies: A reassessment of neurocentrism. ASN Neuro. 4, e00082 (2012).
5. H. Y. Zoghbi, M. F. Bear, Synaptic dysfunction in neurodevelopmental disorders associated with autism and intellectual disabilities. Cold Spring Harb. Perspect. Biol. 4, a009886 (2012).
6. A. McGee, G. Li, Z. Lu, S. Qiu, Convergent synaptic and circuit substrates underlying autism genetic risks. Front. Biol. 9, 137-150 (2014).
7. A. E. Takesian, T. K. Hensch, Balancing plasticity/stability across brain development. Prog. Brain Res. 207, 3-34 (2013).
8. W.-S. Chung, L. E. Clarke, G. X. Wang, B. K. Stafford, A. Sher, C. Chakraborty, J. Joung, L. C. Foo, A. Thompson, C. Chen, S. J. Smith, B. A. Barres, Astrocytes mediate synapse elimination through MEGF10 and MERTK pathways. Nature 504, 394-400 (2013).
9. S. Wiese, M. Karus, A. Faissner, Astrocytes as a source for extracellular matrix molecules and cytokines. Front. Pharmacol. 3, 120 (2012).
10. R. Kanski, M. E. van Strien, P. van Tijn, E. M. Hol, A star is born: New insights into the mechanism of astrogenesis. Cell. Mol. Life Sci. 71, 433-447 (2014).
11. S. A. Sloan, B. A. Barres, Mechanisms of astrocyte development and their contributions to neurodevelopmental disorders. Curr. Opin. Neurobiol. 27C, 75-81 (2014).
12. J. Stipursky, T. C. Spohr, V. O. Sousa, F. C. A. Gomes, Neuron-astroglial interactions in cellfate commitment and maturation in the central nervous system. Neurochem. Res. 37, 2402-2418 (2012).
13. F. Zeidán-Chuliá, A. B. Salmina, N. A. Malinovskaya, M. Noda, A. Verkhratsky, J. C. F. Moreira, The glial perspective of autism spectrum disorders. Neurosci. Biobehav. Rev. 38, 160-172 (2014).
14. R. Krencik, E. M. Ullian, A cellular star atlas: Using astrocytes from human pluripotent stem cells for disease studies. Front. Cell. Neurosci. 7, 25 (2013).
15. R. Krencik, S.-C. Zhang, Stem cell neural differentiation: A model for chemical biology. Curr. Opin. Chem. Biol. 10, 592-597 (2006).
16. T. Kondo, M. Asai, K. Tsukita, Y. Kutoku, Y. Ohsawa, Y. Sunada, K. Imamura, N. Egawa, N. Yahata, K. Okita, K. Takahashi, I. Asaka, T. Aoi, A. Watanabe, K. Watanabe, C. Kadoya, R. Nakano, D. Watanabe, K. Maruyama, O. Hori, S. Hibino, T. Choshi, T. Nakahata, H. Hioki, T. Kaneko, M. Naitoh, K. Yoshikawa, S. Yamawaki, S. Suzuki, R. Hata, S. Ueno, T. Seki, K. Kobayashi, T. Toda, K. Murakami, K. Irie, W. L. Klein, H. Mori, T. Asada, R. Takahashi, N. Iwata, S. Yamanaka, H. Inoue, Modeling Alzheimer's disease with iPSCs reveals stress phenotypes associated with intracellular Ab and differential drug responsiveness. Cell Stem Cell 12, 487-496 (2013).
17. A. Serio, B. Bilican, S. J. Barmada, D. M. Ando, C. Zhao, R. Siller, K. Burr, G. Haghi, D. Story, A. L. Nishimura, M. A. Carrasco, H. P. Phatnani, C. Shum, I. Wilmut, T. Maniatis, C. E. Shaw, S. Finkbeiner, S. Chandran, Astrocyte pathology and the absence of non-cell autonomy in an induced pluripotent stem cell model of TDP-43 proteinopathy. Proc. Natl. Acad. Sci. U.S.A. 110, 4697-4702 (2013).
18. C. Chen, P. Jiang, H. Xue, S. E. Peterson, H. T. Tran, A. E. McCann, M. M. Parast, S. Li, D. E. Pleasure, L. C. Laurent, J. F. Loring, Y. Liu, W. Deng, Role of astroglia in Down's syndrome revealed by patient-derived human-induced pluripotent stem cells. Nat. Commun. 5, 4430 (2014).
19. E. C. Williams, X. Zhong, A.Mohamed, R. Li, Y. Liu, Q. Dong, G. E. Ananiev, J. C.Mok, B. R. Lin, J. Lu, C. Chiao, R. Cherney, H. Li, S.-C. Zhang, Q. Chang, Mutant astrocytes differentiated from Rett syndrome patients-specific iPSCs have adverse effects on wild type neurons. Hum. Mol. Genet. 23, 2968-2980 (2014).
20. W. E. Tidyman, K. A. Rauen, The RASopathies: Developmental syndromes of Ras/MAPK pathway dysregulation. Curr. Opin. Genet. Dev. 19, 230-236 (2009).
21. M. Zenker, Clinical manifestations of mutations in RAS and related intracellular signal transduction factors. Curr. Opin. Pediatr. 23, 443-451 (2011).
22. A. S. Gauthier, O. Furstoss, T. Araki, R. Chan, B. G. Neel, D. R. Kaplan, F. D. Miller, Control of CNS cell-fate decisions by SHP-2 and its dysregulation in Noonan syndrome. Neuron 54, 245-262 (2007).
23. B. Hegedus, B. Dasgupta, J. E. Shin, R. J. Emnett, E. K. Hart-Mahon, L. Elghazi, E. Bernal-Mizrachi, D. H. Gutmann, Neurofibromatosis-1 regulates neuronal and glial cell differentiation from neuroglial progenitors in vivo by both cAMP-and Ras-dependent mechanisms. Cell Stem Cell 1, 443-457 (2007).
24. A. Paquin, C. Hordo, D. R. Kaplan, F. D. Miller, Costello syndrome H-Ras alleles regulate cortical development. Dev. Biol. 330, 440-451 (2009).
25. A.-C. Tien, H.-H. Tsai, A. V. Molofsky, M. McMahon, L. C. Foo, A. Kaul, J. D. Dougherty, N. Heintz, D. H. Gutmann, B. A. Barres, D. H. Rowitch, Regulated temporal-spatial astrocyte precursor cell proliferation involves BRAF signalling in mammalian spinal cord. Development 139, 2477-2487 (2012).
26. X. Li, J. M. Newbern, Y. Wu, M. Morgan-Smith, J. Zhong, J. Charron, W. D. Snider, MEK is a key regulator of gliogenesis in the developing brain. Neuron 75, 1035-1050 (2012).
27. Y. Zhu, T. Harada, L. Liu, M. E. Lush, F. Guignard, C. Harada, D. K. Burns, M. L. Bajenaru, D. H. Gutmann, L. F. Parada, Inactivation of NF1 in CNS causes increased glial progenitor proliferation and optic glioma formation. Development 132, 5577-5588 (2005).
28. B. Adviento, I. L. Corbin, F. Widjaja, G. Desachy, N. Enrique, T. Rosser, S. Risi, E. J. Marco, R. L. Hendren, C. E. Bearden, K. A. Rauen, L. A. Weiss, Autism traits in the RASopathies. J. Med. Genet. 51, 10-20 (2013).
29. C. P. Kratz, C. M. Niemeyer, M. Zenker, An unexpected new role of mutant Ras: Perturbation of human embryonic development. J. Mol. Med. 85, 227-235 (2007).
30. P. Alfieri, G. Piccini, C. Caciolo, F. Perrino, M. L. Gambardella, M. Mallardi, L. Cesarini, C. Leoni, D. Leone, C. Fossati, A. Selicorni, M. C. Digilio, M. Tartaglia, E. Mercuri, G. Zampino, S. Vicari, Behavioral profile in RASopathies. Am. J. Med. Genet. A 164A, 934-942 (2014).
31. K. W. Gripp, E. Hopkins, D. Doyle, W. B. Dobyns, High incidence of progressive postnatal cerebellar enlargement in Costello syndrome: Brain overgrowth associated with HRAS mutations as the likely cause of structural brain and spinal cord abnormalities. Am. J. Med. Genet. A 152A, 1161-1168 (2010).
32. J. M. Costello, A new syndrome: Mental subnormality and nasal papillomata. Aust. Paediatr. J. 13, 114-118 (1977).
33. K. W. Gripp, A. E. Lin, Costello syndrome: A Ras/mitogen activated protein kinase pathway syndrome (rasopathy) resulting from HRAS germline mutations. Genet. Med. 14, 285-292 (2012).
34. S. Schubbert, K. Shannon, G. Bollag, Hyperactive Ras in developmental disorders and cancer. Nat. Rev. Cancer 7, 295-308 (2007).
35. J. Downward, Targeting RAS signalling pathways in cancer therapy. Nat. Rev. Cancer 3, 11-22 (2003).
36. G. Zampino, F. Pantaleoni, C. Carta, G. Cobellis, I. Vasta, C. Neri, E. A. Pogna, E. De Feo, A. Delogu, A. Sarkozy, F. Atzeri, A. Selicorni, K. A. Rauen, C. S. Cytrynbaum, R. Weksberg, B. Dallapiccola, A. Ballabio, B. D. Gelb, G. Neri, M. Tartaglia, Diversity, parental germline origin, and phenotypic spectrum of de novo HRAS missense changes in Costello syndrome. Hum. Mutat. 28, 265-272 (2007).
37. K. Okita, Y. Matsumura, Y. Sato, A. Okada, A. Morizane, S. Okamoto, H. Hong, M. Nakagawa, K. Tanabe, K. Tezuka, T. Shibata, T. Kunisada, M. Takahashi, J. Takahashi, H. Saji, S. Yamanaka, A more efficient method to generate integration-free human iPS cells. Nat. Methods 8, 409-412 (2011).
38. R. Krencik, J. P. Weick, Y. Liu, Z.-J. Zhang, S.-C. Zhang, Specification of transplantable astroglial subtypes from human pluripotent stem cells. Nat. Biotechnol. 29, 528-534 (2011).
39. R. Krencik, S.-C. Zhang, Directed differentiation of functional astroglial subtypes from human pluripotent stem cells. Nat. Protoc. 6, 1710-1717 (2011).
40. A. A. Sosunov, X. Wu, N. M. Tsankova, E. Guilfoyle, G. M. McKhann II, J. E. Goldman, Phenotypic heterogeneity and plasticity of isocortical and hippocampal astrocytes in the human brain. J. Neurosci. 34, 2285-2298 (2014).
41. C. C. Sprenger, S. R. Plymate, M. J. Reed, Aging-related alterations in the extracellular matrix modulate the microenvironment and influence tumor progression. Int. J. Cancer 127, 2739-2748 (2010).
42. C. Santoriello, G. Deflorian, F. Pezzimenti, K. Kawakami, L. Lanfrancone, F. d'Adda di Fagagna, M. Mione, Expression of H-RASV12 in a zebrafish model of Costello syndrome causes cellular senescence in adult proliferating cells. Dis. Model. Mech. 2, 56-67 (2009).
43. T. Niihori, Y. Aoki, N. Okamoto, K. Kurosawa, H. Ohashi, S. Mizuno, H. Kawame, J. Inazawa, T. Ohura, H. Arai, S. Nabatame, K. Kikuchi, Y. Kuroki, M. Miura, T. Tanaka, A. Ohtake, I. Omori, K. Ihara, H. Mabe, K. Watanabe, S. Niijima, E. Okano, H. Numabe, Y. Matsubara, HRAS mutants identified in Costello syndrome patients can induce cellular senescence: Possible implications for the pathogenesis of Costello syndrome. J. Hum. Genet. 56, 707-715 (2011).
44. M. M. Das, C. N. Svendsen, Astrocytes show reduced support of motor neurons with aging that is accelerated in a rodent model of ALS. Neurobiol. Aging 36, 1130-1139 (2015).
45. X. Chen, N. Mitsutake, K. LaPerle, N. Akeno, P. Zanzonico, V. A. Longo, S. Mitsutake, E. T. Kimura, H. Geiger, E. Santos, H. G. Wendel, A. Franco, J. A. Knauf, J. A. Fagin, Endogenous expression of HrasG12V induces developmental defects and neoplasms with copy number imbalances of the oncogene. Proc. Natl. Acad. Sci. U.S.A. 106, 7979-7984 (2009).
46. I. Imayoshi, R. Kageyama, bHLH factors in self-renewal, multipotency, and fate choice of neural progenitor cells. Neuron 82, 9-23 (2014).
47. E. C. Lerner, Y. Qian, M. A. Blaskovich, R. D. Fossum, A. Vogt, J. Sun, A. D. Cox, C. J. Der, A. D. Hamilton, S. M. Sebti, Ras CAAX peptidomimetic FTI-277 selectively blocks oncogenic Ras signaling by inducing cytoplasmic accumulation of inactive Ras-Raf complexes. J. Biol. Chem. 270, 26802-26806 (1995).
48. D. Anastassiou, V. Rumjantseva, W. Cheng, J. Huang, P. D. Canoll, D. J. Yamashiro, J. J. Kandel, Human cancer cells express Slug-based epithelial-mesenchymal transition gene expression signature obtained in vivo. BMC Cancer 11, 529 (2011).
49. H. W. Yang, L. G. Menon, P. M. Black, R. S. Carroll, M. D. Johnson, SNAI2/Slug promotes growth and invasion in human gliomas. BMC Cancer 10, 301 (2010).
50. Y. Wang, V. N. Ngo, M. Marani, Y. Yang, G. Wright, L. M. Staudt, J. Downward, Critical role for transcriptional repressor Snail2 in transformation by oncogenic RAS in colorectal carcinoma cells. Oncogene 29, 4658-4670 (2010).
51. P. B. Gupta, C. Kuperwasser, J.-P. Brunet, S. Ramaswamy, W.-L. Kuo, J. W. Gray, S. P. Naber, R. A. Weinberg, The melanocyte differentiation program predisposes to metastasis after neoplastic transformation. Nat. Genet. 37, 1047-1054 (2005).
52. N. J. Allen, M. L. Bennett, L. C. Foo, G. X. Wang, C. Chakraborty, S. J. Smith, B. A. Barres, Astrocyte glypicans 4 and 6 promote formation of excitatory synapses via GluA1 AMPA receptors. Nature 486, 410-414 (2012).
53. K. S. Christopherson, E. M. Ullian, C. C. Stokes, C. E. Mullowney, J. W. Hell, A. Agah, J. Lawler, D. F. Mosher, P. Bornstein, B. A. Barres, Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 120, 421-433 (2005).
54. H. Kucukdereli, N. J. Allen, A. T. Lee, A. Feng, M. I. Ozlu, L. M. Conatser, C. Chakraborty, G. Workman, M. Weaver, E. H. Sage, B. A. Barres, C. Eroglu, Control of excitatory CNS synaptogenesis by astrocyte-secreted proteins Hevin and SPARC. Proc. Natl. Acad. Sci. U.S.A. 108, E440-E449 (2011).
55. J. A. Dowell, J. A. Johnson, L. Li, Identification of astrocyte secreted proteins with a combination of shotgun proteomics and bioinformatics. J. Proteome Res. 8, 4135-4343 (2009).
56. K. Buysse, M. Riemersma, G. Powell, J. van Reeuwijk, D. Chitayat, T. Roscioli, E.-J. Kamsteeg, C. van den Elzen, E. van Beusekom, S. Blaser, R. Babul-Hirji, W. Halliday, G. J. Wright, D. L. Stemple, Y.-Y. Lin, D. J. Lefeber, H. van Bokhoven, Missense mutations in b-1,3-N-acetylglucosaminyltransferase 1 (B3GNT1) cause Walker-Warburg syndrome. Hum. Mol. Genet. 22, 1746-1754 (2013).
57. M. P. Daniels, The role of agrin in synaptic development, plasticity and signaling in the central nervous system. Neurochem. Int. 61, 848-853 (2012).
58. T. Pizzorusso, P. Medini, N. Berardi, S. Chierzi, J. W. Fawcett, L. Maffei, Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298, 1248-1251 (2002).
59. R. Frischknecht, C. I. Seidenbecher, Brevican: A key proteoglycan in the perisynaptic extracellular matrix of the brain. Int. J. Biochem. Cell Biol. 44, 1051-1054 (2012).
60. C. E. Bandtlow, D. R. Zimmermann, Proteoglycans in the developing brain: New conceptual insights for old proteins. Physiol. Rev. 80, 1267-1290 (2000).
61. A. Faissner, M. Pyka, M. Geissler, T. Sobik, R. Frischknecht, E. D. Gundelfinger, C. Seidenbecher, Contributions of astrocytes to synapse formation and maturation-Potential functions of the perisynaptic extracellular matrix. Brain Res. Rev. 63, 26-38 (2010).
62. Q. Ye, Q.-L. Miao, Experience-dependent development of perineuronal nets and chondroitin sulfate proteoglycan receptors in mouse visual cortex. Matrix Biol. 32, 352-363 (2013).
63. M. A. Anderson, Y. Ao, M. V. Sofroniew, Heterogeneity of reactive astrocytes. Neurosci. Lett. 565, 23-29 (2013).
64. J. E. Burda, M. V. Sofroniew, Reactive gliosis and the multicellular response to CNS damage and disease. Neuron 81, 229-248 (2014).
65. K. Kang, S.-W. Lee, J. E. Han, J. W. Choi, M.-R. Song, The complex morphology of reactive astrocytes controlled by fibroblast growth factor signaling. Glia 62, 1328-1344 (2014).
66. T. Stork, A. Sheehan, O. E. Tasdemir-Yilmaz, M. R. Freeman, Neuron-glia interactions through the Heartless FGF receptor signaling pathway mediate morphogenesis of Drosophila astrocytes. Neuron 83, 388-403 (2014).
67. L. B. Jakeman, K. E. Williams, B. Brautigam, In the presence of danger: The extracellular matrix defensive response to central nervous system injury. Neural Regen. Res. 9, 377-384 (2014).
68. L. E. Clarke, B. A. Barres, Emerging roles of astrocytes in neural circuit development. Nat. Rev. Neurosci. 14, 311-321 (2013).
69. L. Schaefer, R. M. Schaefer, Proteoglycans: From structural compounds to signaling molecules. Cell Tissue Res. 339, 237-246 (2010).
70. D. Wang, J. Fawcett, The perineuronal net and the control of CNS plasticity. Cell Tissue Res. 349, 147-160 (2012).
71. A. Derouiche, W. Härtig, K. Brauer, G. Brückner, Spatial relationship of lectin-labelled extracellular matrix and glutamine synthetase-immunoreactive astrocytes in rat cortical forebrain regions. J. Anat. 189 (Pt. 2), 363-372 (1996).
72. M. Klüppel, P. Samavarchi-Tehrani, K. Liu, J. L. Wrana, A. Hinek, C4ST-1/CHST11-controlled chondroitin sulfation interferes with oncogenic HRAS signaling in Costello syndrome. Eur. J. Hum. Genet. 20, 870-877 (2012).
73. A. Hinek, M. A. Teitell, L. Schoyer, W. Allen, K. W. Gripp, R. Hamilton, R. Weksberg, M. Klüppel, A. E. Lin, Myocardial storage of chondroitin sulfate-containing moieties in Costello syndrome patients with severe hypertrophic cardiomyopathy. Am. J. Med. Genet. A 133A, 1-12 (2005).
74. A. F. Goodwin, W. E. Tidyman, A. H. Jheon, A. Sharir, X. Zheng, C. Charles, J. A. Fagin, M. McMahon, T. G. Diekwisch, B. Ganss, K. A. Rauen, O. D. Klein, Abnormal Ras signaling in Costello syndrome (CS) negatively regulates enamel formation. Hum. Mol. Genet. 23, 682-692 (2014).
75. J. Yamada, T. Ohgomori, S. Jinno, Perineuronal nets affect parvalbumin expression in GABAergic neurons of the mouse hippocampus. Eur. J. Neurosci. 41, 368-378 (2015).
76. S. Miyata, H. Kitagawa, Mechanisms for modulation of neural plasticity and axon regeneration by chondroitin sulphate. J. Biochem. 157, 13-22 (2015).
77. N. Gogolla, A. E. Takesian, G. Feng, M. Fagiolini, T. K. Hensch, Sensory integration in mouse insular cortex reflects GABA circuit maturation. Neuron 83, 894-905 (2014).
78. E. Eggermann, P. Jonas, How the 'slow' Ca2+ buffer parvalbumin affects transmitter release in nanodomain-coupling regimes. Nat. Neurosci. 15, 20-22 (2012).
79. G. Perea, A. Yang, E. S. Boyden, M. Sur, Optogenetic astrocyte activation modulates response selectivity of visual cortex neurons in vivo. Nat. Commun. 5, 3262 (2014).
80. J. T. Davie, M. H. P. Kole, J. J. Letzkus, E. A. Rancz, N. Spruston, G. J. Stuart, M. Häusser, Dendritic patch-clamp recording. Nat. Protoc. 1, 1235-1247 (2006).
81. X. Opitz-Araya, A. Barria, Organotypic hippocampal slice cultures. J. Vis. Exp. e2462 (2011).
82. N. Gogolla, I. Galimberti, V. DePaola, P. Caroni, Staining protocol for organotypic hippocampal slice cultures. Nat. Protoc. 1, 2452-2456 (2006).
83. A. Winzeler, J. T. Wang, Purification and culture of retinal ganglion cells from rodents. Cold Spring Harb. Protoc. 2013, 643-652 (2013).
84. D. M. Ippolito, C. Eroglu, Quantifying synapses: An immunocytochemistry-based assay to quantify synapse number. J. Vis. Exp. 2270 (2010).