Cultured networks of excitatory projection neurons and inhibitory interneurons for studying human cortical neurotoxicity

Science Translational Medicine

Volumn 8, Issue 333, 2016, Pages

  Xu, Jin Chong ^a   Fan, Jing ^a   Wang, Xueqing ^a   Eacker, Stephen M ^a   Kam, Tae In ^a   Chen, Li ^a   Yin, Xiling ^a   Zhu, Juehua ^a,b   Chi, Zhikai ^a   Jiang, Haisong ^a   Chen, Rong ^a   Dawson, Ted M ^a   Dawson, Valina L ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MEDICAL SCHOOL OF NANJING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NITRIC OXIDE; FORKHEAD TRANSCRIPTION FACTOR; FOXG1 PROTEIN, HUMAN; GLUCOSE; N METHYLASPARTIC ACID; NERVE PROTEIN; NEUROTOXIN; OXYGEN; RETINOIC ACID; SONIC HEDGEHOG PROTEIN;

ARTICLE; CELL ISOLATION; CELL POPULATION; CONTROLLED STUDY; EMBRYO; HUMAN; HUMAN CELL; INTERNEURON; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NERVE CELL NECROSIS; NERVE CELL NETWORK; NEUROTOXICITY; PRIORITY JOURNAL; BIOLOGICAL MODEL; BRAIN CORTEX; CELL CULTURE; CELL DEATH; CELL DIFFERENTIATION; CELL LINE; CELL SEPARATION; CYTOLOGY; DEFICIENCY; DRUG EFFECTS; EMBRYONIC STEM CELL; INDUCED PLURIPOTENT STEM CELL; METABOLISM; NERVE CELL INHIBITION; NEURAL STEM CELL; SIGNAL TRANSDUCTION;

CELL DEATH; CELL DIFFERENTIATION; CELL LINE; CELL SEPARATION; CELLS, CULTURED; CEREBRAL CORTEX; EMBRYONIC STEM CELLS; FORKHEAD TRANSCRIPTION FACTORS; GLUCOSE; HEDGEHOG PROTEINS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; INTERNEURONS; MODELS, BIOLOGICAL; N-METHYLASPARTATE; NERVE NET; NERVE TISSUE PROTEINS; NEURAL INHIBITION; NEURAL STEM CELLS; NEUROTOXINS; NITRIC OXIDE; OXYGEN; SIGNAL TRANSDUCTION; TRETINOIN;

EID: 84963623377     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aad0623     Document Type: Article

References (60)

1. C. P. Wonders, S. A. Anderson, The origin and specification of cortical interneurons. Nat. Rev. Neurosci. 7, 687-696 (2006).
2. O. Marín, Interneuron dysfunction in psychiatric disorders. Nat. Rev. Neurosci. 13, 107-120 (2012).
3. S. Lodato, C. Rouaux, K. B. Quast, C. Jantrachotechatchawan, M. Studer, T. K. Hensch, P. Arlotta, Excitatory projection neuron subtypes control the distribution of local inhibitory interneurons in the cerebral cortex. Neuron 69, 763-779 (2011).
4. Y. Shi, P. Kirwan, J. Smith, H. P. Robinson, F. J. Livesey, Human cerebral cortex development from pluripotent stem cells to functional excitatory synapses. Nat. Neurosci. 15, 477-486, S1 (2012).
5. I. Espuny-Camacho, K. A. Michelsen, D. Gall, D. Linaro, A. Hasche, J. Bonnefont, C. Bali, D. Orduz, A. Bilheu, A. Herpoel, N. Lambert, N. Gaspard, S. Péron, S. N. Schiffmann, M. Giugliano, A. Gaillard, P. Vanderhaeghen, Pyramidal neurons derived from human pluripotent stem cells integrate efficiently into mouse brain circuits in vivo. Neuron 77, 440-456 (2013).
6. S. P. Paşca, T. Portmann, I. Voineagu, M. Yazawa, A. Shcheglovitov, A. M. Paşca, B. Cord, T. D. Palmer, S. Chikahisa, S. Nishino, J. A. Bernstein, J. Hallmayer, D. H. Geschwind, R. E. Dolmetsch, Using iPSC-derived neurons to uncover cellular phenotypes associated with Timothy syndrome. Nat. Med. 17, 1657-1662 (2011).
7. A. L. Goulburn, D. Alden, R. P. Davis, S. J. Micallef, E. S. Ng, Q. C. Yu, S. M. Lim, C.-L. Soh, D. A. Elliott, T. Hatzistavrou, J. Bourke, B. Watmuff, R. J. Lang, J. M. Haynes, C. W. Pouton, A. Giudice, A. O. Trounson, S. A. Anderson, E. G. Stanley, A. G. Elefanty, A targeted NKX2.1 human embryonic stem cell reporter line enables identification of human basal forebrain derivatives. Stem Cells 29, 462-473 (2011).
8. J.-E. Kim, M. L. O'Sullivan, C. A. Sanchez, M. Hwang, M. A. Israel, K. Brennand, T. J. Deerinck, L. S. B. Goldstein, F. H. Gage, M. H. Ellisman, A. Ghosh, Investigating synapse formation and function using human pluripotent stem cell-derived neurons. Proc. Natl. Acad. Sci. U.S.A. 108, 3005-3010 (2011).
9. X.-J. Li, X. Zhang, M. A. Johnson, Z.-B. Wang, T. Lavaute, S.-C. Zhang, Coordination of sonic hedgehog and Wnt signaling determines ventral and dorsal telencephalic neuron types from human embryonic stem cells. Development 136, 4055-4063 (2009).
10. L. Ma, B. Hu, Y. Liu, S. C. Vermilyea, H. Liu, L. Gao, Y. Sun, X. Zhang, S.-C. Zhang, Human embryonic stem cell-derived GABA neurons correct locomotion deficits in quinolinic acid-lesioned mice. Cell Stem Cell 10, 455-464 (2012).
11. K. Watanabe, M. Ueno, D. Kamiya, A. Nishiyama, M. Matsumura, T. Wataya, J. B. Takahashi, S. Nishikawa, K. Muguruma, Y. Sasai, A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat. Biotechnol. 25, 681-686 (2007).
12. Y. Liu, J. P. Weick, H. Liu, R. Krencik, X. Zhang, L. Ma, G.-M. Zhou, M. Ayala, S.-C. Zhang, Medial ganglionic eminence-like cells derived from human embryonic stem cells correct learning and memory deficits. Nat. Biotechnol. 31, 440-447 (2013).
13. A. M. Maroof, S. Keros, J. A. Tyson, S.-W. Ying, Y. M. Ganat, F. T. Merkle, B. Liu, A. Goulburn, E. G. Stanley, A. G. Elefanty, H. R. Widmer, K. Eggan, P. A. Goldstein, S. A. Anderson, L. Studer, Directed differentiation and functional maturation of cortical interneurons from human embryonic stem cells. Cell Stem Cell 12, 559-572 (2013).
14. C. R. Nicholas, J. Chen, Y. Tang, D. G. Southwell, N. Chalmers, D. Vogt, C. M. Arnold, Y.-J. Chen, E. G. Stanley, A. G. Elefanty, Y. Sasai, A. Alvarez-Buylla, J. L. R. Rubenstein, A. R. Kriegstein, Functional maturation of hPSC-derived forebrain interneurons requires an extended timeline and mimics human neural development. Cell Stem Cell 12, 573-586 (2013).
15. J. Mariani, M. V. Simonini, D. Palejev, L. Tomasini, G. Coppola, A. M. Szekely, T. L. Horvath, F. M. Vaccarino, Modeling human cortical development in vitro using induced pluripotent stem cells. Proc. Natl. Acad. Sci. U.S.A. 109, 12770-12775 (2012).
16. M. C. N. Marchetto, C. Carromeu, A. Acab, D. Yu, G. W. Yeo, Y. Mu, G. Chen, F. H. Gage, A. R. Muotri, A model for neural development and treatment of Rett syndrome using human induced pluripotent stem cells. Cell 143, 527-539 (2010).
17. K. J. Brennand, A. Simone, J. Jou, C. Gelboin-Burkhart, N. Tran, S. Sangar, Y. Li, Y. Mu, G. Chen, D. Yu, S. McCarthy, J. Sebat, F. H. Gage, Modelling schizophrenia using human induced pluripotent stem cells. Nature 473, 221-225 (2011).
18. S.-C. Zhang, M. Wernig, I. D. Duncan, O. Brüstle, J. A. Thomson, In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat. Biotechnol. 19, 1129-1133 (2001).
19. H. Wu, J. Xu, Z. P. Pang, W. Ge, K. J. Kim, B. Blanchi, C. Chen, T. C. Sudhof, Y. E. Sun, Integrative genomic and functional analyses reveal neuronal subtype differentiation bias in human embryonic stem cell lines. Proc. Natl. Acad. Sci. U.S.A. 104, 13821-13826 (2007).
20. Y. Shi, P. Kirwan, J. Smith, G. MacLean, S. H. Orkin, F. J. Livesey, A human stem cell model of early Alzheimer's disease pathology in Down syndrome. Sci. Transl. Med. 4, 124ra29 (2012).
21. C. Boissart, A. Poulet, P. Georges, H. Darville, E. Julita, R. Delorme, T. Bourgeron, M. Peschanski, A. Benchoua, Differentiation from human pluripotent stem cells of cortical neurons of the superficial layers amenable to psychiatric disease modeling and high-throughput drug screening. Transl. Psychiatry 3, e294 (2013).
22. D. Tornero, S. Wattananit, M. Grønning Madsen, P. Koch, J. Wood, J. Tatarishvili, Y. Mine, R. Ge, E. Monni, K. Devaraju, R. F. Hevner, O. Brüstle, O. Lindvall, Z. Kokaia, Human induced pluri-potent stem cell-derived cortical neurons integrate in stroke-injured cortex and improve functional recovery. Brain 136, 3561-3577 (2013).
23. B. Bilican, M. R. Livesey, G. Haghi, J. Qiu, K. Burr, R. Siller, G. E. Hardingham, D. J. A. Wyllie, S. Chandran, Physiological normoxia and absence of EGF is required for the long-term propagation of anterior neural precursors from human pluripotent cells. PLOS One 9, e85932 (2014).
24. Z. Wen, H. N. Nguyen, Z. Guo, M. A. Lalli, X. Wang, Y. Su, N.-S. Kim, K.-J. Yoon, J. Shin, C. Zhang, G. Makri, D. Nauen, H. Yu, E. Guzman, C.-H. Chiang, N. Yoritomo, K. Kaibuchi, J. Zou, K. M. Christian, L. Cheng, C. A. Ross, R. L. Margolis, G. Chen, K. S. Kosik, H. Song, G.-L. Ming, Synaptic dysregulation in a human iPS cell model of mental disorders. Nature 515, 414-418 (2014).
25. V. L. Dawson, T. M. Dawson, D. A. Bartley, G. R. Uhl, S. H. Snyder, Mechanisms of nitric oxide-mediated neurotoxicity in primary brain cultures. J. Neurosci. 13, 2651-2661 (1993).
26. V. L. Dawson, T. M. Dawson, E. D. London, D. S. Bredt, S. H. Snyder, Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proc. Natl. Acad. Sci. U.S.A. 88, 6368-6371 (1991).
27. M. Gonzalez-Zulueta, L. M. Ensz, G. Mukhina, R. M. Lebovitz, R. M. Zwacka, J. F. Engelhardt, L. W. Oberley, V. L. Dawson, T. M. Dawson, Manganese superoxide dismutase protects nNOS neurons from NMDA and nitric oxide-mediated neurotoxicity. J. Neurosci. 18, 2040-2055 (1998).
28. R. Sattler, Z. Xiong, W.-Y. Lu, M. Hafner, J. F. MacDonald, M. Tymianski, Specific coupling of NMDA receptor activation to nitric oxide neurotoxicity by PSD-95 protein. Science 284, 1845-1848 (1999).
29. J. M. Hebert, G. Fishell, The genetics of early telencephalon patterning: Some assembly required. Nat. Rev. Neurosci. 9, 678-685 (2008).
30. M. Eiraku, K. Watanabe, M. Matsuo-Takasaki, M. Kawada, S. Yonemura, M. Matsumura, T. Wataya, A. Nishiyama, K. Muguruma, Y. Sasai, Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. Cell Stem Cell 3, 519-532 (2008).
31. S. M. Chambers, C. A. Fasano, E. P. Papapetrou, M. Tomishima, M. Sadelain, L. Studer, Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat. Biotechnol. 27, 275-280 (2009).
32. N. Gaspard, T. Bouschet, R. Hourez, J. Dimidschstein, G. Naeije, J. van den Ameele, I. Espuny-Camacho, A. Herpoel, L. Passante, S. N. Schiffmann, A. Gaillard, P. Vanderhaeghen, An intrinsic mechanism of corticogenesis from embryonic stem cells. Nature 455, 351-357 (2008).
33. J. Debnath, S. K. Muthuswamy, J. S. Brugge, Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 30, 256-268 (2003).
34. J. Debnath, J. S. Brugge, Modelling glandular epithelial cancers in three-dimensional cultures. Nat. Rev. Cancer 5, 675-688 (2005).
35. T. Kadoshima, H. Sakaguchi, T. Nakano, M. Soen, S. Ando, M. Eiraku, Y. Sasai, Self-organization of axial polarity, inside-out layer pattern, and species-specific progenitor dynamics in human ES cell-derived neocortex. Proc. Natl. Acad. Sci. U.S.A. 110, 20284-20289 (2013).
36. G. G. Turrigiano, S. B. Nelson, Homeostatic plasticity in the developing nervous system. Nat. Rev. Neurosci. 5, 97-107 (2004).
37. J. D. Shepherd, G. Rumbaugh, J. Wu, S. Chowdhury, N. Plath, D. Kuhl, R. L. Huganir, P. F. Worley, Arc/Arg3.1 mediates homeostatic synaptic scaling of AMPA receptors. Neuron 52, 475-484 (2006).
38. T. Miyamoto, M. J. Petrus, A. E. Dubin, A. Patapoutian, TRPV3 regulates nitric oxide synthase-independent nitric oxide synthesis in the skin. Nat. Commun. 2, 369 (2011).
39. M. Yuan, C. Siegel, Z. Zeng, J. Li, F. Liu, L. D. McCullough, Sex differences in the response to activation of the poly (ADP-ribose) polymerase pathway after experimental stroke. Exp. Neurol. 217, 210-218 (2009).
40. D. V. Hansen, J. L. R. Rubenstein, A. R. Kriegstein, Deriving excitatory neurons of the neo-cortex from pluripotent stem cells. Neuron 70, 645-660 (2011).
41. T. Ma, C. Wang, L. Wang, X. Zhou, M. Tian, Q. Zhang, Y. Zhang, J. Li, Z. Liu, Y. Cai, F. Liu, Y. You, C. Chen, K. Campbell, H. Song, L. Ma, J. L. Rubenstein, Z. Yang, Subcortical origins of human and monkey neocortical interneurons. Nat. Neurosci. 16, 1588-1597 (2013).
42. D. S. Bredt, S. H. Snyder, Nitric oxide: A physiologic messenger molecule. Annu. Rev. Biochem. 63, 175-195 (1994).
43. A. M. Paşca, S. A. Sloan, L. E. Clarke, Y. Tian, C. D. Makinson, N. Huber, C. H. Kim, J.-Y. Park, N. A. O'Rourke, K. D. Nguyen, S. J. Smith, J. R. Huguenard, D. H. Geschwind, B. A. Barres, S. P. Paşca, Functional cortical neurons and astrocytes from human pluripotent stem cells in 3D culture. Nat. Methods 12, 671-678 (2015).
44. O. Yizhar, L. E. Fenno, M. Prigge, F. Schneider, T. J. Davidson, D. J. O'Shea, V. S. Sohal, I. Goshen, J. Finkelstein, J. T. Paz, K. Stehfest, R. Fudim, C. Ramakrishnan, J. R. Huguenard, P. Hegemann, K. Deisseroth, Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 477, 171-178 (2011).
45. G. G. Turrigiano, The self-tuning neuron: Synaptic scaling of excitatory synapses. Cell 135, 422-435 (2008).
46. M. P. Mattson, B. Rychlik, J. S. You, J. E. Sisken, Sensitivity of cultured human embryonic cerebral cortical neurons to excitatory amino acid-induced calcium influx and neuro-toxicity. Brain Res. 542, 97-106 (1991).
47. K. Gupta, G. E. Hardingham, S. Chandran, NMDA receptor-dependent glutamate excitotoxicity in human embryonic stem cell-derived neurons. Neurosci. Lett. 543, 95-100 (2013).
48. G. E. Hardingham, R. Patani, P. Baxter, D. J. Wyllie, S. Chandran, Human embryonic stem cell-derived neurons as a tool for studying neuroprotection and neurodegeneration. Mol. Neurobiol. 42, 97-102 (2010).
49. A. F. Samdani, T. M. Dawson, V. L. Dawson, Nitric oxide synthase in models of focal ischemia. Stroke 28, 1283-1288 (1997).
50. A. F. Samdani, C Newcamp, A. Resink, F. Facchinetti, B. E. Hoffman, V. L. Dawson, T. M. Dawson, Differential susceptibility to neurotoxicity mediated by neurotrophins and neuronal nitric oxide synthase. J. Neurosci. 17, 4633-4641 (1997).
51. D. W. Choi, M. Maulucci-Gedde, A. R. Kriegstein, Glutamate neurotoxicity in cortical cell culture. J. Neurosci. 7, 357-368 (1987).
52. S. Murase, D. F. Owens, R. D. McKay, In the newborn hippocampus, neurotrophin-dependent survival requires spontaneous activity and integrin signaling. J. Neurosci. 31, 7791-7800 (2011).
53. M. J. L Eliasson, K. Sampei, A. S. Mandir, P. D. Hurn, R. J. Traystman, J. Bao, A. Pieper, Z.-Q. Wang, T. M. Dawson, S. H. Snyder, V. L Dawson, Poly(ADP-ribose) polymerase gene disruption renders mice resistant to cerebral ischemia. Nat. Med. 3, 1089-1095 (1997).
54. A. A. Fatokun, V. L. Dawson, T. M. Dawson, Parthanatos: Mitochondrial-linked mechanisms and therapeutic opportunities. Br. J. Pharmacol. 171, 2000-2016 (2014).
55. Z. Huang, P. L. Huang, N. Panahian, T. Dalkara, M. C. Fishman, M. A. Moskowitz, Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. Science 265, 1883-1885 (1994).
56. Y. Wang, N. S. Kim, J. F. Haince, H. C Kang, K. K. David, S. A. Andrabi, G. G. Poirier, V. L Dawson, T. M. Dawson, Poly(ADP-ribose) (PAR) binding to apoptosis-inducing factor is critical for PAR polymerase-1-dependent cell death (parthanatos). Sci. Signal. 4, ra20 (2011).
57. J. Zhang, V. L. Dawson, T. M. Dawson, S. H. Snyder, Nitric oxide activation of poly(ADP-ribose) synthetase in neurotoxicity. Science 263, 687-689 (1994).
58. B. G. Sanganahalli, P. G. Joshi, N. B. Joshi, NMDA and non-NMDA receptors stimulation causes differential oxidative stress in rat cortical slices. Neurochem. Int. 49, 475-480 (2006).
59. Y. Wang, V. L. Dawson, T. M. Dawson, Poly(ADP-ribose) signals to mitochondrial AIF: A key event in parthanatos. Exp. Neurol. 218, 193-202 (2009).
60. S. Fertuzinhos, Ž. Krsnik, Y. I. Kawasawa, M.-R. Rašin, K. Y. Kwan, J.-G. Chen, M. Judaš, M. Hayashi, N. Šestan, Selective depletion of molecularly defined cortical interneurons in human holopro-sencephaly with severe striatal hypoplasia. Cereb. Cortex 19, 2196-2207 (2009).