Sustained synchronized neuronal network activity in a human astrocyte co-culture system

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Kuijlaars, Jacobine ^a   Oyelami, Tutu ^b   Diels, Annick ^b   Rohrbacher, Jutta ^b   Versweyveld, Sofie ^b   Meneghello, Giulia ^b   Tuefferd, Marianne ^b   Verstraelen, Peter ^c   Detrez, Jan R ^c   Verschuuren, Marlies ^c   De Vos, Winnok H ^c,d   Meert, Theo ^a,b   Peeters, Pieter J ^b   Cik, Miroslav ^b   Nuydens, Rony ^b   Brône, Bert ^a   Verheyen, An ^b  

^a HASSELT UNIVERSITY   (Belgium)

^b JANSSEN RESEARCH AND DEVELOPMENT   (Belgium)

^c UNIVERSITY OF ANTWERP   (Belgium)

^d GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; BIOLOGICAL MARKER;

ACTION POTENTIAL; ASTROCYTE; CELL CULTURE; CELL DIFFERENTIATION; COCULTURE; HUMAN; INDUCED PLURIPOTENT STEM CELL; METABOLISM; NERVE CELL; NERVE CELL NETWORK; PHYSIOLOGY; PROCEDURES;

ACTION POTENTIALS; ASTROCYTES; BIOMARKERS; CELL DIFFERENTIATION; CELLS, CULTURED; COCULTURE TECHNIQUES; HUMANS; INDUCED PLURIPOTENT STEM CELLS; NERVE NET; NEURONS; NEUROTRANSMITTER AGENTS;

EID: 84994528824     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep36529     Document Type: Article

References (60)

1. Cohen, E., Ivenshitz, M., Amor-Baroukh, V., Greenberger, V. & Segal, M. Determinants of spontaneous activity in networks of cultured hippocampus. Brain Res. 1235, 21-30 (2008).
2. Ben-Ari, Y. Developing networks play a similar melody. Trends Neurosci. 24, 353-360 (2001).
3. Zhang, L. I. & Poo, M.-m. Electrical activity and development of neural circuits. Nat. Neurosci. 4, 1207-1214 (2001).
4. Kandel, E. & Spencer, W. Electrophysiology of hippocampal neurons: II. After-potentials and repetitive firing. J. Neurophysiol. 24, 243-259 (1961).
5. Miles, R., Traub, R. D. & Wong, R. Spread of synchronous firing in longitudinal slices from the CA3 region of the hippocampus. J. Neurophysiol. 60, 1481-1496 (1988).
6. Silva, L. R., Amitai, Y. & Connors, B. W. Intrinsic oscillations of neocortex generated by layer 5 pyramidal neurons. Science 251, 432 (1991).
7. Verstraelen, P. et al. Pharmacological characterization of cultivated neuronal networks: relevance to synaptogenesis and synaptic connectivity. Cell. Mol. Neurobiol. 34, 757-776 (2014).
8. Katz, L. C. & Shatz, C. J. Synaptic activity and the construction of cortical circuits. Science 274, 1133-1138 (1996).
9. Wen, Z. et al. Synaptic dysregulation in a human iPS cell model of mental disorders. Nature 515, 414-418 (2014).
10. Schipul, S. E., Keller, T. A. & Just, M. A. Inter-regional brain communication and its disturbance in autism. Front. Syst. Neurosci. 5, 10 (2011).
11. Noebels, J. A perfect storm: converging paths of epilepsy and Alzheimer's dementia intersect in the hippocampal formation. Epilepsia 52, 39-46 (2011).
12. Braak, H. & Del Trecidi, K. Neuroanatomy and pathology of sporadic Alzheimer's disease. Adv. Anat. Embryol. Cell Biol. 215, 1-162 (2015).
13. Holtkamp, M. et al. Status epilepticus induces increasing neuronal excitability and hypersynchrony as revealed by optical imaging. Neurobiol. Dis. 43, 220-227 (2011).
14. Morelli, G. et al. Cerebral Cortical Circuitry Formation Requires Functional Glycine Receptors. Cereb. Cortex, 25 (2016).
15. Uhlhaas, P. J. & Singer, W. Abnormal neural oscillations and synchrony in schizophrenia. Nat. Rev. Neurosci. 11, 100-113 (2010).
16. Cornelissen, F. et al. Quantitation of chronic and acute treatment effects on neuronal network activity using image and signal analysis toward a high-content assay. J. Biomol. Screen. 1087057113486518 (2013).
17. Detrez, J. R. et al. Image Informatics Strategies for Deciphering Neuronal Network Connectivity. Adv. Anat. Embryol. Cell Biol. 219, 123-148, doi: 10. 1007/978-3-319-28549-8-5 (2016).
18. Harrill, J. A., Robinette, B. L. & Mundy, W. R. Use of high content image analysis to detect chemical-induced changes in synaptogenesis in vitro. Toxicol. In Vitro 25, 368-387 (2011).
19. Wallace, T. L., Ballard, T. M. & Glavis-Bloom, C. In Cognitive Enhancement 27-57 (Springer, 2015).
20. Kaiser, T. & Feng, G. Modeling psychiatric disorders for developing effective treatments. Nat. Med. 21, 979-988 (2015).
21. Suzuki, I. K. & Vanderhaeghen, P. Is this a brain which I see before me? Modeling human neural development with pluripotent stem cells. Development 142, 3138-3150 (2015).
22. Takahashi, K. et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861-872 (2007).
23. Park, I.-H. et al. Disease-specific induced pluripotent stem cells. Cell 134, 877-886 (2008).
24. Inoue, H., Nagata, N., Kurokawa, H. & Yamanaka, S. iPS cells: a game changer for future medicine. EMBO J. 33, 409-417 (2014).
25. Shi, Y., Kirwan, P. & Livesey, F. J. Directed differentiation of human pluripotent stem cells to cerebral cortex neurons and neural networks. Nat. Protoc. 7, 1836-1846 (2012).
26. Yagi, T. et al. Modeling familial Alzheimer's disease with induced pluripotent stem cells. Hum. Mol. Genet. 20, 4530-4539 (2011).
27. Israel, M. A. et al. Probing sporadic and familial Alzheimer/'s disease using induced pluripotent stem cells. Nature 482, 216-220 (2012).
28. Belinsky, G. S. et al. Patch-clamp recordings and calcium imaging followed by single-cell PCR reveal the developmental profile of 13 genes in iPSC-derived human neurons. Stem Cell Res. 12, 101-118 (2014).
29. Odawara, A., Saitoh, Y., Alhebshi, A., Gotoh, M. & Suzuki, I. Long-term electrophysiological activity and pharmacological response of a human induced pluripotent stem cell-derived neuron and astrocyte co-culture. Biochem. Biophys. Res. Commun. 443, 1176-1181 (2014).
30. Kirwan, P. et al. Development and function of human cerebral cortex neural networks from pluripotent stem cells in vitro. Development 142, 3178-3187 (2015).
31. Tang, X. et al. Astroglial cells regulate the developmental timeline of human neurons differentiated from induced pluripotent stem cells. Stem Cell Res. 11, 743-757 (2013).
32. Johnson, M. A., Weick, J. P., Pearce, R. A. & Zhang, S.-C. Functional neural development from human embryonic stem cells: accelerated synaptic activity via astrocyte coculture. J. Neurosci. 27, 3069-3077 (2007).
33. Oberheim, N. A. et al. Uniquely hominid features of adult human astrocytes. The Journal of Neuroscience 29, 3276-3287 (2009).
34. Zhang, Y. et al. Purification and characterization of progenitor and mature human astrocytes reveals transcriptional and functional differences with mouse. Neuron 89, 37-53 (2016).
35. Borghese, L. et al. Inhibition of notch signaling in human embryonic stem cell-derived neural stem cells delays G1/S phase transition and accelerates neuronal differentiation in vitro and in vivo. Stem Cells 28, 955-964 (2010).
36. Ogura, A., Morizane, A., Nakajima, Y., Miyamoto, S. & Takahashi, J. ?-secretase inhibitors prevent overgrowth of transplanted neural progenitors derived from human-induced pluripotent stem cells. Stem Cells Dev. 22, 374-382 (2012).
37. Liao, C.-C. & Lee, L.-J. Evidence for structural and functional changes of subplate neurons in developing rat barrel cortex. Brain Structure and Function 217, 275-292 (2012).
38. Boissart, C. et al. 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).
39. Araque, A., Parpura, V., Sanzgiri, R. P. & Haydon, P. G. Glutamate?dependent astrocyte modulation of synaptic transmission between cultured hippocampal neurons. Eur. J. Neurosci. 10, 2129-2142 (1998).
40. Wagenaar, D. A., Pine, J. & Potter, S. M. An extremely rich repertoire of bursting patterns during the development of cortical cultures. BMC Neurosci. 7, 1 (2006).
41. Meneghello, G. et al. Evaluation of established human iPSC-derived neurons to model neurodegenerative diseases. Neuroscience 301, 204-212 (2015).
42. Rushton, D. J., Mattis, V. B., Svendsen, C. N., Allen, N. D. & Kemp, P. J. Stimulation of GABA-induced Ca 2+ influx enhances maturation of human induced pluripotent stem cell-derived neurons. PLoS One 8, e81031 (2013).
43. Pr? D. et al. A time course analysis of the electrophysiological properties of neurons differentiated from human induced pluripotent stem cells (iPSCs). PLoS One 9, e103418 (2014).
44. Krencik, R., Weick, J. P., Liu, Y., Zhang, Z.-J. & Zhang, S.-C. Specification of transplantable astroglial subtypes from human pluripotent stem cells. Nat. Biotechnol. 29, 528-534 (2011).
45. Ben-Ari, Y. Excitatory actions of GABA during development: the nature of the nurture. Nat. Rev. Neurosci. 3, 728-739 (2002).
46. Ben-Ari, Y., Gaiarsa, J.-L., Tyzio, R. & Khazipov, R. GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol. Rev. 87, 1215-1284 (2007).
47. Ganguly, K., Schinder, A. F., Wong, S. T. & Poo, M.-m. GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell 105, 521-532 (2001).
48. Mann, E. O. & Paulsen, O. Role of GABAergic inhibition in hippocampal network oscillations. Trends Neurosci. 30, 343-349 (2007).
49. Murphy, T. H., Blatter, L. A., Wier, W. G. & Baraban, J. Spontaneous synchronous synaptic calcium transients in cultured cortical neurons. J. Neurosci. 12, 4834-4845 (1992).
50. Heimer, G., Rivlin, M., Israel, Z. & Bergman, H. In Parkinson's Disease and Related Disorders 17-20 (Springer, 2006).
51. Whitwell, J. et al. Altered functional connectivity in asymptomatic MAPT subjects A comparison to bvFTD. Neurology 77, 866-874 (2011).
52. Stancu, I.-C. et al. Templated misfolding of Tau by prion-like seeding along neuronal connections impairs neuronal network function and associated behavioral outcomes in Tau transgenic mice. Acta Neuropathol. 129, 875-894 (2015).
53. Sorg, C., Riedl, V., Perneczky, R., Kurz, A. & Wohlschlager, A. M. Impact of Alzheimer's disease on the functional connectivity of spontaneous brain activity. Curr. Alzheimer Res. 6, 541-553 (2009).
54. Beers, J. et al. Passaging and colony expansion of human pluripotent stem cells by enzyme-free dissociation in chemically defined culture conditions. Nat. Protoc. 7, 2029-2040 (2012).
55. Wang, X.-s. & Gruenstein, E. I. Mechanism of synchronized Ca 2+ oscillations in cortical neurons. Brain Res. 767, 239-249 (1997).
56. Pickering, M., Pickering, B. W., Murphy, K. J. & O'Connor, J. J. Discrimination of cell types in mixed cortical culture using calcium imaging: a comparison to immunocytochemical labeling. J. Neurosci. Methods 173, 27-33 (2008).
57. Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682 (2012).
58. Huang, L.-K. & Wang, M.-J. J. Image thresholding by minimizing the measures of fuzziness. Pattern Recog. 28, 41-51 (1995).
59. Pani, G. et al. MorphoNeuroNet: An automated method for dense neurite network analysis. Cytometry Part A 85, 188-199 (2014).
60. Zack, G., Rogers, W. & Latt, S. Automatic measurement of sister chromatid exchange frequency. J. Histochem. Cytochem. 25, 741-753 (1977).