Brain-on-a-chip model enables analysis of human neuronal differentiation and chemotaxis

Lab on a Chip

Volumn 16, Issue 21, 2016, Pages 4152-4162

  Kilic, Onur ^a   Pamies, David ^b   Lavell, Emily ^c   Schiapparelli, Paula ^c   Feng, Yun ^c,d   Hartung, Thomas ^b,e   Bal Price, Anna ^f   Hogberg, Helena T ^b   Quinones Hinojosa, Alfredo ^c   Guerrero Cazares, Hugo ^c   Levchenko, Andre ^g  

^a Johns Hopkins University   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

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

^d JIANGSU UNIVERSITY   (China)

^e UNIVERSITY OF KONSTANZ   (Germany)

^f JOINT RESEARCH CENTRE   (Italy)

^g Yale University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; MICROTUBULE ASSOCIATED PROTEIN; NEUROFILAMENT PROTEIN; PROTEIN ZO1; SILASTIC; VASCULOTROPIN;

ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN ON A CHIP; CAPILLARY ENDOTHELIAL CELL; CELL ADHESION; CELL CULTURE; CELL DIFFERENTIATION; CELL INTERACTION; CELL MATURATION; CELL MIGRATION; CHEMOTAXIS; CONTROLLED STUDY; ELECTRIC RESISTANCE; EMBRYO; EX VIVO STUDY; GLIA CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LAB ON A CHIP; LOCOMOTION; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; STEM CELL; BRAIN; CYTOLOGY; GLIA; MICROCHIP ANALYSIS; TUMOR CELL LINE;

BRAIN; CELL DIFFERENTIATION; CELL LINE, TUMOR; CHEMOTAXIS; HUMANS; MICROCHIP ANALYTICAL PROCEDURES; NEUROGLIA; NEURONS;

EID: 84992418466     PISSN: 14730197     EISSN: 14730189     Source Type: Journal    
DOI: 10.1039/c6lc00946h     Document Type: Article

References (60)

1. M. Iijima Y. E. Huang P. Devreotes Temporal and spatial regulation of chemotaxis Dev. Cell 2002 3 4 469 478
2. P. Devreotes C. Janetopoulos Eukaryotic chemotaxis: distinctions between directional sensing and polarization J. Biol. Chem. 2003 278 23 20445 20448
3. P. J. Van Haastert Chemotaxis: insights from the extending pseudopod J. Cell Sci. 2010 123 18 3031 3037
4. R. H. Insall Understanding eukaryotic chemotaxis: a pseudopod-centred view Nat. Rev. Mol. Cell Biol. 2010 11 6 453 458
5. C. Shi C.-H. Huang P. N. Devreotes et al., Interaction of motility, directional sensing, and polarity modules recreates the behaviors of chemotaxing cells PLoS Comput. Biol. 2013 9 7 e1003122
6. M. D. Cahalan I. Parker Choreography of cell motility and interaction dynamics imaged by two-photon microscopy in lymphoid organs Annu. Rev. Immunol. 2008 26 585
7. J. Textor A. Peixoto S. E. Henrickson et al., Defining the quantitative limits of intravital two-photon lymphocyte tracking Proc. Natl. Acad. Sci. U. S. A. 2011 108 30 12401 12406
8. C. D. Sadik A. D. Luster Lipid-cytokine-chemokine cascades orchestrate leukocyte recruitment in inflammation J. Leukocyte Biol. 2012 91 2 207 215
9. P. Niethammer C. Grabher A. T. Look et al., A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish Nature 2009 459 7249 996 999
10. Y. Wang G. Li A. Stanco et al., CXCR4 and CXCR7 have distinct functions in regulating interneuron migration Neuron 2011 69 1 61 76
11. F. Doetsch J. M. García-Verdugo A. Alvarez-Buylla Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain J. Neurosci. 1997 17 13 5046 5061
12. C. Lois J.-M. Garcia-Verdugo A. Alvarez-Buylla Chain migration of neuronal precursors Science 1996 271 5251 978 981
13. C. Wang F. Liu Y.-Y. Liu et al., Identification and characterization of neuroblasts in the subventricular zone and rostral migratory stream of the adult human brain Cell Res. 2011 21 11 1534 1550
14. H. Guerrero-Cázares O. Gonzalez-Perez M. Soriano-Navarro et al., Cytoarchitecture of the lateral ganglionic eminence and rostral extension of the lateral ventricle in the human fetal brain J. Comp. Neurol. 2011 519 6 1165 1180
15. N. Sanai T. Nguyen R. A. Ihrie et al., Corridors of migrating neurons in the human brain and their decline during infancy Nature 2011 478 7369 382 386
16. V. Capilla-Gonzalez, E. Lavell and A. Quiñones-Hinojosa, et al., Regulation of subventricular zone-derived cells migration in the adult brain, Stem Cell Biology in Neoplasms of the Central Nervous System, Springer, 2015, pp. 1-21
17. N. Kaneko O. Marín M. Koike et al., New neurons clear the path of astrocytic processes for their rapid migration in the adult brain Neuron 2010 67 2 213 223
18. K. Sawamoto H. Wichterle O. Gonzalez-Perez et al., New neurons follow the flow of cerebrospinal fluid in the adult brain Science 2006 311 5761 629 632
19. K. J. Christie A. M. Turnley Regulation of endogenous neural stem/progenitor cells for neural repair - factors that promote neurogenesis and gliogenesis in the normal and damaged brain Front. Cell. Neurosci. 2012 6 70
20. J. C. Conover F. Doetsch J.-M. Garcia-Verdugo et al., Disruption of Eph/ephrin signaling affects migration and proliferation in the adult subventricular zone Nat. Neurosci. 2000 3 11 1091 1097
21. J. Imitola K. Raddassi K. I. Park et al., Directed migration of neural stem cells to sites of CNS injury by the stromal cell-derived factor 1α/CXC chemokine receptor 4 pathway Proc. Natl. Acad. Sci. U. S. A. 2004 101 52 18117 18122
22. D. Zagzag M. Esencay O. Mendez et al., Hypoxia-and vascular endothelial growth factor-induced stromal cell-derived factor-1α/CXCR4 expression in glioblastomas: one plausible explanation of Scherer's structures Am. J. Pathol. 2008 173 2 545 560
23. E. Y. Snyder C. Yoon J. D. Flax et al., Multipotent neural precursors can differentiate toward replacement of neurons undergoing targeted apoptotic degeneration in adult mouse neocortex Proc. Natl. Acad. Sci. U. S. A. 1997 94 21 11663 11668
24. K. S. Aboody A. Brown N. G. Rainov et al., Neural stem cells display extensive tropism for pathology in adult brain: evidence from intracranial gliomas Proc. Natl. Acad. Sci. U. S. A. 2000 97 23 12846 12851
25. N. Alepee A. Bahinski M. Daneshian et al., t4 Workshop Report: State-of-the-Art of 3D Cultures (Organs-on-a-Chip) in Safety Testing and Pathophysiology Altex 2014 31 4 441
26. T. Hartung 3D - A new dimension of in vitro research Adv. Drug Delivery Rev. 2014 69 vi
27. S. N. Bhatia D. E. Ingber Microfluidic organs-on-chips Nat. Biotechnol. 2014 32 8 760 772
28. E. W. Esch A. Bahinski D. Huh Organs-on-chips at the frontiers of drug discovery Nat. Rev. Drug Discovery 2015 14 4 248 260
29. D. Pamies T. Hartung H. T. Hogberg Biological and medical applications of a brain-on-a-chip Exp. Biol. Med. 2014 1535370214537738
30. A. Kunze M. Giugliano A. Valero et al., Micropatterning neural cell cultures in 3D with a multi-layered scaffold Biomaterials 2011 32 8 2088 2098
31. D. Majumdar Y. Gao D. Li et al., Co-culture of neurons and glia in a novel microfluidic platform J. Neurosci. Methods 2011 196 1 38 44
32. J. Park H. Koito J. Li et al., A multi-compartment CNS neuron-glia co-culture microfluidic platform J. Visualized Exp. 2009 31 e1399 e1399
33. J. Park B. K. Lee G. S. Jeong et al., Three-dimensional brain-on-a-chip with an interstitial level of flow and its application as an in vitro model of Alzheimer's disease Lab Chip 2015 15 1 141 150
34. A. K. H. Achyuta A. J. Conway R. B. Crouse et al., A modular approach to create a neurovascular unit-on-a-chip Lab Chip 2013 13 4 542 553
35. P. W. Andrews Retinoic acid induces neuronal differentiation of a cloned human embryonal carcinoma cell line in vitro Dev. Biol. 1984 103 2 285 293
36. S. Pleasure V. Y. Lee NTera 2 cells: a human cell line which displays characteristics expected of a human committed neuronal progenitor cell J. Neurosci. Res. 1993 35 6 585 602
37. S. J. Pleasure C. Page V. Lee Pure, postmitotic, polarized human neurons derived from NTera 2 cells provide a system for expressing exogenous proteins in terminally differentiated neurons J. Neurosci. 1992 12 5 1802 1815
38. I. Guillemain G. Alonso G. Patey et al., Human NT2 neurons express a large variety of neurotransmission phenotypes in vitro J. Comp. Neurol. 2000 422 3 380 395
39. T. R. Neelands A. P. King R. L. Macdonald Functional expression of L-, N-, P/Q-, and R-type calcium channels in the human NT2-N cell line J. Neurophysiol. 2000 84 6 2933 2944
40. R. S. Hartley M. Margulis P. S. Fishman et al., Functional synapses are formed between human NTera2 (NT2N, hNT) neurons grown on astrocytes J. Comp. Neurol. 1999 407 1 1 10
41. Y. Haile W. Fu B. Shi et al., Characterization of the NT2-derived neuronal and astrocytic cell lines as alternative in vitro models for primary human neurons and astrocytes J. Neurosci. Res. 2014 92 9 1187 1198
42. I. Laurenza G. Pallocca M. Mennecozzi et al., A human pluripotent carcinoma stem cell-based model for in vitro developmental neurotoxicity testing: effects of methylmercury, lead and aluminum evaluated by gene expression studies Int. J. Dev. Neurosci. 2013 31 7 679 691
43. G. Pallocca M. Fabbri M. G. Sacco et al., miRNA expression profiling in a human stem cell-based model as a tool for developmental neurotoxicity testing Cell Biol. Toxicol. 2013 29 4 239 257
44. D. Pamies M. A. Sogorb M. Fabbri et al., Genomic and phenotypic alterations of the neuronal-like cells derived from human embryonal carcinoma stem cells (NT2) caused by exposure to organophosphorus compounds paraoxon and mipafox Int. J. Mol. Sci. 2014 15 1 905 926
45. D. Pamies A. Bal-Price M. Fabbri et al., Silencing of PNPLA6, the neuropathy target esterase (NTE) codifying gene, alters neurodifferentiation of human embryonal carcinoma stem cells (NT2) Neuroscience 2014 281 54 67
46. L. J. Millet M. E. Stewart J. V. Sweedler et al., Microfluidic devices for culturing primary mammalian neurons at low densities Lab Chip 2007 7 8 987 994
47. M. Zhu Y. Feng S. Dangelmajer et al., Human cerebrospinal fluid regulates proliferation and migration of stem cells through insulin-like growth factor-1 Stem Cells Dev. 2014 24 2 160 171
48. A. L. Placone P. M. McGuiggan D. E. Bergles et al., Human astrocytes develop physiological morphology and remain quiescent in a novel 3D matrix Biomaterials 2015 42 134 143
49. A. F. Levy M. Zayats H. Guerrero-Cazares et al., Influence of basement membrane proteins and endothelial cell-derived factors on the morphology of human fetal-derived astrocytes in 2D PLoS One 2014 9 3 e92165
50. R. Ravin P. S. Blank A. Steinkamp et al., Shear forces during blast, not abrupt changes in pressure alone, generate calcium activity in human brain cells PLoS One 2012 7 6 e39421
51. M. F. Stins F. Gilles K. S. Kim Selective expression of adhesion molecules on human brain microvascular endothelial cells J. Neuroimmunol. 1997 76 1 81 90
52. B. Lin A. Levchenko Spatial manipulation with microfluidics Front. Bioeng. Biotechnol. 2015 3 39
53. J. Madri Modeling the neurovascular niche: implications for recovery from CNS injury J. Physiol. Pharmacol. 2009 60 Suppl 4 95 104
54. D. Cai D. J. Montell Diverse and dynamic sources and sinks in gradient formation and directed migration Curr. Opin. Cell Biol. 2014 30 91 98
55. B. Lin T. Yin Y. I. Wu et al., Interplay between chemotaxis and contact inhibition of locomotion determines exploratory cell migration Nat. Commun. 2015 6 6619
56. M. W. Toepke D. J. Beebe PDMS absorption of small molecules and consequences in microfluidic applications Lab Chip 2006 6 12 1484 1486
57. K. J. Regehr M. Domenech J. T. Koepsel et al., Biological implications of polydimethylsiloxane-based microfluidic cell culture Lab Chip 2009 9 15 2132 2139
58. B. Wang S. Jedlicka X. Cheng Maintenance and Neuronal Cell Differentiation of Neural Stem Cells C17. 2 Correlated to Medium Availability Sets Design Criteria in Microfluidic Systems PLoS One 2014 9 10 e109815
59. L. Smirnova H. T. Hogberg M. Leist et al., Food for Thought...: Developmental Neurotoxicity-Challenges in the 21st Century and In Vitro Opportunities Altex 2014 31 2 129
60. A. D. Doyle F. W. Wang K. Matsumoto et al., One-dimensional topography underlies three-dimensional fibrillar cell migration J. Cell Biol. 2009 184 4 481 490