Human pluripotent stem cell-derived neural constructs for predicting neural toxicity

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 40, 2015, Pages 12516-12521

  Schwartz, Michael P ^a   Hou, Zhonggang ^b,g   Propson, Nicholas E ^b   Zhang, Jue ^b   Engstrom, Collin J ^c,d   Costa, Vitor Santos ^e   Jiang, Peng ^b   Nguyen, Bao Kim ^b   Bolin, Jennifer M ^b   Daly, William ^a   Wang, Yu ^b,h   Stewart, Ron ^b   Page, C David ^c,d   Murphy, William L ^a,c   Thomson, James A ^b,c,f  

^a University of Wisconsin Madison   (United States)

^b MORGRIDGE INSTITUTE FOR RESEARCH   (United States)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^d University of Wisconsin   (United States)

^e UNIVERSITY OF PORTO   (Portugal)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g HARVARD MEDICAL SCHOOL   (United States)

^h INSTITUTE OF ZOOLOGY   (China)

Author keywords

Differentiation; Machine learning; Organoid; Tissue engineering; Toxicology

Indexed keywords

CHEMICAL AGENT; MACROGOL; HYDROGEL; MACROGOL DERIVATIVE; SERUM-FREE MEDIUM; XENOBIOTIC AGENT;

ARTICLE; BRAIN DEVELOPMENT; CELL INTERACTION; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; ENDOTHELIUM CELL; GENE EXPRESSION; GLIA; HUMAN; HUMAN CELL; HYDROGEL; MACROPHAGE; MESENCHYMAL STEM CELL; MICROGLIA; NERVE CELL NETWORK; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROTOXICITY; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; RNA SEQUENCE; SUPPORT VECTOR MACHINE; BIOLOGICAL MODEL; BRAIN; CELL COMMUNICATION; CELL CULTURE; CELL DIFFERENTIATION; CLASSIFICATION; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENE ONTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; MESENCHYMAL STROMA CELL; METABOLISM; PHARMACOLOGY; PROCEDURES; SERUM-FREE MEDIUM; TISSUE ENGINEERING;

BRAIN; CELL COMMUNICATION; CELL DIFFERENTIATION; CELLS, CULTURED; CULTURE MEDIA, SERUM-FREE; EMBRYONIC STEM CELLS; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE ONTOLOGY; HUMANS; HYDROGELS; MACROPHAGES; MESENCHYMAL STROMAL CELLS; MICROGLIA; MODELS, BIOLOGICAL; NEURAL STEM CELLS; NEUROGENESIS; PLURIPOTENT STEM CELLS; POLYETHYLENE GLYCOLS; SUPPORT VECTOR MACHINE; TISSUE ENGINEERING; XENOBIOTICS;

EID: 84943372486     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1516645112     Document Type: Article

References (63)

1. Fabre KM, Livingston C, Tagle DA (2014) Organs-on-chips (microphysiological systems): Tools to expedite efficacy and toxicity testing in human tissue. Exp Biol Med (Maywood) 239(9): 1073-1077.
2. Judson R, et al. (2014) In vitro and modelling approaches to risk assessment from the U.S. Environmental Protection Agency ToxCast programme. Basic Clin Pharmacol Toxicol 115(1): 69-76.
3. Crofton KM, et al. (2011) Developmental neurotoxicity testing: Recommendations for developing alternative methods for the screening and prioritization of chemicals. ALTEX 28(1): 9-15.
4. Grandjean P, Landrigan PJ (2014) Neurobehavioural effects of developmental toxicity. Lancet Neurol 13(3): 330-338.
5. Bal-Price A, et al. (2015) International STakeholder NETwork (ISTNET): Creating a developmental neurotoxicity (DNT) testing road map for regulatory purposes. Arch Toxicol 89(2): 269-287.
6. Hay M, Thomas DW, Craighead JL, Economides C, Rosenthal J (2014) Clinical development success rates for investigational drugs. Nat Biotechnol 32(1): 40-51.
7. Olson H, et al. (2000) Concordance of the toxicity of pharmaceuticals in humans and in animals. Regul Toxicol Pharmacol 32(1): 56-67.
8. Rice D, Barone S, Jr (2000) Critical periods of vulnerability for the developing nervous system: Evidence from humans and animal models. Environ Health Perspect 108(Suppl 3): 511-533.
9. Bystron I, Blakemore C, Rakic P (2008) Development of the human cerebral cortex: Boulder Committee revisited. Nat Rev Neurosci 9(2): 110-122.
10. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A (2011) Physiology of microglia. Physiol Rev 91(2): 461-553.
11. Verney C, Monier A, Fallet-Bianco C, Gressens P (2010) Early microglial colonization of the human forebrain and possible involvement in periventricular white-matter injury of preterm infants. J Anat 217(4): 436-448.
12. Arnold T, Betsholtz C (2013) The importance of microglia in the development of the vasculature in the central nervous system. Vasc Cell 5(1): 4.
13. Stolp H, Neuhaus A, Sundramoorthi R, Molnár Z (2012) The long and the short of it: Gene and environment interactions during early cortical development and consequences for long-term neurological disease. Front Psychiatry 3: 50.
14. Marín-Padilla M (2012) The human brain intracerebral microvascular system: Development and structure. Front Neuroanat 6: 38.
15. James JM, Mukouyama YS (2011) Neuronal action on the developing blood vessel pattern. Semin Cell Dev Biol 22(9): 1019-1027.
16. Lidsky TI, Schneider JS (2003) Lead neurotoxicity in children: Basic mechanisms and clinical correlates. Brain 126(Pt 1): 5-19.
17. Block ML, Hong JS (2005) Microglia and inflammation-mediated neurodegeneration: Multiple triggers with a common mechanism. Prog Neurobiol 76(2): 77-98.
18. de Groot MW, Westerink RHS, Dingemans MML (2013) Don't judge a neuron only by its cover: Neuronal function in in vitro developmental neurotoxicity testing. Toxicol Sci 132(1): 1-7.
19. Monnet-Tschudi F, Zurich MG, Honegger P (2007) Neurotoxicant-induced inflammatory response in three-dimensional brain cell cultures. Hum Exp Toxicol 26(4): 339-346.
20. Eskes C, Juillerat-Jeanneret L, Leuba G, Honegger P, Monnet-Tschudi F (2003) Involvement of microglia-neuron interactions in the tumor necrosis factor-alpha release, microglial activation, and neurodegeneration induced by trimethyltin. J Neurosci Res 71(4): 583-590.
21. Thomson JA, et al. (1998) Embryonic stem cell lines derived from human blastocysts. Science 282(5391): 1145-1147.
22. Yu J, et al. (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318(5858): 1917-1920.
23. Takahashi K, et al. (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131(5): 861-872.
24. Chambers SM, et al. (2009) Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotechnol 27(3): 275-280.
25. Vodyanik MA, et al. (2010) A mesoderm-derived precursor for mesenchymal stem and endothelial cells. Cell Stem Cell 7(6): 718-729.
26. Stratman AN, Davis GE (2012) Endothelial cell-pericyte interactions stimulate basement membrane matrix assembly: Influence on vascular tube remodeling, maturation, and stabilization. Microsc Microanal 18(1): 68-80.
27. Fairbanks BD, et al. (2009) A versatile synthetic extracellular matrix mimic via thiolnorbornene photopolymerization. Adv Mater 21(48): 5005-5010.
28. Hansen TD, et al. (2014) Biomaterial arrays with defined adhesion ligand densities and matrix stiffness identify distinct phenotypes for tumorigenic and nontumorigenic human mesenchymal cell types. Biomater Sci 2(5): 745-756.
29. Hou Z, et al. (2015) A cost-effective RNA sequencing protocol for large-scale gene expression studies. Sci Rep 5: 9570.
30. Miller JA, et al. (2014) Transcriptional landscape of the prenatal human brain. Nature 508(7495): 199-206.
31. Hawrylycz MJ, et al. (2012) An anatomically comprehensive atlas of the adult human brain transcriptome. Nature 489(7416): 391-399.
32. Leng N, et al. (2013) EBSeq: An empirical Bayes hierarchical model for inference in RNA-seq experiments. Bioinformatics 29(8): 1035-1043.
33. Huang W, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4(1): 44-57.
34. Ashburner M, et al.; The Gene Ontology Consortium (2000) Gene ontology: Tool for the unification of biology. Nat Genet 25(1): 25-29.
35. Zecevic N, Milosevic A, Rakic S, Marín-Padilla M (1999) Early development and composition of the human primordial plexiform layer: An immunohistochemical study. J Comp Neurol 412(2): 241-254.
36. Ip BK, Bayatti N, Howard NJ, Lindsay S, Clowry GJ (2011) The corticofugal neuron-associated genes ROBO1, SRGAP1, and CTIP2 exhibit an anterior to posterior gradient of expression in early fetal human neocortex development. Cereb Cortex 21(6): 1395-1407.
37. Bystron I, Rakic P, Molnár Z, Blakemore C (2006) The first neurons of the human cerebral cortex. Nat Neurosci 9(7): 880-886.
38. Zecevic N (2004) Specific characteristic of radial glia in the human fetal telencephalon. Glia 48(1): 27-35.
39. Lui JH, Hansen DV, Kriegstein AR (2011) Development and evolution of the human neocortex. Cell 146(1): 18-36.
40. Uenishi G, et al. (2014) Tenascin C promotes hematoendothelial development and T lymphoid commitment from human pluripotent stem cells in chemically defined conditions. Stem Cell Rep 3(6): 1073-1084.
41. Ginhoux F, et al. (2010) Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330(6005): 841-845.
42. Vapnik VN (1998) Statistical Learning Theory (Wiley, New York).
43. Cortes C, Vapnik V (1995) Support-Vector Networks. Mach Learn 20(3): 273-297.
44. Furey TS, et al. (2000) Support vector machine classification and validation of cancer tissue samples using microarray expression data. Bioinformatics 16(10): 906-914.
45. Struyf J, Dobrin S, Page D (2008) Combining gene expression, demographic and clinical data in modeling disease: A case study of bipolar disorder and schizophrenia. BMC Genomics 9: 531.
46. Hardin J, et al. (2004) Evaluation of multiple models to distinguish closely related forms of disease using DNA microarray data: An application to multiple myeloma. Stat Appl Genet Mol Biol 3: e10.
47. Golub TR, et al. (1999) Molecular classification of cancer: Class discovery and class prediction by gene expression monitoring. Science 286(5439): 531-537.
48. Guyon I, Weston J, Barnhill S, Vapnik V (2002) Gene selection for cancer classification using support vector machines. Mach Learn 46(1-3): 389-422.
49. Zhang SC, Wernig M, Duncan ID, Brüstle O, Thomson JA (2001) In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat Biotechnol 19(12): 1129-1133.
50. Stein JL, et al. (2014) A quantitative framework to evaluate modeling of cortical development by neural stem cells. Neuron 83(1): 69-86.
51. Gaspard N, Vanderhaeghen P (2010) Mechanisms of neural specification from embryonic stem cells. Curr Opin Neurobiol 20(1): 37-43.
52. Eiraku M, Sasai Y (2012) Self-formation of layered neural structures in three-dimensional culture of ES cells. Curr Opin Neurobiol 22(5): 768-777.
53. Lancaster MA, Knoblich JA (2014) Organogenesis in a dish: Modeling development and disease using organoid technologies. Science 345(6194): 1247125.
54. Hughes CS, Postovit LM, Lajoie GA (2010) Matrigel: A complex protein mixture required for optimal growth of cell culture. Proteomics 10(9): 1886-1890.
55. Nagase H, Fields GB (1996) Human matrix metalloproteinase specificity studies using collagen sequence-based synthetic peptides. Biopolymers 40(4): 399-416.
56. Pierschbacher MD, Ruoslahti E (1984) Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule. Nature 309(5963): 30-33.
57. Krug AK, et al. (2013) Human embryonic stem cell-derived test systems for developmental neurotoxicity: A transcriptomics approach. Arch Toxicol 87(1): 123-143.
58. Pennings JLA, Theunissen PT, Piersma AH (2012) An optimized gene set for tran-scriptomics based neurodevelopmental toxicity prediction in the neural embryonic stem cell test. Toxicology 300(3): 158-167.
59. Teubert A, Thome J, Büttner A, Richter J, Irmisch G (2013) Elevated oleic acid serum concentrations in patients suffering from alcohol dependence. J Mol Psychiatry 1(1): 13.
60. Polo-Hernández E, De Castro F, García-García AG, Tabernero A, Medina JM (2010) Oleic acid synthesized in the periventricular zone promotes axonogenesis in the striatum during brain development. J Neurochem 114(6): 1756-1766.
61. Edmond J (2001) Essential polyunsaturated fatty acids and the barrier to the brain: The components of a model for transport. J Mol Neurosci 16(2-3): 181-193, discussion 215-221
62. Moya ML, Hsu Y, Lee AP, Hughes CCW, George SC (2013) In vitro perfused human capillary networks. Tiss. Eng. Part C Methods 19(9): 730-737.
63. Domansky K, et al. (2010) Perfused multiwell plate for 3D liver tissue engineering. Lab Chip 10(1): 51-58.