Rapid induction of cerebral organoids from human induced pluripotent stem cells using a chemically defined hydrogel and defined cell culture medium

Stem Cells Translational Medicine

Volumn 5, Issue 7, 2016, Pages 970-979

  Lindborg, Beth A ^a,b   Brekke, John H ^b   Vegoe, Amanda L ^a   Ulrich, Connor B ^a   Haider, Kerri T ^a   Subramaniam, Sandhya ^a   Venhuizen, Scott L ^a   Eide, Cindy R ^a,c   Orchard, Paul J ^c   Chen, Weili ^a,c   Wang, Qi ^a   Pelaez, Francisco ^d   Scott, Carolyn M ^d   Kokkoli, Efrosini ^d   Keirstead, Susan A ^a   Dutton, James R ^a   Tolar, Jakub ^a,c   O’Brien, Timothy D ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b Bioactive Regenerative Therapeutics   (United States)

^c UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^d University of Minnesota   (United States)

Author keywords

Adrenoleukodystrophy; Brain; In vitro techniques; Organoids; Stem cells

Indexed keywords

BETA TUBULIN; CALCIUM; CHITOSAN; DOUBLECORTIN; EARLY GROWTH RESPONSE FACTOR 2; FORKHEAD TRANSCRIPTION FACTOR; FORKHEAD TRANSCRIPTION FACTOR G1; GLUTAMIC ACID; HYALURONIC ACID; NESTIN; NUCLEAR RECEPTOR RELATED FACTOR 1; REELIN; TRANSCRIPTION FACTOR SIX3; TRANSCRIPTION FACTOR SOX1; TRANSCRIPTION FACTOR SOX2; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG; CULTURE MEDIUM; HYDROGEL;

ADRENOLEUKODYSTROPHY; ARTICLE; ARTIFICIAL ORGAN; BRAIN CELL; BRAIN DEVELOPMENT; CASE REPORT; CEREBRAL ORGANOID; CONTROLLED STUDY; CULTURE MEDIUM; DEPOLARIZATION; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; HYDROGEL; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; MALE; MECHANICS; PLURIPOTENT STEM CELL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; BIOMECHANICS; BRAIN; CELL CULTURE; CELL DIFFERENTIATION; CHEMISTRY; CYTOLOGY; CYTOPLASM; GENETICS; INDUCED PLURIPOTENT STEM CELL; METABOLISM; NERVE CELL; PHARMACOLOGY; PHYSIOLOGY; PROCEDURES; TISSUE CULTURE TECHNIQUE;

BIOMECHANICAL PHENOMENA; BRAIN; CELL DIFFERENTIATION; CELLS, CULTURED; CULTURE MEDIA; GENE EXPRESSION; HUMANS; HYDROGEL; INDUCED PLURIPOTENT STEM CELLS; NEURONS; ORGANOIDS; TISSUE CULTURE TECHNIQUES;

EID: 84976402821     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.5966/sctm.2015-0305     Document Type: Article

References (36)

1. Baker BM, Chen CS. Deconstructing the third dimension: How 3D culture microenvironments alter cellular cues. J Cell Sci 2012; 125: 3015–3024.
2. Sasai Y, Eiraku M, Suga H. In vitro organogenesis in three dimensions: Self-organising stem cells. Development 2012; 139: 4111–4121.
3. Karus M, Blaess S, Brüstle O. Self-organization of neural tissue architectures from pluripotent stem cells. J Comp Neurol 2014; 522: 2831–2844.
4. Lancaster MA, Knoblich JA. Organogenesis in a dish: Modeling development and disease using organoid technologies. Science 2014; 345: 1247125.
5. Lancaster MA, Renner M, Martin CA et al. Cerebral organoids model human brain development and microcephaly. Nature 2013; 501: 373–379.
6. Kadoshima T, Sakaguchi H, Nakano T et al. Self-organization of axial polarity, inside-out layer pattern, and species-specific progenitor dynamics in human ES cell-derived neocortex [published correction appears in Proc Natl Acad Sci USA 2014; 111: 7498]. Proc Natl Acad Sci USA 2013; 110: 20284–20289.
7. Berger J, Gärtner J. X-linked adrenoleukodystrophy: Clinical, biochemical and pathogenetic aspects. Biochim Biophys Acta 2006; 1763: 1721–1732.
8. Berger J, Forss-Petter S, Eichler FS. Pathophysiology of X-linked adrenoleukodystrophy. Biochimie 2014; 98: 135–142.
9. Miller WP, Rothman SM, Nascene D et al. Outcomes after allogeneic hematopoietic cell transplantation for childhood cerebral adrenoleukodystrophy: The largest single-institution cohort report. Blood 2011; 118: 1971–1978.
10. Lund TC, Stadem PS, Panoskaltsis-Mortari A et al. Elevated cerebral spinal fluid cytokine levels in boyswithcerebral adrenoleukodystrophycorrelates with MRI severity. PLo S One 2012; 7: e32218.
11. McKinney AM, Nascene D, Miller WP et al. Childhood cerebral X-linked adrenoleukodystrophy: diffusion tensor imaging measurements for prediction of clinical outcome after hematopoietic stem cell transplantation. AJNR Am J Neuroradiol 2013; 34: 641–649.
12. Orchard PJ, Lund T, Miller W et al. Chitotriosidase as a biomarker of cerebral adrenoleukodystrophy. J Neuroinflammation 2011; 8: 144.
13. Lindborg B, Brekke JH, Scott CM et al. A novel chitosan-hyaluronan based hydrocolloid supports in vitro culture and differentiation of human mesenchymal stem/ stromal cells (MSC). Tissue Eng A 2015; 21: 1952–1962.
14. Wu J, Okamura D, Li M et al. An alternative pluripotent state confers interspecies chimaeric competency. Nature 2015; 521: 316–321.
15. Rathjen J, Lake JA, Bettess MD et al. Formation of a primitive ectoderm like cell population, EPL cells, from ES cells in response to biologically derived factors. J Cell Sci 1999; 112: 601–612.
16. Rathjen J, Haines BP, Hudson KM et al. Directed differentiation of pluripotent cells to neural lineages: Homogeneous formation and differentiation of a neurectoderm population. Development 2002; 129: 2649–2661.
17. Mariani J, Simonini MV, Palejev D et al. Modeling human cortical development in vitro using induced pluripotent stem cells. Proc Natl Acad Sci USA 2012; 109: 12770–12775.
18. Eiraku M, Sasai Y. Mouseembryonic stem cell culture for generation of three-dimensional retinal and cortical tissues. Nat Protoc 2011; 7: 69–79.
19. Eiraku M, Watanabe K, Matsuo-Takasaki M et al. Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. Cell Stem Cell 2008; 3: 519–532.
20. Nasu M, Takata N, Danjo T et al. Robust formation and maintenance of continuous stratified cortical neuroepithelium by laminincontaining matrix in mouse ES cell culture. PLo S One 2012; 7: e53024.
21. Brekke J, Thacker K. Hyaluronan as a biomaterial. In: Hollinger J, Guelcher S, eds. Introduction to Biomaterials. Boca Raton, FL: CRC Press, 2006: 219–248.
22. Preston M, Sherman LS. Neural stem cell niches: Roles for the hyaluronan-based extracellular matrix. Front Biosci (Schol Ed) 2011; 3: 1165–1179.
23. Choudhary M, Zhang X, Stojkovic P et al. Putative role of hyaluronan and its related genes, HAS2 and RHAMM, in human early preimplantation embryogenesis and embryonic stem cell characterization. STEM CELLS 2007; 25: 3045–3057.
24. Termeer C, Benedix F, Sleeman J et al. Oligosaccharides of hyaluronan activate dendritic cells via toll-like receptor 4. J Exp Med 2002; 195: 99–111.
25. Jiang D, Liang J, Noble PW. Hyaluronan as an immune regulator in human diseases. Physiol Rev 2011; 91: 221–264.
26. Engler AJ, Sen S, Sweeney HL et al. Matrix elasticity directs stem cell lineage specification. Cell 2006; 126: 677–689.
27. Lee J, Abdeen AA, Kilian KA. Rewiring mesenchymal stem cell lineage specification by switching the biophysical microenvironment. Sci Rep 2014; 4: 5188.
28. Sun Y, Yong KMA, Villa-Diaz LG et al. Hippo/YAP-mediated rigidity-dependent motor neuron differentiation of human pluripotent stem cells. Nat Mater 2014; 13: 599–604.
29. Scott CM, Forster CL, Kokkoli E. Three-dimensional cell entrapment as a function of the weight percent of peptideamphiphile hydrogels. Langmuir 2015; 31: 6122–6129.
30. Leipzig ND, Shoichet MS. The effect of substrate stiffness on adult neural stem cell behavior. Biomaterials 2009; 30: 6867–6878.
31. Pashuck ET, Cui H, Stupp SI. Tuning supramolecular rigidity of peptide fibers through molecular structure. J Am Chem Soc 2010; 132: 6041–6046.
32. Meijering E, Jacob M, Sarria J-CF et al. Design and validation of a tool for neurite tracing and analysis in fluorescence microscopy images. Cytometry A 2004; 58: 167–176.
33. Paramonov SE, Jun HW, Hartgerink JD. Self-assembly of peptide-amphiphile nanofibers: The roles of hydrogen bonding and amphiphilic packing. J Am Chem Soc 2006; 128: 7291–7298.
34. Seidlits SK, Khaing ZZ, Petersen RR et al. The effects of hyaluronic acid hydrogels with tunable mechanical properties on neural progenitor cell differentiation. Biomaterials 2010; 31: 3930–3940.
35. Pan L, Ren Y, Cui F et al. Viability and differentiation of neural precursors on hyaluronic acid hydrogel scaffold. J Neurosci Res 2009; 87: 3207–3220.
36. Brännvall K, Bergman K, Wallenquist U et al. Enhanced neuronal differentiation in a three-dimensional collagen-hyaluronan matrix. J Neurosci Res 2007; 85: 2138–2146.