Engineered human pluripotent-stem-cell-derived intestinal tissues with a functional enteric nervous system

Nature Medicine

Volumn 23, Issue 1, 2017, Pages 49-59

  Workman, Michael J ^a   Mahe, Maxime M ^a   Trisno, Stephen ^a   Poling, Holly M ^a   Watson, Carey L ^a   Sundaram, Nambirajan ^a   Chang, Ching Fang ^a   Schiesser, Jacqueline ^a   Aubert, Philippe ^b   Stanley, Edouard G ^c,d,e   Elefanty, Andrew G ^c,d,e   Miyaoka, Yuichiro ^f   Mandegar, Mohammad A ^f   Conklin, Bruce R ^f,g   Neunlist, Michel ^b   Brugmann, Samantha A ^a   Helmrath, Michael A ^a   Wells, James M ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b UNIVERSITÉ DE NANTES   (France)

^c ROYAL CHILDREN'S HOSPITAL   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e MONASH UNIVERSITY   (Australia)

^f GLADSTONE INSTITUTES   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; HOMEODOMAIN PROTEIN; NBPHOX PROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; CELL DIFFERENTIATION; CYTOPLASM; EMBRYONIC STEM CELL; EXCITATION CONTRACTION COUPLING; GASTROINTESTINAL TRACT; GENE; GENE MUTATION; GLIA; GLIA CELL; HIRSCHSPRUNG DISEASE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; INDUCED PLURIPOTENT STEM CELL; INTERSTITIAL CELL OF CAJAL; INTESTINE INNERVATION; INTESTINE TISSUE; MESENCHYME; NERVE CELL; NEURAL CREST CELL; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; SUBMUCOUS PLEXUS; TISSUE ENGINEERING; ANIMAL; BIOLOGICAL MODEL; CELL LINE; CHICK EMBRYO; CONFOCAL MICROSCOPY; GASTROINTESTINAL MOTILITY; GENETICS; IMMUNOHISTOCHEMISTRY; INTESTINE; METABOLISM; MOUSE; MUTATION; MYENTERIC PLEXUS; NERVOUS SYSTEM DEVELOPMENT; NEURAL CREST; PATHOPHYSIOLOGY; PERMEABILITY; PHYSIOLOGY; PROCEDURES; REAL TIME POLYMERASE CHAIN REACTION; SCID MOUSE;

ANIMALS; CALCIUM; CELL LINE; CHICK EMBRYO; ENTERIC NERVOUS SYSTEM; GASTROINTESTINAL MOTILITY; HIRSCHSPRUNG DISEASE; HOMEODOMAIN PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; IN VITRO TECHNIQUES; INDUCED PLURIPOTENT STEM CELLS; INTERSTITIAL CELLS OF CAJAL; INTESTINES; MICE; MICE, SCID; MICROSCOPY, CONFOCAL; MODELS, BIOLOGICAL; MUTATION; MYENTERIC PLEXUS; NEURAL CREST; NEUROGENESIS; NEUROGLIA; NEURONS; ORGANOIDS; PERMEABILITY; REAL-TIME POLYMERASE CHAIN REACTION; SUBMUCOUS PLEXUS; TISSUE ENGINEERING; TRANSCRIPTION FACTORS;

EID: 84996968386     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.4233     Document Type: Article

References (46)

1. Furness, J.B. The enteric nervous system and neurogastroenterology. Nat. Rev. Gastroenterol. Hepatol. 9, 286-294 (2012).
2. Sasselli, V., Pachnis, V. & Burns, A.J. The enteric nervous system. Dev. Biol. 366, 64-73 (2012).
3. Obermayr, F., Hotta, R., Enomoto, H. & Young, H.M. Development and developmental disorders of the enteric nervous system. Nat. Rev. Gastroenterol. Hepatol. 10, 43-57 (2013).
4. Saffrey, M.J. Cellular changes in the enteric nervous system during ageing. Dev. Biol. 382, 344-355 (2013).
5. McKeown, S.J., Stamp, L., Hao, M.M. & Young, H.M. Hirschsprung disease: a developmental disorder of the enteric nervous system. Wiley Interdiscip. Rev. Dev. Biol. 2, 113-129 (2013).
6. Burns, A.J. & Thapar, N. Neural stem cell therapies for enteric nervous system disorders. Nat. Rev. Gastroenterol. Hepatol. 11, 317-328 (2014).
7. Hao, M.M. & Young, H.M. Development of enteric neuron diversity. J. Cell. Mol. Med. 13, 1193-1210 (2009).
8. Lancaster, M.A. & Knoblich, J.A. Organogenesis in a dish: modeling development and disease using organoid technologies. Science 345, 1247125 (2014).
9. McCracken, K.W., Howell, J.C., Wells, J.M. & Spence, J.R. Generating human intestinal tissue from pluripotent stem cells in vitro. Nat. Protoc. 6, 1920-1928 (2011).
10. Spence, J.R. et al. Directed differentiation of human pluripotent stem cells into intestinal tissue in vitro. Nature 470, 105-109 (2011).
11. Watson, C.L. et al. An in vivo model of human small intestine using pluripotent stem cells. Nat. Med. 20, 1310-1314 (2014).
12. Bajpai, R. et al. CHD7 cooperates with PBAF to control multipotent neural crest formation. Nature 463, 958-962 (2010).
13. Mica, Y., Lee, G., Chambers, S.M., Tomishima, M.J. & Studer, L. Modeling neural crest induction, melanocyte specifcation, and disease-related pigmentation defects in hESCs and patient-specifc iPSCs. Cell Rep. 3, 1140-1152 (2013).
14. Kudoh, T., Wilson, S.W. & Dawid, I.B. Distinct roles for Fgf, Wnt and retinoic acid in posteriorizing the neural ectoderm. Development 129, 4335-4346 (2002).
15. Fu, M., Tam, P.K., Sham, M.H. & Lui, V.C. Embryonic development of the ganglion plexuses and the concentric layer structure of human gut: a topographical study. Anat. Embryol. (Berl.) 208, 33-41 (2004).
16. Young, H.M., Ciampoli, D., Hsuan, J. & Canty, A.J. Expression of Ret-, p75(NTR)-, Phox2a-, Phox2b-, and tyrosine hydroxylase-immunoreactivity by undifferentiated neural crest-derived cells and different classes of enteric neurons in the embryonic mouse gut. Dev. Dyn. 216, 137-152 (1999).
17. Young, H.M. et al. GDNF is a chemoattractant for enteric neural cells. Dev. Biol. 229, 503-516 (2001).
18. Chen, T.W. et al. Ultrasensitive fuorescent proteins for imaging neuronal activity. Nature 499, 295-300 (2013).
19. Huebsch, N. et al. Automated video-based analysis of contractility and calcium fux in human-induced pluripotent stem cell-derived cardiomyocytes cultured over different spatial scales. Tissue Eng. Part C Methods 21, 467-479 (2015).
20. Hao, M.M. et al. Enteric nervous system assembly: functional integration within the developing gut. Dev. Biol. 417, 168-181 (2016).
21. Bohórquez, D.V. et al. Neuroepithelial circuit formed by innervation of sensory enteroendocrine cells. J. Clin. Invest. 125, 782-786 (2015).
22. Bajaj, R. et al. Congenital central hypoventilation syndrome and Hirschsprung's disease in an extremely preterm infant. Pediatrics 115, e737-e738 (2005).
23. Pattyn, A., Morin, X., Cremer, H., Goridis, C. & Brunet, J.F. The homeobox gene Phox2b is essential for the development of autonomic neural crest derivatives. Nature 399, 366-370 (1999).
24. Fu, M., Lui, V.C., Sham, M.H., Cheung, A.N. & Tam, P.K. HOXB5 expression is spatially and temporarily regulated in human embryonic gut during neural crest cell colonization and differentiation of enteric neuroblasts. Dev. Dyn. 228, 1-10 (2003).
25. Lui, V.C. et al. Perturbation of hoxb5 signaling in vagal neural crests down-regulates ret leading to intestinal hypoganglionosis in mice. Gastroenterology 134, 1104-1115 (2008).
26. Denham, M. et al. Multipotent caudal neural progenitors derived from human pluripotent stem cells that give rise to lineages of the central and peripheral nervous system. Stem Cells 33, 1759-1770 (2015).
27. Wallace, A.S. & Burns, A.J. Development of the enteric nervous system, smooth muscle and interstitial cells of Cajal in the human gastrointestinal tract. Cell Tissue Res. 319, 367-382 (2005).
28. Kabouridis, P.S. et al. Microbiota controls the homeostasis of glial cells in the gut lamina propria. Neuron 85, 289-295 (2015).
29. Bergner, A.J. et al. Birthdating of myenteric neuron subtypes in the small intestine of the mouse. J. Comp. Neurol. 522, 514-527 (2014).
30. Erickson, C.S. et al. Appearance of cholinergic myenteric neurons during enteric nervous system development: comparison of different ChAT fuorescent mouse reporter lines. Neurogastroenterol. Motil. 26, 874-884 (2014).
31. Baetge, G. & Gershon, M.D. Transient catecholaminergic (TC) cells in the vagus nerves and bowel of fetal mice: relationship to the development of enteric neurons. Dev. Biol. 132, 189-211 (1989).
32. Blaugrund, E. et al. Distinct subpopulations of enteric neuronal progenitors defned by time of development, sympathoadrenal lineage markers and Mash-1-dependence. Development 122, 309-320 (1996).
33. Anlauf, M., Schäfer, M.K., Eiden, L. & Weihe, E. Chemical coding of the human gastrointestinal nervous system: cholinergic, VIPergic, and catecholaminergic phenotypes. J. Comp. Neurol. 459, 90-111 (2003).
34. Anderson, G. et al. Loss of enteric dopaminergic neurons and associated changes in colon motility in an MPTP mouse model of Parkinson's disease. Exp. Neurol. 207, 4-12 (2007).
35. Burns, A.J. et al. White paper on guidelines concerning enteric nervous system stem cell therapy for enteric neuropathies. Dev. Biol. 417, 229-251 (2016).
36. Fattahi, F. et al. Deriving human ENS lineages for cell therapy and drug discovery in Hirschsprung disease. Nature 531, 105-109 (2016).
37. Hotta, R. et al. Transplanted progenitors generate functional enteric neurons in the postnatal colon. J. Clin. Invest. 123, 1182-1191 (2013).
38. Lindley, R.M. et al. Human and mouse enteric nervous system neurosphere transplants regulate the function of aganglionic embryonic distal colon. Gastroenterology 135, 205-216 (2008).
39. Burns, A.J., Roberts, R.R., Bornstein, J.C. & Young, H.M. Development of the enteric nervous system and its role in intestinal motility during fetal and early postnatal stages. Semin. Pediatr. Surg. 18, 196-205 (2009).
40. Miyaoka, Y. et al. Isolation of single-base genome-edited human iPS cells without antibiotic selection. Nat. Methods 11, 291-293 (2014).
41. Costa, M. et al. A method for genetic modifcation of human embryonic stem cells using electroporation. Nat. Protoc. 2, 792-796 (2007).
42. Hockemeyer, D. et al. Genetic engineering of human pluripotent cells using TALE nucleases. Nat. Biotechnol. 29, 731-734 (2011).
43. Tang, W. et al. Faithful expression of multiple proteins via 2A-peptide self-processing: a versatile and reliable method for manipulating brain circuits. J. Neurosci. 29, 8621-8629 (2009).
44. Lee, G. et al. Isolation and directed differentiation of neural crest stem cells derived from human embryonic stem cells. Nat. Biotechnol. 25, 1468-1475 (2007).
45. Chen, J., Bardes, E.E., Aronow, B.J. & Jegga, A.G. ToppGene Suite for gene list enrichment analysis and candidate gene prioritization. Nucleic Acids Res. 37, W305-11 (2009).
46. Supek, F., Bošnjak, M., Škunca, N. & Šmuc, T. REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One 6, e21800 (2011).