Isolation of enteric nervous system progenitor cells from the aganglionic gut of patients with Hirschsprung's disease

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Wilkinson, David J ^a   Bethell, George S ^a   Shukla, Rajeev ^b   Kenny, Simon E ^a,b   Edgar, David H ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b ALDER HEY CHILDREN'S NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CALRETININ; GLIAL FIBRILLARY ACIDIC PROTEIN; NITRIC OXIDE SYNTHASE; PROTEIN P75; PROTEIN VIP; UNCLASSIFIED DRUG; NEURONAL NITRIC OXIDE SYNTHASE; NOS1 PROTEIN, HUMAN; VASOACTIVE INTESTINAL POLYPEPTIDE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUTOTRANSPLANTATION; CELL ISOLATION; CELL TRANSPLANTATION; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; EMBRYO; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; HIRSCHSPRUNG DISEASE; HUMAN; HUMAN CELL; INFANT; INTESTINE INNERVATION; MOUSE; MUSCLE CONTRACTILITY; NERVE CELL; NERVE CELL CULTURE; NEURAL CREST; NEUROSPHERE CELL; NONHUMAN; PROTEIN EXPRESSION; STEM CELL; ADULT STEM CELL; ANIMAL; CELL CULTURE TECHNIQUE; CELL DIFFERENTIATION; CELL SEPARATION; FLOW CYTOMETRY; INNERVATION; LARGE INTESTINE; METABOLISM; NEURAL STEM CELL; PATHOLOGY; PROCEDURES; TRANSPLANTATION; XENOGRAFT;

ADULT STEM CELLS; ANIMALS; BIOMARKERS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL SEPARATION; ENTERIC NERVOUS SYSTEM; FLOW CYTOMETRY; GLIAL FIBRILLARY ACIDIC PROTEIN; HETEROGRAFTS; HIRSCHSPRUNG DISEASE; HUMANS; INTESTINE, LARGE; MICE; NEURAL STEM CELLS; NITRIC OXIDE SYNTHASE TYPE I; VASOACTIVE INTESTINAL PEPTIDE;

EID: 84930622141     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0125724     Document Type: Article

References (31)

1. Yntema CL, Hammond WS. The origin of intrinsic ganglia of trunk viscera from vagal neural crest in the chick embryo. J Comp Neurol. 1954; 101: 515-541. PMID: 13221667
2. Obermayr F, Hotta R, Enomoto H, Young HM. Development and developmental disorders of the enteric nervous system. Nature Rev Gastroenterol. 2013; 10: 43-57. doi: 10.1038/nrgastro.2012.234 PMID: 23229326
3. Sasselli V, Pachnis V, Burns AJ. The enteric nervous system. Dev Biol. 2012; 366: 64-73. doi: 10.1016/j.ydbio.2012.01.012 PMID: 22290331
4. Burns AJ, Thapar N. Neural stem cell therapies for enteric nervous system disorders. Nature Rev Gastroenterol. 2014; 11: 317-328. doi: 10.1038/nrgastro.2013.226 PMID: 24322895
5. Almond SN, Lindley RM, Kenny SE, Connell MG, Edgar DH. Characterisation and transplantation of enteric nervous system progenitor cells. Gut. 2007; 56: 489-496. PMID: 16973717
6. Becker L, Kulkarni S, Tiwari G, Micci MA, Pasricha PJ. Divergent fate and origin of neurosphere-like bodies from different layers of the gut. Am J Physiol-Gastrl L. 2012; 302: G958-G965. doi: 10.1152/ajpgi.00511.2011 PMID: 22361728
7. Dettmann HM, Zhang Y, Wronna N, Kraushaar U, Guenther E, Mohr R, et al. Isolation, expansion and transplantation of postnatal murine progenitor cells of the enteric nervous system. Plos One. 2014; 9: 1-11.
8. Heanue TA, Pachnis V. Prospective identification and isolation of enteric nervous system progenitors using Sox2. Stem Cells. 2011; 29: 128-140. doi: 10.1002/stem.557 PMID: 21280162
9. Hotta R, Stamp LA, Foong JPP, McConnell SN, Bergner AJ, Anderson RB, et al. Transplanted progenitors generate functional enteric neurons in the postnatal colon. J Clin Invest. 2013; 123: 1182-1191. doi: 10.1172/JCI65963 PMID: 23454768
10. Lindley RM, Hawcutt DB, Connell MG, Almond SL, Vannucchi MG, Faussone-Pellegrini MS, et al. Human and mouse enteric nervous system neurosphere transplants regulate the function of aganglionic embryonic distal colon. Gastroenterol. 2008; 135: 205-216.
11. Joseph NM, He SH, Quintana E, Kim YG, Nunez G, Morrison SJ. Enteric glia are multipotent in culture but primarily form glia in the adult rodent gut. J Clin Invest. 2011; 121: 3398-3411. doi: 10.1172/JCI58186 PMID: 21865643
12. Laranjeira C, Sandgren K, Kessaris N, Richardson W, Potocnik A, Vanden Berghe P et al. Glial cells in the mouse enteric nervous system can undergo neurogenesis in response to injury. J Clin Invest. 2011; 121: 3412-3424. doi: 10.1172/JCI58200 PMID: 21865647
13. Kenny SE, Tam PKH, Garcia-Barcelo M. Hirschsprung's disease. Semin Pediatr Surg. 2010; 19: 194-200. doi: 10.1053/j.sempedsurg.2010.03.004 PMID: 20610192
14. Theocharatos S, Kenny SE. Hirschsprung's disease: Current management and prospects for transplantation of enteric nervous system progenitor cells. Early Hum Dev. 2008; 84: 801-804. doi: 10.1016/j.earlhumdev.2008.09.007 PMID: 18835114
15. Lindley RM, Hawcutt DB, Connell MG, Edgar DH, Kenny SE. Properties of secondary and tertiary human enteric nervous system neurospheres. J Pediatr Surg. 2009; 44: 1249-1256. doi: 10.1016/j.jpedsurg.2009.02.048 PMID: 19524749
16. Theocharatos S, Wilkinson DJ, Darling S, Wilm B, Kenny SE, et al. Regulation of progenitor cell proliferation and neuronal differentiation in enteric nervous system neurospheres. Plos One. 2013; 8: 1-8.
17. Barshack I, Fridman E, Goldberg I, Chowers Y, Kopolovic J. The loss of calretinin expression indicates aganglionosis in Hirschsprung's disease. J Clin Pathol. 2004; 57: 712-716. PMID: 15220363
18. Kapur RP. Practical pathology and genetics of Hirschsprung's disease. Semin Pediatr Surg. 2009; 18: 212-223. doi: 10.1053/j.sempedsurg.2009.07.003 PMID: 19782303
19. Baumgartner HG, Holstein AF, Stelzner F. Nervous elements in human colon of hirschsprungs disease. Virchows Arch A. 1973; 358: 113-136. PMID: 4632410
20. Kobayashi H, Obriain DS, Puri P. NGF receptor immunostaining suggests an extrinsic origin for hypertrophic nerves in Hirschsprungs-disease. Gut. 1994; 35: 1605-1607. PMID: 7828981
21. Erickson CS, Zaitoun I, Haberman KM, Gosain A, Druckenbrod NR, Epstein ML. Sacral neural crest-derived cells enter the aganglionic colon of Ednrb-/- mice along extrinsic nerve fibers. J Comp Neurol. 2012; 520: 620-632. doi: 10.1002/cne.22755 PMID: 21858821
22. Wang X, Chan AKK, Sham MH, Burns AJ, Chan WY. Analysis of the sacral neural crest cell contribution to the hindgut enteric nervous system in the mouse embryo. Gastroenterol. 2011; 141: 992-994.
23. Joseph NM, Mukouyama YS, Mosher JT, Jaegle M, Crone SA, Dormand EL, et al. Neural crest stem cells undergo multilineage differentiation in developing peripheral nerves to generate endoneurial fibroblasts in addition to Schwann cells. Development. 2004; 131: 5599-5612. PMID: 15496445
24. Akbareian SE, Nagy N, Steiger CE, Mably JD, Miller SA, Hotta R, et al. Enteric neural crest-derived cells promote their migration by modifying their microenvironment through tenascin-C production. Dev Biol. 2013; 382: 446-456. doi: 10.1016/j.ydbio.2013.08.006 PMID: 23958436
25. Miyahara K, Kato Y, Suzuki R, Azakawa C, Tanaka N, Koga H, et al. Anorectal neural crest derived cell behavior after the migration of vagal neural crest derived cells is surgically disrupted: implications for the etiology of Hirschsprung's disease. Pediatr Surg Int. 2013; 29: 9-12. doi: 10.1007/s00383-012-3201-8 PMID: 23143079
26. Kruger GM, Mosher JT, Tsai TH, Yeager KJ, Iwashita T, Gariepy CE. Temporally distinct requirements for endothelin receptor B in the generation and migration of gut neural crest stem cells. Neuron. 2003; 40: 917-929. PMID: 14659091
27. Liu MT, Kuan YH, Wang JW, Hen R, Gershon MD. 5-HT4 Receptor-mediated neuroprotection and neurogenesis in the enteric nervous system of adult mice. J Neurosci. 2009; 29: 9683-9699. doi: 10.1523/JNEUROSCI.1145-09.2009 PMID: 19657021
28. Dyachuk V, Furlan A, Shahidi MK, Giovenco M, Kaukua N, Konstantinidou C, et al. Parasympathetic neurons originate from nerve-associated peripheral glial progenitors. Science. 2014; 345: 82-87. doi: 10.1126/science.1253281 PMID: 24925909
29. Espinosa-Medina I, Outin E, Picard CA, Chettouh Z, Dymecki S, Consalez GG, et al. Parasympathetic ganglia derive from Schwann cell precursors. Science. 2014; 345: 87-90. doi: 10.1126/science.1253286 PMID: 24925912
30. Martin I, Nguyen TD, Krell V, Greiner JFW, Muller J, Hauser S, et al. Generation of Schwann sell-derived multipotent neurospheres isolated from intact sciatic nerve. Stem Cell Rev Rep. 2012; 8: 1178-1187. doi: 10.1007/s12015-012-9387-2 PMID: 22664741
31. Solari V, Piotrowska AP, Puri P. Histopathological differences between recto-sigmoid Hirschsprung's disease and total colonic aganglionosis. Pediatr Surg Int. 2003; 19: 349-354. PMID: 12756596