Enhancement of enteric neural stem cell neurogenesis by glial cell-derived neurotrophic factor in experimental Hirschsprung's disease.
Glial Cell Line-Derived Neurotrophic Factor
/ pharmacology
Animals
Hirschsprung Disease
/ genetics
Mice
Neural Stem Cells
Neurogenesis
/ physiology
Disease Models, Animal
Enteric Nervous System
Cell Differentiation
Mice, Knockout
Cells, Cultured
Neural Crest
/ cytology
Receptor, Endothelin B
/ genetics
Ednrb model mouse
Enteric nervous system
GDNF
Hirschsprung’s disease
Journal
Pediatric surgery international
ISSN: 1437-9813
Titre abrégé: Pediatr Surg Int
Pays: Germany
ID NLM: 8609169
Informations de publication
Date de publication:
26 Oct 2024
26 Oct 2024
Historique:
accepted:
16
10
2024
medline:
26
10
2024
pubmed:
26
10
2024
entrez:
26
10
2024
Statut:
epublish
Résumé
Stem cell therapy offers a promising solution for congenital diseases like Hirschsprung's disease (HSCR). Optimizing stem cell efficacy by modifying the cells and their environment is crucial, but in vitro culture conditions need to be further improved. Glial cell-derived neurotrophic factor (GDNF) plays an important role in neuronal survival, proliferation, migration and differentiation during enteric nervous system (ENS) development. In this study, the effects of GDNF on neurites derived from an Ednrb knockout model were investigated with the aim of enhancing the neurogenic potential of enteric neural crest cells (ENCCs). Neurospheres were generated form Ednrb GDNF-treated Ednrb GDNF effectively enhanced the neurogenic potential of ENCCs from HSCR animal model. This finding is crucial for the development of cell therapy in HSCR.
Identifiants
pubmed: 39460767
doi: 10.1007/s00383-024-05861-3
pii: 10.1007/s00383-024-05861-3
doi:
Substances chimiques
Glial Cell Line-Derived Neurotrophic Factor
0
EDNRB protein, mouse
0
Receptor, Endothelin B
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
274Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Heuckeroth RO (2018) Hirschsprung disease–integrating basic science and clinical medicine to improve outcomes. Nat Rev Gastroenterol Hepatol 15:152–167. https://doi.org/10.1038/nrgastro.2017.149
doi: 10.1038/nrgastro.2017.149
pubmed: 29300049
Burns AJ, Goldstein AM, Newgreen DF, Stamp L, Schäfer KH, Metzger M, Hotta R, Young HM, Andrews PW, Thapar N, Belkind-Gerson J, Bondurand N, Bornstein JC, Chan WY, Cheah K, Gershon MD, Heuckeroth RO, Hofstra RM, Just L, Kapur RP, King SK, McCann CJ, Nagy N, Ngan E, Obermayr F, Pachnis V, Pasricha PJ, Sham MH, Tam P, Vanden Berghe P (2016) White paper on guidelines concerning enteric nervous system stem cell therapy for enteric neuropathies. Dev Biol 417:229–251. https://doi.org/10.1016/j.ydbio.2016.04.001
doi: 10.1016/j.ydbio.2016.04.001
pubmed: 27059883
pmcid: 5026875
Goldstein AM, Thapar N, Karunaratne TB, De Giorgio R (2016) Clinical aspects of neurointestinal disease: pathophysiology, diagnosis, and treatment. Dev Biol 417:217–228. https://doi.org/10.1016/j.ydbio.2016.03.032
doi: 10.1016/j.ydbio.2016.03.032
pubmed: 27059882
Westfal ML, Goldstein AM (2017) Pediatric enteric neuropathies: diagnosis and current management. Curr Opin Pediatr 29:347–353. https://doi.org/10.1097/mop.0000000000000486
doi: 10.1097/mop.0000000000000486
pubmed: 28319561
pmcid: 5475271
Zimmer J, Tomuschat C, Puri P (2016) Long-term results of transanal pull-through for Hirschsprung’s disease: a meta-analysis. Pediatr Surg Int 32:743–749. https://doi.org/10.1007/s00383-016-3908-z
doi: 10.1007/s00383-016-3908-z
pubmed: 27385111
Laughlin DM, Friedmacher F, Puri P (2012) Total colonic aganglionosis: a systematic review and meta-analysis of long-term clinical outcome. Pediatr Surg Int 28:773–779. https://doi.org/10.1007/s00383-012-3117-3
doi: 10.1007/s00383-012-3117-3
pubmed: 22842648
Alhawaj AF (2022) Stem cell-based therapy for Hirschsprung disease, do we have the guts to treat? Gene Ther 29:578–587. https://doi.org/10.1038/s41434-021-00268-4
doi: 10.1038/s41434-021-00268-4
pubmed: 34121091
Trounson A, McDonald C (2015) Stem cell therapies in clinical trials: progress and challenges. Cell Stem Cell 17:11–22. https://doi.org/10.1016/j.stem.2015.06.007
doi: 10.1016/j.stem.2015.06.007
pubmed: 26140604
McCann CJ, Borrelli O, Thapar N (2018) Stem cell therapy in severe pediatric motility disorders. Curr Opin Pharmacol 43:145–149. https://doi.org/10.1016/j.coph.2018.09.004
doi: 10.1016/j.coph.2018.09.004
pubmed: 30340053
Metzger M, Bareiss PM, Danker T, Wagner S, Hennenlotter J, Guenther E, Obermayr F, Stenzl A, Koenigsrainer A, Skutella T, Just L (2009) Expansion and differentiation of neural progenitors derived from the human adult enteric nervous system. Gastroenterology 137:2063-2073.e2064. https://doi.org/10.1053/j.gastro.2009.06.038
doi: 10.1053/j.gastro.2009.06.038
pubmed: 19549531
Metzger M, Caldwell C, Barlow AJ, Burns AJ, Thapar N (2009) Enteric nervous system stem cells derived from human gut mucosa for the treatment of aganglionic gut disorders. Gastroenterology 136:2214–2225. https://doi.org/10.1053/j.gastro.2009.02.048
doi: 10.1053/j.gastro.2009.02.048
pubmed: 19505425
Hotta R, Natarajan D, Thapar N (2009) Potential of cell therapy to treat pediatric motility disorders. Semin Pediatr Surg 18:263–273. https://doi.org/10.1053/j.sempedsurg.2009.07.008
doi: 10.1053/j.sempedsurg.2009.07.008
pubmed: 19782309
Micci MA, Pasricha PJ (2007) Neural stem cells for the treatment of disorders of the enteric nervous system: strategies and challenges. Dev Dyn 236:33–43. https://doi.org/10.1002/dvdy.20975
doi: 10.1002/dvdy.20975
pubmed: 17029286
Laranjeira C, Pachnis V (2009) Enteric nervous system development: recent progress and future challenges. Auton Neurosci 151:61–69. https://doi.org/10.1016/j.autneu.2009.09.001
doi: 10.1016/j.autneu.2009.09.001
pubmed: 19783483
Sasselli V, Pachnis V, Burns AJ (2012) The enteric nervous system. Dev Biol 366:64–73. https://doi.org/10.1016/j.ydbio.2012.01.012
doi: 10.1016/j.ydbio.2012.01.012
pubmed: 22290331
Taraviras S, Marcos-Gutierrez CV, Durbec P, Jani H, Grigoriou M, Sukumaran M, Wang LC, Hynes M, Raisman G, Pachnis V (1999) Signalling by the RET receptor tyrosine kinase and its role in the development of the mammalian enteric nervous system. Development 126:2785–2797. https://doi.org/10.1242/dev.126.12.2785
doi: 10.1242/dev.126.12.2785
pubmed: 10331988
Airaksinen MS, Saarma M (2002) The GDNF family: signalling, biological functions and therapeutic value. Nat Rev Neurosci 3:383–394. https://doi.org/10.1038/nrn812
doi: 10.1038/nrn812
pubmed: 11988777
Young HM, Hearn CJ, Farlie PG, Canty AJ, Thomas PQ, Newgreen DF (2001) GDNF is a chemoattractant for enteric neural cells. Dev Biol 229:503–516. https://doi.org/10.1006/dbio.2000.0100
doi: 10.1006/dbio.2000.0100
pubmed: 11150245
Natarajan D, Marcos-Gutierrez C, Pachnis V, de Graaff E (2002) Requirement of signalling by receptor tyrosine kinase RET for the directed migration of enteric nervous system progenitor cells during mammalian embryogenesis. Development 129:5151–5160. https://doi.org/10.1242/dev.129.22.5151
doi: 10.1242/dev.129.22.5151
pubmed: 12399307
McKeown SJ, Mohsenipour M, Bergner AJ, Young HM, Stamp LA (2017) Exposure to GDNF enhances the ability of enteric neural progenitors to generate an enteric nervous system. Stem Cell Reports 8:476–488. https://doi.org/10.1016/j.stemcr.2016.12.013
doi: 10.1016/j.stemcr.2016.12.013
pubmed: 28089669
pmcid: 5312076
Heanue TA, Pachnis V (2007) Enteric nervous system development and Hirschsprung’s disease: advances in genetic and stem cell studies. Nat Rev Neurosci 8:466–479. https://doi.org/10.1038/nrn2137
doi: 10.1038/nrn2137
pubmed: 17514199
Shibata S, Yasuda A, Renault-Mihara F, Suyama S, Katoh H, Inoue T, Inoue YU, Nagoshi N, Sato M, Nakamura M, Akazawa C, Okano H (2010) Sox10-Venus mice: a new tool for real-time labeling of neural crest lineage cells and oligodendrocytes. Mol Brain 3:31. https://doi.org/10.1186/1756-6606-3-31
doi: 10.1186/1756-6606-3-31
pubmed: 21034515
pmcid: 2989948
Schriemer D, Sribudiani Y, IJpma A, Natarajan D, MacKenzie KC, Metzger M, Binder E, Burns AJ, Thapar N, Hofstra RMW, Eggen BJL (2016) Regulators of gene expression in enteric neural crest cells are putative Hirschsprung disease genes. Dev Biol 416:255–265. https://doi.org/10.1016/j.ydbio.2016.06.004
doi: 10.1016/j.ydbio.2016.06.004
pubmed: 27266404
Baloh RH, Enomoto H, Johnson EM Jr, Milbrandt J (2000) The GDNF family ligands and receptors–implications for neural development. Curr Opin Neurobiol 10:103–110. https://doi.org/10.1016/s0959-4388(99)00048-3
doi: 10.1016/s0959-4388(99)00048-3
pubmed: 10679429
Moore MW, Klein RD, Fariñas I, Sauer H, Armanini M, Phillips H, Reichardt LF, Ryan AM, Carver-Moore K, Rosenthal A (1996) Renal and neuronal abnormalities in mice lacking GDNF. Nature 382:76–79. https://doi.org/10.1038/382076a0
doi: 10.1038/382076a0
pubmed: 8657308
Airaksinen MS, Titievsky A, Saarma M (1999) GDNF family neurotrophic factor signaling: four masters, one servant? Mol Cell Neurosci 13:313–325. https://doi.org/10.1006/mcne.1999.0754
doi: 10.1006/mcne.1999.0754
pubmed: 10356294
Enomoto H, Crawford PA, Gorodinsky A, Heuckeroth RO, Johnson EM Jr, Milbrandt J (2001) RET signaling is essential for migration, axonal growth and axon guidance of developing sympathetic neurons. Development 128:3963–3974. https://doi.org/10.1242/dev.128.20.3963
doi: 10.1242/dev.128.20.3963
pubmed: 11641220
Schuchardt A, D’Agati V, Larsson-Blomberg L, Costantini F, Pachnis V (1994) Defects in the kidney and enteric nervous system of mice lacking the tyrosine kinase receptor Ret. Nature 367:380–383. https://doi.org/10.1038/367380a0
doi: 10.1038/367380a0
pubmed: 8114940
Ngan ES, Shum CK, Poon HC, Sham MH, Garcia-Barcelo MM, Lui VC, Tam PK (2008) Prokineticin-1 (Prok-1) works coordinately with glial cell line-derived neurotrophic factor (GDNF) to mediate proliferation and differentiation of enteric neural crest cells. Biochim Biophys Acta 1783:467–478. https://doi.org/10.1016/j.bbamcr.2007.09.005
doi: 10.1016/j.bbamcr.2007.09.005
pubmed: 18006159
Anitha M, Chandrasekharan B, Salgado JR, Grouzmann E, Mwangi S, Sitaraman SV, Srinivasan S (2006) Glial-derived neurotrophic factor modulates enteric neuronal survival and proliferation through neuropeptide Y. Gastroenterology 131:1164–1178. https://doi.org/10.1053/j.gastro.2006.07.019
doi: 10.1053/j.gastro.2006.07.019
pubmed: 17030186
Barlow AJ, Wallace AS, Thapar N, Burns AJ (2008) Critical numbers of neural crest cells are required in the pathways from the neural tube to the foregut to ensure complete enteric nervous system formation. Development 135:1681–1691. https://doi.org/10.1242/dev.017418
doi: 10.1242/dev.017418
pubmed: 18385256
Paratore C, Eichenberger C, Suter U, Sommer L (2002) Sox10 haploinsufficiency affects maintenance of progenitor cells in a mouse model of Hirschsprung disease. Hum Mol Genet 11:3075–3085. https://doi.org/10.1093/hmg/11.24.3075
doi: 10.1093/hmg/11.24.3075
pubmed: 12417529
Peters-van der Sanden MJ, Kirby ML, Gittenberger-de Groot A, Tibboel D, Mulder MP, Meijers C (1993) Ablation of various regions within the avian vagal neural crest has differential effects on ganglion formation in the fore-, mid- and hindgut. Dev Dyn 196:183–194. https://doi.org/10.1002/aja.1001960305
doi: 10.1002/aja.1001960305
pubmed: 8400404
Heuckeroth RO, Lampe PA, Johnson EM, Milbrandt J (1998) Neurturin and GDNF promote proliferation and survival of enteric neuron and glial progenitors in vitro. Dev Biol 200:116–129. https://doi.org/10.1006/dbio.1998.8955
doi: 10.1006/dbio.1998.8955
pubmed: 9698461
Chalazonitis A, Rothman TP, Chen J, Gershon MD (1998) Age-dependent differences in the effects of GDNF and NT-3 on the development of neurons and glia from neural crest-derived precursors immunoselected from the fetal rat gut: expression of GFRalpha-1 in vitro and in vivo. Dev Biol 204:385–406. https://doi.org/10.1006/dbio.1998.9090
doi: 10.1006/dbio.1998.9090
pubmed: 9882478
Amiel J, Sproat-Emison E, Garcia-Barcelo M, Lantieri F, Burzynski G, Borrego S, Pelet A, Arnold S, Miao X, Griseri P, Brooks AS, Antinolo G, de Pontual L, Clement-Ziza M, Munnich A, Kashuk C, West K, Wong KK, Lyonnet S, Chakravarti A, Tam PK, Ceccherini I, Hofstra RM, Fernandez R (2008) Hirschsprung disease, associated syndromes and genetics: a review. J Med Genet 45:1–14. https://doi.org/10.1136/jmg.2007.053959
doi: 10.1136/jmg.2007.053959
pubmed: 17965226
Carrasquillo MM, McCallion AS, Puffenberger EG, Kashuk CS, Nouri N, Chakravarti A (2002) Genome-wide association study and mouse model identify interaction between RET and EDNRB pathways in Hirschsprung disease. Nat Genet 32:237–244. https://doi.org/10.1038/ng998
doi: 10.1038/ng998
pubmed: 12355085
Zhou B, Feng C, Sun S, Chen X, Zhuansun D, Wang D, Yu X, Meng X, Xiao J, Wu L, Wang J, Wang J, Chen K, Li Z, You J, Mao H, Yang S, Zhang J, Jiao C, Li Z, Yu D, Wu X, Zhu T, Yang J, Xiang L, Liu J, Chai T, Shen J, Mao CX, Hu J, Hao X, Xiong B, Zheng S, Liu Z, Feng J (2024) Identification of signaling pathways that specify a subset of migrating enteric neural crest cells at the wavefront in mouse embryos. Dev Cell 59:1689-1706.e1688. https://doi.org/10.1016/j.devcel.2024.03.034
doi: 10.1016/j.devcel.2024.03.034
pubmed: 38636517
Cheng LS, Graham HK, Pan WH, Nagy N, Carreon-Rodriguez A, Goldstein AM, Hotta R (2016) Optimizing neurogenic potential of enteric neurospheres for treatment of neurointestinal diseases. J Surg Res 206:451–459. https://doi.org/10.1016/j.jss.2016.08.035
doi: 10.1016/j.jss.2016.08.035
pubmed: 27884342
pmcid: 5125510
Soret R, Schneider S, Bernas G, Christophers B, Souchkova O, Charrier B, Righini-Grunder F, Aspirot A, Landry M, Kembel SW, Faure C, Heuckeroth RO, Pilon N (2020) Glial cell-derived neurotrophic factor induces enteric neurogenesis and improves colon structure and function in mouse models of Hirschsprung disease. Gastroenterology 159:1824-1838.e1817. https://doi.org/10.1053/j.gastro.2020.07.018
doi: 10.1053/j.gastro.2020.07.018
pubmed: 32687927