Differentiation of enteric neural crest cells transplanted from SOX10-Venus mouse embryonic stem cells into the gut of the endothelin receptor B null mouse model

Pediatric Surgery International - Tập 39 - Trang 1-8 - 2022
Naho Fujiwara1, Katsumi Miyahara1, Nana Nakazawa-Tanaka1,2, Yoshie Oishi3, Chihiro Akazawa4, Norihiro Tada5, Atsuyuki Yamataka1
1Department of Pediatric General and Urogenital Surgery, Juntendo University Graduate School of Medicine, Tokyo, Japan
2Department of Pediatric Surgery, Juntendo Nerima Hospital, Tokyo, Japan
3Medical Technology Innovation Center, Juntendo University Graduate School of Medicine, Tokyo, Japan
4Intractable Disease Research Center, Juntendo University School of Medicine, Tokyo, Japan
5Atopy Research Center, Juntendo University School of Medicine, Tokyo, Japan

Tóm tắt

Failure of enteric neural crest-derived cells (ENCCs) to correctly colonize the embryonic gut results in Hirschsprung’s disease (HD). Embryonic stem cells (ESCs) have the potential to differentiate into all tissue-specific cells and lineages, including ENCCs. We investigated the cellular differentiation of ESCs from Sox10-Venus + mice into both control and endothelin receptor-B knockout (Ednrb KO) mouse gut to assess each region. We established ESCs from Sox10-Venus + mice. These cells were cultured for 2 days, then selected and co-cultured with either a dissociated control or Sox10-Venus – Ednrb KO mouse gut (both small intestine and colon) on embryonic day (E) 13.5. Four days later, cells were immunolabeled for Tuj1 and visualized using confocal microscopy. Confocal microscopy revealed that transplanted Sox10-Venu + cells from ESCs migrated extensively within the host gut. Moreover, Tuj1-positive neurites were detected in the transplanted ESCs. Tuj1 expression was significantly decreased in aganglionic HD colon compared to controls (p < 0.05) and the HD small intestine (p < 0.05). This study demonstrated that an appropriate host environment is crucial for normal and complete colonization of the gut. Further investigations are required to confirm whether modifying this environment can improve the results of this model.

Tài liệu tham khảo

Furness JB (2012) The enteric nervous system and neurogastroenterology. Nat Rev Gastroenterol Hepatol 9(5):286–294 Burns AJ (2005) Migration of neural crest-derived enteric nervous system precursor cells to and within the gastrointestinal tract. Int J Dev Biol 49(2–3):143–150 Goldstein AM, Hofstra RM, Burns AJ (2013) Building a brain in the gut: development of the enteric nervous system. Clin Genet 83(4):307–316 Granström AL, Danielson J, Husberg B et al (2015) Adult outcomes after surgery for Hirschsprung’s disease: evaluation of bowel function and quality of life. J Pediatr Surg 50(11):1865–1869 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(8):743–749 Sood S, Lim R, Collins L et al (2018) The long-term quality of life outcomes in adolescents with Hirschsprung disease. J Pediatr Sur 53(12):2430–2434 Burns AJ et al (2016) White paper on guidelines concerning enteric nervous system stem cell therapy for enteric neuropathies. Dev Biol 417(2):229–251 Hotta R, Cheng L, Graham HK et al (2016) Delivery of enteric neural progenitors with 5-HT4 agonist-loaded nanoparticles and thermosensitive hydrogel enhances cell proliferation and differentiation following transplantation in vivo. Biomaterials 88:1–11 Lindley RM, Hawcutt DB, Connell MG et al (2009) Properties of secondary and tertiary human enteric nervous system neurospheres. J Pediatr Surg 44(6):1249–1255 Fattahi F, Steinbeck JA, Kriks S et al (2016) Deriving human ENS lineages for cell therapy and drug discovery in Hirschsprung disease. Nature 531(7592):105–109 Zuber SM, Grikscheit TC (2019) Stem cells for babies and their surgeons: The future is now. J Pediatr Surg 54(1):16–20 Iannaccone PM et al (1994) Pluripotent embryonic stem cells from the rat are capable of producing chimeras. Dev Biol 163(1):288–292 Giles JR, Yang X, Mark W et al (1993) Pluripotency of cultured rabbit inner cell mass cells detected by isozyme analysis and eye pigmentation of fetuses following injection into blastocysts or morulae. Mol Reprod Dev 36(2):130–138 Notarianni E, Laurie S, Moor M et al (1990) Maintenance and differentiation in culture of pluripotential embryonic cell lines from pig blastocysts. J Reprod Fertil Suppl 41:51–56 Handyside A, Hooper ML, Kaufman MH (1987) Towards the isolation of embryonal stem cell lines from the sheep. Rouxs Arch Dev Biol 196(3):185–219 Thomson JA et al (1998) Embryonic stem cell lines derived from human blastocyst. Science 282(5391):1145–1147 Kanda A et al (2012) Establishment of ES cells from inbred strain mice by dual inhibition (2i). J Reprod 58(1):77–83 Bondurand N, Sham MH (2013) The role of SOX10 during enteric nervous system development. Dev Biol 382(1):330–343 Shibata S, Yasuda A, Renault-Mihara F et al (2010) Sox10-Venus mice: a new tool for real-time labeling of neural crest lineage cells and oligodendrocytes. Mol Brain 3:31 Fujiwara N, Miyahara K, Nakazawa-Tanaka N et al (2016) Altered differentiation of enteric neural crest-derived cells from endothelin receptor-B null mouse model of Hirschsprung’s disease. Pediatr Surg Int 32(12):1095–1101 Buehr M et al (2003) Genesis of embryonic stem cells. Philos Trans R Soc Lond B Biol Sci 358(1436):1397–1402 Ying QL, Wray J, Nichols J et al (2008) The ground state of embryonic stem cell self-renewal. Nature 453(7194):519–523 Fujiwara N, Miyahara K, Nakazawa-Tanaka N et al (2022) In vitro investigation of the differentiation of enteric neural crest-derived cells following transplantation of aganglionic gut in a mouse model. Pediatr Surg Int 38(5):755–759 Kawaguchi J, Nichols J, Gierl MS et al (2010) Isolation and propagation of enteric neural crest progenitor cells from mouse embryonic stem cells and embryos. Development 137:693–704 Ying QL, Smith AG (2003) Defined conditions for neural commitment and differentiation. Methods Enzymol 365:327–341 Aoki Y, Saint-Germain N, Gyda M (2003) Sox10 regulates the development of neural crest-derived melanocytes in Xenopus. Dev Biol 259(1):19–33 Bondurand N, Kobetz A, Pingault V (1998) Expression of the SOX10 gene during human development. FEBS Lett 432(3):168–172 Stavely R, Bhave S, Ho WLN (2021) Enteric mesenchymal cells support the growth of postnatal enteric neural stem cells. Stem Cells 39(9):1236–1252 Obermayr F, Seitz G (2018) Recent developments in cell-based ENS regeneration – a short review. Innov Surg Sci 3(2):93–99 Mueller JL, Goldstein AM (2022) The science of Hirschsprung disease: what we know and where we are headed. Semin Pediatr Surg 31(2):151157 Rajabzadeh N, Fathi E, Farahzadi R (2019) Stem cell-based regenerative medicine. Stem Cell Investig 18(6):19 Hagl CI, Rauch U, Klotz M (2012) The microenvironment in the Hirschsprung’s disease gut supports myenteric plexus growth. Int J Colorectal Dis 27(6):817–829