Premigratory neural crest stem cells generate enteric neurons populating the mouse colon and regulating peristalsis in tissue-engineered intestine

Yuan, Huixin; Hu, Hui; Chen, Rui; Mu, Wenbo; Wang, Liangliang; Liu, Ying; Chen, Yue‐Lei; Ding, Xiaoyan; Xi, Yongmei; Mao, Shanshan; Jiang, Mizu; Chen, Jie; He, Yong; Wang, Lang; Dong, Yi; Tou, Jinfa; Chen, Wei

doi:10.1002/sctm.20-0469

Cited by 14 publications

(14 citation statements)

References 54 publications

(131 reference statements)

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“…To further advance this concept, the precursors of all three germ layers have been combined to form stomach and esophageal organoids with an innervated smooth muscle layer [ 251 ]. Alternatively, engineered scaffolds are populated by primary or PSC-derived cells to create innervated mini-intestines [ 252 , 253 , 254 ]. Outside of the digestive system, sensorimotor organoids with functional neuronal components have been created from neuromuscular progenitors [ 255 , 256 ] or in a gastruloid approach to study the developmental process [ 257 ].…”

Section: Discussionmentioning

confidence: 99%

Schwann Cells in Digestive System Disorders

Goluba

Kunrade

Riekstiņa

et al. 2022

Cells

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Proper functioning of the digestive system is ensured by coordinated action of the central and peripheral nervous systems (PNS). Peripheral innervation of the digestive system can be viewed as intrinsic and extrinsic. The intrinsic portion is mainly composed of the neurons and glia of the enteric nervous system (ENS), while the extrinsic part is formed by sympathetic, parasympathetic, and sensory branches of the PNS. Glial cells are a crucial component of digestive tract innervation, and a great deal of research evidence highlights the important status of ENS glia in health and disease. In this review, we shift the focus a bit and discuss the functions of Schwann cells (SCs), the glial cells of the extrinsic innervation of the digestive system. For more context, we also provide information on the basic findings regarding the function of innervation in disorders of the digestive organs. We find diverse SC roles described particularly in the mouth, the pancreas, and the intestine. We note that most of the scientific evidence concerns the involvement of SCs in cancer progression and pain, but some research identifies stem cell functions and potential for regenerative medicine.

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Section: Discussionmentioning

confidence: 99%

Schwann Cells in Digestive System Disorders

Goluba

Kunrade

Riekstiņa

et al. 2022

Cells

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“…Several groups have reported the incorporation of a neural element to HIOs to generate TESI, most of which have involved seeding HIOs onto hydrolysable synthetic scaffolds 42,56,134 . In 2017, Workman et al showed that iPSC-derived NCCs and ENS progenitors can be incorporated into HIOs with evidence neuronal function (by calcium transients) and nerve-mediated contractile activity in vitro and in vivo 73 .…”

Section: Engineering Muscle Enteric Nerves and Vasculaturementioning

confidence: 99%

Building gut from scratch — progress and update of intestinal tissue engineering

Tullie

Jones

Coppi

et al. 2022

Nat Rev Gastroenterol Hepatol

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Short bowel syndrome (SBS), a condition defined by insufficient absorptive intestinal epithelium, is a rare disease, with an estimated prevalence up to 0.4 in 10,000 people. However, it has substantial morbidity and mortality for affected patients. The mainstay of treatment in SBS is supportive, in the form of intravenous parenteral nutrition, with the aim of achieving intestinal autonomy. The lack of a definitive curative therapy has led to attempts to harness innate developmental and regenerative mechanisms to engineer neo-intestine as an alternative approach to address this unmet clinical need. Exciting advances have been made in the field of intestinal tissue engineering (ITE) over the past decade, making a review in this field timely. In this Review, we discuss the latest advances in the components required to engineer intestinal grafts and summarise the progress of ITE. We also explore some key factors to consider and challenges to overcome when transitioning tissue engineered intestine towards clinical translation and provide the future outlook of ITE in therapeutic applications and beyond. BlurbIntestinal tissue engineering offers a potential therapeutic option for short bowel syndrome. This Review examines the progress in intestinal tissue engineering, discusses the components required for engineered intestinal grafts, preclinical progress and efforts towards clinical translation, including challenges to overcome. Key points• Intestinal tissue engineering has the potential to offer curative therapy for patients with short bowel syndrome • Multiple components, including an absorptive mucosa, smooth muscle, enteric nerves and vasculature are required to generate a functional full thickness intestinal graft• Advances in intestinal tissue engineering include endothelial cell reprogramming and vascular engineering, generation of mucosal grafts using patient-derived materials and colon mucosal repurposing using small intestinal organoids.• Vascularisation and lymphatic engineering, generation of multi-layered personalised intestinal grafts and scaling-up of graft size present some of the future challenges in

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“…During embryonic development, the PNS, of which the ENS is a part, arises from NCSCs, multipotent and highly migratory stem cells that move throughout the embryo to colonize multiple organ primordia and differentiate into numerous cell types (Bronner and LeDouarin, 2012;Le Douarin and Teillet, 1973;Nagy and Goldstein, 2017;Yntema and Hammond, 1954). Recently, self-renewing NCSCs have been discovered in postnatal tissue (Adameyko et al, 2009;Dyachuk et al, 2014;Espinosa-Medina et al, 2014;Jinno et al, 2010;Morrison et al, 1999), including the adult gut (Kruger et al, 2002;Uesaka et al, 2015), and can generate enteric neurons that innervate the intestine in adult mice (Yuan et al, 2021). However, the degree to which these cells contribute to the adult tissue is not known.…”

Section: Llmentioning

confidence: 99%