Hostname: page-component-8448b6f56d-c47g7 Total loading time: 0 Render date: 2024-04-25T04:41:27.060Z Has data issue: false hasContentIssue false
  • English
  • Français

Temporal and spatial development of intestinal smooth muscle layers of human embryos and fetuses

Published online by Cambridge University Press:  04 August 2022

Xuelai Liu Open the ORCID record for Xuelai Liu [Opens in a new window] ,
Vincent Chi Hang Lui Open the ORCID record for Vincent Chi Hang Lui [Opens in a new window] ,
Huan Wang ,
Mao Ye ,
Rentao Fan ,
Xianghui Xie ,
Long Li  and
Zhe-Wu Jin
Xuelai Liu
Affiliation:
Department of Surgery, Capital Institute of Pediatrics affiliated Children Hospital, Beijing, China
Vincent Chi Hang Lui
Affiliation:
Department of Surgery, School of Clinical Medicine, The University of Hong Kong, Hong Kong, Hong Kong
Huan Wang
Affiliation:
Department of Pathology, Harbin Children Hospital, Harbin, Heilongjiang, China
Mao Ye
Affiliation:
Department of Surgery, Capital Institute of Pediatrics affiliated Children Hospital, Beijing, China
Rentao Fan
Affiliation:
Department of Anatomy, Wuxi School of Medicine, Jiangnan University, WuXi, Jiangsu, China
Xianghui Xie
Affiliation:
Department of Surgery, Capital Institute of Pediatrics affiliated Children Hospital, Beijing, China
Long Li*
Affiliation:
Department of Surgery, Capital Institute of Pediatrics affiliated Children Hospital, Beijing, China
Zhe-Wu Jin
Affiliation:
Department of Anatomy, Wuxi School of Medicine, Jiangnan University, WuXi, Jiangsu, China
*
Address for correspondence: Long Li, Department of Surgery, Capital Institute of Pediatrics affiliated Children Hospital, No.2, Yabao Rd, Chaoyang District, Beijing, 100020, China. Email: lilong23@126.com
Get access Rights & Permissions [Opens in a new window]

Abstract

The sequential occurrence of three layers of smooth muscle layers (SML) in human embryos and fetus is not known. Here, we investigated the process of gut SML development in human embryos and fetuses and compared the morphology of SML in fetuses and neonates. The H&E, Masson trichrome staining, and Immunohistochemistry were conducted on 6–12 gestation week human embryos and fetuses and on normal neonatal intestine. We showed that no lumen was seen in 6–7th gestation week embryonic gut, neither gut wall nor SML was developed in this period. In 8–9th gestation week embryonic and fetal gut, primitive inner circular SML (IC-SML) was identified in a narrow and discontinuous gut lumen with some vacuoles. In 10th gestation week fetal gut, the outer longitudinal SML (OL-SML) in gut wall was clearly identifiable, both the inner and outer SML expressed α-SMA. In 11–12th gestation week fetal gut, in addition to the IC-SML and OL-SML, the muscularis mucosae started to develop as revealed by α-SMA immune-reactivity beneath the developing mucosal epithelial layer. Comparing with the gut of fetuses of 11–12th week of gestation, the muscularis mucosae, IC-SML, and OL-SML of neonatal intestine displayed different morphology, including branching into glands of lamina propria in mucosa and increased thickness. In conclusions, in the human developing gut between week-8 to week-12 of gestation, the IC-SML develops and forms at week-8, followed by the formation of OL-SML at week-10, and the muscularis mucosae develops and forms last at week-12.

Keywords

Inner circularouter longitudinalsmooth muscle layerembryosfetuses
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 14 , Issue 1 , February 2023 , pp. 24 - 32
Check for updates
Copyright
© The Author(s), 2022. Published by Cambridge University Press in association with International Society for Developmental Origins of Health and Disease

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Watson, CL, Mahe, MM, Munera, J, et al. An in vivo model of human small intestine using pluripotent stem cells. Nat. Med. 2014; 20(11), 1310–1314.CrossRefGoogle Scholar
Tattoli, I, Corleto, VD, Taffuri, M, et al. Optimisation of isolation of richly pure and homogeneous primary human colonic smooth muscle cells. Dig. Liver Dis. 2004; 36(11), 735–743.CrossRefGoogle ScholarPubMed
Nair, DG, Han, TY, Lourenssen, S, Blennerhassett, MG. Proliferation modulates intestinal smooth muscle phenotype in vitro and in colitis in vivo. Am. J. Physiol. Gastrointest. Liver Physiol. 2011; 300(5), G903–913.CrossRefGoogle ScholarPubMed
Kobayashi, M, Khalil, HA, Lei, NY, et al. Bioengineering functional smooth muscle with spontaneous rhythmic contraction in vitro. Sci. Rep. 2018; 8(1), 13544.CrossRefGoogle ScholarPubMed
Li, L, Ren, X, Xiao, H, et al. Normal anorectal musculatures and changes in anorectal malformation. Pediatr. Surg. Int. 2020; 36(1), 103–111.CrossRefGoogle ScholarPubMed
Li, L, Diao, M, Ren, X, Liu, X. Reply to the letter to the editor concerning: "Normal anorectal musculatures and changes in anorectal malformation. Pediatr. Surg. Int. 2020; 36(8), 987–990.CrossRefGoogle Scholar
Kedinger, M, Duluc, I, Fritsch, C, Lorentz, O, Plateroti, M, Freund, JN. Intestinal epithelial-mesenchymal cell interactions. Ann. N. Y. Acad. Sci. 1998; 859, 1–17.CrossRefGoogle ScholarPubMed
Ferenc, K, Pietrzak, P, Godlewski, MM, et al. Intrauterine growth retarded piglet as a model for humans--studies on the perinatal development of the gut structure and function. Reprod. Biol. 2014; 14(1), 51–60.CrossRefGoogle Scholar
Liu, X, Song, Y, Hao, P, et al. Delayed development of vacuoles and recanalization in the duodenum: a study in human fetuses to understand susceptibility to duodenal atresia/stenosis. Fetal Pediatr. Pathol. 2021; 1–7. DOI 10.1080/15513815.2021.1876191.Google ScholarPubMed
Powell, DW, Pinchuk, IV, Saada, JI, Chen, X, Mifflin, RC. Mesenchymal cells of the intestinal lamina propria. Annu. Rev. Physiol. 2011; 73(1), 213–237.CrossRefGoogle ScholarPubMed
Pinchuk, IV, Mifflin, RC, Saada, JI, Powell, DW. Intestinal mesenchymal cells. Curr. Gastroenterol. Rep. 2010; 12(5), 310–318.CrossRefGoogle ScholarPubMed
Pastula, A, Marcinkiewicz, J. Cellular interactions in the intestinal stem cell niche. Arch. Immunol. Ther. Exp. (Warsz.). 2019; 67(1), 19–26.CrossRefGoogle ScholarPubMed
McLin, VA, Henning, SJ, Jamrich, M. The role of the visceral mesoderm in the development of the gastrointestinal tract. Gastroenterology. 2009; 136(7), 2074–2091.CrossRefGoogle ScholarPubMed
Fu, M, Tam, PK, Sham, MH, Lui, VC. Embryonic development of the ganglion plexuses and the concentric layer structure of human gut: a topographical study. Anat. Embryol. (Berl.). 2004; 208(1), 33–41.CrossRefGoogle Scholar
Zhang, S, Liu, X, Wang, H, Peng, J, Wong, KK. Silver nanoparticle-coated suture effectively reduces inflammation and improves mechanical strength at intestinal anastomosis in mice. J. Pediatr. Surg. 2014; 49(4), 606–613.CrossRefGoogle ScholarPubMed
Liu, X, Hao, W, Lok, CN, Wang, YC, Zhang, R, Wong, KK. Dendrimer encapsulation enhances anti-inflammatory efficacy of silver nanoparticles. J. Pediatr. Surg. 2014; 49(12), 1846–1851.CrossRefGoogle ScholarPubMed
Liu, X, Gao, P, Du, J, Zhao, X, Wong, KKY. Long-term anti-inflammatory efficacy in intestinal anastomosis in mice using silver nanoparticle-coated suture. J. Pediatr. Surg. 2017; 52(12), 2083–2087.CrossRefGoogle ScholarPubMed
Faussone-Pellegrini, MS. Relationships between neurokinin receptor-expressing interstitial cells of Cajal and tachykininergic nerves in the gut. J. Cell. Mol. Med. 2006; 10(1), 20–32.CrossRefGoogle ScholarPubMed
Tatekawa, Y, Yamanaka, H, Hasegawa, T, Sonobe, H. Caudal appendage derived from a vestigial remnant of the tailgut. Fetal Pediatr. Pathol. 2013; 32(5), 346–350.CrossRefGoogle ScholarPubMed
Yamada, M, Udagawa, J, Matsumoto, A, et al. Ror2 is required for midgut elongation during mouse development. Dev. Dyn. 2010; 239(3), 941–953.CrossRefGoogle ScholarPubMed
Walton, KD, Whidden, M, Kolterud, A, et al. Villification in the mouse: BMP signals control intestinal villus patterning. Development. 2016; 143(3), 427–436.Google ScholarPubMed
Jahan, E, Rafiq, AM, Matsumoto, A, Jahan, N, Otani, H. Development of the smooth muscle layer in the ileum of mouse embryos. Anat. Sci. Int. 2021; 96(1), 97–105.CrossRefGoogle ScholarPubMed
McHugh, KM. Molecular analysis of gastrointestinal smooth muscle development. J. Pediatr. Gastroenterol. Nutr. 1996; 23(4), 379–394.CrossRefGoogle ScholarPubMed
Muranaka, F, Nakajima, T, Iwaya, M, et al. A comparative immunohistochemical study of anal canal epithelium in humans and swine, focusing on the anal transitional zone epithelium and the anal glands. Anat. Rec. (Hoboken). 2018; 301(5), 796–805.CrossRefGoogle ScholarPubMed
Keef, KD, Cobine, CA. Control of motility in the internal anal sphincter. J. Neurogastroenterol. Motil. 2019; 25(2), 189–204.CrossRefGoogle ScholarPubMed