Exploring the microscopic terrain of the small intestinal epithelium: a comprehensive overview of general architecture and the present understanding of intestinal stem cells

Nowak, Bernadetta; Wanat, Marta; Świątko, Ada; Mirkowski, Karol; Tarkowski, Victoria; Mrożek, Andrzej; Mazurek, Mateusz; Domanski, Jurand; Domagała, Zygmunt

doi:10.2478/acb-2023-0015

Abstract

This paper provides a comprehensive overview of the microscopic landscape of the small intestinal epithelium, focusing on its general structure and the current state of knowledge regarding intestinal stem cells. The small intestine’s epithelial layer is intricately organized, comprising various cell types with specialized functions, including goblet cells, enterocytes, enteroendocrine cells, Paneth cells, microfold cells (M cells), and tuft cells. These cells collectively contribute to essential physiological processes such as digestion, absorption, and immune response regulation. The review delves into the role of intestinal stem cells, residing in the crypts, and their significance in maintaining tissue homeostasis and regeneration. Understanding the microscopic intricacies of the small intestinal epithelium is crucial for unraveling its physiological functions and exploring potential therapeutic avenues.

References

Gourevitch D. The anatomy and physiology of the small bowel. In: Fielding JWL, Hallissey MT, editors. Upper gastrointestinal surgery. London: Śpringer-Verlag; 2005, p. 39-44. DOI:10.1007/1-84628-066-4_3.
Search in Google Scholar Back to article
Volk N, Lacy B. Anatomy and physiology of the small bowel. Gastrointest Endosc Clin N Am. 2017;27(1):1-13; DOI:10.1016/j.giec.2016.08.001.
Search in Google Scholar Back to article
Wozniak Ś, Pytrus T, Kobierzycki C, Grabowski K, Paulsen F. The large intestine from fetal period to adulthood and its impact on the course of colonoscopy. Ann Anat. 2019;224:17-22; DOI:10.1016/j. aanat.2019.02.004.
Search in Google Scholar Back to article
Coşkun I, Yildiz H, Arslan K, Yildiz B. A geometric description of human intestine. Ital J Anat Embryol. 2007;112(1):27-36.
Search in Google Scholar Back to article
Woźniak Ś, Kempiński R, Grzelak J, Domagała Z, Paulsen F. Anatomy-related ratios predict colonoscopy incompleteness in similar examination conditions. Adv Clin Exp Med. 2020;29(5):573-80; DOI:10.17219/acem/118847.
Search in Google Scholar Back to article
Wozniak Ś, Florjanski J, Kordecki H, Podhorska-Okolow M, Domagala Z. Fetal sigmoid colon mesentery – in relevance in fetal ultrasound application. A pilot study. Ann Anat. 2018;216:152-158; DOI:10.1016/j. aanat.2017.12.003.
Search in Google Scholar Back to article
Gworys B, Domagała Z, Markocka-Maczka K. Development of the descending colon during the human foetal period. Folia Morphol (Warsz). 2004;63(2):173-8.
Search in Google Scholar Back to article
Fawkner-Corbett D, Antanaviciute A, Parikh K, Jagielowicz M, Gero s AŚ, Gupta T, Ashley N, Khamis D, Fowler D, Morrissey E, Cunningham C, Johnson PRV, Koohy H, Śimmons A. Śpatiotemporal analysis of human intestinal development at single-cell resolution. Cell. 2021;184(3):810-26.e23; DOI:10.1016/j.cell.2020.12.016.
Search in Google Scholar Back to article
Rubin W. The epithelial “membrane” of the small intestine. Am J Clin Nutr. 1971;24(1):45-64; DOI:10.1093/ajcn/24.1.45.
Search in Google Scholar Back to article
Camilleri M, Madsen K, Śpiller R, Greenwood-Van Meerveld B, Verne GN. Intestinal barrier function in health and gastrointestinal disease. Neurogastroenterol Motil. 2012;24(6):503-12; DOI:10.1111/j.1365-2982.2012.01921.x.
Search in Google Scholar Back to article
Olivares-Villago mez D, Van Kaer L. Intestinal intraepithelial lymphocytes: sentinels of the mucosal barrier. Trends Immunol. 2018;39(4):264-75; DOI:10.1016/j.it.2017.11.003.
Search in Google Scholar Back to article
Zhang Z, Tanaka I, Pan Z, Ernst PB, Kiyono H, Kurashima Y. Intestinal homeostasis and inflammation: gut microbiota at the crossroads of pancreas-intestinal barrier axis. Eur J Immunol. 2022;52(7):1035-46; DOI:10.1002/eji.202149532.
Search in Google Scholar Back to article
Maloy KJ, Powrie F. Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature. 2011;474(7351):298-306; DOI:10.1038/nature10208.
Search in Google Scholar Back to article
Serek P, Oleksy-Wawrzyniak M. The effect of bacterial infections, probiotics and zonulin on intestinal barrier integrity. Int J Mol Sci. 2021;22(21):11359; DOI:10.3390/ijms222111359.
Search in Google Scholar Back to article
Tong Y, Tang J. Candida albicans infection and intestinal immunity. Microbiol Res. 2017;198:27-35; DOI:10.1016/j.micres.2017.02.002.
Search in Google Scholar Back to article
Kogut MH, Lee A, Śantin E. Microbiome and pathogen interaction with the immune system. Poult Sci. 2020;99(4):1906-13; DOI:10.1016/j. psj.2019.12.011.
Search in Google Scholar Back to article
Gommerman JL, Rojas OL, Fritz JH. Re-thinking the functions of IgA(+) plasma cells. Gut Microbes. 2014;5(5):652-62; DOI:10.4161/19490976.2014.969977.
Search in Google Scholar Back to article
Wei X, Zhang L, Zhang R, Wu R, Si D, Ahmad B, Petitte JN, Mozdziak PE, Li Z, Guo H, Zhang M. A highly efficient hybrid peptide ameliorates intestinal inflammation and mucosal barrier damage by neutralizing lipopoly-saccharides and antagonizing the lipopolysaccharide-receptor interaction. FASEB J. 2020;34(12):16049-72; DOI:10.1096/fj.201903263RRR.
Search in Google Scholar Back to article
Al-Toma A, Volta U, Auricchio R, Castillejo G, Śanders DŚ, Cellier C, Mulder CJ, Lundin KEA. European society for the study of coeliac disease (ESsCD) guideline for coeliac disease and other gluten-related disorders. United European Gastroenterol J. 2019;7(5):583-613; DOI:10.1177/2050640619844125.
Search in Google Scholar Back to article
Nolan JD, Johnston IM, Walters JRF. Physiology of malabsorption. Surgery (Oxford) 2015;33:193-9; DOI:10.1016/j.mpsur.2015.02.003.
Search in Google Scholar Back to article
Montoro-Huguet MA, Belloc B, Domí nguez-Cajal M. Śmall and large intestine (I): malabsorption of nutrients. Nutrients. 2021;13(4):1254; DOI:10.3390/nu13041254.
Search in Google Scholar Back to article
Śuzuki T, Aoki K, Śhimokobe K, Omiya Ś, Funayama C, Takahashi T, Kato M. Age-related morphological and functional changes in the small intestine of senescence-accelerated mouse. Exp Gerontol. 2022;163:111795; DOI:10.1016/j.exger.2022.111795.
Search in Google Scholar Back to article
Bielak-Zmijewska A, Mosieniak G. What is what is not cell senescence. Postepy Biochem. 2018;64:110-8.
Search in Google Scholar Back to article
Zhou J, Boutros M. Intestinal stem cells and their niches in home-ostasis and disease. Cells Dev. 2023;175:203862; DOI:10.1016/j. cdev.2023.203862.
Search in Google Scholar Back to article
Śoderholm AT, Pedicord VA. Intestinal epithelial cells: at the interface of the microbiota and mucosal immunity. Immunology. 2019;158(4):267-80; DOI:10.1111/imm.13117.
Search in Google Scholar Back to article
Lin JE, Li P, Pitari GM, Schulz S, Waldman SA. Guanylyl cyclase C in colorectal cancer: susceptibility gene and potential therapeutic target. Future Oncol. 2009;5(4):509-22; DOI:10.2217/fon.09.14.
Search in Google Scholar Back to article
Burclaff J, Bliton RJ, Breau KA, Ok MT, Gomez-Martinez I, Ranek JŚ, Bhatt AP, Purvis JE, Woosley JT, Magness ST. A proximal-to-distal survey of healthy adult human small intestine and colon epithelium by single-cell transcriptomics. Cell Mol Gastroenterol Hepatol. 2022;13(5):1554-89; DOI:10.1016/j.jcmgh.2022.02.007.
Search in Google Scholar Back to article
Tian H, Biehs B, Warming Ś, Leong KG, Rangell L, Klein OD, de Śauvage FJ. A reserve stem cell population in small intestine renders Lgr5-positive cells dispensable. Nature. 2011;478(7368):255-9; DOI:10.1038/nature10408.
Search in Google Scholar Back to article
Takahashi T, Shiraishi A. Stem cell signaling pathways in the small intestine. Int J Mol Sci. 2020;21(6):2032; DOI:10.3390/ijms21062032.
Search in Google Scholar Back to article
Cheng H, Leblond CP. Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. V. Unitarian Theory of the origin of the four epithelial cell types. Am J Anat. 1974;141(4):537-61; DOI:10.1002/aja.1001410407.
Search in Google Scholar Back to article
Carlone DL, Breault DT. Tales from the crypt: the expanding role of slow cycling intestinal stem cells. Cell Stem Cell. 2012;10(1):2-4; DOI:10.1016/j.stem.2011.12.012.
Search in Google Scholar Back to article
Takahashi T, Fujishima K, Kengaku M. Modeling intestinal stem cell function with organoids. Int J Mol Sci. 2021;22(20):10912; DOI:10.3390/ijms222010912.
Search in Google Scholar Back to article
Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, Haegebarth A, Korving J, Begthel H, Peters PJ, Clevers H. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature. 2007;449(7165):1003-7; DOI:10.1038/nature06196.
Search in Google Scholar Back to article
Hou Q, Huang J, Ayansola H, Masatoshi H, Zhang B. Intestinal stem cells and immune cell relationships: potential therapeutic targets for inflammatory bowel diseases. Front Immunol. 2021;11:623691; DOI:10.3389/fimmu.2020.623691.
Search in Google Scholar Back to article
Richmond CA, Rickner H, Shah MS, Ediger T, Deary L, Zhou F, Tovaglieri A, Carlone DL, Breault DT. JAK/ŚTAT-1 signaling is required for reserve intestinal stem cell activation during intestinal regeneration following acute inflammation. Stem Cell Reports. 2018;10(1):17-26; DOI:10.1016/j.stemcr.2017.11.015.
Search in Google Scholar Back to article
Billipp TE, Fung C, Webeck LM, Sargent DB, Gologorsky MB, McDaniel MM, Kasal DN, McGinty JW, Barrow KA, Rich LM, Barilli A, Śabat M, Debley JS, Myers R, Howitt MR, von Moltke J. Tuft cell-derived acetylcholine regulates epithelial fluid secretion. bioRxiv [Preprint]. 2023:2023.03.17.533208; DOI:10.1101/2023.03.17.533208.
Search in Google Scholar Back to article
Uwada J, Nakazawa H, Muramatsu I, Masuoka T, Yazawa T. Role of muscarinic acetylcholine receptors in intestinal epithelial homeostasis: insights for the treatment of inflammatory bowel disease. Int J Mol Sci. 2023;24(7):6508; DOI:10.3390/ijms24076508.
Search in Google Scholar Back to article
Lindemans CA, Calafiore M, Mertelsmann AM, O’Connor MH, Dudakov JA, Jenq RR, Velardi E, Young LF, Śmith OM, Lawrence G, Ivanov JA, Fu YY, Takashima Ś, Hua G, Martin ML, O’Rourke KP, Lo YH, Mokry M, Romera-Hernandez M, Cupedo T, Dow L, Nieuwenhuis EE, Shroyer NF, Liu C, Kolesnick R, van den Brink MRM, Hanash AM. Interleukin-22 promotes intestinal-stem-cell-mediated epithelial regeneration. Nature. 2015;528(7583):560-4; DOI:10.1038/nature16460.
Search in Google Scholar Back to article
Kurokawa K, Hayakawa Y, Koike K. Plasticity of intestinal epithelium: stem cell niches and regulatory signals. Int J Mol Sci. 2020;22(1):357; DOI:10.3390/ijms22010357.
Search in Google Scholar Back to article

Exploring the microscopic terrain of the small intestinal epithelium: a comprehensive overview of general architecture and the present understanding of intestinal stem cells

Abstract

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