Gut Microbiota-stem Cell Niche Crosstalk: A New Territory for Maintaining Intestinal Homeostasis

Overview

Journal Imeta

Specialty Biology

Date 2024 Jun 13

PMID 38867904

Authors

Ning Ma

Xiyue Chen

Lee J Johnston

Xi Ma

Affiliations

Soon will be listed here.

Abstract

Intestinal epithelium undergoes rapid cellular turnover, relying on the local niche, to support intestinal stem cells (ISCs) function and self-renewal. Research into the association between ISCs and disease continues to expand at a rapid rate. However, the detailed interaction of ISCs and gut microbes remains to be elucidated. Thus, this review witnessed major advances in the crosstalk between ISCs and gut microbes, delivering key insights into (1) construction of ISC niche and molecular mechanism of how to jointly govern epithelial homeostasis and protect against intestinal diseases with the participation of Wnt, bone morphogenetic protein, and Notch; (2) differentiation fate of ISCs affect the gut microbiota. Meanwhile, the presence of intestinal microbes also regulates ISC function; (3) microbiota regulation on ISCs by Wnt and Notch signals through pattern recognition receptors; (4) how do specific microbiota-related postbiotics influence ISCs to maintain intestinal epithelial regeneration and homeostasis that provide insights into a promising alternative therapeutic method for intestinal diseases. Considering the detailed interaction is still unclear, it is necessary to further explore the regulatory role of gut microbiota on ISCs to utilize microbes to alleviate gut disorders. Furthermore, these major advances collectively drive us ever closer to breakthroughs in regenerative medicine and cancer treatment by microbial transplantation in the clinic.

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References

Metidji A, Omenetti S, Crotta S, Li Y, Nye E, Ross E . The Environmental Sensor AHR Protects from Inflammatory Damage by Maintaining Intestinal Stem Cell Homeostasis and Barrier Integrity. Immunity. 2018; 49(2):353-362.e5. PMC: 6104739. DOI: 10.1016/j.immuni.2018.07.010. View

Wu H, Xie S, Miao J, Li Y, Wang Z, Wang M . maintains intestinal epithelial regeneration and repairs damaged intestinal mucosa. Gut Microbes. 2020; 11(4):997-1014. PMC: 7524370. DOI: 10.1080/19490976.2020.1734423. View

Iankov I, Petrov D, Mladenov I, Haralambieva I, Kalev O, Balabanova M . Protective efficacy of IgA monoclonal antibodies to O and H antigens in a mouse model of intranasal challenge with Salmonella enterica serotype Enteritidis. Microbes Infect. 2004; 6(10):901-10. DOI: 10.1016/j.micinf.2004.05.007. View

Sigal M, Reines M, Mullerke S, Fischer C, Kapalczynska M, Berger H . R-spondin-3 induces secretory, antimicrobial Lgr5 cells in the stomach. Nat Cell Biol. 2019; 21(7):812-823. DOI: 10.1038/s41556-019-0339-9. View

Matricon J, Barnich N, Ardid D . Immunopathogenesis of inflammatory bowel disease. Self Nonself. 2011; 1(4):299-309. PMC: 3062384. DOI: 10.4161/self.1.4.13560. View

Bloemendaal A, Buchs N, George B, Guy R . Intestinal stem cells and intestinal homeostasis in health and in inflammation: A review. Surgery. 2016; 159(5):1237-48. DOI: 10.1016/j.surg.2016.01.014. View

Chakrabarti S, Liehl P, Buchon N, Lemaitre B . Infection-induced host translational blockage inhibits immune responses and epithelial renewal in the Drosophila gut. Cell Host Microbe. 2012; 12(1):60-70. DOI: 10.1016/j.chom.2012.06.001. View

Hold G, Smith M, Grange C, Watt E, El-Omar E, Mukhopadhya I . Role of the gut microbiota in inflammatory bowel disease pathogenesis: what have we learnt in the past 10 years?. World J Gastroenterol. 2014; 20(5):1192-210. PMC: 3921503. DOI: 10.3748/wjg.v20.i5.1192. View

Peterson L, Artis D . Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat Rev Immunol. 2014; 14(3):141-53. DOI: 10.1038/nri3608. View

10.

Koo B, Spit M, Jordens I, Low T, Stange D, van de Wetering M . Tumour suppressor RNF43 is a stem-cell E3 ligase that induces endocytosis of Wnt receptors. Nature. 2012; 488(7413):665-9. DOI: 10.1038/nature11308. View

11.

Beyaz S, Mana M, Roper J, Kedrin D, Saadatpour A, Hong S . High-fat diet enhances stemness and tumorigenicity of intestinal progenitors. Nature. 2016; 531(7592):53-8. PMC: 4846772. DOI: 10.1038/nature17173. View

12.

Agus A, Planchais J, Sokol H . Gut Microbiota Regulation of Tryptophan Metabolism in Health and Disease. Cell Host Microbe. 2018; 23(6):716-724. DOI: 10.1016/j.chom.2018.05.003. View

13.

Cronin S, Nehme N, Limmer S, Liegeois S, Pospisilik J, Schramek D . Genome-wide RNAi screen identifies genes involved in intestinal pathogenic bacterial infection. Science. 2009; 325(5938):340-3. PMC: 2975362. DOI: 10.1126/science.1173164. View

14.

Clevers H . Wnt/beta-catenin signaling in development and disease. Cell. 2006; 127(3):469-80. DOI: 10.1016/j.cell.2006.10.018. View

15.

Li Y, Shi J, Yang J, Ma Y, Cheng L, Zeng J . A Wnt/β-catenin negative feedback loop represses TLR-triggered inflammatory responses in alveolar epithelial cells. Mol Immunol. 2014; 59(2):128-35. DOI: 10.1016/j.molimm.2014.02.002. View

16.

Macpherson A, Gomez de Aguero M, Ganal-Vonarburg S . How nutrition and the maternal microbiota shape the neonatal immune system. Nat Rev Immunol. 2017; 17(8):508-517. DOI: 10.1038/nri.2017.58. View

17.

Ma N, He T, Johnston L, Ma X . Host-microbiome interactions: the aryl hydrocarbon receptor as a critical node in tryptophan metabolites to brain signaling. Gut Microbes. 2020; 11(5):1203-1219. PMC: 7524279. DOI: 10.1080/19490976.2020.1758008. View

18.

Spiljar M, Merkler D, Trajkovski M . The Immune System Bridges the Gut Microbiota with Systemic Energy Homeostasis: Focus on TLRs, Mucosal Barrier, and SCFAs. Front Immunol. 2017; 8:1353. PMC: 5670327. DOI: 10.3389/fimmu.2017.01353. View

19.

Aaltonen L, Roth S . Direct Sequencing for Juvenile Polyposis Gene SMAD4/DPC4 Mutations. Methods Mol Med. 2011; 50:167-74. DOI: 10.1385/1-59259-084-5:167. View

20.

Rinttila T, Lyra A, Krogius-Kurikka L, Palva A . Real-time PCR analysis of enteric pathogens from fecal samples of irritable bowel syndrome subjects. Gut Pathog. 2011; 3(1):6. PMC: 3111350. DOI: 10.1186/1757-4749-3-6. View