The Critical Role of Acyl Hydrocarbon Receptor on the Combined Benefits of Postbiotic Propionate on Active Vitamin D3-Orchestrated Innate Immunity in Colitis

Overview

Journal Biomedicines

Specialty Biomedical Engineering

Date 2023 Jan 21

PMID 36672703

Authors

Fu-Chen Huang

Shun-Chen Huang

Affiliations

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Abstract

Our recent study observed the combined beneficial effects of postbiotic butyrate on active vitamin D3-orchestrated innate immunity to Colitis. There is increasing interest in the role of acyl hydrocarbon receptor (AhR) on colitis and innate immunity. Therefore, we investigated the involvement of AhR in the effects. colitis model is conducted with 6-8 w/o male C57BL/6 mice: Streptomycin (20 mg/mouse p.o.)-pretreated C57BL/6 mice were mock infected with sterile PBS or infected orally with 1 × 10 CFU of an wild-type strain SL1344 for 48 h. Before and after the colitis induction, mice were oral gavage with active vitamin D3 0.2 μg/25 g mice (VD3) and/or postbiotics propionate (PP), in the absence of the presence of intraperitoneal injection of AhR inhibitor for 4 and 7 days, respectively. We observed AhR inhibitor counteracted the synergistic effects of PP and VD3 on reducing the severity of colitis and body weight loss in C57BL/6 mice, reducing the cecal inflammatory but enhancing antimicrobial peptide mRNAs expression, and reducing the bacterial translocation in liver/spleen, compared to single treatment. It suggests the involvement of AhR on the synergistic effects of postbiotics PP and VD3 on the antibacterial and anti-inflammatory responses in colitis and the potential biological treatment of colitis.

Citing Articles

Therapeutic Potential of Nutritional Aryl Hydrocarbon Receptor Ligands in Gut-Related Inflammation and Diseases.

Huang F Biomedicines. 2025; 12(12.

PMID: 39767818 PMC: 11673835. DOI: 10.3390/biomedicines12122912.

Unveiling the Novel Benefits of Co-Administering Butyrate and Active Vitamin D3 in Mice Subjected to Chemotherapy-Induced Gut-Derived Sepsis.

Huang F, Huang S Biomedicines. 2024; 12(5).

PMID: 38790988 PMC: 11118095. DOI: 10.3390/biomedicines12051026.

References

Huang F, Huang S . Active vitamin D3 attenuates the severity of Salmonella colitis in mice by orchestrating innate immunity. Immun Inflamm Dis. 2021; 9(2):481-491. PMC: 8127544. DOI: 10.1002/iid3.408. View

Collins J, Keeney K, Crepin V, Rathinam V, Fitzgerald K, Finlay B . Citrobacter rodentium: infection, inflammation and the microbiota. Nat Rev Microbiol. 2014; 12(9):612-23. DOI: 10.1038/nrmicro3315. View

Helms M, Vastrup P, Gerner-Smidt P, Molbak K . Excess mortality associated with antimicrobial drug-resistant Salmonella typhimurium. Emerg Infect Dis. 2002; 8(5):490-5. PMC: 2732497. DOI: 10.3201/eid0805.010267. View

Schiering C, Wincent E, Metidji A, Iseppon A, Li Y, Potocnik A . Feedback control of AHR signalling regulates intestinal immunity. Nature. 2017; 542(7640):242-245. PMC: 5302159. DOI: 10.1038/nature21080. View

Furumatsu K, Nishiumi S, Kawano Y, Ooi M, Yoshie T, Shiomi Y . A role of the aryl hydrocarbon receptor in attenuation of colitis. Dig Dis Sci. 2011; 56(9):2532-44. DOI: 10.1007/s10620-011-1643-9. View

Huang F, Huang S . The Combined Beneficial Effects of Postbiotic Butyrate on Active Vitamin D3-Orchestrated Innate Immunity to Colitis. Biomedicines. 2021; 9(10). PMC: 8533643. DOI: 10.3390/biomedicines9101296. View

Monteleone I, Rizzo A, Sarra M, Sica G, Sileri P, Biancone L . Aryl hydrocarbon receptor-induced signals up-regulate IL-22 production and inhibit inflammation in the gastrointestinal tract. Gastroenterology. 2011; 141(1):237-48, 248.e1. DOI: 10.1053/j.gastro.2011.04.007. View

Gaschott T, Steinhilber D, Milovic V, Stein J . Tributyrin, a stable and rapidly absorbed prodrug of butyric acid, enhances antiproliferative effects of dihydroxycholecalciferol in human colon cancer cells. J Nutr. 2001; 131(6):1839-43. DOI: 10.1093/jn/131.6.1839. View

Bajic D, Niemann A, Hillmer A, Mejias-Luque R, Bluemel S, Docampo M . Gut Microbiota-Derived Propionate Regulates the Expression of Reg3 Mucosal Lectins and Ameliorates Experimental Colitis in Mice. J Crohns Colitis. 2020; 14(10):1462-1472. PMC: 8921751. DOI: 10.1093/ecco-jcc/jjaa065. View

10.

Matsunawa M, Amano Y, Endo K, Uno S, Sakaki T, Yamada S . The aryl hydrocarbon receptor activator benzo[a]pyrene enhances vitamin D3 catabolism in macrophages. Toxicol Sci. 2009; 109(1):50-8. DOI: 10.1093/toxsci/kfp044. View

11.

Agus A, Richard D, Fais T, Vazeille E, Chervy M, Bonnin V . Propionate catabolism by CD-associated adherent-invasive counteracts its anti-inflammatory effect. Gut Microbes. 2021; 13(1):1-18. PMC: 8007151. DOI: 10.1080/19490976.2020.1839318. View

12.

Xiong H, Guo B, Gan Z, Song D, Lu Z, Yi H . Butyrate upregulates endogenous host defense peptides to enhance disease resistance in piglets via histone deacetylase inhibition. Sci Rep. 2016; 6:27070. PMC: 4882515. DOI: 10.1038/srep27070. View

13.

Bustin S, Benes V, Garson J, Hellemans J, Huggett J, Kubista M . The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem. 2009; 55(4):611-22. DOI: 10.1373/clinchem.2008.112797. View

14.

Sekine H, Mimura J, Oshima M, Okawa H, Kanno J, Igarashi K . Hypersensitivity of aryl hydrocarbon receptor-deficient mice to lipopolysaccharide-induced septic shock. Mol Cell Biol. 2009; 29(24):6391-400. PMC: 2786870. DOI: 10.1128/MCB.00337-09. View

15.

Jin U, Cheng Y, Park H, Davidson L, Callaway E, Chapkin R . Short Chain Fatty Acids Enhance Aryl Hydrocarbon (Ah) Responsiveness in Mouse Colonocytes and Caco-2 Human Colon Cancer Cells. Sci Rep. 2017; 7(1):10163. PMC: 5579248. DOI: 10.1038/s41598-017-10824-x. View

16.

Takaishi H, Matsuki T, Nakazawa A, Takada T, Kado S, Asahara T . Imbalance in intestinal microflora constitution could be involved in the pathogenesis of inflammatory bowel disease. Int J Med Microbiol. 2007; 298(5-6):463-72. DOI: 10.1016/j.ijmm.2007.07.016. View

17.

Lauderdale T, Aarestrup F, Chen P, Lai J, Wang H, Shiau Y . Multidrug resistance among different serotypes of clinical Salmonella isolates in Taiwan. Diagn Microbiol Infect Dis. 2006; 55(2):149-55. DOI: 10.1016/j.diagmicrobio.2006.01.002. View

18.

Lin H, Huang Y, Tian T, Wang P, Li Y . Propionate promotes vitamin D receptor expression via yes-associated protein in rats with short bowel syndrome. Biochem Biophys Res Commun. 2020; 523(3):645-650. DOI: 10.1016/j.bbrc.2019.12.127. View

19.

Pernomian L, Duarte-Silva M, de Barros Cardoso C . The Aryl Hydrocarbon Receptor (AHR) as a Potential Target for the Control of Intestinal Inflammation: Insights from an Immune and Bacteria Sensor Receptor. Clin Rev Allergy Immunol. 2020; 59(3):382-390. DOI: 10.1007/s12016-020-08789-3. View

20.

Li H, Li W, Wang Q . 1,25-dihydroxyvitamin D suppresses lipopolysaccharide-induced interleukin-6 production through aryl hydrocarbon receptor/nuclear factor-κB signaling in oral epithelial cells. BMC Oral Health. 2019; 19(1):236. PMC: 6829944. DOI: 10.1186/s12903-019-0935-x. View