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Food Science and Human Wellness 2024, 13(1): 173-182 https://doi.org/10.26599/FSHW.2022.9250046
Research Article | Open Access | Issue | Published: 01 June 2023

D-Psicose intake exacerbates dextran sulfate sodium-induced colitis in mice through alteration in the gut microbiota and dysfunction of mucosal barrier

Show Author's Information Xuejiao Zhanga,b,,  Ang Lia,  Yuanyifei Wanga,  Jin Wanga,  Bowei Zhanga,  Yan Zhanga,  Jingmin Liua,  Shuo Wanga( )
Tianjin Key Laboratory of Food Science and Health, School of Medicine, Nankai University, Tianjin 300072, China
College of Food Science and Technology, Hebei Agricultural University, Baoding 071001, China

Peer review under responsibility of Tsinghua University Press.

Keywords:
Gut microbiota, Short chain fatty acids, Colitis, D-Psicose, Mucin 2
Cite this article:
Zhang X, Li A, Wang Y, et al. D-Psicose intake exacerbates dextran sulfate sodium-induced colitis in mice through alteration in the gut microbiota and dysfunction of mucosal barrier. Food Science and Human Wellness, 2024, 13(1): 173-182. https://doi.org/10.26599/FSHW.2022.9250046
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Abstract Full text Electronic supplementary material About this article

D-Psicose, as a low-calorie rare sugar, has attracted a lot of attention in recent years for alternating to sucrose. The anti-obesity effect of D-psicose has been extensively confirmed in previous studies, however, the impact of D-psicose on colitis remains vague. Here, we firstly evaluated the effect of the D-psicose prophylactic intervention on dextran sulfate sodium-induced colitis in C57BL/6 mice. The pathological symptoms, inflammatory cytokines levels, gut microbiota composition, short chain fatty acids (SCFAs) production and colonic barrier integrity were comprehensively evaluated. The results confirmed that D-psicose intervention aggravated colitis, characterized by the exacerbation of colon shortening, increase of colonic inflammatory infiltration, and marked exaltation of disease activity indices and IL-6, IL-1β and TNF-α levels. Further, the dysfunction of gut microbiota was identified in the psicose group. The abundance of pro-inflammatory bacteria Lachnospiraceae_NK4A136_group was significantly up-regulated while the abundance of probiotics Akkermansia and Lactobacillus were significantly down-regulated in the psicose group compared to the model group. Moreover, the production of SCFAs was suppressed in the psicose group, accompanied by a decrease in the level of mucin 2 (Muc-2). Collectively, the underlying mechanism of the exacerbation of colitis by D-psicose intervention might be attributed to microbiota dysfunction accompanied by the reduction of SCFAs, which leads to the damage of the mucosal barrier and the intensification of inflammatory invasion.


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About this article

D-Psicose intake exacerbates dextran sulfate sodium-induced colitis in mice through alteration in the gut microbiota and dysfunction of mucosal barrier

Show Author's information Xuejiao Zhanga,b,, Ang Lia, Yuanyifei Wanga, Jin Wanga, Bowei Zhanga, Yan Zhanga, Jingmin Liua, Shuo Wanga( )
Tianjin Key Laboratory of Food Science and Health, School of Medicine, Nankai University, Tianjin 300072, China
College of Food Science and Technology, Hebei Agricultural University, Baoding 071001, China

Peer review under responsibility of Tsinghua University Press.

Abstract

D-Psicose, as a low-calorie rare sugar, has attracted a lot of attention in recent years for alternating to sucrose. The anti-obesity effect of D-psicose has been extensively confirmed in previous studies, however, the impact of D-psicose on colitis remains vague. Here, we firstly evaluated the effect of the D-psicose prophylactic intervention on dextran sulfate sodium-induced colitis in C57BL/6 mice. The pathological symptoms, inflammatory cytokines levels, gut microbiota composition, short chain fatty acids (SCFAs) production and colonic barrier integrity were comprehensively evaluated. The results confirmed that D-psicose intervention aggravated colitis, characterized by the exacerbation of colon shortening, increase of colonic inflammatory infiltration, and marked exaltation of disease activity indices and IL-6, IL-1β and TNF-α levels. Further, the dysfunction of gut microbiota was identified in the psicose group. The abundance of pro-inflammatory bacteria Lachnospiraceae_NK4A136_group was significantly up-regulated while the abundance of probiotics Akkermansia and Lactobacillus were significantly down-regulated in the psicose group compared to the model group. Moreover, the production of SCFAs was suppressed in the psicose group, accompanied by a decrease in the level of mucin 2 (Muc-2). Collectively, the underlying mechanism of the exacerbation of colitis by D-psicose intervention might be attributed to microbiota dysfunction accompanied by the reduction of SCFAs, which leads to the damage of the mucosal barrier and the intensification of inflammatory invasion.

Keywords: Gut microbiota, Short chain fatty acids, Colitis, D-Psicose, Mucin 2

References(49)

[1]

R. Yermek, L. Wang, K. Kaneko, et al., D-Allulose cooperates with glucagon-like peptide-1 and activates proopiomelanocortin neurons in the arcuate nucleus and central injection inhibits feeding in mice, Biochem. Biophys. Res. Commun. 613 (2022) 159-165. https://doi.org/10.1016/j.bbrc.2022.04.027.
DOI Google Scholar
[2]

Z. Chen, J. Chen, W. Zhang, et al., Recent research on the physiological functions, applications, and biotechnological production of D-allose, Appl. Microbiol. Biotechnol. 102 (2018) 4269-4278. https://doi.org/10.1007/s00253-018-8916-6.
DOI Google Scholar
[3]

Z. Chen, X.D. Gao, Z. Li, Recent advances regarding the physiological functions and biosynthesis of D-allulose, Front. Microbiol. 13 (2022). https://doi.org/10.3389/fmicb.2022.881037.
DOI Google Scholar
[4]

F. Franchi, D.M. Yaranov, F. Rollini, et al., Effects of D-allulose on glucose tolerance and insulin response to a standard oral sucrose load: results of a prospective, randomized, crossover study, BMJ Open Diab. Res. Ca. 9 (2021). https://doi.org/10.1136/bmjdrc-2020-001939.
DOI Google Scholar
[5]

T. Shintani, H. Sakoguchi, A. Yoshihara, et al., D-Allulose, a stereoisomer of D-fructose, extends Caenorhabditis elegans lifespan through a dietary restriction mechanism: a new candidate dietary restriction mimetic, Biochem. Bioph. Res. Co. 493 (2017) 1528-1533. https://doi.org/10.1016/j.bbrc.2017.09.147.
DOI Google Scholar
[6]

K. Tsukamoto, A. Hossain, F. Yamaguchi, et al., Intestinal absorption, organ distribution, and urinary excretion of the rare sugar D-psicose, Drug Des. Dev. Ther. 8 (2014) 1955-1964. https://doi.org/10.2147/dddt.S60247.
DOI Google Scholar
[7]

W. Pongkan, K. Jinawong, W. Pratchayasakul, et al., D-allulose provides cardioprotective effect by attenuating cardiac mitochondrial dysfunction in obesity-induced insulin-resistant rats, Eur. J. Nutr. 60 (2021) 2047-2061. https://doi.org/10.1007/s00394-020-02394-y.
DOI Google Scholar
[8]

A. Hossain, F. Yamaguchi, T. Matsuo, et al., Rare sugar D-allulose: potential role and therapeutic monitoring in maintaining obesity and type 2 diabetes mellitus, Pharmacol. Therapeut. 155 (2015) 49-59. https://doi.org/10.1016/j.pharmthera.2015.08.004.
DOI Google Scholar
[9]

M. Ochiai, Y. Nakanishi, T. Yamada, et al., Inhibition by dietary D-psicose of body fat accumulation in adult rats fed a high-sucrose diet, Biosci. Biotech. Bioch. 77 (2013) 1123-1126. https://doi.org/10.1271/bbb.130019.
DOI Google Scholar
[10]

Y. Han, H. Park, B.R. Choi, et al., Alteration of microbiome profile by D-allulose in amelioration of high-fat-diet-induced obesity in mice, Nutrients 12 (2020) 352. https://doi.org/10.3390/nu12020352.
DOI Google Scholar
[11]

R. Martin, J. Cao, W. Wu, et al., Identification of pathogenicity-associated loci in Klebsiella pneumoniae from hospitalized patients, mSystems 3 (2018) e00015-00018. https://doi.org/10.1128/mSystems.00015-18.
DOI Google Scholar
[12]

D.R. Plichta, D.B. Graham, S. Subramanian, et al., Therapeutic opportunities in inflammatory bowel disease: mechanistic dissection of host-microbiome relationships, Cell 178 (2019) 1041-1056. https://doi.org/10.1016/j.cell.2019.07.045.
DOI Google Scholar
[13]

A. Mullee, D. Romaguera, J. Pearson-Stuttard, et al., Association between soft drink consumption and mortality in 10 European countries, JAMA Intern. Med. 179(11) (2019) 1479-1490. https://doi.org/10.1001/jamainternmed.2019.2478.
DOI Google Scholar
[14]

S.S.M. Chan, R. Luben, F. van Schaik, et al., Carbohydrate intake in the etiology of Crohn’s disease and ulcerative colitis, Inflamm. Bowel Dis. 20 (2014) 2013-2021. https://doi.org/10.1097/mib.0000000000000168.
DOI Google Scholar
[15]

N. Sakamoto, S. Kono, K. Wakai, et al., Dietary risk factors for inflammatory bowel disease: a multicenter case-control study in Japan, Inflamm. Bowel Dis. 11 (2005) 154-163. https://doi.org/10.1097/00054725-200502000-00009.
DOI Google Scholar
[16]

A. Levine, J.M. Rhodes, J.O. Lindsay, et al., Dietary guidance from the international organization for the study of inflammatory bowel diseases, Clin. Gastroenterol. Hepatol. 18 (2020) 1381-1392. https://doi.org/10.1016/j.cgh.2020.01.046.
DOI Google Scholar
[17]

J. Lloyd-Price, C. Arze, A.N. Ananthakrishnan, et al., Multi-omics of the gut microbial ecosystem in inflammatory bowel diseases, Nature 569 (2019) 655-662. https://doi.org/10.1038/s41586-019-1237-9.
DOI Google Scholar
[18]

S. Hu, S. Li, Y. Liu, et al., Aged ripe Pu-erh tea reduced oxidative stress-mediated inflammation in dextran sulfate sodium-induced colitis mice by regulating intestinal microbes, J Agr. Food Chem. 69 (2021) 10592-10605. https://doi.org/10.1021/acs.jafc.1c04032.
DOI Google Scholar
[19]

C. Li, G. Ai, Y. Wang, et al., Oxyberberine, a novel gut microbiota-mediated metabolite of berberine, possesses superior anti-colitis effect: Impact on intestinal epithelial barrier, gut microbiota profile and TLR4-MyD88-NF-kappaB pathway, Pharmacol Res, 152 (2019) 104603. https://doi.org/10.1016/j.phrs.2019.104603.
DOI Google Scholar
[20]

P.D. Cani, C. Depommier, M. Derrien, et al., Akkermansia muciniphila: paradigm for next-generation beneficial microorganisms, Nat. Rev. Gastroenterol. Hepatol. 19 (2022) 625-637. https://doi.org/10.1038/s41575-022-00631-9.
DOI Google Scholar
[21]

M. Laffin, R. Fedorak, A. Zalasky, et al., A high-sugar diet rapidly enhances susceptibility to colitis via depletion of luminal short-chain fatty acids in mice, Sci. Rep. 9 (2019) 12294. https://doi.org/10.1038/s41598-019-48749-2.
DOI Google Scholar
[22]

M. Niibo, A. Kanasaki, T. Iida, et al., D-allulose protects against diabetic nephropathy progression in Otsuka Long-Evans Tokushima Fatty rats with type 2 diabetes, PLoS ONE 17 (2022) e0263300. https://doi.org/10.1371/journal.pone.0263300.
DOI Google Scholar
[23]

Y. Gou, B. Liu, M. Cheng, et al., D-Allulose ameliorates skeletal muscle insulin resistance in high-fat diet-fed rats, Molecules 26 (2021) 310. https://doi.org/10.3390/molecules26206310.
DOI Google Scholar
[24]

Y. Han, B.R. Choi, S.Y. Kim, et al., Gastrointestinal tolerance of D-allulose in healthy and young adults. A non-randomized controlled trial, Nutrients 10 (2018) 2010. https://doi.org/10.3390/nu10122010.
DOI Google Scholar
[25]

W. Strober, I.J. Fuss, Proinflammatory cytokines in the pathogenesis of inflammatory bowel diseases, Gastroenterology 140 (2011) 1756-1767. https://doi.org/10.1053/j.gastro.2011.02.016.
DOI Google Scholar
[26]

M. Yamamoto, K. Yoshizaki, T. Kishimoto, et al., IL-6 is required for the development of Th1 cell-mediated murine colitis, J. Immunol. 164 (2000) 4878-4882. https://doi.org/10.4049/jimmunol.164.9.4878.
DOI Google Scholar
[27]

H.C. Reinecker, M. Steffen, T. Witthoeft, et al., Enhanced secretion of tumour necrosis factor-alpha, IL-6, and IL-1 beta by isolated lamina propria mononuclear cells from patients with ulcerative colitis and Crohn’s disease, Clin. Exp. Immunol. 94 (1993) 174-181.
DOI Google Scholar
[28]

I. Atreya, R. Atreya, M.F. Neurath, NF-kappa B in inflammatory bowel disease, J. Intern. Med. 263 (2008) 591-596. https://doi.org/10.1111/j.1365-2796.2008.01953.x.
DOI Google Scholar
[29]

L. Jostins, S. Ripke, R.K. Weersma, et al., Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease, Nature 491 (2012) 119-124. https://doi.org/10.1038/nature11582.
DOI Google Scholar
[30]

R.J. Xavier, D.K. Podolsky, Unravelling the pathogenesis of inflammatory bowel disease, Nature 448 (2007) 427-434. https://doi.org/10.1038/nature06005.
DOI Google Scholar
[31]

J.L. Round, S.K. Mazmanian, The gut microbiota shapes intestinal immune responses during health and disease, Nat. Rev. Immunol. 9 (2009) 313-323. https://doi.org/10.1038/nri2515.
DOI Google Scholar
[32]

D.N. Frank, A.L.S. Amand, R.A. Feldman, et al., Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases, P. Natl. Acad. Sci. USA 104 (2007) 13780-13785. https://doi.org/10.1073/pnas.0706625104.
DOI Google Scholar
[33]

R. Caruso, B.C. Lo, G. Nunez, Host-microbiota interactions in inflammatory bowel disease, Nat. Rev. Immunol. 20 (2020) 411-426. https://doi.org/10.1038/s41577-019-0268-7.
DOI Google Scholar
[34]

Y. Han, J. Yoon, M.S. Choi, Tracing the anti-inflammatory mechanism/triggers of D-allulose: a profile study of microbiome composition and mRNA expression in diet-induced obese mice, Mol. Nutr. Food Res. 64 (2020) e1900982. https://doi.org/10.1002/mnfr.201900982.
DOI Google Scholar
[35]

L.E. Ritchie, J.M. Sturino, R.J. Carroll, et al., Polyphenol-rich sorghum brans alter colon microbiota and impact species diversity and species richness after multiple bouts of dextran sodium sulfate-induced colitis, FEMS Microbiol. Ecol. 91 (2015). https://doi.org/10.1093/femsec/fiv008.
DOI Google Scholar
[36]

S. Guo, W. Geng, S. Chen, et al., Ginger alleviates DSS-induced ulcerative colitis severity by improving the diversity and function of gut microbiota, Front. Pharmacol. 12 (2021) 632569. https://doi.org/10.3389/fphar.2021.632569.
DOI Google Scholar
[37]

H.X. Cui, L.S. Zhang, Y. Luo, et al., A purified anthraquinone-glycoside preparation from rhubarb ameliorates type 2 diabetes mellitus by modulating the gut microbiota and reducing inflammation, Front. Microbiol. 10 (2019) 1423. https://doi.org/10.3389/fmicb.2019.01423.
DOI Google Scholar
[38]

Y. Zhou, M.H. Zhang, Q.X. Liu, et al., The alterations of tracheal microbiota and inflammation caused by different levels of ammonia exposure in broiler chickens, Poultry Sci. 100 (2021) 685-696. https://doi.org/10.1016/j.psj.2020.11.026.
DOI Google Scholar
[39]

P.D. Cani, C. Depommier, M. Derrien, et al., Akkermansia muciniphila: paradigm for next-generation beneficial microorganisms, Nat. Rev. Gastro. Hepat. (2022). https://doi.org/10.1038/s41575-022-00631-9.
DOI Google Scholar
[40]

A. Everard, C. Belzer, L. Geurts, et al., Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity, P. Natl. Acad. Sci. USA 110 (2013) 9066-9071. https://doi.org/10.1073/pnas.1219451110.
DOI Google Scholar
[41]

H. Ge, Z. Cai, J. Chai, et al., Egg white peptides ameliorate dextran sulfate sodium-induced acute colitis symptoms by inhibiting the production of pro-inflammatory cytokines and modulation of gut microbiota composition, Food Chem. 360 (2021) 129981. https://doi.org/10.1016/j.foodchem.2021.129981.
DOI Google Scholar
[42]

M.S. Desai, A.M. Seekatz, N.M. Koropatkin, et al., A dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility, Cell 167 (2016) 1339-1353. https://doi.org/10.1016/j.cell.2016.10.043.
DOI Google Scholar
[43]

Y. Wang, Y. Zou, J. Wang, et al., The protective effects of 2’-fucosyllactose against E. coli O157 infection are mediated by the regulation of gut microbiota and the inhibition of pathogen adhesion, Nutrients 12 (2020) 1284. https://doi.org/10.3390/nu12051284.
DOI Google Scholar
[44]

P.D. Cani, R. Bibiloni, C. Knauf, et al., Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice, Diabetes 57 (2008) 1470-1481. https://doi.org/10.2337/db07-1403.
DOI Google Scholar
[45]

Z. Wu, Q. Xu, S. Gu, et al., Akkermansia muciniphila ameliorates clostridioides difficile infection in mice by modulating the intestinal microbiome and metabolites, Front. Microbiol. 13 (2022). https://doi.org/10.3389/fmicb.2022.841920.
DOI Google Scholar
[46]

M. Sun, D. Li, M. Hua, et al., Black bean husk and black rice anthocyanin extracts modulated gut microbiota and serum metabolites for improvement in type 2 diabetic rats, Food Funct. 13 (2022) 7377-7391. https://doi.org/10.1039/d2fo01165d.
DOI Google Scholar
[47]

T. Suzuki, Y. Sato, S. Kadoya, et al., Comparative effects of allulose, fructose, and glucose on the small intestine, Nutrients 14 (2022) 3230. https://doi.org/10.3390/nu14153230.
DOI Google Scholar
[48]

Y.S. Kim, S.B. Ho, Intestinal goblet cells and mucins in health and disease: recent insights and progress, Curr. Gastroenterol. Rep. 12 (2010) 319-330. https://doi.org/10.1007/s11894-010-0131-2.
DOI Google Scholar
[49]

M.E. Johansson, M. Phillipson, J. Petersson, et al., The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria, Proc. Natl. Acad. Sci. USA 105 (2008) 15064-15069. https://doi.org/10.1073/pnas.0803124105.
DOI Google Scholar
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Received: 07 November 2022
Revised: 06 December 2022
Accepted: 26 February 2023
Published: 01 June 2023
Issue date: January 2024

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© 2024 Beijing Academy of Food Sciences. Publishing services by Tsinghua University Press.

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This work was funded by the National Natural Science Foundation of China (No. 32030083).

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This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

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