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26.05.2020 | Original Contribution

Dietary riboflavin deficiency induces ariboflavinosis and esophageal epithelial atrophy in association with modification of gut microbiota in rats

verfasst von: Feng Pan, Ling-Li Zhang, Hong-Jun Luo, Ye Chen, Lin Long, Xuan Wang, Pei-Tong Zhuang, En-Min Li, Li-Yan Xu

Erschienen in: European Journal of Nutrition | Ausgabe 2/2021

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Abstract

Purpose

Riboflavin deficiency causes ariboflavinosis, a common nutritional deficiency disease. The purpose of this study is to investigate the effects of riboflavin deficiency on the important internal organs and its potential mechanisms.

Methods

Experiment 1, male F344 rats were randomly assigned to R₆ (normal riboflavin, 6 mg/kg) and R₀ (riboflavin-deficient, 0 mg/kg) groups. Experiment 2 rats were assigned to R₆, R_0.6 (0.6 mg/kg) and R_0.06 (0.06 mg/kg) groups. Experiment 3 rats were assigned to R₆ and R₀ → R₆ (riboflavin replenishment) groups. Bacterial communities were analyzed based on 16S rRNA gene sequencing.

Results

Riboflavin deficiency induced ariboflavinosis (R_0.06 46.7%; R₀ 72%) and esophageal epithelial atrophy (R_0.06 40%; R₀ 44%) in rats, while the R₆ group did not display symptoms (P < 0.001, respectively). Esophageal epithelial atrophy occurred simultaneously (R_0.06 66.7%; R₀ 63.6%) with ariboflavinosis or appeared alone (R_0.06 33.3%; R₀ 36.4%). Esophagus is the most vulnerable internal organ. Riboflavin deficiency followed by replenishment (R₀ → R₆) was effective in treating ariboflavinosis (83.3% vs. 0%, P < 0.001) and esophageal epithelial atrophy (66.7% vs. 20%, P = 0.17). Riboflavin deficiency modulated gut microbiota composition. The several key genera (Romboutsia, Turicibacter and Clostridium sensu stricto 1) were strongly correlated with ariboflavinosis and esophageal epithelial atrophy (P < 0.01 or P < 0.05). The potential mechanism is that gut microbiota affects body's xenobiotic biodegradation and metabolism, and genomic instability.

Conclusions

Riboflavin deficiency induces ariboflavinosis and esophageal epithelial atrophy by modulating the gut microbiota, and offers new Queryinsight into riboflavin deficiency and esophageal lesions.

Nur mit Berechtigung zugänglich

Powers HJ (2003) Riboflavin (vitamin B-2) and health. Am J Clin Nutr 77(6):1352–1360. https://doi.org/10.1093/ajcn/77.6.1352CrossRefPubMed

Juarez Del Valle M, Laino JE, de Moreno de LeBlanc A, de Savoy Giori G, LeBlanc JG (2016) Soyamilk fermented with riboflavin-producing Lactobacillus plantarum CRL 2130 reverts and prevents ariboflavinosis in murine models. B J Nutr 116(7):1229–1235CrossRef

Powers HJ, Hill MH, Mushtaq S, Dainty JR, Majsak-Newman G, Williams EA (2011) Correcting a marginal riboflavin deficiency improves hematologic status in young women in the United Kingdom (RIBOFEM). Am J Clin Nutr 93(6):1274–1284. https://doi.org/10.3945/ajcn.110.008409CrossRefPubMed

Whitfield KC, Karakochuk CD, Liu Y, McCann A, Talukder A, Kroeun H, Ward M, McNulty H, Lynd LD, Kitts DD, Li-Chan EC, McLean J, Green TJ (2015) Poor thiamin and riboflavin status is common among women of childbearing age in rural and urban Cambodia. J Nutr 145(3):628–633. https://doi.org/10.3945/jn.114.203604CrossRefPubMed

Choi JY, Kim YN, Cho YO (2014) Evaluation of riboflavin intakes and status of 20–64-year-old adults in South Korea. Nutrients 7(1):253–264. https://doi.org/10.3390/nu7010253CrossRefPubMedPubMedCentral

O'Brien MM, Kiely M, Harrington KE, Robson PJ, Strain JJ, Flynn A (2001) The North/South Ireland food consumption survey: vitamin intakes in 18–64-year-old adults. Public Health Nutr 4(5a):1069–1079CrossRef

LeBlanc JG, Milani C, de Giori GS, Sesma F, van Sinderen D, Ventura M (2013) Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Curr Opin Biotechnol 24(2):160–168. https://doi.org/10.1016/j.copbio.2012.08.005CrossRefPubMed

Sydenstricker VP (1941) Clinical manifestations of ariboflavinosis. Am J Public Health Nations Health 31(4):344–350. https://doi.org/10.2105/ajph.31.4.344CrossRefPubMedPubMedCentral

Thakur K, Tomar SK, Singh AK, Mandal S, Arora S (2017) Riboflavin and health: a review of recent human research. Crit Rev Food Sci Nutr 57(17):3650–3660. https://doi.org/10.1080/10408398.2016.1145104CrossRefPubMed

10.

Mensink GB, Fletcher R, Gurinovic M, Huybrechts I, Lafay L, Serra-Majem L, Szponar L, Tetens I, Verkaik-Kloosterman J, Baka A, Stephen AM (2013) Mapping low intake of micronutrients across Europe. Br J Nutr 110(4):755–773. https://doi.org/10.1017/s000711451200565xCrossRefPubMedPubMedCentral

11.

Hannon EM, Kiely M, Harrington KE, Robson PJ, Strain JJ, Flynn A (2001) The North/South Ireland food consumption survey: mineral intakes in 18–64-year-old adults. Public Health Nutr 4(5a):1081–1088CrossRef

12.

Mataix J, Aranda P, Sanchez C, Montellano MA, Planells E, Llopis J (2003) Assessment of thiamin (vitamin B1) and riboflavin (vitamin B2) status in an adult Mediterranean population. Br J Nutr 90(3):661–666. https://doi.org/10.1079/bjn2003926CrossRefPubMed

13.

Richards JL, Yap YA, McLeod KH, Mackay CR, Marino E (2016) Dietary metabolites and the gut microbiota: an alternative approach to control inflammatory and autoimmune diseases. Clin Transl Immunol 5(5):e82. https://doi.org/10.1038/cti.2016.29CrossRef

14.

Petta I, Fraussen J, Somers V, Kleinewietfeld M (2018) Interrelation of diet, gut microbiome, and autoantibody production. Front Immunol 9:439. https://doi.org/10.3389/fimmu.2018.00439CrossRefPubMedPubMedCentral

15.

Aqil F, Jeyabalan J, Munagala R, Singh IP, Gupta RC (2016) Prevention of hormonal breast cancer by dietary jamun. Mol Nutr Food Res 60(6):1470–1481. https://doi.org/10.1002/mnfr.201600013CrossRefPubMedPubMedCentral

16.

Long L, Pang XX, Lei F, Zhang JS, Wang W, Liao LD, Xu XE, He JZ, Wu JY, Wu ZY, Wang LD, Lin DC, Li EM, Xu LY (2018) SLC52A3 expression is activated by NF-kappaB p65/Rel-B and serves as a prognostic biomarker in esophageal cancer. Cell Mol Life Sci 75(14):2643–2661. https://doi.org/10.1007/s00018-018-2757-4CrossRefPubMedPubMedCentral

17.

Zhu Z, Zhu B, Sun Y, Ai C, Wang L, Wen C, Yang J, Song S, Liu X (2018) Sulfated polysaccharide from sea cucumber and its depolymerized derivative prevent obesity in association with modification of gut microbiota in high-fat diet-fed mice. Mol Nutr Food Res 62(23):e1800446. https://doi.org/10.1002/mnfr.201800446CrossRefPubMed

18.

Magoc T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27(21):2957–2963. https://doi.org/10.1093/bioinformatics/btr507CrossRefPubMedPubMedCentral

19.

Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10(10):996–998. https://doi.org/10.1038/nmeth.2604CrossRefPubMed

20.

Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336. https://doi.org/10.1038/nmeth.f.303CrossRefPubMedPubMedCentral

21.

Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31(9):814–821. https://doi.org/10.1038/nbt.2676CrossRefPubMedPubMedCentral

22.

Parks DH, Tyson GW, Hugenholtz P, Beiko RG (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30(21):3123–3124. https://doi.org/10.1093/bioinformatics/btu494CrossRefPubMedPubMedCentral

23.

Koppel N, Maini Rekdal V (2017) Chemical transformation of xenobiotics by the human gut microbiota. Science. https://doi.org/10.1126/science.aag2770CrossRefPubMed

24.

Wynder EL, Klein UE (1965) The possible role of riboflavin deficiency in epithelial neoplasia. I. epithelial changes of mice in simple deficiency. Cancer 18:167–180CrossRef

25.

Foy H, Kondi A (1984) The vulnerable esophagus: riboflavin deficiency and squamous cell dysplasia of the skin and the esophagus. J Natl Cancer Inst 72(4):941–948PubMed

26.

Gerritsen J, Umanets A, Staneva I, Hornung B, Ritari J, Paulin L, Rijkers GT, de Vos WM, Smidt H (2018) Romboutsia hominis sp. nov., the first human gut-derived representative of the genus Romboutsia, isolated from ileostoma effluent. Int J Syst Evol Microbiol 68(11):3479–3486. https://doi.org/10.1099/ijsem.0.003012CrossRefPubMed

27.

O'Neal L, Obregón-Tito AJ, Tito RY, Ozga AT, Polo SI, Lewis CM Jr, Lawson PA (2015) Clostridium amazonense sp. nov. an obliqately anaerobic bacterium isolated from a remote Amazonian community in Peru. Anaerobe 35(Pt B):33–37. https://doi.org/10.1016/j.anaerobe.2015.06.005CrossRefPubMedPubMedCentral

28.

Mangifesta M, Mancabelli L, Milani C (2018) Mucosal microbiota of intestinal polyps reveals putative biomarkers of colorectal cancer. Sci Rep 8(1):13974. https://doi.org/10.1038/s41598-018-32413-2CrossRefPubMedPubMedCentral

29.

Zhao F, Feng J, Li J, Zhao L, Liu Y, Chen H, Jin Y, Zhu B, Wei Y (2018) Alterations of the gut microbiota in Hashimoto’s thyroiditis patients. Thyroid 28(2):175–186. https://doi.org/10.1089/thy.2017.0395CrossRefPubMed

30.

Call L, Stoll B, Oosterloo B, Ajami N, Sheikh F, Wittke A, Waworuntu R, Berg B, Petrosino J, Olutoye O, Burrin D (2018) Metabolomic signatures distinguish the impact of formula carbohydrates on disease outcome in a preterm piglet model of NEC. Microbiome 6(1):111. https://doi.org/10.1186/s40168-018-0498-0CrossRefPubMedPubMedCentral

31.

Li Y, Han H, Yin J, He X, Tang Z, Li T, Yao K, Yin Y (2019) D- and l-aspartate regulates growth performance, inflammation and intestinal microbial community in young pigs. Food Funct 10(2):1028–1037. https://doi.org/10.1039/c8fo01410hCrossRefPubMed

32.

Bosshard PP, Zbinden R, Altwegg M (2002) Turicibacter sanguinis gen. nov., sp. nov., a novel anaerobic, Gram-positive bacterium. Int J Syst Evol Microbiol 52(Pt 4):1263–1266. https://doi.org/10.1099/00207713-52-4-1263CrossRefPubMed

33.

Liu G, Bei J, Liang L, Yu G, Li L, Li Q (2018) Stachyose improves inflammation through modulating gut microbiota of high-fat diet/streptozotocin-induced type 2 diabetes in rats. Mol Nutr Food Res 62(6):e1700954. https://doi.org/10.1002/mnfr.201700954CrossRefPubMed

34.

Anhe FF, Varin TV, Le Barz M, Pilon G, Dudonne S, Trottier J, St-Pierre P, Harris CS, Lucas M, Lemire M, Dewailly E, Barbier O, Desjardins Y, Roy D, Marette A (2018) Arctic berry extracts target the gut-liver axis to alleviate metabolic endotoxaemia, insulin resistance and hepatic steatosis in diet-induced obese mice. Diabetologia 61(4):919–931. https://doi.org/10.1007/s00125-017-4520-zCrossRefPubMed

35.

Henning SM, Yang J, Hsu M, Lee RP, Grojean EM, Ly A, Tseng CH, Heber D, Li Z (2018) Decaffeinated green and black tea polyphenols decrease weight gain and alter microbiome populations and function in diet-induced obese mice. Eur J Nutr 57(8):2759–2769. https://doi.org/10.1007/s00394-017-1542-8CrossRefPubMed

36.

Plottel CS, Blaser MJ (2011) Microbiome and malignancy. Cell Host Microbe 10(4):324–335. https://doi.org/10.1016/j.chom.2011.10.003CrossRefPubMedPubMedCentral

37.

Kjer-Nielsen L, Patel O, Corbett AJ, Le Nours J, Meehan B, Liu L, Bhati M, Chen Z, Kostenko L, Reantragoon R, Williamson NA, Purcell AW, Dudek NL, McConville MJ, O'Hair RA, Khairallah GN, Godfrey DI, Fairlie DP, Rossjohn J, McCluskey J (2012) MR1 presents microbial vitamin B metabolites to MAIT cells. Nature 491(7426):717–723. https://doi.org/10.1038/nature11605CrossRefPubMed

38.

Legoux F, Bellet D (2019) Microbial metabolites control the thymic development of mucosal-associated invariant T cells. Science 366(6464):494–499. https://doi.org/10.1126/science.aaw2719CrossRefPubMed

39.

Pan F, Chen Y, He JZ, Long L, Chen Y, Luo HJ, Xu YW, Pang XX, Yang Q, Wang JJ, Xu XE, Wang SH, Li EM, Xu LY (2019) Dietary riboflavin deficiency promotes N-nitrosomethylbenzylamine-induced esophageal tumorigenesis in rats by inducing chronic inflammation. Am J Cancer Res 9(11):2469–2481PubMedPubMedCentral

40.

Ratnaparkhe M, Wong JKL, Wei PC, Hlevnjak M, Kolb T, Simovic M, Haag D, Paul Y, Devens F, Northcott P, Jones DTW, Kool M, Jauch A, Pastorczak A, Mlynarski W, Korshunov A, Kumar R (2018) Defective DNA damage repair leads to frequent catastrophic genomic events in murine and human tumors. Nat Commun 9(1):4760. https://doi.org/10.1038/s41467-018-06925-4CrossRefPubMedPubMedCentral

41.

Nickoloff JA, Jones D, Lee SH, Williamson EA, Hromas R (2017) Drugging the cancers addicted to DNA repair. J Natl Cancer Inst. https://doi.org/10.1093/jnci/djx059CrossRefPubMedPubMedCentral

Titel: Dietary riboflavin deficiency induces ariboflavinosis and esophageal epithelial atrophy in association with modification of gut microbiota in rats
verfasst von: Feng Pan
Ling-Li Zhang
Hong-Jun Luo
Ye Chen
Lin Long
Xuan Wang
Pei-Tong Zhuang
En-Min Li
Li-Yan Xu
Publikationsdatum: 26.05.2020
Verlag: Springer Berlin Heidelberg
Erschienen in: European Journal of Nutrition / Ausgabe 2/2021
Print ISSN: 1436-6207
Elektronische ISSN: 1436-6215
DOI: https://doi.org/10.1007/s00394-020-02283-4

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Dietary riboflavin deficiency induces ariboflavinosis and esophageal epithelial atrophy in association with modification of gut microbiota in rats