A novel strain of <i>Levilactobacillus brevis</i> PDD-5 isolated from salty vegetables has beneficial effects on hyperuricemia through anti-inflammation and improvement of kidney damage

Jue Xu; Maolin Tu; Xiankang Fan; Yuxing Guo; Tao Zhang; Xiaoqun Zeng; Zhendong Cai; Zhen Wu; Daodong Pan

doi:10.26599/FSHW.2022.9250077

Food Science and Human Wellness 2024, 13(2): 898-908 https://doi.org/10.26599/FSHW.2022.9250077

Open Access | Issue | Published: 25 September 2023

A novel strain of Levilactobacillus brevis PDD-5 isolated from salty vegetables has beneficial effects on hyperuricemia through anti-inflammation and improvement of kidney damage

Show Author's Information Hide Author's Information Jue Xu^{^a^,^b}, Maolin Tu^{^a^,^b}, Xiankang Fan^{^a^,^b}, Yuxing Guo^{^c}, Tao Zhang^{^c}, Xiaoqun Zeng^{^a^,^b}, Zhendong Cai^{^a^,^b}, Zhen Wu^{^a^,^b}, Daodong Pan^{^a^,^b^,}(

)

State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo 315211, China

Key Laboratory of Animal Protein Food Deep Processing Technology of Zhejiang Province, College of Food and Pharmaceutical Sciences, Ningbo University, Ningbo 315211, China

Department of Food Science and Technology, School of Food Science and Pharmaceutical Engineering, Nanjing Normal University, Nanjing 210023, China

Peer review under responsibility of Tsinghua University Press.

Keywords:

Lactic acid bacteria, Hyperuricemia, Purine nucleoside, Uric acid nephropathy

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Xu J, Tu M, Fan X, et al. A novel strain of Levilactobacillus brevis PDD-5 isolated from salty vegetables has beneficial effects on hyperuricemia through anti-inflammation and improvement of kidney damage. Food Science and Human Wellness, 2024, 13(2): 898-908. https://doi.org/10.26599/FSHW.2022.9250077

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Abstract

Hyperuricemia is a metabolic disorder caused by abnormal purine metabolism, resulting in abnormally high serum uric acid. In this study, a novel Levilactobacillus brevis PDD-5 isolated from salty vegetables was verified with the function of alleviating hyperuricemia. The relevant effects of L. brevis PDD-5 in lowering uric acid were analyzed by in vitro and in vivo experiments. The results showed that the L. brevis PDD-5 has (68.86 ± 15.46)% of inosine uptake capacity and (95.75 ± 3.30)% of guanosine uptake capacity in vitro. Oral administration of L. brevis PDD-5 to hyperuricemia rats reduced uric acid, creatinine, and urea nitrogen in serum, as well as decreased inosine and guanosine levels in the intestinal contents of rats. Analysis of relevant markers in the kidney by ELISA kits revealed that L. brevis PDD-5 alleviated oxidative stress and inflammation. Moreover, the gene expression of uric acid transporter 1 (URAT1) and glucose transporter 9 (GLUT9) was down-regulated, and the gene expression of organic anion transporter 1 (OAT1) was up-regulated after treatment with L. brevis PDD-5. Western blot analysis showed that L. brevis PDD-5 alleviated hyperuricemia-induced kidney injury through the NLRP3 pathway. These findings suggest that L. brevis PDD-5 can lower uric acid, repair kidney damage, and also has the potential to prevent uric acid nephropathy.

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A novel strain of Levilactobacillus brevis PDD-5 isolated from salty vegetables has beneficial effects on hyperuricemia through anti-inflammation and improvement of kidney damage

Show Author's information Hide Author's Information Jue Xu^{^a^,^b}, Maolin Tu^{^a^,^b}, Xiankang Fan^{^a^,^b}, Yuxing Guo^{^c}, Tao Zhang^{^c}, Xiaoqun Zeng^{^a^,^b}, Zhendong Cai^{^a^,^b}, Zhen Wu^{^a^,^b}, Daodong Pan^{^a^,^b^,}(

)

State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo 315211, China

Key Laboratory of Animal Protein Food Deep Processing Technology of Zhejiang Province, College of Food and Pharmaceutical Sciences, Ningbo University, Ningbo 315211, China

Department of Food Science and Technology, School of Food Science and Pharmaceutical Engineering, Nanjing Normal University, Nanjing 210023, China

Peer review under responsibility of Tsinghua University Press.

Abstract

Keywords: Lactic acid bacteria, Hyperuricemia, Purine nucleoside, Uric acid nephropathy

References(49)

[1]

A. Dehghan, A. Köttgen, Q. Yang, et al., Association of three genetic loci with uric acid concentration and risk of gout: a genome-wide association study, Lancet 372 (2008) 1953-1961. https://doi.org/10.1016/s0140-6736(08)61343-4.

DOI Google Scholar

[2]

R.P. Obermayr, C. Temml, G. Gutjahr, et al., Elevated uric acid increases the risk for kidney disease, J. Am. Soc. Nephrol. 19 (2008) 2407-2413. https://doi.org/10.1681/asn.2008010080.

DOI Google Scholar

[3]

DOI Google Scholar

[4]

Q. Luo, X. Xia, B. Li, et al. Serum uric acid and cardiovascular mortality in chronic kidney disease: a meta-analysis, BMC Nephrol. 20 (2019) 18. https://doi.org/10.1186/s12882-018-1143-7.

DOI Google Scholar

[5]

H.K. Choi, K. Atkinson, E.W. Karlson, et al., Purine-rich foods, dairy and protein intake, and the risk of gout in men, New Engl. J. Med. 350 (2004) 1093-1103. https://doi.org/10.1056/NEJMoa035700.

DOI Google Scholar

[6]

M.H. Pillinger, B.F. Mandell, Therapeutic approaches in the treatment of gout, Semin. Arthritis Rheum. 50 (2020) S24-S30. https://doi.org/10.1016/j.semarthrit.2020.04.010.

DOI Google Scholar

[7]

H. Shuwen, D. Kefeng, Intestinal phages interact with bacteria and are involved in human diseases, Gut Microbes. 14 (2022) 2113717. https://doi.org/10.1080/19490976.2022.2113717.

DOI Google Scholar

[8]

L. Gan, W.H. Xu, Y. Xiong, et al., Probiotics: their action against pathogens can be turned around, Sci. Rep. 11 (2021) 13247. https://doi.org/10.1038/s41598-021-91542-3.

DOI Google Scholar

[9]

Y. Xiao, C. Zhang, X. Zeng, et al., Microecological treatment of hyperuricemia using Lactobacillus from pickles, BMC Microbiol. 20 (2020) 195. https://doi.org/10.1186/s12866-020-01874-9.

DOI Google Scholar

[10]

N. Yamada, C. Saito-Iwamoto, M. Nakamura, et al., Lactobacillus gasseri PA-3 uses the purines IMP, inosine and hypoxanthine and reduces their absorption in rats, Microorganisms 5 (2017) 10. https://doi.org/10.3390/microorganisms5010010.

DOI Google Scholar

[11]

H. Wang, L. Mei, Y. Deng, et al., Lactobacillus brevis DM9218 ameliorates fructose-induced hyperuricemia through inosine degradation and manipulation of intestinal dysbiosis, Nutrition 62 (2019) 63-73. https://doi.org/10.1016/j.nut.2018.11.018.

DOI Google Scholar

[12]

A.T. Vieira, I. Galvao, F.A. Amaral, et al., Oral treatment with Bifidobacterium longum 5^1A reduced inflammation in a murine experimental model of gout, Benef. Microbes. 6 (2015) 799-806. https://doi.org/10.3920/BM2015.0015.

DOI Google Scholar

[13]

A. de Moreno de LeBlanc, C. Matar, E. Farnworth, et al., Study of cytokines involved in the prevention of a murine experimental breast cancer by Kefir, Cytokine 34 (2006) 1-8. https://doi.org/10.1016/j.cyto.2006.03.008.

DOI Google Scholar

[14]

G. Wang, Q. Si, S. Yang, et al., Lactic acid bacteria reduce diabetes symptoms in mice by alleviating gut microbiota dysbiosis and inflammation in different manners, Food Funct. 11 (2020) 5898-5914. https://doi.org/10.1039/C9FO02761K.

DOI Google Scholar

[15]

P.L. Conway, S.L. Gorbach, B.R. Goldin, Survival of lactic acid bacteria in the human stomach and adhesion to intestinal cells, J. Dairy Sci. 70 (1987) 1-12. https://doi.org/10.3168/jds.S0022-0302(87)79974-3.

DOI Google Scholar

[16]

J. He, W. Wang, Z. Wu, et al., Effect of Lactobacillus reuteri on intestinal microbiota and immune parameters: involvement of sex differences, J. Funct. Foods 53 (2019) 36-43. https://doi.org/10.1016/j.jff.2018.12.010.

DOI Google Scholar

[17]

U. Schillinger, F.K. Lücke, Antibacterial activity of Lactobacillus sake isolated from meat, Appl. Environ. Microb. 55 (1989) 1901-1906. https://doi.org/10.1128/aem.55.8.1901-1906.1989.

DOI Google Scholar

[18]

M. Rosenberg, D. Gutnick, E. Rosenberg, Adherence of bacteria to hydrocarbons: a simple method for measuring cell-surface hydrophobicity, FEMS Microbiol. Lett. 9 (1980) 29-33. https://doi.org/10.1111/j.1574-6968.1980.tb05599.x.

DOI Google Scholar

[19]

H.V. Herck, V. Baumans, C. Brandt, et al., Orbital sinus blood sampling in rats as performed by different animal technicians: the influence of technique and expertise, Lab. Anim.-UK 32 (1998) 377-386. https://doi.org/10.1177/0023677217741332.

DOI Google Scholar

[20]

R. Chavez, D.J. Fraser, T. Bowen, et al., Kidney ischaemia reperfusion injury in the rat: the EGTI scoring system as a valid and reliable tool for histological assessment, J. Histology Histopathology 3 (2016) 1. https://doi.org/10.7243/2055-091X-3-1.

DOI Google Scholar

[21]

R. van der Westen, J. Sjollema, R. Molenaar, et al., Floating and tether-coupled adhesion of bacteria to hydrophobic and hydrophilic surfaces, Langmuir 34 (2018) 4937-4944. https://doi.org/10.1021/acs.langmuir.7b04331.

DOI Google Scholar

[22]

P.F. Pérez, Y. Minnaard, E.A. Disalvo, et al., Surface properties of bifidobacterial strains of human origin, Appl. Environ. Microb. 64 (1998) 21-26. https://doi.org/10.1002/abio.370180412.

DOI Google Scholar

[23]

D. Vedder, W. Walrabenstein, M. Heslinga, et al., Dietary interventions for gout and effect on cardiovascular risk factors: a systematic review, Nutrients 11 (2019) 2955. https://doi.org/10.3390/nu11122955.

DOI Google Scholar

[24]

L.M. Salati, C.J. Gross, L.M. Henderson, et al., Absorption and metabolism of adenine, adenosine-5’-monophosphate, adenosine and hypoxanthine by the isolated vascularly perfused rat small intestine, J. Nutr. 114 (1984) 753-760. https://doi.org/10.1093/jn/114.4.753.

DOI Google Scholar

[25]

E.B.M. Daliri, B.H. Lee, New perspectives on probiotics in health and disease, Food Sci. Hum. Well. 4 (2015) 56-65. https://doi.org/10.1016/j.fshw.2015.06.002.

DOI Google Scholar

[26]

J. Wang, Y. Chen, H. Zhong, et al., The gut microbiota as a target to control hyperuricemia pathogenesis: potential mechanisms and therapeutic strategies, Crit. Rev. Food Sci. 62 (2022) 3979-3989. https://doi.org/10.1080/10408398.2021.1874287.

DOI Google Scholar

[27]

C. Huang, M. Zheng, Y. Huang, et al., The effect of purine content on sensory quality of pork, Meat Sci. 172 (2021) 108346. https://doi.org/10.1016/j.meatsci.2020.108346.

DOI Google Scholar

[28]

Y. Lee, P. Werlinger, J.W. Suh, et al., Potential probiotic Lacticaseibacillus paracasei MJM60396 prevents hyperuricemia in a multiple way by absorbing purine, suppressing xanthine oxidase and regulating urate excretion in mice, Microorganisms 10 (2022) 851. https://doi.org/10.3390/microorganisms10050851.

DOI Google Scholar

[29]

T.H. Nguyen, Y. Kim, J.S. Kim, et al., Evaluating the cryoprotective encapsulation of the lactic acid bacteria in simulated gastrointestinal conditions, Biotechnol. Bioprocess E. 25 (2020) 287-292. https://doi.org/10.1007/s12257-019-0406-x.

DOI Google Scholar

[30]

J.H. Jung, S.J. Kim, J.Y. Lee, et al., Multifunctional properties of Lactobacillus plantarum strains WiKim83 and WiKim87 as a starter culture for fermented food, Food Sci. Nutr. 7 (2019) 2505-2516. https://doi.org/10.1002/fsn3.1075.

DOI Google Scholar

[31]

V. Santarmaki, Y. Kourkoutas, G. Zoumpopoulou, et al., Survival, intestinal Mucosa Adhesion, and immunomodulatory potential of Lactobacillus plantarum strains, Curr. Microbiol. 74 (2017) 1061-1067. https://doi.org/10.1007/s00284-017-1285-z.

DOI Google Scholar

[32]

K. McDowell, P. Welsh, K.F. Docherty, et al., Dapagliflozin reduces uric acid concentration, an independent predictor of adverse outcomes in DAPA-HF, Eur. J. Heart Fail 24 (2022) 1066-1076. https://doi.org/10.1002/ejhf.2433.

DOI Google Scholar

[33]

J. Cao, Q. Liu, H. Hao, et al., Lactobacillus paracasei X11 ameliorates hyperuricemia and modulates gut microbiota in mice, Front. Immunol. 13 (2022) 940228. https://doi.org/10.3389/fimmu.2022.940228.

DOI Google Scholar

[34]

E. Altermann, W.M. Russell, M.A. Azcarate Peril, et al., Complete genome sequence of the probiotic lactic acid bacterium Lactobacillus acidophilus NCFM, Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 3906-3912. https://doi.org/10.1073/pnas.0409188102.

DOI Google Scholar

[35]

Lesinurad/Allopurinol (duzallo) for gout-associated hyperuricemia, JAMA 319 (2018) 188-189. https://doi.org/10.1001/jama.2017.20189.

DOI

[36]

C.T. Lee, L.C. Chang, C.W. Liu, et al., Negative correlation between serum uric acid and kidney URAT1 mRNA expression caused by resveratrol in rats, Mol. Nutr. Food Res. 61 (2017) 1601030. https://doi.org/10.1002/mnfr.201601030.

DOI Google Scholar

[37]

G. Chen, M.L. Tan, K.K. Li, et al., Green tea polyphenols decreases uric acid level through xanthine oxidase and renal urate transporters in hyperuricemic mice, J. Ethnopharmacol. 175 (2015) 14-20. https://doi.org/10.1016/j.jep.2015.08.043.

DOI Google Scholar

[38]

C. Grant, U. Oh, K. Yao, et al., Dysregulation of TGF-beta signaling and regulatory and effector T-cell function in virus-induced neuroinflammatory disease, Blood 111 (2008) 5601-5609. https://doi.org/10.1182/blood-2007-11-123430.

DOI Google Scholar

[39]

G. Wang, H. Tang, Y. Zhang, et al., The intervention effects of Lactobacillus casei LC2W on Escherichia coli O157:H7-induced mouse colitis, Food Sci. Hum. Well. 9 (2020) 289-294. https://doi.org/10.1016/j.fshw.2020.04.008.

DOI Google Scholar

[40]

Y. Wu, Z. Ye, P. Feng, et al., Limosilactobacillus fermentum JL-3 isolated from “Jiangshui” ameliorates hyperuricemia by degrading uric acid, Gut Microbes. 13 (2021) 1897211. https://doi.org/10.1080/19490976.2021.1897211.

DOI Google Scholar

[41]

G. Agirman, K.B. Yu, E.Y. Hsiao, Signaling inflammation across the gutbrain axis, Science 374 (2021) 1087-1092. https://doi.org/10.1126/science.abi6087.

DOI Google Scholar

[42]

I. Calabuig, M. Gómez-Garberí, M. Andrés, Gout is prevalent but underregistered among patients with cardiovascular events: a field study, Front. Med. 7 (2020) 560. https://doi.org/10.3389/fmed.2020.00560.

DOI Google Scholar

[43]

Y. Zhou, M. Zhao, Z. Pu, et al., Relationship between oxidative stress and inflammation in hyperuricemia: analysis based on asymptomatic young patients with primary hyperuricemia, Medicine 97 (2018) e13108. https://doi.org/10.1097/MD.0000000000013108.

DOI Google Scholar

[44]

J. Huo, Y. Ming, H. Li, et al., The protective effects of peptides from Chinese baijiu on AAPH-induced oxidative stress in HepG2 cells via Nrf2-mediated signaling pathway, Food Sci. Hum. Well. 11 (2022) 1527-1538. https://doi.org/10.1016/j.fshw.2022.06.010.

DOI Google Scholar

[45]

T. Hu, R. Chen, Y. Qian, et al., Antioxidant effect of Lactobacillus fermentum HFY02-fermented soy milk on D-galactose-induced aging mouse model, Food Sci. Hum. Well. 11 (2022) 1362-1372. https://doi.org/10.1016/j.fshw.2022.04.036.

DOI Google Scholar

[46]

T. Nutmakul, A review on benefits of quercetin in hyperuricemia and gouty arthritis, Saudi. Pharm. J. 30 (2022) 918-926. https://doi.org/10.1016/j.jsps.2022.04.013.

DOI Google Scholar

[47]

Z.R. Sun, H.R. Liu, D. Hu, et al., Ellagic acid exerts beneficial effects on hyperuricemia by inhibiting xanthine oxidase and NLRP3 inflammasome activation, J. Agr. Food Chem. 69 (2021) 12741-12752. https://doi.org/10.1021/acs.jafc.1c05239.

DOI Google Scholar

[48]

M. Kanbay, A. Ozkara, Y. Selcoki, et al., Effect of treatment of hyperuricemia with allopurinol on blood pressure, creatinine clearence, and proteinuria in patients with normal renal functions, Int. Urol. Nephrol. 39 (2007) 1227-1233. https://doi.org/10.1007/s11255-007-9253-3.

DOI Google Scholar

[49]

R.J. Fontana, Y.J. Li, E. Phillips, et al., Allopurinol hepatotoxicity is associated with human leukocyte antigen Class I alleles, Liver Int. 41 (2021) 1884-1893. https://doi.org/10.1111/liv.14903.

DOI Google Scholar

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Received: 11 July 2022

Revised: 27 September 2022

Accepted: 26 October 2022

Published: 25 September 2023

Issue date: March 2024

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The authors thank the National Natural Science Foundation of China (31972048; 32272339) and the National Key R & D Program of China (2021YFD2100104) for financial support.

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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/).