Prolonged consumption of dietary advanced lipoxidation end products contributes to renal impairment in mice through dysregulated intestinal homeostasis
Graphical Abstract
Abstract
Heat processing of food has been well validated as the trigger to generate heat-processing side product of advanced lipoxidation end products (ALEs), which potentially engenders the threat on systemic health or progression of diseases, especially the accumulated effect after long-term intake. Thus, the study was proposed to evaluate the effect of dietary ALEs on health after long-term ingestion, specifically through simulating the intake of dietary ALE in mice within 9 months to investigate the intervention effect and underlying mechanism. The unexpected observation of renal insufficiency or impairment after long-term intake of dietary ALEs indicated the negative impact on renal health, which has been verified by the pathological analysis. Further studies revealed that a high-ALEs diet disrupted the intestinal barrier, with enhanced impact after disturbing the gut microbiota to potentially lower the abundance of beneficial microbiome through producing nephrotoxic metabolites. Correlation analysis showed that the proliferation of harmful bacteria and the reduction of beneficial bacteria were strongly correlated with intestinal barrier damage and the development of renal insufficiency. Furthermore, the underlying mechanism was unveiled as that ALEs could inhibit AMPK/SIRT1 signaling to fundamentally induce renal inflammation and oxidative stress. Thus, it was revealed that long-term intake of dietary ALE could result in renal impairment, and the results emphasized the control or intervention on dietary ALE to decrease to accumulated impairment on systemic health.
Keywords
Electronic Supplementary Material
References
M.R. Alexander, K. Richard, Dietary patterns and the risk of obesity, type 2 diabetes mellitus, cardiovascular diseases, asthma, and neurodegenerative diseases, Crit. Rev. Food Sci. 25 (2018) 262-296. https://doi.org/10.1080/10408398.2016.1158690.
M.D. Eggen, P. Merboth, H. Neukirchner, et al., Lipid peroxidation has major impact on malondialdehyde-derived but only minor influence on glyoxal and methylglyoxal-derived protein modifications in carbohydrate-rich foods, J. Agric. Food Chem. 70 (2022) 10271-10283. https://doi.org/10.1021/acs.jafc.2c04052.
J. Giron-Calle, M. Alaiz, F. Millan, et al., Bound malondialdehyde in foods: bioavailability of the N-2-propenals of lysine, J. Agric. Food Chem. 50 (2002) 6194-6198. https://doi.org/10.1021/jf025681r.
X.Y. Niu, X.Y. Wang, Y.T. Han, et al., Influence of malondialdehyde-induced modifications on physicochemical and digestibility characteristics of whey protein isolate, J. Food Biochem. 43 (2019) e13041. https://doi.org/10.1111/jfbc.13041.
F. Ashkar, J.P. Wu, Effects of food factors and processing on protein digestibility and gut microbiota, J. Agric. Food Chem. 71 (2023) 8685-8698. https://doi.org/10.1021/acs.jafc.3c00442.
Y.Y. Wang, T.C. Zhang, L.Q. Nie, et al., Digestibility of malondialdehyde-induced dietary advanced lipoxidation end products and their effects on hepatic lipid accumulation in mice, J. Agric. Food Chem. 71 (2023) 10403-10416. https://doi.org/10.1021/acs.jafc.3c01956.
T. Miyata, S. Sugiyama, A. Saito, et al., Reactive carbonyl compounds related uremic toxicity, Kidney Int. 59 (2001) S25-S31. https://doi.org/10.1093/ndt/16.suppl_4.8.
C. Iacobini, S. Menini, C. Ricci, et al., Advanced lipoxidation end-products mediate lipid-induced glomerular injury: role of receptor-mediated mechanisms, J. Pathol. 218 (2009) 360-369. https://doi.org/10.1002/path.2536.
A.S. Januszewski, N.L. Alderson, T.O. Metz, et al., Role of lipids in chemical modification of proteins and development of complications in diabetes, Biochem. Soc. T. 31 (2003) 1413-1416. https://doi.org/10.3724/SP.J.1206.2011.00230.
D.S.C. Raj, D. Choudhury, T.C. Welbourne, et al., advanced glycation end products: a nephrologist’s perspective, Am. J. Kidney Dis. 35 (2000) 365-380. https://doi.org/10.1016/S0272-6386(00)70189-2.
B.O. Nilsson, Biological effects of aminoguanidine: an update, Inflamm. Res. 48 (1999) 509-515. https://doi.org/10.1007/s000110050495.
Y. Wang, T. Zhang, L. Nie, et al., Digestibility of malondialdehyde-induced dietary advanced lipoxidation end products and their effects on hepatic lipid accumulation in mice, J. Agric. Food Chem. 71 (2023) 10403-10416. https://doi.org/10.1021/acs.jafc.3c01956.
J. Scheijen, E. Clevers, L. Engelen, et al., Analysis of advanced glycation endproducts in selected food items by ultra-performance liquid chromatography tandem mass spectrometry: presentation of a dietary AGE database, Food. Chem. 190 (2016) 1145-1150. https://doi.org/10.1016/j.foodchem.2015.06.049.
W.T. Qu, C.X. Nie, J.S. Zhao, et al., Microbionne-metabolomics analysis of the impacts of long-term dietary advanced-glycation-end-product consumption on C57BL/6 mouse fecal microbiota and metabolites, J. Agric. Food Chem. 66 (2018) 8864-8875. https://doi.org/10.1021/acs.jafc.8b01466.
C.J. Cao, H. Zhu, Y. Yao, et al., Gut dysbiosis and kidney diseases, Front. Med. 9 (2022) 829349. https://doi.org/10.3389/fmed.2022.829349.
N.L.R. Mikusic, N.M. Kouyoumdzian, M.R. Choi, Gut microbiota and chronic kidney disease: evidences and mechanisms that mediate a new communication in the gastrointestinal-renal axis, Pflug. Arch. Eur. J. Phy. 472 (2020) 303-320. https://doi.org/10.1007/s00424-020-02352-x.
S. Bengmark, L. Kompan, The role of food in glycation and lipoxidation of end products and - amplifiers of inflammation, Zdr. Vestn. 77 (2008) 307-312. https://doi.org/10.1177/0148607107031005430.
N.B. Ruderman, X.J. Xu, L. Nelson, et al., AMPK and SIRT1: a long-standing partnership? AM. J. Physiol-Endoc. M. 298 (2010) E751-E760. https://doi.org/10.1152/ajpendo.00745.2009.
X.Y. Xia, X.D. Wang, H. Wang, et al., Ameliorative effect of white tea from 50-year-old tree of Camellia sinensis L. (Theaceae) on kidney damage in diabetic mice via SIRT1/AMPK pathway, J. Ethnopharmacol. 272 (2021) 113919. https://doi.org/10.1016/j.jep.2021.113919.
B. Meijers, R. Farre, S. Dejongh, et al., Intestinal barrier function in chronic kidney disease, Toxins 10 (2018) 298. https://doi.org/10.3390/toxins10070298.
C. Pellegrini, L. Antonioli, R. Colucci, et al., Interplay among gut microbiota, intestinal mucosal barrier and enteric neuro-immune system: a common path to neurodegenerative diseases? Acta Neuropathol. 136 (2018) 345-361. https://doi.org/10.1007/s00401-018-1856-5.
S. Lobionda, P. Sittipo, H.Y. Kwon, et al., The role of gut microbiota in intestinal inflammation with respect to diet and extrinsic stressors, Microorganisms 7 (2019) 271. https://doi.org/10.3390/microorganisms7080271.
P.S. Tucker, A.T. Scanlan, V.J. Dalbo, Chronic kidney disease influences multiple systems: describing the relationship between oxidative stress, inflammation, kidney damage, and concomitant disease, Oxid. Med. Cell. Longev. 2015 (2015) 806358. https://doi.org/10.1155/2015/806358.
J. Ishigami, J. Taliercio, H.I. Feldman, et al., Inflammatory markers and incidence of hospitalization with infection in chronic kidney disease the chronic renal insufficiency cohort study, Am. J. Epidemiol. 189 (2020) 433-444. https://doi.org/10.1093/aje/kwz246.
B.H. Song, W.H. Zhou, Amarogentin has protective effects against sepsis-induced brain injury via modulating the AMPK/SIRT1/NF-κB pathway, Brain. Res. Bull. 189 (2022) 44-56. https://doi.org/10.1016/j.brainresbull.2022.08.018.
A.A. Shati, Salidroside ameliorates diabetic nephropathy in rats by activating renal AMPK/SIRT1 signaling pathway, J. Food Biochem. 44 (2020) e13158. https://doi.org/10.1111/jfbc.13158.
A. Sabatino, G. Regolisti, C. Cosola, et al., Intestinal microbiota in type 2 diabetes and chronic kidney disease, Curr. Diabetes. Rep. 17 (2017) 16. https://doi.org/10.1007/s11892-017-0841-z.
F. Mahmoodpoor, Y.R. Saadat, A. Barzegari, et al., The impact of gut microbiota on kidney function and pathogenesis, Biomed. Pharmacother. 93 (2017) 412-419. https://doi.org/10.1016/j.biopha.2017.06.066.
N. Thevaranjan, A. Puchta, C. Schulz, et al., Age-associated microbial dysbiosis promotes intestinal permeability, systemic inflammation, and macrophage dysfunction, Cell Host Microbe. 21 (2017) 455. https://doi.org/10.1016/j.chom.2017.03.002.
Y. Li, J. Huang, S.L. Zhang, et al., Sodium alginate and galactooligosaccharides ameliorate metabolic disorders and alter the composition of the gut microbiota in mice with high-fat diet-induced obesity, Int. J. Biol. Macromol. 215 (2022) 113-122. https://doi.org/10.1016/j.ijbiomac.2022.06.073.
D.L. Liu, S.B. Zhang, S.J. Li, et al., Indoleacrylic acid produced by Parabacteroides distasonis alleviates type 2 diabetes via activation of AhR to repair intestinal barrier, Bmc. Biol. 21 (2023) 90. https://doi.org/10.1186/s12915-023-01578-2.
T.J. Khan, Y.M. Ahmed, M.A. Zamzami, et al., Effect of atorvastatin on the gut microbiota of high fat diet-induced hypercholesterolemic rats, Sci. Rep. 8 (2018) 662. https://doi.org/10.1038/s41598-017-19013-2.
X.M. Liu, B.Y. Mao, J.Y. Gu, et al., Blautia-a new functional genus with potential probiotic properties? Gut Microbes. 13 (2021). https://doi.org/10.1080/19490976.2021.1875796.
A. Benitez-Paez, E.M.G. del Pugar, I. Lopez-Almela, et al., Depletion of Blautia Species in the microbiota of obese children relates to intestinal inflammation and metabolic phenotype worsening, Msystems 5 (2020) e00857-19. https://doi.org/10.1128/mSystems.00857-19.
M. El-Salhy, Intestinal bacteria associated with irritable bowel syndrome and chronic fatigue, Neurogastroent Motil. 35 (2023) e14621 https://doi.org/10.1111/nmo.14621.
K. Andersen, M.S. Kesper, J.A. Marschner, et al., Intestinal dysbiosis, barrier dysfunction, and bacterial translocation account for ckd-related systemic inflammation, J. Am. Soc. Nephrol. 28 (2017) 76-83. https://doi.org/10.1681/ASN.2015111285.
W. Wei, W.B. Jiang, Z. Tian, et al., Fecal g. Streptococcus and g. Eubacterium_coprostanoligenes_group combined with sphingosine to modulate the serum dyslipidemia in high-fat diet mice, Clin. Nutr. 40 (2021) 4234-4245. https://doi.org/10.1016/j.clnu.2021.01.031.
R.Q. Chen, J. Wang, R.H. Zhan, et al., Fecal metabonomics combined with 16S rRNA gene sequencing to analyze the changes of gut microbiota in rats with kidney-yang deficiency syndrome and the intervention effect of You-gui pill, J. Ethnopharmacol. 244 (2019) 112139. https://doi.org/10.1016/j.jep.2019.112139.
K. Taki, S. Nakamura, M. Miglinas, et al., Accumulation of indoxyl sulfate in OAT1/3-positive tubular cells in kidneys of patients with chronic renal failure, J. Renal. Nutr. 16 (2006) 199-203. https://doi.org/10.1053/j.jrn.2006.04.020.
S.J. Rosochacki, E. Juszczuk-Kubiak, J. Poloszynowicz, et al., Proteolysis in muscle and liver - similarities and differences - a review, Prace. I Materialy Zootechniczne 62 (2004) 9-22. https://doi.org/10.1073/pnas.88.2.340.
I. Dugail, Lysosome/lipid droplet interplay in metabolic diseases, Biochimie 96 (2014) 102-105. https://doi.org/10.1016/j.biochi.2013.07.008.
S. Watanabe, F. Fukumori, M. Miyazaki, et al., Characterization of a novel L-fuconate dehydratase involved in the non-phosphorylated pathway of L-fucose metabolism from bacteria, J. Bacteriol. 199 (2017) 177-180. https://doi.org/10.1093/bbb/zbad161.
B. Pugin, W. Barcik, P. Westermann, et al., A wide diversity of bacteria from the human gut produces and degrades biogenic amines, Microbial Ecology in Health and Disease 28 (2017) 1353881. https://doi.org/10.1080/16512235.2017.1353881.
L. Pretorius, C. Smith, Tyramine-induced gastrointestinal dysregulation is attenuated via estradiol associated mechanisms in a zebrafish larval model, Toxicol. Appl. Pharm. 461 (2023) 116399. https://doi.org/10.1016/j.taap.2023.116399.
G. Vistoli, D. De Maddis, A. Cipak, et al., Advanced glycoxidation and lipoxidation end products (AGEs and ALEs): an overview of their mechanisms of formation, Free Radical Res. 47 (2013) 3-27. https://doi.org/10.3109/10715762.2013.815348.
京公网安备11010802044758号