ORIGINAL PAPER
Effect of feeding high fat diets differing in fatty acid composition on oxidative stress markers and protein expression in mouse kidney
1
West Pomeranian University of Technology, Faculty of Biotechnology and Animal Husbandry, Department of Physiology, Cytobiology and Proteomics, Szczecin 71-270, Poland
2
The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences, Department of Animal Nutrition, 05-110 Jabłonna, Poland
3
Medical University of Warsaw, Centre for Preclinical Research and Technology, Laboratory of Regenerative Medicine, 02-091 Warsaw, Poland
4
Institute of Genetics and Animal Biotechnology of the Polish Academy of Sciences, Department of Genomics and Biodiversity, 05-552 Magdalenka, Poland
Publication date: 2024-02-19
Corresponding author
A. Wypych
West Pomeranian University of Technology, Faculty of Biotechnology and Animal Husbandry, Department of Physiology, Cytobiology and Proteomics, Szczecin 71-270, Poland
West Pomeranian University of Technology, Faculty of Biotechnology and Animal Husbandry, Department of Physiology, Cytobiology and Proteomics, Szczecin 71-270, Poland
J. Anim. Feed Sci. 2024;33(2):170-184
KEYWORDS
TOPICS
ABSTRACT
High-fat diets (HFDs) are associated with the development
of metabolic disorders. However, the type of dietary fat may also be a critical
risk factor. The study aimed to determine the effect of three months of feeding
HFDs with different fatty acid composition on oxidative stress markers and the
proteome of mouse kidneys. The study involved 24 Swiss-Webster mice, which
were divided into four groups (n = 6) fed for three months a standard chow (STD),
an HFD rich in saturated fatty acids (SFA), and HFDs rich in polyunsaturated fatty
acids with linoleic acid to α-linolenic acid ratios of 14:1 (HR) or 5:1 (LR). Feeding
the SFA and HR diets increased triglyceride levels compared to the STD and
LR groups. The HR group also had higher concentrations of thiobarbituric acid
reactive substances compared to the other groups. There was no effect of HFD
on cholesterol concentration and activity of antioxidant enzymes. The SFA diet
increased the expression of acyl-CoA thioesterase 2 and D-lactate dehydrogenase,
while decreasing that of apolipoprotein E. All HFDs led to downregulation of ATP
synthase F1 subunit beta, mitochondrial, while only the LR diet increased the
expression of persulphide dioxygenase ETHE1 and electron transfer flavoprotein
subunit A, suggesting an enhanced oxidation of fatty acids. Ingestion of the SFA
and HR diets caused downregulation of molecular chaperones and upregulation
of the inflammation and apoptosis regulator peptidylprolyl isomerase A. In
conclusion, feeding SFA and HR diets induces oxidative stress and proteome
changes in the mouse kidney. The SFA diet most significantly influenced the
expression pattern of proteins related to energetic metabolism.
FUNDING
This work was financially supported by two sources. The dietary experiment was carried out with the support of the KNOW (Leading National Research Centre) Scientific Consortium “Healthy Animal – Safe Food under the decision of the Ministry of Science and Higher Education No. 05-1/KNOW2/2015, grant No. KNOW2015/CB/PRO1/44. The analyses performed were supported by the Rector of the West Pomeranian University of Technology in Szczecin for PhD students of the Doctoral School, grant number: 35/2022.
CONFLICT OF INTEREST
The Authors declare that there is no conflict of interest.
REFERENCES (68)
1.
Arriga R., Pacifici F., Capuani B. et al., 2019. Peroxiredoxin 6 is a key antioxidant enzyme in modulating the link between glycemic and lipogenic metabolism. Oxid. Med. Cell. Longev. 2019, 9685607, https://doi.org/10.1155/2019/9....
2.
Bayliak M.M., Lylyk M.P., Vytvytska O.M., Lushchak V.I., 2016. Assessment of antioxidant properties of alpha-keto acids in vitro and in vivo. Eur. Food Res. Technol. 242, 179–188, https://doi.org/http://dx.doi.....
3.
Bekeova C., Anderson-Pullinger L., Boye K., Boos F., Sharpadskaya Y., Herrmann J.M., Seifert E.L., 2019. Multiple mitochondrial thioesterases have distinct tissue and substrate specificity and CoA regulation, suggesting unique functional roles. J. Biol. Chem. 294, 19034–19047, https://doi.org/10.1074/jbc.RA....
4.
Bhargava P., Schnellmann R.G., 2017. Mitochondrial energetics in the kidney. Nat. Rev. Nephrol. 13, 629–646, https://doi.org/10.1038/nrneph....
5.
Blue M.L., Williams D.L., Zucker S., Khan S.A., Blum C.B., 1983. Apolipoprotein E synthesis in human kidney, adrenal gland, and liver. Proc. Natl. Acad. Sci. USA 80, 283–287, https://doi.org/10.1073/pnas.8....
6.
Burczynski M.E., Sridhar G.R., Palackal N.T., Penning T.M., 2001. The reactive oxygen species- and michael acceptor-inducible human aldo-keto reductase AKR1C1 reduces the α,β-unsaturated aldehyde 4-hydroxy-2-nonenal to 1,4-dihydroxy-2-nonene. J. Biol. Chem. 276, 2890–2897, https://doi.org/10.1074/jbc.M0....
7.
Cabello R., Fontecha-Barriuso M., Martin-Sanchez D., Lopez-Diaz A.M., Carrasco S., Mahillo I., Gonzalez-Enguita C., Sanchez-Nino M.D., Ortiz A., Sanz A.B., 2021. Urinary cyclophilin a as marker of tubular cell death and kidney injury. Biomedicines 9, 1–19, https://doi.org/10.3390/biomed....
8.
Chi D.H., Kahyo T., Islam A. et al., 2022. NAD+ levels are augmented in aortic tissue of ApoE-/-mice by dietary omega-3 fatty acids. Arterioscler. Thromb. Vasc. Biol. 42, 395–406, https://doi.org/10.1161/ATVBAH....
9.
Chodkowska K.A., Abramowicz-Pindor P.A., Tuśnio A., Gawin K., Taciak M., Barszcz M., 2022. Effect of phytobiotic composition on production parameters, oxidative stress markers and myokine levels in blood and pectoral muscle of broiler chickens. Animals 12, 2625, https://doi.org/10.3390/ani121....
10.
Dominguez J.H., Wu P., Hawes J.W., Deeg M., Walsh J., Packer S.C., Nagase M., Temm C., Goss E., Peterson R., 2006. Renal injury: Similarities and differences in male and female rats with the metabolic syndrome. Kidney Int. 69, 1969–1976, https://doi.org/10.1038/sj.ki.....
11.
Dozio E., Maffioli E., Vianello E., Nonnis S., Scalvini F.G., Spatola L., Roccabianca P., Tedeschi G., Romanelli M.M.C., 2022. A wide-proteome analysis to identify molecular pathways involved in kidney response to high-fat diet in mice. Int. J. Mol. Sci. 23, 3809, https://doi.org/10.3390/ijms23....
12.
Fu J., Gao J., Liang Z., Yang D., 2021. PDI-regulated disulfide bond formation in protein folding and biomolecular assembly. Molecules 26, 171, https://doi.org/10.3390/molecu....
13.
Gabbay K.H., Bohren K.M., Morello R., Bertin,T., Liu J., Vogel P., 2010. Ascorbate synthesis pathway: Dual role of ascorbate in bone homeostasis. J. Biol. Chem. 285, 19510–19520, https://doi.org/10.1074/jbc.M1....
14.
Gallazzini M., Pallet N., 2018. Endoplasmic reticulum stress and kidney dysfunction. Biol. Cell. 110, 205–216, https://doi.org/10.1111/boc.20....
15.
Gewin L.S., 2021. Sugar or fat? Renal tubular metabolism reviewed in health and disease. Nutrients 13, 1580, https://doi.org/10.3390/nu1305....
16.
Henriques B.J., Olsen R.K.J., Gomes C.M., Bross, P., 2021. Electron transfer flavoprotein and its role in mitochondrial energy metabolism in health and disease. Gene 776, 145407, https://doi.org/10.1016/j.gene....
17.
Herosimczyk A., Lepczyński A., Werkowska M. et al., 2022. Dietary inclusion of dried chicory root affects cecal mucosa proteome of nursery pigs. Animals 12, 1710, https://doi.org/10.3390/ani121....
18.
Hunt M.C., Alexson S.E.H., 2002. The role Acyl-CoA thioesterases play in mediating intracellular lipid metabolism. Prog. Lipid Res. 41, 99–130, https://doi.org/10.1016/S0163-....
19.
Jang C., Oh S.F., Wada S., et al., 2016. A branched-chain amino acid metabolite drives vascular fatty acid transport and causes insulin resistance. Nat. Med. 22, 421–426, https://doi.org/10.1038/nm.405....
20.
Jeong J., Kim Y., Kyung Seong J., Lee K.J., 2012. Comprehensive identification of novel post-translational modifications in cellular peroxiredoxin 6. Proteomics 12, 1452–1462, https://doi.org/10.1002/pmic.2....
21.
Jiménez‐Uribe A.P., Hernández‐Cruz E.Y., Ramírez‐Magaña K.J., Pedraza‐Chaverri J., 2021. Involvement of tricarboxylic acid cycle metabolites in kidney diseases. Biomolecules 11, 1259, https://doi.org/10.3390/biom11....
22.
Jo S.H., Son M.K., Koh, H.J. et al., 2001. Control of mitochondrial redox balance and cellular defense against oxidative damage by mitochondrial NADP+-dependent isocitrate dehydrogenase. J. Biol. Chem. 276, 16168–16176, https://doi.org/10.1074/jbc.M0....
23.
Krzystanek M., Pedersen T.X., Bartels E.D., Kjaehr J., Straarup E.M., Nielsen L.B., 2010. Expression of apolipoprotein B in the kidney attenuates renal lipid accumulation. J. Biol. Chem. 285, 10583–10590, https://doi.org/10.1074/jbc.M1....
24.
Lepczyński A., Ożgo M., Michałek K., Dratwa-Chałupnik A., Grabowska M., Herosimczyk A., Liput K.P., Poławska E., Kram A., Pierzchała M., 2021. Effects of three-month feeding high fat diets with different fatty acid composition on myocardial proteome in mice. Nutrients 13, 330, https://doi.org/10.3390/nu1302....
25.
Li Y., Sha Z., Peng H., 2021. Metabolic reprogramming in kidney diseases: Evidence and therapeutic opportunities. Int. J. Nephrol. 2021, 5497346, https://doi.org/10.1155/2021/5....
26.
Linnan B., Yanzhe W., Ling Z., Yuyuan L., Sijia C., Xinmiao X., Fengqin L., Xiaoxia W., 2021. In situ metabolomics of metabolic reprogramming involved in a mouse model of type 2 diabetic kidney disease. Front. Physio. 12, 779683, https://doi.org/10.3389/fphys.....
27.
Liput K.P., Lepczyński A., Ogłuszka M., Nawrocka A., Poławska E., Grzesiak A., Ślaska B., Pareek C.S., Czarnik U., Pierzchała M., 2021. Effects of dietary n-3 and n-6 polyunsaturated fatty acids in inflammation and cancerogenesis. Int. J. Mol. Sci. 22, 6965, https://doi.org/10.3390/ijms22....
28.
Liput K.P., Lepczyński A., Nawrocka A. et al., 2021. Effects of three-month administration of high-saturated fat diet and high-polyunsaturated fat diets with different linoleic acid (LA, C18:2n-6) to α-linolenic acid (ALA, C18:3n-3) ratio on the mouse liver proteome. Nutrients 13, 1678, https://doi.org/10.3390/nu1305....
29.
Mantha O.L., Polakof S., Huneau J.F., Mariotti F., Poupin N., Zalko D., Fouillet H., 2018. Early changes in tissue amino acid metabolism and nutrient routing in rats fed a high-fat diet: Evidence from natural isotope abundances of nitrogen and carbon in tissue proteins. Br. J. Nut. 119, 981–991, https://doi.org/10.1017/S00071....
30.
Marklund S., Marklund G., 1974. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur. J. Biochem. 47, 469–474, https://doi.org/10.1111/j.1432....
31.
Mei W., Peng Z., Lu M. et al., 2015. Peroxiredoxin 1 inhibits the oxidative stress induced apoptosis in renal tubulointerstitial fibrosis. Nephrology 20, 832–842, https://doi.org/10.1111/nep.12....
32.
Neinast M.D., Jang C., Hui S. et al., 2019. Quantitative analysis of the whole-body metabolic fate of branched-chain amino acids. Cell Metab. 29, 417–429, https://doi.org/10.1016/j.cmet....
33.
Neumann C.A., Cao J., Manevich Y., 2009. Peroxiredoxin 1 and its role in cell signaling. Cell Cycle 8, 4072–4078, https://doi.org/10.4161/cc.8.2....
34.
Noh M.R., Kong M.J., Han S.J., Kim J.I., Park K.M., 2020. Isocitrate dehydrogenase 2 deficiency aggravates prolonged high-fat diet intake-induced hypertension. Redox Biol. 34, 101548, https://doi.org/10.1016/j.redo....
35.
Omar R.A., Chyan Y.-J., Andorn A.C., Poeggeler B., Robakis N.K., Pappolla M.A., 1999. Increased expression but reduced activity of antioxidant enzymes in Alzheimer’s disease. J. Alzheimer’s Dis. 1, 139–145, https://doi.org/10.3233/JAD-19....
36.
Ong K.L., Marklund M., Huang L. et al., 2023. Association of omega 3 polyunsaturated fatty acids with incident chronic kidney disease: pooled analysis of 19 cohorts. B. Med. J. 380, e072909, https://doi.org/10.1136/bmj-20....
37.
Ożgo M., Lepczynski A., Herosimczyk A., 2015. Two-dimensional gel-based serum protein profile of growing piglets. Turk. J. Biol. 39, 320–327, https://doi.org/10.3906/biy-14....
38.
Ożgo M., Skrzypczak W.F., Herosimczyk A., Mazur A., 2007. Proteomics in relation to renal physiology and pathophysiology. Med. Wet. 63, 1146–1150.
39.
Pan X., 2022. The roles of fatty acids and apolipoproteins in the kidneys. Metabolites 12, 462, https://doi.org/10.3390/metabo....
40.
Paul B.D., Snyder S.H., Kashfi K., 2021. Effects of hydrogen sulfide on mitochondrial function and cellular bioenergetics. Redox Biol. 38, 101772, https://doi.org/10.1016/j.redo....
41.
Provenzano M., Serra R., Garofalo C. et al., 2022. OMICS in chronic kidney disease: Focus on prognosis and prediction. Int. J. Mol. Sci. 23, 336, https://doi.org/10.3390/ijms23....
42.
Ralto K.M., Rhee E.P., Parikh S.M., 2020. NAD+ homeostasis in renal health and disease. Nat. Rev. Nephrol. 16, 99–111, https://doi.org/10.1038/s41581....
43.
Rombaldova M., Janovska P., Kopecky J., Kuda O., 2017. Omega-3 fatty acids promote fatty acid utilization and production of pro-resolving lipid mediators in alternatively activated adipose tissue macrophages. Biochem. Biophys. Res. Commun. 490, 1080–1085, https://doi.org/10.1016/j.bbrc....
44.
Ruggiero C., Ehrenshaft M., Cleland E., Stadler K., 2011. High-fat diet induces an initial adaptation of mitochondrial bioenergetics in the kidney despite evident oxidative stress and mitochondrial ROS production. Am. J. Physiol. Endocrinol. Metab. 300, E1047–E1058, https://doi.org/10.1152/ajpend....
45.
Sánchez-Navarro A., Martínez-Rojas M.Á., Caldiño-Bohn R.I., Pérez-Villalva R., Zambrano E., Castro-Rodríguez, D.C., Bobadilla N.A., 2021. Early triggers of moderately high-fat diet-induced kidney damage. Physiol. Rep. 9, e14937, https://doi.org/10.14814/phy2.....
46.
Sas K.M., Kayampilly P., Byun J. et al., 2016. Tissue-specific metabolic reprogramming drives nutrient flux in diabetic complications. JCI Insight. 1, e86976, https://doi.org/10.1172/jci.in....
47.
Shi H., Enriquez A., Rapadas M. et al., 2017. NAD deficiency, congenital malformations, and niacin supplementation. N. Engl. J. Med. 377, 544–552, https://doi.org/10.1056/nejmoa....
48.
Singh M., Kapoor A., Bhatnagar A., 2015. Oxidative and reductive metabolism of lipid-peroxidation derived carbonyls. Chem. Biol. Interact. 234, 261–273, https://doi.org/10.1016/j.cbi.....
49.
Soares Moretti A.I., Martins Laurindo F.R., 2017. Protein disulfide isomerases: Redox connections in and out of the endoplasmic reticulum. Arch. Biochem. Biophys. 617, 106–119, https://doi.org/10.1016/j.abb.....
50.
Sochor M., Kunjara S., McLean P., 1988. Regulation of pathways of glucose metabolism in the kidney. The activity of the pentose phosphate pathway, glycolytic route and the regulation of phosphofructokinase in the kidney of lean and genetically obese (ob/ob) mice; comparison with effects of diab. Horm. Metab. Res. 20, 676–681, https://doi.org/10.1055/s-2007....
51.
Soe N.N., Sowden M., Baskaran P., Kim Y., Nigro P., Smolock E.M., Berk B.C., 2014. Acetylation of cyclophilin A is required for its secretion and vascular cell activation. Cardiovasc. Res. 101, 444–453, https://doi.org/10.1093/cvr/cv....
52.
Sun Y., Ge X., Li X. et al., 2020. High-fat diet promotes renal injury by inducing oxidative stress and mitochondrial dysfunction. Cell Death Dis. 11, 914, https://doi.org/10.1038/s41419....
53.
Syren M.L., Turolo S., Marangoni F., Milani G.P., Edefonti A., Montini G., Agostoni C., 2018. The polyunsaturated fatty acid balance in kidney health and disease: A review. Clin. Nutr. 37, 1829–1839, https://doi.org/10.1016/j.clnu....
54.
Szeto H.H., Liu S., Soong Y., Alam N., Prusky G.T., Seshan S.V., 2016. Protection of mitochondria prevents high-fat diet-induced glomerulopathy and proximal tubular injury. Kidney Int. 90, 997–1011, https://doi.org/10.1016/j.kint....
55.
Szklarczyk D., Kirsch R., Koutrouli M. et al., 2023. The STRING database in 2023: protein–protein association networks and functional enrichment analyses for any sequenced genome of interest. Nucleic Acids Res. 51, D638–D646, https://doi.org/10.1093/nar/gk....
56.
Tang C., Cai J., Dong Z., 2016. Mitochondrial dysfunction in obesity-related kidney disease: a novel therapeutic target. Kidney Int. 90, 930-933, https://doi.org/10.1016/j.kint....
57.
Than W.H., Chan G.C.-K., Ng J.K.-C., Szeto C.-C., 2020. The role of obesity on chronic kidney disease development, progression, and cardiovascular complications. Adv. Biomark. Sci. Technol. 2, 24–34, https://doi.org/10.1016/j.abst....
58.
Timerga A., Haile K., 2021. Patterns of calcium- and chloride-ion disorders and predictors among obese outpatient adults in southern ethiopia. Diabetes Metab. Syndr. Obes. 14, 1349–1358, https://doi.org/10.2147/DMSO.S....
59.
Tiranti V., Viscomi C., Hildebrandt T. et al., 2009. Loss of ETHE1, a mitochondrial dioxygenase, causes fatal sulfide toxicity in ethylmalonic encephalopathy. Nat. Med. 15, 200–205, https://doi.org/10.1038/nm.190....
60.
Verrey F., Ristic Z., Romeo E., Ramadan T., Makrides V., Dave M.H., Wagner C.A., Camargo S.M.R., 2005. Novel renal amino acid transporters. Annu. Rev. Physiol. 67, 557–572, https://doi.org/10.1146/annure....
61.
Wetterau J.R., Aggerbeck L.P., Laplaud P.M., McLean L.R., 1991. Structural properties of the microsomal triglyceride-transfer protein complex. Biochem. 30, 4406-4412, https://doi.org/10.1021/bi0023....
62.
Wu F., Mao L., Zhang Y., Chen X., Zhuang P., Wang W., Wang J., Jiao J., 2022. Individual SFA intake and risk of overweight/obesity: Findings from a population-based nationwide cohort study. Br. J. Nutr. 128, 75–83, https://doi.org/doi:10.1017/S0....
63.
Wypych A., Dunisławska A., Grabowska M., Michałek K., Ożgo M., Liput K., Herosimczyk A., Poławska E., Pierzchała M., Lepczyński A., 2023. Effects of three-month feeding high-fat diets with different fatty acid composition on kidney histology and expression of genes related to cellular stress and water-electrolyte homeostasis in mice. J. Anim. Feed Sci. 32, 372-384, https://doi.org/10.22358/jafs/....
64.
Xiao W., Wang R.S., Handy D.E., Loscalzo J., 2018. NAD(H) and NADP(H) redox couples and cellular energy metabolism. Antioxid. Redox Signal. 28, 251–272, https://doi.org/10.1089/ars.20....
65.
Xie H., Huang L., Li Y., Zhang H., Liu H., 2016. Endoplasmic reticulum stress and renal lesion in mice with combination of high-fat diet and streptozotocin-induced diabetes. Acta Cir. Bras. 31, 150–155, https://doi.org/10.1590/S0102-....
66.
Xue C., Sowden M., Berk B.C., 2017. Extracellular cyclophilin A, especially acetylated, causes pulmonary hypertension by stimulating endothelial apoptosis, redox stress, and inflammation. Arterioscler. Thromb. Vasc. Biol. 37, 1138–1146, https://doi.org/10.1161/ATVBAH....
67.
Yang P., Xiao Y., Luo X., Zhao Y., Zhao L., Wang Y., Wu T., Wei L., Chen Y., 2017. Inflammatory stress promotes the development of obesity-related chronic kidney disease via CD36 in mice. J. Lipid Res. 58, 1417–1427, https://doi.org/10.1194/jlr.M0....
68.
Zhu H., Bai M., Xie X., Wang J., Weng C., Dai H., Chen J., Han F., Lin W., 2022. Impaired amino acid metabolism and its correlation with diabetic kidney disease progression in type 2 diabetes mellitus. Nutrients 14, 3345, https://doi.org/10.3390/nu1416....
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