Home Carotenoids in Sporidiobolus pararoseus ameliorate diabetic nephropathy in mice through attenuating oxidative stress
Article
Licensed
Unlicensed Requires Authentication

Carotenoids in Sporidiobolus pararoseus ameliorate diabetic nephropathy in mice through attenuating oxidative stress

  • Chao Du EMAIL logo , Tianqi Lv , Quanwen Liu , Yuliang Cheng , Chang Liu , Mei Han , Weiguo Zhang and He Qian
Published/Copyright: March 15, 2021

Abstract

Diabetic nephropathy (DN) is the major life-threatening complication of diabetes, and oxidative stress takes part in its initiation and development. This study was performed to evaluate the effects of carotenoids from Sporidiobolus pararoseus (CSP) on the renal function and oxidative stress status of mice with streptozotocin (STZ)-induced DN. The results indicated that CSP significantly attenuated symptoms of STZ-induced DN shown by decreased fasting blood glucose, reduced urine volume, urine albumin, serum creatinine and serum urea nitrogen, and improved kidney histological morphology. Furthermore, biochemical analysis of serum and kidney revealed a marked increase in oxidative stress of DN mice as evidenced by reduced total antioxidant capacity (T-AOC), decreased activity of antioxidant enzyme -superoxide dismutase (SOD) and increased level of malondialdehyde (MDA). However, treatment with CSP improved oxidative stress status in DN mice as compared with the mice in model group. Exploration of the potential mechanism validated that CSP ameliorated the oxidative stress status in DN mice by activating the expressions of Nrf2, NQO-1, HO-1, GST and CAT in kidney. These data revealed that CSP may retard the progression of DN by ameliorating renal function, improving the oxidative stress status and activating the Nrf2/ARE pathway.


Corresponding author: Chao Du, School of Food Engineering, Ludong University, 186 Middle Hongqi Road, Yantai264025, Shandong Province, P. R. China; BioNanotechnology Institute, Ludong University, 186 Middle Hongqi Road, Yantai264025, Shandong Province, P. R. China; and School of Food Science and Technology, Jiangnan University, Wuxi, P. R. China, E-mail:

Funding source: National Key Research and Development Program of China

Award Identifier / Grant number: 2017YFC1601806

Award Identifier / Grant number: 2018YFC1604202

Award Identifier / Grant number: 2017YFC1601704

Funding source: National first-class discipline program of Food Science and Technology

Award Identifier / Grant number: JUFSTR20180303

Funding source: Key Research and Development Program of Yantai, P. R. China

Award Identifier / Grant number: 2017ZH059

Acknowledgements

The research was conducted in the School of Food Science and Technology of Jiangnan University.

  1. Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

  2. Research funding: This work is supported by the National Key Research and Development Program of China (Project Nos. 2017YFC1601806, 2018YFC1604202, 2017YFC1601704), the National first-class discipline program of Food Science and Technology (JUFSTR20180303) and the Key Research and Development Program of Yantai, P. R. China (No. 2017ZH059).

  3. Conflict of interest statement: The authors declare that they have no competing interests.

References

Afshari, A.T., Shirpoor, A., Farshid, A., Saadatian, R., Rasmi, Y., Saboory, E., Ilkhanizadeh, B., and Allameh, A. (2007). The effect of ginger on diabetic nephropathy, plasma antioxidant capacity and lipid peroxidation in rats. Food Chem. 101: 148–153, https://doi.org/10.1016/j.foodchem.2006.01.013.Search in Google Scholar

Ahmed, S., Mundhe, N., Borgohain, M., Chowdhury, L., Kwatra, M., Bolshette, N., Ahmed, A., and Lahkar, M. (2016). Diosmin modulates the NF-κB signal transduction pathways and downregulation of various oxidative stress markers in alloxan-induced diabetic nephropathy. Inflammation 39: 1783–1797, https://doi.org/10.1007/s10753-016-0413-4.Search in Google Scholar

Badal, S.S. and Danesh, F.R. (2014). New insights into molecular mechanisms of diabetic kidney disease. Am. J. Kidney Dis. 63: S63–83, https://doi.org/10.1053/j.ajkd.2013.10.047.Search in Google Scholar

Bayrasheva, V.K., Babenko, A.Y., Dobronravov, V.A., Dmitriev, Y.V., Chefu, S.G., Pchelin, I.Y., Ivanova, A.N., Bairamov, A.A., Alexeyeva, N.P., Shatalov, I.S., et al.. (2016). Uninephrectomized high-fat-fed nicotinamide-streptozotocin-induced diabetic rats: a model for the investigation of diabetic nephropathy in type 2 diabetes. J. Diabetes Res. 2016: 8317850, https://doi.org/10.1155/2016/8317850.Search in Google Scholar

Cheng, Y., Liu, C., Cui, Y., Lv, T., Guo, Y., Liang, J., and Qian, H. (2019). Sporidiobolus pararoseus wall-broken powder ameliorates oxidative stress in diabetic nephropathy in type-2 diabetic mice by activating the Nrf2/ARE pathway. RSC Adv. 9: 8394–8403, https://doi.org/10.1039/c8ra10484k.Search in Google Scholar

Cooper, M.E. (1998). Pathogenesis, prevention, and treatment of diabetic nephropathy. Lancet 352: 213–219, https://doi.org/10.1016/s0140-6736(98)01346-4.Search in Google Scholar

Cui, W., Min, X., Xu, X., Du, B., and Luo, P. (2017). Role of nuclear factor erythroid 2-related factor 2 in diabetic nephropathy. J. Diabetes Res. 2017: 3797802, https://doi.org/10.1155/2017/3797802.Search in Google Scholar

Du, C., Guo, Y., Cheng, Y., Han, M., Zhang, W., and Qian, H. (2017). Torulene and torularhodin, protects human prostate stromal cells from hydrogen peroxide-induced oxidative stress damage through the regulation of Bcl-2/Bax mediated apoptosis. Free Radic. Res. 51: 113–123, https://doi.org/10.1080/10715762.2017.1285024.Search in Google Scholar

Du, C., Ying, D., Guo, Y., Cheng, Y., Han, M., Zhang, W., and Qian, H. (2018). Ameliorating effects of Sporidiobolus pararoseus extract on dyslipidemia in mice with high fat diet induced obesity. Biochem. Cell. Biol. 96: 695–701, https://doi.org/10.1139/bcb-2017-0332.Search in Google Scholar

Figueroa-Pérez, M.G., Pérez-Ramírez, I.F., Enciso-Moreno, J.A., Gallegos-Corona, M.A., Salgado, L.M., and Reynoso-Camacho, R. (2018). Diabetic nephropathy is ameliorated with peppermint (Mentha piperita) infusions prepared from salicylic acid-elicited plants. J. Funct. Foods 43: 55–61, https://doi.org/10.1016/j.jff.2018.01.029.Search in Google Scholar

Gnudi, L. (2012). Cellular and molecular mechanisms of diabetic glomerulopathy. Nephrol. Dial. Transpl. 27: 2642–2649, https://doi.org/10.1093/ndt/gfs121.Search in Google Scholar

Guo, W., Tian, D., Jia, Y., Huang, W., Jiang, M., Wang, J., Sun, W., and Wu, H. (2018). MDM2 controls NRF2 antioxidant activity in prevention of diabetic kidney disease. BBA-Mol. Basis Dis. 1865: 1034–1045, https://doi.org/10.1016/j.bbamcr.2018.04.011.Search in Google Scholar

Guo, Y., Liu, Y., and Wang, Y. (2015). Beneficial effect of lycopene on anti-diabetic nephropathy through diminishing inflammatory response and oxidative stress. Food Funct. 6: 1150–1156, https://doi.org/10.1039/c5fo00004a.Search in Google Scholar

Han, M., Xu, Z., Du, C., Qian, H., and Zhang, W. (2016). Effects of nitrogen on the lipid and carotenoid accumulation of oleaginous yeast Sporidiobolus pararoseus. Bioproc. Biosyst. Eng. 39: 1425–1433, https://doi.org/10.1007/s00449-016-1620-y.Search in Google Scholar

Huang, Y., Shen, Y., Han, X., Li, H., Wang, Q., and Liu, Y. (2014). Research on the effects of exhaustive swimming mice’ cardio-pulmonary function after united supplements of HMB and glutamine. J. Am. Coll. Cardiol. 64: C212.10.1016/j.jacc.2014.06.989Search in Google Scholar

Isermann, B., Vinnikov, I.A., Madhusudhan, T., Herzog, S., Kashif, M., Blautzik, J., Corat, M.A., Zeier, M., Blessing, E., Oh, J., et al.. (2007). Activated protein C protects against diabetic nephropathy by inhibiting endothelial and podocyte apoptosis. Nat. Med. 13: 1349–1358, https://doi.org/10.1038/nm1667.Search in Google Scholar

Ishak, N.A., Ismail, M., Hamid, M., Ahmad, Z., and Ghafar, S.A.A. (2013). Antidiabetic and hypolipidemic activities of Curculigo latifolia fruit: root extract in high fat fed diet and low dose STZ induced diabetic rats. Evid. Based Complement. Alternat. Med. 2013: 601838, https://doi.org/10.1155/2013/601838.Search in Google Scholar

Jia, Z., Pang, X., and Lv, J. (2018). Reduced-fat response of Lactobacillus casei subsp. casei SY13 on a time and dose-dependent model. Front. Microbiol. 9: 3200, https://doi.org/10.3389/fmicb.2018.03200.Search in Google Scholar

Jimenez, R., Toral, M., Gomez-Guzman, M., Romero, M., Sanchez, M., Mahmoud, A.M., and Duarte, J. (2018). The role of Nrf2 signaling in PPARbeta/delta-mediated vascular protection against hyperglycemia-induced oxidative stress. Oxid. Med. Cell. Longev. 2018: 5852706.10.1155/2018/5852706Search in Google Scholar

Kanwar, Y.S., Wada, J., Sun, L., Xie, P., Wallner, E.I., Chen, S., Chugh, S., and Danesh, F.R. (2008). Diabetic nephropathy: mechanisms of renal disease progression. Exp. Biol. Med. 233: 4–11, https://doi.org/10.3181/0705-mr-134.Search in Google Scholar

Khatami, P.G., Soleimani, A., Sharifi, N., Aghadavod, E., and Asemi, Z. (2016). The effects of high-dose vitamin E supplementation on biomarkers of kidney injury, inflammation, and oxidative stress in patients with diabetic nephropathy: a randomized, double-blind, placebo-controlled trial. J. Clin. Lipidol. 10: 922–929, https://doi.org/10.1016/j.jacl.2016.02.021.Search in Google Scholar

Logan, J.L. (1996). Studies on the impact of dietary fat composition on proteinuria in diabetic rats. Diabetes Res. Clin. Pract. 33: 21–29, https://doi.org/10.1016/0168-8227(96)01272-7.Search in Google Scholar

Ma, S.T., Liu, D.L., Deng, J.J., Niu, R., and Liu, R.B. (2013). Effect of arctiin on glomerular filtration barrier damage in STZ-induced diabetic nephropathy rats. Phytother Res. 27: 1474–1480, https://doi.org/10.1002/ptr.4884.Search in Google Scholar

Madhusudhan, T., Wang, H., Dong, W., Ghosh, S., Bock, F., Thangapandi, V.R., Ranjan, S., Wolter, J., Kohli, S., Shahzad, K., et al.. (2015). Defective podocyte insulin signalling through p85-XBP1 promotes ATF6-dependent maladaptive ER-stress response in diabetic nephropathy. Nat. Commun. 6: 1–15, https://doi.org/10.1038/ncomms7496.Search in Google Scholar

Mao, G.X., Zheng, L.D., Cao, Y.B., Chen, Z.M., Lv, Y.D., Wang, Y.Z., Hu, X.L., Wang, G.F., and Yan, J. (2012). Antiaging effect of pine pollen in human diploid fibroblasts and in a mouse model induced by D-galactose. Oxid. Med. Cell. Longev. 2012: 750963, https://doi.org/10.1155/2012/750963.Search in Google Scholar

Maria, S.W. and Bo, A. (2004). The high-fat diet-fed mouse: a model for studying mechanisms and treatment of impaired glucose tolerance and type 2 diabetes. Diabetes 53: S215–S219.10.2337/diabetes.53.suppl_3.S215Search in Google Scholar

Miyata, T., Suzuki, N., and Strihou, C.Y. (2013). Diabetic nephropathy: are there new and potentially promising therapies targeting oxygen biology? Kidney Int. 84: 693–702, https://doi.org/10.1038/ki.2013.74.Search in Google Scholar

Mohan, T., Velusamy, P., Chakrapani, L.N., Srinivasan, A.K., Singh, A., Johnson, T., and Periandavan, K. (2017). Impact of EGCG supplementation on the progression of diabetic nephropathy in rats: an insight into fibrosis and apoptosis. J. Agric. Food Chem. 65: 8028–8036, https://doi.org/10.1021/acs.jafc.7b03301.Search in Google Scholar

Nakai, K., Fujii, H., Kono, K., Goto, S., Kitazawa, R., Kitazawa, S., Hirata, M., Shinohara, M., Fukagawa, M., and Nishi, S. (2014). Vitamin D activates the Nrf2-Keap1 antioxidant pathway and ameliorates nephropathy in diabetic rats. Am. J. Hypertens. 27: 586–595, https://doi.org/10.1093/ajh/hpt160.Search in Google Scholar

Nguyen, T., Nioi, P., and Pickett, C.B. (2009). The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress. J. Biol. Chem. 284: 13291–13295, https://doi.org/10.1074/jbc.r900010200.Search in Google Scholar

Nishikawa, T. and Araki, E. (2007). Impact of mitochondrial ROS production in the pathogenesis of diabetes mellitus and its complications. Antioxidants Redox Signal. 9: 343–353, https://doi.org/10.1089/ars.2006.1458.Search in Google Scholar

Pal, P.B., Sinha, K., and Sil, P.C. (2014). Mangiferin attenuates diabetic nephropathy by inhibiting oxidative stress mediated signaling cascade, TNF-α related and mitochondrial dependent apoptotic pathways in streptozotocin-induced diabetic rats. PLoS One 9: e107220, https://doi.org/10.1371/journal.pone.0107220.Search in Google Scholar

Sharma, S., Kulkarni, S.K., and Chopra, K. (2006). Curcumin, the active principle of turmeric (Curcuma longa), ameliorates diabetic nephropathy in rats. Clin. Exp. Pharmacol. Physiol. 33: 940–945, https://doi.org/10.1111/j.1440-1681.2006.04468.x.Search in Google Scholar

Shi, Q., Wang, H., Du, C., Zhang, W., and Qian, H. (2013). Tentative identification of torulene cis/trans geometrical isomers isolated from Sporidiobolus pararoseus by high-performance liquid chromatography–diode array detection–mass spectrometry and preparation by column chromatography. Anal. Sci. 29: 997–1002, https://doi.org/10.2116/analsci.29.997.Search in Google Scholar

Singh, D.K., Winocour, P., and Farrington, K. (2011). Oxidative stress in early diabetic nephropathy: fueling the fire. Nat. Rev. Endocrinol. 7: 176–184, https://doi.org/10.1038/nrendo.2010.212.Search in Google Scholar

Wu, Y., Tang, L., and Chen, B. (2014). Oxidative stress: implications for the development of diabetic retinopathy and antioxidant therapeutic perspectives. Oxid. Med. Cell. Longev. 2014: 752387, https://doi.org/10.1155/2014/752387.Search in Google Scholar

Yeh, W.J., Yang, H.Y., and Chen, J.R. (2014). Soy beta-conglycinin retards progression of diabetic nephropathy via modulating the insulin sensitivity and angiotensin-converting enzyme activity in rats fed with high salt diet. Food Funct. 5: 2898–2904, https://doi.org/10.1039/c4fo00379a.Search in Google Scholar

Zhang, Y.M., Zhang, X.H., Zhu, P., Tan, R.H., Zhao, J.S., Wang, F., Zhang, J.J., Yan, W., Xi, Y., Wan, J.B., et al.. (2018). Endogenous synthesis of n − 3 polyunsaturated fatty acids in fat-1 transgenic mice ameliorates streptozocin-induced diabetic nephropathy. J. Funct. Foods 45: 427–434, https://doi.org/10.1016/j.jff.2018.04.010.Search in Google Scholar

Zhao, P., Duan, L., Guo, L., Dou, L.L., Dong, X., Zhou, P., Li, P., and Liu, E.H. (2015). Chemical and biological comparison of the fruit extracts of Citrus wilsonii Tanaka and Citrus medica L. Food Chem. 173: 54–60. https://doi.org/10.1016/j.foodchem.2014.10.010.Search in Google Scholar

Zheng, H., Whitman, S.A., Wu, W., Wondrak, G.T., Wong, P.K., Fang, D., and Zhang, D.D. (2011). Therapeutic potential of Nrf2 activators in streptozotocin-induced diabetic nephropathy. Diabetes 60: 3055–3066, https://doi.org/10.2337/db11-0807.Search in Google Scholar


Supplementary Material

The online version of this article offers supplementary material (https://doi.org/10.1515/hsz-2021-0127).


Received: 2021-01-29
Accepted: 2021-03-02
Published Online: 2021-03-15
Published in Print: 2021-06-25

© 2021 Walter de Gruyter GmbH, Berlin/Boston

Downloaded on 23.9.2025 from https://www.degruyterbrill.com/document/doi/10.1515/hsz-2021-0127/html
Scroll to top button