Combined Treatment with Tauroursodeoxycholic Acid and SCD Probiotics Reduces Oxidative Stress in Lung Tissue of Aged Rats

Yıl 2024, , 673 - 680, 26.09.2024

Burcu Baba , Hüseyin Allahverdi

https://doi.org/10.17798/bitlisfen.1472539

Öz

Aging is associated with an increased level of oxidative stress, resulting from an elevated production of reactive oxygen species, which can lead to cellular and tissue damage, particularly in the lungs. This study examined the effects of Tauroursodeoxycholic acid (TUDCA) and SCD Probiotics, both individually and in combination, on oxidative stress markers in the lung tissue of aged Sprague-Dawley rats. The primary objective was to assess the potential of these agents in reducing malondialdehyde (MDA), advanced oxidation protein products (AOPP), and myeloperoxidase (MPO) levels, which are indicative of oxidative damage and inflammation. The results showed that TUDCA significantly decreased MDA and AOPP levels, suggesting its role in maintaining mitochondrial stability and inhibiting apoptotic pathways. SCD Probiotics also demonstrated a reduction in AOPP levels, highlighting their immunomodulatory and antioxidant effects. Furthermore, the combined treatment of TUDCA and SCD Probiotics led to a more pronounced decrease in both MDA and AOPP levels, along with a significant reduction in MPO activity. This suggests a synergistic interaction that enhances the antioxidative and anti-inflammatory properties of the individual treatments. These findings support the therapeutic potential of TUDCA and SCD Probiotics in mitigating oxidative damage in aging lung tissues, proposing that their concurrent use could be an effective strategy against age-related oxidative stress. Further research is warranted to explore these effects across different models and long-term applications.

Anahtar Kelimeler

Oxidative stress, Aging, TUDCA, SCD Probiotics, Lung, Myeloperoxidase

Etik Beyan

The animals were housed according to standard animal care protocols, and the study was approved by the Ethics Committee (approval number: 2022/03) of the Saki Yenilli Experimental Animal Production and Practice Laboratory.

Teşekkür

We extend our sincere gratitude to Taha Ceylani and Hikmet Taner Teker for their invaluable contributions to this work.

Kaynakça

• [1] J. Guo, X. Huang, L. Dou, et al., “Aging and aging-related diseases: from molecular mechanisms to interventions and treatments,” Signal Transduct. Target. Ther., vol. 7, p. 391, 2022.
• [2] J. L. Schneider, J. H. Rowe, C. Garcia-de-Alba, et al., “The aging lung: Physiology, disease, and immunity,” Cell, vol. 184, pp. 1990–2019, 2021.
• [3] H. Cui, Y. Kong, H. Zhang, “Oxidative stress, mitochondrial dysfunction, and aging,” J. Signal Transduct., vol. 2012, p. 646354, 2012.
• [4] D. P. Rosanna, C. Salvatore. “Reactive oxygen species, inflammation, and lung diseases,” Curr Pharm Des., vol. 18, no. 26, pp. 3889-900, 2012.
• [5] S. K. Bardaweel, M. Gul, M. Alzweiri, A. Ishaqat, H. A. ALSalamat, R. M. Bashatwah. “Reactive oxygen species: the dual role in physiological and pathological conditions of the human body,” Eurasian J Med., vol. 50, no. 3, pp. 193-201, 2018.
• [6] I. Liguori, G. Russo, F. Curcio, G. Bulli, L. Aran, D. Della-Morte, G. Gargiulo, G. Testa, F. Cacciatore, D. Bonaduce, P. Abete. “Oxidative stress, aging, and diseases,” Clin Interv Aging., vol. 13, pp. 757-772, 2018.
• [7] T. G. Son, Y. Zou, B. P. Yu, et al., “Aging effect on myeloperoxidase in rat kidney and its modulation by calorie restriction,” Free Radic. Res., vol. 39, pp. 283–289, 2005.
• [8] J. Aguilar Diaz De Leon and C. R. Borges, “Evaluation of Oxidative Stress in Biological Samples Using the Thiobarbituric Acid Reactive Substances Assay,” J. Vis. Exp., vol. 12, no. 159, 2020.
• [9] Y. A. Hajam, R. Rani, S. Y. Ganie, T. A. Sheikh, D. Javaid, S. S. Qadri, S. Pramodh, A. Alsulimani, M. F. Alkhanani, S. Harakeh, A. Hussain, S. Haque, M. S. Reshi. “Oxidative stress in human pathology and aging: molecular mechanisms and perspectives,” Cells., vol. 11, no. 3, p. 552, 2022.
• [10] G. Martínez-Sánchez, A. Giuliani, G. Pérez-Davison, et al., “Oxidized proteins and their contribution to redox homeostasis,” Redox Rep., vol. 10, pp. 175–185, 2005.
• [11] S. J. Cho and H. W. Stout-Delgado, “Aging and Lung Disease,” Annu. Rev. Physiol., vol. 82, pp. 433–459, 2020.
• [12] Y. Hou, J. Luan, T. Huang, et al., “Tauroursodeoxycholic acid alleviates secondary injury in spinal cord injury mice by reducing oxidative stress, apoptosis, and inflammatory response,” J. Neuroinflammation, vol. 18, p. 216, 2021.
• [13] J. Weng, L. Wang, K. Wang, et al., “Tauroursodeoxycholic Acid Inhibited Apoptosis and Oxidative Stress in H(2)O(2)-Induced BMSC Death via Modulating the Nrf-2 Signaling Pathway: the Therapeutic Implications in a Rat Model of Spinal Cord Injury,” Mol. Neurobiol., 2023, DOI: 10.1007/s12035-023-03754-5.
• [14] E. Mortaz, I. M. Adcock, G. Folkerts, et al., “Probiotics in the management of lung diseases,” Mediators Inflamm., 2013, p. 751068.
• [15] L. Keulers, A. Dehghani, L. Knippels, et al., “Probiotics, prebiotics, and synbiotics to prevent or combat air pollution consequences: The gut-lung axis,” Environ. Pollut., vol. 302, p. 119066, 2022.
• [16] T. Ceylani, “Effect of SCD Probiotics supplemented with tauroursodeoksikolik asit (TUDCA) application on the aged rat gut microbiota composition,” J. Appl. Microbiol., 2023, DOI: 10.1093/jambio/lxad092.
• [17] M. M. Bradford, “A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding,” Anal. Biochem., vol. 72, pp. 248–254, 1976.
• [18] P. P. Bradley, D. A. Priebat, R. D. Christensen, et al., “Measurement of cutaneous inflammation: estimation of neutrophil content with an enzyme marker,” J. Invest. Dermatol., vol. 78, pp. 206–209, 1982.
• [19] T. F. Slater and B. C. Sawyer, “The stimulatory effects of carbon tetrachloride and other halogenoalkanes on peroxidative reactions in rat liver fractions in vitro. General features of the systems used,” Biochem. J., vol. 123, pp. 805–814, 1971.
• [20] V. Witko-Sarsat, M. Friedlander, C. Capeillère-Blandin, et al., “Advanced oxidation protein products as a novel marker of oxidative stress in uremia,” Kidney Int., vol. 49, pp. 1304–1313, 1996.
• [21] J. A. Amorim, G. Coppotelli, A. P. Rolo, C. M. Palmeira, J. M. Ross, D. A. Sinclair. “Mitochondrial and metabolic dysfunction in ageing and age-related diseases,” Nat Rev Endocrinol., vol. 18, no. 4, pp. 243-258, 2022.
• [22] Y. H. Lee, M. U. Kuk, M. K. So, E. S. Song, H. Lee, S. K. Ahn, H. W. Kwon, J. T. Park, S. C. Park. “Targeting mitochondrial oxidative stress as a strategy to treat aging and age-related diseases,” Antioxidants (Basel)., vol. 12, no. 4, p. 934, 2023.
• [23] M. Tosato, V. Zamboni, A. Ferrini, M. Cesari. “The aging process and potential interventions to extend life expectancy,” Clin Interv Aging., vol. 2, no. 3, pp. 401-12, 2007.
• [24] Zgutka K, Tkacz M, Tomasiak P, Tarnowski M. “A role for advanced glycation end products in molecular ageing,” Int J Mol Sci., vol. 24, no. 12, p. 9881, 2023.
• [25] J. Neves, P. Sousa-Victor. “Regulation of inflammation as an anti-aging intervention,” FEBS J., vol. 287, no. 1, pp. 43-52, 2020.
• [26] H. T. Teker, T. Ceylani, S. Keskin, et al., “Supplementing probiotics during intermittent fasting proves more effective in restoring ileum and colon tissues in aged rats,” J. Cell. Mol. Med., vol. 28, pp. 1–13, 2024.
• [27] H. T. Teker, T. Ceylani, S. Keskin, et al., “Reduced liver damage and fibrosis with combined SCD Probiotics and intermittent fasting in aged rat,” J. Cell. Mol. Med., pp. 1–11, 2023.
• [28] R. S. Sohal, H. H. Ku, S. Agarwal, M. J. Forster, H. Lal. “Oxidative damage, mitochondrial oxidant generation and antioxidant defenses during aging and in response to food restriction in the mouse,” Mech Ageing Dev., vol. 74, no. 1-2, pp. 121-33, 1994.
• [29] P. Arivazhagan, T. Thilakavathy, C. Panneerselvam. “Antioxidant lipoate and tissue antioxidants in aged rats,” J Nutr Biochem., vol. 11, no. 3, pp. 122-7, 2000.
• [30] G. Li, Y. Chen, H. Hu, L. Liu, X. Hu, J. Wang, W. Shi, D. Yin. “Association between age-related decline of kidney function and plasma malondialdehyde,” Rejuvenation Res., vol. 15, no. 3, pp. 257-64, 2012.
• [31] A. I. Rosa, I. Fonseca, M. J. Nunes, S. Moreira, E. Rodrigues, A. N. Carvalho, C. M. P. Rodrigues, M. J. Gama, M. Castro-Caldas. “Novel insights into the antioxidant role of tauroursodeoxycholic acid in experimental models of Parkinson’s disease,” Biochim Biophys Acta Mol Basis Dis., vol. 1863, no. 9, pp. 2171-2181, 2017.
• [32] R. H. Alhasani, M. Almarhoun, X. Zhou, J. Reilly, S. Patterson, Z. Zeng, X. Shu. “Tauroursodeoxycholic acid protects retinal pigment epithelial cells from oxidative injury and endoplasmic reticulum stress in vitro,” Biomedicines., vol. 8, no. 9, p. 367, 2020.
• [33] V. Mishra, C. Shah, N. Mokashe, R. Chavan, H. Yadav, J. Prajapati. “Probiotics as potential antioxidants: a systematic review.” J Agric Food Chem., vol. 63, no. 14, pp. 3615–3626, 2015.
• [34] Y. Wang, Y. Wu, Y. Wang, H. Xu, X. Mei, D. Yu, Y. Wang, W. Li. “Antioxidant properties of probiotic bacteria,” Nutrients., vol. 9, no. 5, p. 521, 2017.
• [35] J. Zhao, F. Tian, S. Yan, Q. Zhai, H. Zhang, W. Chen. “Lactobacillus plantarum CCFM10 alleviating oxidative stress and restoring the gut microbiota in D-galactose-induced oxidative stress model,” Food Funct., vol. 9, no. 2, pp. 917-924, 2018.
• [36] R. Soares, F. F. Ribeiro, S. Xapelli, T. Genebra, M. F. Ribeiro, A. M. Sebastião, C. M. P. Rodrigues, S. Solá. “Tauroursodeoxycholic acid enhances mitochondrial biogenesis, neural stem cell pool, and early neurogenesis in adult rats,” Mol Neurobiol., vol. 55, no. 5, pp. 3725-3738, 2018.
• [37] M. Lamprecht, S. Bogner, G. Schippinger, et al., “Probiotic supplementation affects markers of intestinal barrier, oxidation, and inflammation in trained men; a randomized, double-blinded, placebo-controlled trial,” J. Int. Soc. Sports Nutr., vol. 9, p. 45, 2012.
• [38] Y. Wu, R. Jha, A. Li, et al., “Probiotics (Lactobacillus plantarum HNU082) Supplementation Relieves Ulcerative Colitis by Affecting Intestinal Barrier Functions, Immunity-Related Gene Expression, Gut Microbiota, and Metabolic Pathways in Mice,” Microbiol. Spectr., vol. 10, p. e0165122, 2022.
• [39] R. Liu, B. Sun. “Lactic acid bacteria and aging: unraveling the interplay for healthy longevity,” Aging Dis., vol. 15, no. 4, pp. 1487–98, 2023.
• [40] W. Li, W. Huang, Y. Ma, I. Muhammad, A. Hanif, Z. Ding, et al. “Antioxidant properties of lactic acid bacteria isolated from traditional fermented yak milk and their probiotic effects on the oxidative senescence of Caenorhabditis elegans,” Food Funct., vol. 13, pp. 3690–3703, 2022.
• [41] H. Nakagawa, T. Miyazaki. “Beneficial effects of antioxidative lactic acid bacteria,” AIMS Microbiol, vol. 3, p. 1, 2017.
• [42] D. Michalickova, J. Kotur-Stevuljevic, M. Miljkovic, N. Dikic, M. Kostic-Vucicevic, M. Andjelkovic, V. Koricanac, B. Djordjevic. “Effects of probiotic supplementation on selected parameters of blood prooxidant-antioxidant balance in elite athletes: a double-blind randomized placebo-controlled study,” J Hum Kinet., vol. 64, pp. 111-122, 2018.
• [43] N. Aba, E. F. Koçpınar, T. Ceylani, “The Hepatic Antioxidant System Damage Induced with the Cafeteria (CAF) Diet Is Largely Counteracted Using SCD Probiotics during Development of Male Wistar Rats,” Nutrients, vol. 15, 2023.
• [44] M. O. Mendes, A. I. Rosa, A. N. Carvalho, et al. “Neurotoxic effects of MPTP on mouse cerebral cortex: Modulation of neuroinflammation as a neuroprotective strategy,” Mol Cell Neurosci., vol. 96, pp. 1-9, 2019.
• [45] R. P. Dickson and G. B. Huffnagle, “The Lung Microbiome: New Principles for Respiratory Bacteriology in Health and Disease,” PloS Pathog., vol. 11, p. e1004923, 2015.
• [46] M. A. K. Azad, M. Sarker, T. Li, J. Yin. “Probiotic Species in the Modulation of Gut Microbiota: An Overview”, Biomed Res Int., 2018, 9478630, 2018.
• [47] L. A. T. Cannarella, N. L. Mari, C. C. Alcântara, et al., “Mixture of probiotics reduces inflammatory biomarkers and improves the oxidative/nitrosative profile in people with rheumatoid arthritis,” Nutrition, vol. 89, 2021.
• [48] B. Weiss, Y. Bujanover, Y. Yahav, et al., “Probiotic supplementation affects pulmonary exacerbations in patients with cystic fibrosis: a pilot study,” Pediatr. Pulmonol., vol. 45, pp. 536–540, 2010.
• [49] A. Kazemi, S. Soltani, S. Ghorabi, A. Keshtkar, E. Daneshzad, F. Nasri, and S. M. Mazloomi, "Effect of probiotic and synbiotic supplementation on inflammatory markers in health and disease status: A systematic review and meta-analysis of clinical trials," Clinical Nutrition (Edinburgh, Scotland), vol. 39, no. 3, pp. 789–819, 2020.
• [50] T. P. Ivanovska, K. Mladenovska, Z. Zhivikj, M. J. Pavlova, I. Gjurovski, T. Ristoski, and L. Petrushevska-Tozi, "Synbiotic loaded chitosan-Ca-alginate microparticles reduces inflammation in the TNBS model of rat colitis," International Journal of Pharmaceutics, vol. 527, no. 1-2, pp. 126–134, 2017.