Effects of lipoperoxidation and mitochondrial state on milk yield of dairy cows under technological stress

A.V. Deryugina; M.N. Ivashchenko; V.B. Metelin; D.A. Danilova; A.V. Polozova; M.N. Talamanova

doi:10.18006/2023.11(2).436.443

Authors

A.V. Deryugina Department of Physiology and Anatomy, Lobachevsky State University, Nizhny Novgorod, Russia https://orcid.org/0000-0001-8812-8559
M.N. Ivashchenko Department of Physiology and Anatomy, Lobachevsky State University, Nizhny Novgorod, Russia https://orcid.org/0000-0001-6642-8518
V.B. Metelin Vladimirsky Moscow Regional Clinical Research Institute, Moscow, Russia https://orcid.org/0000-0003-0600-5729
D.A. Danilova Department of Physiology and Anatomy, Lobachevsky State University, Nizhny Novgorod, Russia https://orcid.org/0000-0002-7511-5123
A.V. Polozova Department of Physiology and Anatomy, Lobachevsky State University, Nizhny Novgorod, Russia https://orcid.org/0000-0003-1255-9760
M.N. Talamanova Department of Physiology and Anatomy, Lobachevsky State University, Nizhny Novgorod, Russia https://orcid.org/0000-0003-0512-6940

DOI:

https://doi.org/10.18006/2023.11(2).436.443

Keywords:

Stress, Cows, Hematological parameters, Free-radical oxidation, Mitochondria

Abstract

Evaluation of the physiological state of cattle is crucial in creating healthy, high-performing dairy cattle herds. Technological stress is one of the most critical factors determining the biological potential of higher-yielding cows. This work aimed to assess the effect of technological stress on various oxidative parameters and mitochondrial states in dairy cows' blood, milk yield and milk composition. The study was conducted on the black-and-white breed of healthy herds. Regrouping, changing service personnel, and carrying out veterinary and sanitary manipulations were considered technological stress factors. The concentration of cortisol in the blood serum was studied by the immunological method. The concentrations of malonic dialdehyde (MDA), diene conjugates (D.C.), Schiff bases (S.B.), reduced glutathione and catalase activity were measured spectrophotometrically. The mitochondrial state was estimated by laser interference microscopy. While the milk yield, protein and lipid composition of cow milk were studied using an ultrasound analyzer. The researched indicators were analyzed before and for 30 days after the effect of technological stress. Results of the study suggested that technological stress caused an increase in oxidative processes, along with a reduction of antioxidant activity of blood and milk at the initial stages of registration (1-7 days). The concentration of glutathione remained reduced for 30 days after technological stress. A decrease in mitochondrial refractoriness and disintegration accompanied these processes. The milk yield indicator decreased was not restored to the values of intact animals by 30 days after technological stress. Further, the protein and lipid composition also reduced. Thus, a decrease in the quantity and quality of milk under technological stress may be mediated by the development of oxidative stress, which the refractoriness and disintegration of mitochondria might trigger.

References

Akinmoladun O. F. (2021). Stress amelioration potential of vitamin C in ruminants: a review. Tropical animal health and production, 54(1), 24. doi: 10.1007/s11250-021-03026-1 DOI: https://doi.org/10.1007/s11250-021-03026-1

Asanuma, M., & Miyazaki, I. (2021). Glutathione and Related Molecules in Parkinsonism. International journal of molecular sciences, 22(16), 8689. doi: 10.3390/ijms22168689 DOI: https://doi.org/10.3390/ijms22168689

Asuzu, D. T., Bhatt, S., Nwokoye, D., Hayes, C., et al. (2023). Cortisol and ACTH Measurements at Extubation From Pituitary Surgery Predicts Hypothalamic-Pituitary-Adrenal Axis Function. Journal of the Endocrine Society, 7(4), bvad025. doi.org/10.1210/jendso/bvad025 DOI: https://doi.org/10.1210/jendso/bvad025

Bagath, M., Krishnan, G., Devaraj, C., Rashamol, V. P., Pragna, P., Lees, A. M., & Sejian, V. (2019). The impact of heat stress on the immune system in dairy cattle: A review. Research in veterinary science, 126, 94–102. doi: 10.1016/j.rvsc.2019.08.011 DOI: https://doi.org/10.1016/j.rvsc.2019.08.011

Bayır, H., Anthonymuthu, T. S., Tyurina, Y. Y., Patel, S. J., et al. (2020). Achieving Life through Death: Redox Biology of Lipid Peroxidation in Ferroptosis. Cell chemical biology, 27(4), 387–408. doi: 10.1016/j.chembiol.2020.03.014 DOI: https://doi.org/10.1016/j.chembiol.2020.03.014

Bernardi, P., Rasola, A., Forte, M., & Lippe, G. (2015). The Mitochondrial Permeability Transition Pore: Channel Formation by F-ATP Synthase, Integration in Signal Transduction, and Role in Pathophysiology. Physiological reviews, 95(4), 1111–1155. doi: 10.1152/physrev.00001.2015 DOI: https://doi.org/10.1152/physrev.00001.2015

Breuer, K., Hemsworth, P.H., & Coleman G.J. (2003). The effect of positive and negative handling on the behavioural and physiological responses of nonlactating heifers. Applied Animal Behaviour Science, 84, 3-22. doi:10.1016/S0168-1591(03)00146-1 DOI: https://doi.org/10.1016/S0168-1591(03)00146-1

Chauhan, S. S., Celi, P., Leury, B. J., Clarke, I. J., & Dunshea, F. R. (2014). Dietary antioxidants at supranutritional doses improve oxidative status and reduce the negative effects of heat stress in sheep. Journal of animal science, 92(8), 3364–3374. doi: 10.2527/jas.2014-7714 DOI: https://doi.org/10.2527/jas.2014-7714

Chen, S., Wang, J., Peng, D., Li, G., Chen, J., & Gu, X. (2018). Exposure to heat-stress environment affects the physiology, circulation levels of cytokines, and microbiome in dairy cows. Scientific reports, 8(1), 14606. doi: 10.1038/s41598-018-32886-1 DOI: https://doi.org/10.1038/s41598-018-32886-1

Chikkagoudara, K. P., Singh, P., Bhatt, N., Barman, D., et al. (2022). Effect of heat stress mitigations on physiological, behavioural, and hormonal responses of Buffalo calves. International journal of biometeorology, 66(5), 995–1003. doi: 10.1007/s00484-022-02255-9 DOI: https://doi.org/10.1007/s00484-022-02255-9

Deryugina, A.V., Boyarinov, G.A., Simutis, I.S., Nikolskiy, V.O., Kuznetsov A.V., & Efimova T.S. (2018a). Correction of Metabolic Indicators of Erythrocytes and Myocardium Structure with Ozonized Red Blood-Cell Mass. Cell and Tissue Biology, 12, 207-212. doi: 10.1134/S1990519X18030033 DOI: https://doi.org/10.1134/S1990519X18030033

Deryugina, A.V., Ivashchenko, M.N., Ignatiev, P.S., Ice, M.S., & Samodelkin, A.G. (2019a). Changes in the phase portrait and electrophoretic mobility of erythrocytes in various types of diseases. Modern Technologies in Medicine, 11(2), 63-68. doi: 10.17691/stm2019.11.2.09 DOI: https://doi.org/10.17691/stm2019.11.2.09

Deryugina, A.V., Ivashchenko, M.N., Ignatiev, P.S., Talamanova, M.N., & Samodelkin, A.G. (2018b). The capabilities of interference microscopy in studying the in vitro state of erythrocytes exposed to low-intensity laser radiation for stress correction. Modern Technologies in Medicine, 10(4), 78-83. doi: 10.17691/stm2018.10.4.09 DOI: https://doi.org/10.17691/stm2018.10.4.09

Deryugina, A.V., Ivashchenko, M.N., Ignatyev, P.S., Samodelkin, A.G., Zolotova, M. V., Shabalin, M. A., & Gracheva, E.A. (2019b) Diagnostic capabilities of the electrophoretic mobility of red blood cells and buccal cells in stress. International Journal of Physiology and Pathophysiology, 63, 106 – 111. doi: 10.21103/Article8(4)_OA16 DOI: https://doi.org/10.21103/Article8(4)_OA16

Egorova, M.V. & Afanasiev, S.A. (2011). The isolation of mitochondria from cells and tissues of animals and humans. Current methodological approaches Siberian Medical Journal, 26(1), 22-28.

Ellman, G.L. (1959). Tissue sulfhydryl groups. Archives of biochemistry and biophysics, 82(1), 70–77. doi: 10.1016/0003-9861(59)90090-6 DOI: https://doi.org/10.1016/0003-9861(59)90090-6

Fomichev, Y., Sulima, N., Sidorov, E. & Bardin, O. (2012). Heat stress in lactating dairy cows and methods for its prevention. Dairy and beef cattle breeding, 2, 30-32.

Gaschler, M. M., & Stockwell, B. R. (2017). Lipid peroxidation in cell death. Biochemical and biophysical research communications, 482(3), 419–425. doi: 10.1016/j.bbrc.2016.10.086 DOI: https://doi.org/10.1016/j.bbrc.2016.10.086

Guevara, R., Gianotti, M., Roca, P., & Oliver, J. (2011). Age and sex-related changes in rat brain mitochondrial function. Cellular physiology and biochemistry: international journal of experimental cellular physiology, biochemistry, and pharmacology, 27(3-4), 201–206. doi: 10.1159/000327945 DOI: https://doi.org/10.1159/000327945

Gupta, S., Earley, B., & Crowe, M. A. (2007). Pituitary, adrenal, immune and performance responses of mature Holstein x Friesian bulls housed on slatted floors at various space allowances. Veterinary journal, 173(3), 594–604. doi: 10.1016/j.tvjl.2006.02.011. DOI: https://doi.org/10.1016/j.tvjl.2006.02.011

Hammerschmid, D., Calvaresi, V., Bailey, C., Russell Lewis, B., et al. (2023). Chromatographic Phospholipid Trapping for Automated H/D Exchange Mass Spectrometry of Membrane Protein-Lipid Assemblies. Analytical chemistry, 95(5), 3002–3011. doi: 10.1021/acs.analchem.2c04876 DOI: https://doi.org/10.1021/acs.analchem.2c04876

Hernandez C. E., Thierfelder Т., Svennersten-Sjaunja К., Berg С., Orihuela А., & Lidfors L. (2014). Time lag between peak concentrations of plasma and salivary cortisol following a stressful procedure in dairy cattle. Acta Veterinaria Scandinavica, 56(1), 61. doi: 10.1186/s13028-014-0061-3 DOI: https://doi.org/10.1186/s13028-014-0061-3

Ibrahim, S., Al-Sharif, M., Younis, F., Ateya, A., Abdo, M., & Fericean, L. (2023). Analysis of Potential Genes and Economic Parameters Associated with Growth and Heat Tolerance in Sheep (Ovis aries). Animals, 13(3), 353. doi.org/10.3390/ani13030353 DOI: https://doi.org/10.3390/ani13030353

Ighodaro, O.M., & Akinloye O.A. (2018). First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): Their fundamental role in the entire antioxidant defence grid. Alexandria Journal of Medicine, 54 (4), 287-293. doi:10.1016/j.ajme.2017.09.001 DOI: https://doi.org/10.1016/j.ajme.2017.09.001

Kuhn, V., Diederich, L., Keller, T. C. S., Kramer, C. M., et al. (2017). Red Blood Cell Function and Dysfunction: Redox Regulation, Nitric Oxide Metabolism, Anemia. Antioxidants & redox signaling, 26(13), 718–742. doi: 10.1089/ ars.2016.6954 DOI: https://doi.org/10.1089/ars.2016.6954

Long, J., Gao, F., Tong, L., Cotman, C. W., Ames, B. N., & Liu, J. (2009). Mitochondrial decay in the brains of old rats: ameliorating effect of alpha-lipoic acid and acetyl-L-carnitine. Neurochemical research, 34(4), 755–763. doi: 10.1089/ ars.2016.6954 DOI: https://doi.org/10.1007/s11064-008-9850-2

Lvovskaya, I.E., Volchegorsky, I.A. Shemyakov, S.E., & Lifshits, R.I. (1991). Spectrophotometric determination of final products of lipid peroxidation. Voprosi medical chemistries, 4, 92-93.

Mandal, D.K., Bhakat, C., & Dutta, T.K. (2021). Impact of environmental factors on physiological adaptability, thermo-tolerance indices, and productivity in Jersey crossbred cows. International journal of biometeorology, 65(12),1999-2009. doi: 10.1007/s00484-021-02157-2. DOI: https://doi.org/10.1007/s00484-021-02157-2

Mormède, P., Andanson, S., Aupérin, B., Beerda, B., et al. (2007). Exploration of the hypothalamic-pituitary-adrenal function as a tool to evaluate animal welfare. Physiology & behavior, 92(3), 317–339. https://doi.org/10.1016/j.physbeh.2006.12.003 DOI: https://doi.org/10.1016/j.physbeh.2006.12.003

Raghunandan, T., Sultana, J.R., Chandra, A.S. Prakash, M.G., Venkateswarlu, M., & Ramana, D.B.V. (2022). Effect of dietary Chromium, vitamin E and Selenium supplementation on biochemical and physiological parameters of Holstein Friesian cows under heat stress. The Indian Journal of Animal, 92 (7). doi.org/10.56093/ijans.v92i7.109736 DOI: https://doi.org/10.56093/ijans.v92i7.109736

Schenkel, L. C. & Bakovic, M. (2014). Formation and regulation of mitochondrial membranes. International journal of cell biology, 709828. https://doi.org/10.1155/2014/709828 DOI: https://doi.org/10.1155/2014/709828

Semsirmboon, S., Do Nguyen, D.K., Chaiyabutr, N., Poonyachoti, S., Lutz, T.A., & Thammacharoen S. (2023). High Dietary Cation

and Anion Difference and High-Dose Ascorbic Acid Modify Acid–Base and Antioxidant Balance in Dairy Goats Fed under Tropical Conditions. Animals, 13(6), 970. doi.org/10.3390/ani13060970 DOI: https://doi.org/10.3390/ani13060970

Shimura, T., Shiga, R., Sasatani, M., Kamiya, K., & Ushiyama, A. (2022). Melatonin and MitoEbselen-2 Are Radioprotective Agents to Mitochondria. Genes, 14(1), 45. doi: 10.3390/genes14010045 DOI: https://doi.org/10.3390/genes14010045

Skulachev, V.P., Bogachev, A.V., & Kasparinsky, F.O. (2012). Membrane bioenergetics. Moscow: Moscow University Press.

Slimen, B.I., Najar, T., Ghram, A., & Abdrrabba, M. (2016). Heat stress effects on livestock: molecular, cellular and metabolic aspects, a review. Journal of animal physiology and animal nutrition, 100(3), 401–412. doi: 10.1111/jpn.12379 DOI: https://doi.org/10.1111/jpn.12379

Villalón-García, I., Povea-Cabello, S., Álvarez-Córdoba, M., Talaverón-Rey, M., et al. (2023). Vicious cycle of lipid peroxidation and iron accumulation in neurodegeneration. Neural regeneration research, 18(6), 1196–1202. doi: 10.4103/1673-5374.358614 DOI: https://doi.org/10.4103/1673-5374.358614

Volchegorsky, I.A., Nalimov, A.G., & Yarovinsky, B.G. (1989). Comparison of different approaches to the determination of lipid peroxidation products in heptane-isopropanol blood extracts. Laboratornoe delo, 4, 127-31.

Yaguzhinsky, L.S., Vyshenskaya, T.V., Kretushev, A.V., & Tychinsky, V.P. (2008). Identification of two discrete states of energized mitochondria: experiments on single mitochondria. Biochemistry, 2(2), 144-149. doi:10.1134/S1990747808020086 DOI: https://doi.org/10.1134/S1990747808020086