Keywords: oxidatively modified proteins, plasma, exercise, seasonal alterations, photoperiods, Shetland ponies, mares and stallions
This study focuses on the photoperiod-induced variability in the levels of oxidatively modified proteins in the plasma of Shetland pony mares and stallions before and after exercise. We have analyzed the effect of photoperiods and exercise on the levels of aldehydic (AD) and ketonic (KD) derivatives of oxidatively modified proteins (OMP) in the blood of Shetland pony mares and stallions involved in recreational horseback riding in the central Pomeranian region (Pomeranian Voivodeship, northern part of Poland). Twenty-one healthy adult Shetland ponies (11 mares and 10 stallions) aged 6.5 ± 1.4 years old were used in this study. All horses participated in recreational horseback riding. Training started at 10:00 AM, lasted 1 hour, and consisted of a ride of cross country by walking (5 min), trotting (15 min), walking (10 min), trotting (10 min), walking (5 min), galloping (5 min), and walking (10 min). Blood was drawn from the jugular veins of the animals in the morning, 90 minutes after feeding, while the horses were in the stables (between 8:30 and 10 AM), and immediately after the exercise test (between 11 AM and 12 AM). Blood samples were taken once per season for one year: summer and winter. The level of oxidatively modified proteins (OMP) was evaluated by the content of protein carbonyl derivatives in the reaction with 2,4-dinitro-phenylhydrazine (DNFH). There was a statistically significant reduction in the levels of aldehydic derivatives of OMP in the plasma of ponies during the winter photoperiods only after exercise in both sexes. A decrease in the levels of ketonic derivatives of OMP in the summer photoperiod was observed. These changes were observed independently of the sex and only after exercise. Levels of aldehydic and ketonic derivatives of OMP varied depending on the photoperiod and exercise session in our studies. These changes were dependent on the baseline levels of the enzymatic and non-enzymatic antioxidant defense systems in the ponies, which differed between the mares and the stallions (statistically significant differences in the winter period) both before and after exercise (winter).
- Andriichuk, A., & Tkachenko, H. (2017). Effect of gender and exercise on haematological and biochemical parameters in Holsteiner horses. Journal of animal physiology and animal nutrition, 101(5), e404–e413. https://doi.org/10.1111/jpn.12620.
- Andriichuk, A., Tkachenko, H. (2015). Seasonal variations of hematological indices in equines involved in recreational horse riding. Journal of Ecology and Protection of the Coastline (Baltic Coastal Zone), 19, 11-22.
- Andriichuk, A., Tkachenko, H., Kurhaluk, N. (2014). Gender Differences of Oxidative Stress Biomarkers and Erythrocyte Damage in Well-Trained Horses During Exercise. Journal of Equine Veterinary Science, 34(8), 978-985. https://doi.org/10.1016/j.jevs.2014.05.005.
- Andriichuk, A., Tkachenko, H., Kurhaluk, N., Tkachova, I. (2013). Markery stresu oksydacyjnego i parametry biochemiczne we krwi koni biorących udział we Wszechstronnym Konkursie Konia Wierzchowego w dynamice treningu. Słupskie Prace Biologiczne, 10, 5-25.
- Andriichuk, A., Tkachenko, H., Tkachova, I. (2016). Oxidative Stress Biomarkers and Erythrocytes Hemolysis in Well-Trained Equine Athletes Before and After Exercise. Journal of Equine Veterinary Science, 36, 32-43. https://doi.org/10.1016/j.jevs.2015.09.011.
- Bernabucci, U., Ronchi, B., Lacetera, N., & Nardone, A. (2002). Markers of oxidative status in plasma and erythrocytes of transition dairy cows during hot season. Journal of dairy science, 85(9), 2173–2179. https://doi.org/10.3168/jds.S0022-0302(02)74296-3.
- Bhat, S., Rao, G., Murthy, K. D., & Bhat, P. G. (2008). Seasonal variations in markers of stress and oxidative stress in rats. Indian journal of clinical biochemistry: IJCB, 23(2), 191–194. https://doi.org/10.1007/s12291-008-0042-2.
- Brinkmann, L., Gerken, M., & Riek, A. (2012). Adaptation strategies to seasonal changes in environmental conditions of a domesticated horse breed, the Shetland pony (Equus ferus caballus). The Journal of experimental biology, 215 (Pt 7), 1061–1068. https://doi.org/10.1242/jeb.064832.
- Brinkmann, L., Gerken, M., Hambly, C., Speakman, J. R., & Riek, A. (2016). Thyroid hormones correlate with field metabolic rate in ponies, Equus ferus caballus. The Journal of experimental biology, 219 (Pt 16), 2559–2566. https://doi.org/10.1242/jeb.138784.
- Brinkmann, L., Gerken, M., Hambly, C., Speakman, J. R., & Riek, A. (2014). Saving energy during hard times: energetic adaptations of Shetland pony mares. The Journal of experimental biology, 217 (Pt 24), 4320–4327. https://doi.org/10.1242/jeb.111815.
- Brzezinski, A., Rai, S., Purohit, A., & Pandi-Perumal, S. R. (2021). Melatonin, Clock Genes, and Mammalian Reproduction: What Is the Link?. International journal of molecular sciences, 22(24), 13240. https://doi.org/10.3390/ijms222413240.
- Davies K. J. (2001). Degradation of oxidized proteins by the 20S proteasome. Biochimie, 83(3-4), 301–310. https://doi.org/10.1016/s0300-9084(01)01250-0.
- Fisher-Wellman, K., & Bloomer, R. J. (2009). Acute exercise and oxidative stress: a 30 year history. Dynamic medicine: DM, 8, 1. https://doi.org/10.1186/1476-5918-8-1.
- Guerin, M. V., & Wang, X. J. (1994). Environmental temperature has an influence on timing of the first ovulation of seasonal estrus in the mare. Theriogenology, 42(6), 1053–1060. https://doi.org/10.1016/0093-691x(94)90127-5.
- Guh, Y. J., Tamai, T. K., & Yoshimura, T. (2019). The underlying mechanisms of vertebrate seasonal reproduction. Proceedings of the Japan Academy. Series B, Physical and biological sciences, 95(7), 343–357. https://doi.org/10.2183/pjab.95.025.
- Hawkins, C. L., & Davies, M. J. (2019). Detection, identification, and quantification of oxidative protein modifications. The Journal of biological chemistry, 294(51), 19683–19708. https://doi.org/10.1074/jbc.REV119.006217.
- Ikegami, K., & Yoshimura, T. (2016). Comparative analysis reveals the underlying mechanism of vertebrate seasonal reproduction. General and comparative endocrinology, 227, 64–68. https://doi.org/10.1016/j.ygcen.2015.05.009
- Kurhaluk, N. (2021). Alcohol and melatonin. Chronobiology international, 38(6), 785–800. https://doi.org/10.1080/07420528.2021.1899198.
- Kurhaluk, N., & Tkachenko, H. (2020). Melatonin and alcohol-related disorders. Chronobiology international, 37(6), 781–803. https://doi.org/10.1080/07420528.2020.1761372.
- Lee, B. H., Hille, B., & Koh, D. S. (2021). Serotonin modulates melatonin synthesis as an autocrine neurotransmitter in the pineal gland. Proceedings of the National Academy of Sciences of the United States of America, 118(43), e2113852118. https://doi.org/10.1073/pnas.2113852118.
- Martarelli, D., & Pompei, P. (2009). Oxidative stress and antioxidant changes during a 24-hours mountain bike endurance exercise in master athletes. The Journal of sports medicine and physical fitness, 49(1), 122–127.
- Martarelli, D., Cocchioni, M., Scuri, S., Spataro, A., & Pompei, P. (2011). Cold exposure increases exercise-induced oxidative stress. The Journal of sports medicine and physical fitness, 51(2), 299–304.
- Muñoz Marín, D., Barrientos, G., Alves, J., Grijota, F. J., Robles, M. C., & Maynar, M. (2018). Oxidative stress, lipid peroxidation indexes and antioxidant vitamins in long and middle distance athletes during a sport season. The Journal of sports medicine and physical fitness, 58(12), 1713–1719. https://doi.org/10.23736/S0022-4707.17.07887-2.
- Olcese, J. M. (2020). Melatonin and Female Reproduction: An Expanding Universe. Frontiers in endocrinology, 11, 85. https://doi.org/10.3389/fendo.2020.00085.
- Pang, S. F., Tsang, C. W., Hong, G. X., Yip, P. C., Tang, P. L., & Brown, G. M. (1990). Fluctuation of blood melatonin concentrations with age: result of changes in pineal melatonin secretion, body growth, and aging. Journal of pineal research, 8(2), 179–192. https://doi.org/10.1111/j.1600-079x.1990.tb00678.x.
- Pażontka-Lipiński, P., Witaszek, M., Tkachenko, H. (2017). Seasonal alterations in exercise-induced resistance of erythrocytes in horses involved in recreational horseback riding. Scientific and technical bulletin of Institute of Animal Husbandry, National Academy of Agrarian Sciences of Ukraine, Kharkiv, 118, 22-29.
- Pingitore, A., Lima, G. P., Mastorci, F., Quinones, A., Iervasi, G., & Vassalle, C. (2015). Exercise and oxidative stress: potential effects of antioxidant dietary strategies in sports. Nutrition (Burbank, Los Angeles County, Calif.), 31(7-8), 916–922. https://doi.org/10.1016/j.nut.2015.02.005.
- Pohlin, F., Brabender, K., Fluch, G., Stalder, G., Petit, T., & Walzer, C. (2017). Seasonal Variations in Heart Rate Variability as an Indicator of Stress in Free-Ranging Pregnant Przewalski’s Horses (E. ferus przewalskii) within the Hortobágy National Park in Hungary. Frontiers in physiology, 8, 664. https://doi.org/10.3389/fphys.2017.00664.
- Radak, Z., Chung, H. Y., & Goto, S. (2008). Systemic adaptation to oxidative challenge induced by regular exercise. Free radical biology & medicine, 44(2), 153–159. https://doi.org/10.1016/j.freeradbiomed.2007.01.029.
- Radák, Z., Sasvári, M., Nyakas, C., Taylor, A. W., Ohno, H., Nakamoto, H., & Goto, S. (2000). Regular training modulates the accumulation of reactive carbonyl derivatives in mitochondrial and cytosolic fractions of rat skeletal muscle. Archives of biochemistry and biophysics, 383(1), 114–118. https://doi.org/10.1006/abbi.2000.2042
- Radak, Z., Zhao, Z., Koltai, E., Ohno, H., & Atalay, M. (2013). Oxygen consumption and usage during physical exercise: the balance between oxidative stress and ROS-dependent adaptive signaling. Antioxidants & redox signaling, 18(10), 1208–1246. https://doi.org/10.1089/ars.2011.4498.
- Reznick, A. Z., & Packer, L. (1994). Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods in enzymology, 233, 357–363. https://doi.org/10.1016/s0076-6879(94)33041-7.
- Schmidt, K., Deichsel, K., de Oliveira, R. A., Aurich, J., Ille, N., & Aurich, C. (2017). Effects of environmental temperature and season on hair coat characteristics, physiologic and reproductive parameters in Shetland pony stallions. Theriogenology, 97, 170–178. https://doi.org/10.1016/j.theriogenology.2017.04.035.
- Stanisz, A. (2006, 2007). An affordable course of statistics using STATISTICA PL on examples from medicine. Vol. 1-3. Basic Statistics. StatSoft Polska, Krakow. 532.
- Takahashi, Y., & Takahashi, T. (2017). Seasonal fluctuations in body weight during growth of Thoroughbred racehorses during their athletic career. BMC veterinary research, 13(1), 257. https://doi.org/10.1186/s12917-017-1184-3.
- Tamura, H., Takasaki, A., Taketani, T., Tanabe, M., Lee, L., Tamura, I., Maekawa, R., Aasada, H., Yamagata, Y., & Sugino, N. (2014). Melatonin and female reproduction. The journal of obstetrics and gynaecology research, 40(1), 1–11. https://doi.org/10.1111/jog.12177.
- Tan, D. X., Xu, B., Zhou, X., & Reiter, R. J. (2018). Pineal Calcification, Melatonin Production, Aging, Associated Health Consequences and Rejuvenation of the Pineal Gland. Molecules (Basel, Switzerland), 23(2), 301. https://doi.org/10.3390/molecules23020301.
- Tkachenko, H., Pażontka-Lipiński, P., Witaszek, P. (2016). Seasonal alterations in exercise-induced oxidative stress of horses involved in recreational horseback ride. In: Globalisation and regional environmental protection. Technique, technology, ecology. Eds Tadeusz Noch, Wioleta Mikołajczewska, Alicja Wesołowska. Gdańsk, Gdańsk High School Publ., P. 193–212.
- Vanitallie, T. B. (2006). Sleep and energy balance: Interactive homeostatic systems. Metabolism: clinical and experimental, 55(10 Suppl 2), S30–S35. https://doi.org/10.1016/j.metabol.2006.07.010.
- Wehr, T. A. (1997). Melatonin and seasonal rhythms. Journal of biological rhythms, 12(6), 518–527. https://doi.org/10.1177/074873049701200605.
- Witaszek, M., Pażontka-Lipiński, P., & Tkachenko, H. (2017). Sezonowe zmiany markerów stresu oksydacyjnego w osoczu krwi koni biorących udział w rekreacyjnych jazdach konnych w dynamice treningu. Słupskie Prace Biologiczne, 14, 185–208.