Beneficial effect of sodium butyrate, a histone deacetylase inhibitor, on the honey bee’s (Apis mellifera) immune response and oxidative status

References

• Aebi, H. (1984). Catalase in vitro. Methods in Enzymology, 105, 121–126. https://doi.org/10.1016/s0076-6879(84)05016-3
   PubMed Web of Science ®Google Scholar
• Amdam, G. V., Simões, Z. L. P., Hagen, A., Norberg, K., Schrøder, K., Mikkelsen, Ø., Kirkwood, T. B. L., & Omholt, S. W. (2004). Hormonal control of the yolk precursor vitellogenin regulates immune function and longevity in honeybees. Experimental Gerontology, 39(5), 767–773. https://doi.org/10.1016/j.exger.2004.02.010
   PubMed Web of Science ®Google Scholar
• Beaulieu, M., & Costantini, D. (2014). Biomarkers of oxidative status: Missing tools in conservation physiology. Conservation Physiology, 2(1), cou014–cou014. https://doi.org/10.1093/conphys/cou014
   PubMed Web of Science ®Google Scholar
• Behrends, A., Scheiner, R., Baker, N., & Amdam, G. V. (2007). Cognitive aging is linked to social role in honey bees (Apis mellifera). Experimental Gerontology, 42(12), 1146–1153. https://doi.org/10.1016/j.exger.2007.09.003
   PubMed Web of Science ®Google Scholar
• Benzie, I. F. F., & Strain, J. J. (1996). The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: The FRAP assay. Analytical Biochemistry, 239(1), 70–76. https://doi.org/10.1006/abio.1996.0292
   PubMed Web of Science ®Google Scholar
• Bird, A. (2002). DNA methylation patterns and epigenetic memory. Genes & Development, 16(1), 6–21. https://doi.org/10.1101/gad.947102
   PubMed Web of Science ®Google Scholar
• Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1-2), 248–254. https://doi.org/10.1006/abio.1976.9999
   PubMed Web of Science ®Google Scholar
• Chang, K. T., & Min, K. T. (2002). Regulation of lifespan by histone deacetylase. Ageing Research Reviews, 1(3), 313–326. https://doi.org/10.1016/s1568-1637(02)00003-x
   PubMed Web of Science ®Google Scholar
• Consalvi, S., Saccone, V., Giordani, L., Minetti, G., Mozzetta, C., & Puri, P. L. (2011). Histone deacetylase inhibitors in the treatment of muscular dystrophies: Epigenetic drugs for genetic diseases. Molecular Medicine (Cambridge, Mass.), 17(5-6), 457–465. https://doi.org/10.2119/molmed.2011.00049
   PubMed Web of Science ®Google Scholar
• Corona, M., & Robinson, G. E. (2006). Genes of the antioxidant system of the honey bee: Annotation and phylogeny. Insect Molecular Biology, 15(5), 687–701. https://doi.org/10.1111/j.1365-2583.2006.00695.x
   PubMed Web of Science ®Google Scholar
• Corona, M., Libbrecht, R., & Wheeler, D. E. (2016). Molecular mechanisms of phenotypic plasticity in social insects. Current Opinion in Insect Science, 13, 55–60. https://doi.org/10.1016/j.cois.2015.12.003
   PubMed Web of Science ®Google Scholar
• Đorđievski, S., Celic, T. V., Vukasinovic, E. L., Kojic, D., & Purac, J. (2022). Epigenetic changes in eusocial insects which affect age and longevity. Current Science, 123(2), 154. https://doi.org/10.18520/cs/v123/i2/154-159
   Web of Science ®Google Scholar
• Ellman, G. L. (1959). Tissue sulfhydryl groups. Archives of Biochemistry and Biophysics, 82(1), 70–77. https://doi.org/10.1016/0003-9861(59)90090-6
   PubMed Web of Science ®Google Scholar
• FAO. (2021). Good beekeeping practices for sustainable apiculture. FAO, IZSLT, Apimondia and CAAS. https://doi.org/10.4060/cb5353en
   Google Scholar
• Farjan, M., Dmitryjuk, M., Lipiński, Z., Biernat-Łopieńska, E., & Żółtowska, K. (2012). Supplementation of the honey bee diet with vitamin C: The effect on the antioxidative system of Apis mellifera carnica brood at different stages. Journal of Apicultural Research, 51(3), 263–270. https://doi.org/10.3896/IBRA.1.51.3.07
   Web of Science ®Google Scholar
• Feil, R., & Fraga, M. F. (2012). Epigenetics and the environment: Emerging patterns and implications. Nature Reviews. Genetics, 13(2), 97–109. https://doi.org/10.1038/nrg3142
   PubMed Web of Science ®Google Scholar
• Ganai, S. A. (2019). Histone deacetylase inhibitors—Epidrugs for neurological disorders. Springer. https://doi.org/10.1007/978-981-13-8019-8
   Google Scholar
• González-Santoyo, I., & Córdoba-Aguilar, A. (2012). Phenoloxidase: A key component of the insect immune system. Entomologia Experimentalis et Applicata, 142(1), 1–16. https://doi.org/10.1111/j.1570-7458.2011.01187.x
   Web of Science ®Google Scholar
• Habig, W. H., Pabst, M. J., & Jakoby, W. B. (1974). Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. The Journal of Biological Chemistry, 249(22), 7130–7139. https://doi.org/10.1016/S0021-9258(19)42083-8
   PubMed Web of Science ®Google Scholar
• Haigis, M. C., & Yankner, B. A. (2010). The aging stress response. Molecular Cell, 40(2), 333–344. https://doi.org/10.1016/j.molcel.2010.10.002
   PubMed Web of Science ®Google Scholar
• Hu, Y. T., Tang, C. K., Wu, C. P., Wu, P. C., Yang, E. C., Tai, C. C., & Wu, Y. L. (2018). Histone deacetylase inhibitor treatment restores memory-related gene expression and learning ability in neonicotinoid-treated Apis mellifera. Insect Molecular Biology, 27(4), 512–521. https://doi.org/10.1111/imb.12390
   PubMed Web of Science ®Google Scholar
• Hu, Y. T., Wu, T. C., Yang, E. C., Wu, P. C., Lin, P. T., & Wu, Y. L. (2017). Regulation of genes related to immune signaling and detoxification in Apis mellifera by an inhibitor of histone deacetylation. Scientific Reports, 7(1), 41255. https://doi.org/10.1038/srep41255
   PubMed Web of Science ®Google Scholar
• Jacques, A., Laurent, M., Ribière-Chabert, M., Saussac, M., Bougeard, S., Budge, G. E., Hendrikx, P., & Chauzat, M. P. (2017). A pan-European epidemiological study reveals honey bee colony survival depends on beekeeper education and disease control. PLoS One, 12(3), e0172591. https://doi.org/10.1371/journal.pone.0172591
   PubMed Web of Science ®Google Scholar
• Jones, M. J., Goodman, S. J., & Kobor, M. S. (2015). DNA methylation and healthy human aging. Aging Cell, 14(6), 924–932. https://doi.org/10.1111/acel.12349
   PubMed Web of Science ®Google Scholar
• Kang, H. L., Benzer, S., & Min, K. T. (2002). Life extension in Drosophila by feeding a drug. Proceedings of the National Academy of Sciences, 99(2), 838–843. https://doi.org/10.1073/pnas.022631999
   PubMed Web of Science ®Google Scholar
• Kautenburger, T., Beyer-Sehlmeyer, G., Festag, G., Haag, N., Kühler, S., Küchler, A., Weise, A., Marian, B., Peters, W. H. M., Liehr, T., Claussen, U., & Pool-Zobel, B. L. (2005). The gut fermentation product butyrate, a chemopreventive agent, suppresses glutathione S-transferase theta (hGSTT1) and cell growth more in human colon adenoma (LT97) than tumor (HT29) cells. Journal of Cancer Research and Clinical Oncology, 131(10), 692–700. https://doi.org/10.1007/s00432-005-0013-4
   PubMed Web of Science ®Google Scholar
• Lan, R., Zhao, Z., Li, S., & An, L. (2020). Sodium butyrate as an effective feed additive to improve performance, liver function, and meat quality in broilers under hot climatic conditions. Poultry Science, 99(11), 5491–5500. https://doi.org/10.1016/j.psj.2020.06.042
   PubMed Web of Science ®Google Scholar
• Laughton, A. M., & Siva-Jothy, M. T. (2011). A standardised protocol for measuring phenoloxidase and prophenoloxidase in the honey bee, Apis mellifera. Apidologie, 42(2), 140–149. https://doi.org/10.1051/apido/2010046
   Web of Science ®Google Scholar
• Leonhardt, S. D., Gallai, N., Garibaldi, L. A., Kuhlmann, M., & Klein, A. M. (2013). Economic gain, stability of pollination and bee diversity decrease from southern to northern Europe. Basic and Applied Ecology, 14(6), 461–471. https://doi.org/10.1016/j.baae.2013.06.003
   Web of Science ®Google Scholar
• Li, Y., & Seto, E. (2016). HDACs and HDAC inhibitors in cancer development and therapy. Cold Spring Harbor Perspectives in Medicine, 6(10), a026831. https://doi.org/10.1101/cshperspect.a026831
   PubMed Web of Science ®Google Scholar
• Li, Z., Yi, C. X., Katiraei, S., Kooijman, S., Zhou, E., Chung, C. K., Gao, Y., van den Heuvel, J. K., Meijer, O. C., Berbée, J. F. P., Heijink, M., Giera, M., van Dijk, K. W., Groen, A. K., Rensen, P. C. N., & Wang, Y. (2018). Butyrate reduces appetite and activates brown adipose tissue via the gut-brain neural circuit. Gut, 67(7), 1269–1279. https://doi.org/10.1136/gutjnl-2017-314050
   PubMed Web of Science ®Google Scholar
• Lin, W., & Dent, S. Y. R. (2006). Functions of histone-modifying enzymes in development. Current Opinion in Genetics & Development, 16(2), 137–142. https://doi.org/10.1016/j.gde.2006.02.002
   PubMed Web of Science ®Google Scholar
• McCord, J. M., & Fridovich, I. (1968). The reduction of cytochrome c by milk xanthine oxidase. The Journal of Biological Chemistry, 243(21), 5753–5760. https://doi.org/10.1016/S0021-9258(18)91929-0
   PubMed Web of Science ®Google Scholar
• McKinsey, T. A. (2011). Targeting inflammation in heart failure with histone deacetylase inhibitors. Molecular Medicine (Cambridge, Mass.), 17(5-6), 434–441. https://doi.org/10.2119/molmed.2011.00022
   PubMed Web of Science ®Google Scholar
• Melov, S., Ravenscroft, J., Malik, S., Gill, M. S., Walker, D. W., Clayton, P. E., Wallace, D. C., Malfroy, B., Doctrow, S. R., & Lithgow, G. J. (2000). Extension of life-span with superoxide dismutase/catalase mimetics. Science (New York, N.Y.), 289(5484), 1567–1569. https://doi.org/10.1126/science.289.5484.1567
   PubMed Web of Science ®Google Scholar
• Mikuła-Pietrasik, J., Pakuła, M., Markowska, M., Uruski, P., Szczepaniak-Chicheł, L., Tykarski, A., & Książek, K. (2021). Nontraditional systems in aging research: An update. Cellular and Molecular Life Sciences: CMLS, 78(4), 1275–1304. https://doi.org/10.1007/s00018-020-03658-w
   PubMed Web of Science ®Google Scholar
• Mukherjee, K., Fischer, R., & Vilcinskas, A. (2012). Histone acetylation mediates epigenetic regulation of transcriptional reprogramming in insects during metamorphosis, wounding and infection. Frontiers in Zoology, 9(1), 25. https://doi.org/10.1186/1742-9994-9-25
   PubMedGoogle Scholar
• Münch, D., & Amdam, G. V. (2010). The curious case of aging plasticity in honey bees. FEBS Letters, 584(12), 2496–2503. https://doi.org/10.1016/j.febslet.2010.04.007
   PubMed Web of Science ®Google Scholar
• Münch, D., Ihle, K. E., Salmela, H., & Amdam, G. V. (2015). Vitellogenin in the honey bee brain: Atypical localization of a reproductive protein that promotes longevity. Experimental Gerontology, 71, 103–108. https://doi.org/10.1016/j.exger.2015.08.001
   PubMed Web of Science ®Google Scholar
• Nakhleh, J., El Moussawi, L., & Osta, M. A. (2017). The melanization response in insect immunity. In Advances in insect physiology, 52, 83–109. https://doi.org/10.1016/bs.aiip.2016.11.002
   Google Scholar
• Pallos, J., Bodai, L., Lukacsovich, T., Purcell, J. M., Steffan, J. S., Thompson, L. M., & Marsh, J. L. (2008). Inhibition of specific HDACs and sirtuins suppresses pathogenesis in a Drosophila model of Huntington’s disease. Human Molecular Genetics, 17(23), 3767–3775. https://doi.org/10.1093/hmg/ddn273
   PubMed Web of Science ®Google Scholar
• Pham, L. N., & Schneider, D. S. (2008). Evidence for specificity and memory in the insect innate immune response. In Insect immunology (pp. 97–127). Elsevier. https://doi.org/10.1016/B978-012373976-6.50007-0
   Google Scholar
• Rando, T. A., & Chang, H. Y. (2012). Aging, rejuvenation, and epigenetic reprogramming: Resetting the aging clock. Cell, 148(1-2), 46–57. https://doi.org/10.1016/j.cell.2012.01.003
   PubMed Web of Science ®Google Scholar
• Rosignoli, P., Fabiani, R., De Bartolomeo, A., Spinozzi, F., Agea, E., Pelli, M. A., & Morozzi, G. (2001). Protective activity of butyrate on hydrogen peroxide-induced DNA damage in isolated human colonocytes and HT29 tumour cells. Carcinogenesis, 22(10), 1675–1680. https://doi.org/10.1093/carcin/22.10.1675
   PubMed Web of Science ®Google Scholar
• Seehuus, S.-C., Norberg, K., Gimsa, U., Krekling, T., & Amdam, G. V. (2006). Reproductive protein protects functionally sterile honey bee workers from oxidative stress. Proceedings of the National Academy of Sciences of the United States of America, 103(4), 962–967. https://doi.org/10.1073/pnas.0502681103
   PubMed Web of Science ®Google Scholar
• Shein, N. A., & Shohami, E. (2011). Histone deacetylase inhibitors as therapeutic agents for acute central nervous system injuries. Molecular Medicine (Cambridge, Mass.), 17(5-6), 448–456. https://doi.org/10.2119/molmed.2011.00038
   PubMed Web of Science ®Google Scholar
• Slater, T. F. (1984). Overview of methods used for detecting lipid peroxidation. Methods in Enzymology, 105, 283–293. https://doi.org/10.1016/s0076-6879(84)05036-9
   PubMed Web of Science ®Google Scholar
• Tang, C. K., Lin, Y. H., Jiang, J. A., Lu, Y. H., Tsai, C. H., Lin, Y. C., Chen, Y. R., Wu, C. P., & Wu, Y.-L. (2021). Real-time monitoring of deformed wing virus-infected bee foraging behavior following histone deacetylase inhibitor treatment. iScience, 24(10), 103056. https://doi.org/10.1016/j.isci.2021.103056
   PubMed Web of Science ®Google Scholar
• Timmermann, S., Lehrmann, H., Polesskaya, A., & Harel-Bellan, A. (2001). Histone acetylation and disease. Cellular and Molecular Life Sciences: CMLS, 58(5-6), 728–736. https://doi.org/10.1007/pl00000896
   PubMed Web of Science ®Google Scholar
• Turner, B. M. (1991). Histone acetylation and control of gene expression. Journal of Cell Science, 99 (Pt 1)), 13–20. https://doi.org/10.1242/jcs.99.1.13
   PubMed Web of Science ®Google Scholar
• Vaiserman, A. M., Kolyada, A. K., Koshel, N. M., Simonenko, A. V., & Pasyukova, E. G. (2013). Effect of histone deacetylase inhibitor sodium butyrate on viability and life span in Drosophila melanogaster. Advances in Gerontology, 3(1), 30–34. https://doi.org/10.1134/S2079057013010153
   Google Scholar
• Vaiserman, A. M., Koshel, N. M., Zabuga, O. G., Kolyada, A. K., Roshina, N. V., & Pasyukova, E. G. (2013). Determination of geroprotective potential of sodium butyrate in Drosophila melanogaster: Long-term effects. Advances in Gerontology = Uspekhi Gerontologii/Rossiǐskai a Akademii a Nauk, Gerontologicheskoe Obshchestvo, 26(1), 111–116.
   PubMedGoogle Scholar
• Valko, M., Leibfritz, D., Moncol, J., Cronin, M. T. D., Mazur, M., & Telser, J. (2007). Free radicals and antioxidants in normal physiological functions and human disease. The International Journal of Biochemistry & Cell Biology, 39(1), 44–84. https://doi.org/10.1016/j.biocel.2006.07.001
   PubMed Web of Science ®Google Scholar
• Williams, G. R., Tarpy, D. R., vanEngelsdorp, D., Chauzat, M.-P., Cox-Foster, D. L., Delaplane, K. S., Neumann, P., Pettis, J. S., Rogers, R. E. L., & Shutler, D. (2010). Colony collapse disorder in context. BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology, 32(10), 845–846. https://doi.org/10.1002/bies.201000075
   PubMed Web of Science ®Google Scholar
• Wu, Y., Starzinski-Powitz, A., & Guo, S. W. (2007). Trichostatin A, a histone deacetylase inhibitor, attenuates invasiveness and reactivates E-cadherin expression in immortalized endometriotic cells. Reproductive Sciences (Thousand Oaks, Calif.), 14(4), 374–382. https://doi.org/10.1177/1933719107302913
   PubMed Web of Science ®Google Scholar
• Xiao, C., Zhang, Y., & Zhu, F. (2021). Effect of dietary sodium butyrate on the innate immune response of Procambarus clarkii and disease resistance against white spot syndrome virus. Aquaculture, 541, 736784. https://doi.org/10.1016/j.aquaculture.2021.736784
   Web of Science ®Google Scholar
• Xing, X., Jiang, Z., Tang, X., Wang, P., Li, Y., Sun, Y., Le, G., & Zou, S. (2016). Sodium butyrate protects against oxidative stress in HepG2 cells through modulating Nrf2 pathway and mitochondrial function. Journal of Physiology and Biochemistry, 73(3), 405–414. https://doi.org/10.1007/s13105-017-0568-y
   PubMed Web of Science ®Google Scholar
• Yaku, K., Enami, Y., Kurajyo, C., Matsui-Yuasa, I., Konishi, Y., & Kojima-Yuasa, A. (2012). The enhancement of phase 2 enzyme activities by sodium butyrate in normal intestinal epithelial cells is associated with Nrf2 and p53. Molecular and Cellular Biochemistry, 370(1-2), 7–14. https://doi.org/10.1007/s11010-012-1392-x
   PubMed Web of Science ®Google Scholar
• Zhang, L., Liu, C., Jiang, Q., & Yin, Y. (2021). Butyrate in energy metabolism: There is still more to learn. Trends in Endocrinology and Metabolism: TEM, 32(3), 159–169. https://doi.org/10.1016/j.tem.2020.12.003
   PubMed Web of Science ®Google Scholar
• Zheng, H., Powell, J. E., Steele, M. I., Dietrich, C., & Moran, N. A. (2017). Honeybee gut microbiota promotes host weight gain via bacterial metabolism and hormonal signaling. Proceedings of the National Academy of Sciences, 114(18), 4775–4780. https://doi.org/10.1073/pnas.1701819114
   PubMed Web of Science ®Google Scholar