Enhancement of Vitamin D2 Levels in Pleurotus ostreatus Using Ultraviolet Irradiation and Assessing Its Effect on Dexamethasone-Induced Osteoporosis in Mice
Keywords:
Vitamin D; Pleurotus ostreatus; UV irradiation; osteoporosis
Abstract
Mushrooms are a dietary source of vitamin D2 because they contain ergosterol, which can be converted into vitamin D2 after exposure to ultraviolet (UV) irradiation. UVB irradiated mushrooms contain high active vitamin D. A regular consumption of UVB‐irradiated mushrooms has been shown to be effective to increase bone calcification and modulation of host immunity. This study aimed to enhance vitamin D2 formation in oyster mushrooms (Pleurotus ostreatus) using UVB irradiation and to assess its effect on dexamethasone induced osteoporosis in mice.) Oyster mushrooms were UVB-irradiated with a UVB lamp at the dose of 8.01 J/cm2 - 24.03 J/cm2. The vitamin D2 level was measured using high performance liquid chromatography (HPLC) with calciferol as the standard. The powder of vitamin D enriched oyster mushroom powder was then referred to as Oyster-D. Dexamethasone (0.01 ml/g) induced osteoporosis in BALB/c mice. The number of osteoclasts, osteoblasts, osteocytes of the femur was assessed using hematoxylin-eosin staining. Serum calcium level was measured with spectrophotometry. UVB irradiation with the dose of 48.06 J/cm2 resulted in a highest vitamin D2 concentration, up to 11.333 µg/g. There was a significant increase in the number of osteoclasts, osteoblasts and serum calcium levels and decrease in the number of osteoclasts. The results suggest that UVB irradiation increased vitamin D2 levels in white oyster mushrooms and vitamin D enriched oyster mushrooms have a potential as anti-osteoporosis.
References
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Holick, M. F. (1996). Vitamin D and bone health. Journal of Nutrition, 126(4 SUPPL.). https://doi.org/10.1093/jn/126.suppl_4.1159s
Iwaki, T., Iefuji, H., Hiraga, Y., Hosomi, A., Morita, T., Giga-Hama, Y., & Takegawa, K. (2008). Multiple functions of ergosterol in the fission yeast Schizosaccharomyces pombe. Microbiology, 154(3), 830–841. https://doi.org/10.1099/mic.0.2007/011155-0
Jasinghe, V. J., & Perera, C. O. (2005). Distribution of ergosterol in different tissues of mushrooms and its effect on the conversion of ergosterol to vitamin D2 by UV irradiation. Food Chemistry, 92(3), 541–546. https://doi.org/10.1016/j.foodchem.2004.08.022
Keflie, T. S., Nölle, N., Lambert, C., Nohr, D., & Biesalski, H. K. (2019). Impact of the natural resource of UVB on the content of vitamin D2 in oyster mushroom (Pleurotus ostreatus) under subtropical settings. Saudi Journal of Biological Sciences, 26(7), 1724–1730. https://doi.org/10.1016/j.sjbs.2018.07.014
Kim, M. Y., Lee, K., Shin, H. I., Lee, K. J., & Jeong, D. (2021). Metabolic activities affect femur and lumbar vertebrae remodeling, and anti-resorptive risedronate disturbs femoral cortical bone remodeling. Experimental and Molecular Medicine, 53(1), 103–114. https://doi.org/10.1038/s12276-020-00548-w
Koyyalamudi, S. R., Jeong, S. C., Song, C. H., Cho, K. Y., & Pang, G. (2009). Vitamin D2 formation and bioavailability from agaricus bisporus button mushrooms treated with ultraviolet irradiation. Journal of Agricultural and Food Chemistry, 57(8), 3351–3355. https://doi.org/10.1021/jf803908q
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Phillips, K. M., Ruggio, D. M., Horst, R. L., Minor, B., Simon, R. R., Feeney, M. J., Byrdwell, W. C., & Haytowitz, D. B. (2011). Vitamin D and sterol composition of 10 types of mushrooms from retail suppliers in the United States. Journal of Agricultural and Food Chemistry, 59(14), 7841–7853. https://doi.org/10.1021/jf104246z
Pike, J. W., Meyer, M. B., Lee, S. M., Onal, M., & Benkusky, N. A. (2017). The Vitamin D receptor: Contemporary genomic approaches reveal new basic and translational insights. Journal of Clinical Investigation, 127(4), 1146–1154. https://doi.org/10.1172/JCI88887
Prideaux, M., Findlay, D. M., & Atkins, G. J. (2016). Osteocytes: The master cells in bone remodelling. Current Opinion in Pharmacology, 28, 24–30. https://doi.org/10.1016/j.coph.2016.02.003
Roberts, J. S., Teichert, A., & McHugh, T. H. (2008). Vitamin D2 formation from post-harvest UV-B treatment of mushrooms (Agaricus bisporus) and retention during storage. Journal of Agricultural and Food Chemistry, 56(12), 4541–4544. https://doi.org/10.1021/jf0732511
Sánchez, C. (2017). Reactive oxygen species and antioxidant properties from mushrooms. Synthetic and Systems Biotechnology, 2(1), 13–22. https://doi.org/10.1016/j.synbio.2016.12.001
Sarafin, K., Durazo-Arvizu, R., Tian, L., Phinney, K. W., Tai, S., Camara, J. E., Merkel, J., Green, E., Sempos, C. T., & Brooks, S. P. J. (2015). Standardizing 25-hydroxyVitamin D values from the Canadian Health Measures Survey. American Journal of Clinical Nutrition, 102(5), 1044–1050. https://doi.org/10.3945/ajcn.114.103689
Schleicher, R. L., Sternberg, M. R., Looker, A. C., Yetley, E. A., Lacher, D. A., Sempos, C. T., Taylor, C. L., Durazo-Arvizu, R. A., Maw, K. L., Chaudhary-Webb, M., Johnson, C. L., & Pfeiffer, C. M. (2016). National estimates of serum total 25-hydroxyvitamin D and metabolite concentrations measured by liquid chromatography-tandem mass spectrometry in the US population during 2007-2010. Journal of Nutrition, 146(5), 1051–1061. https://doi.org/10.3945/jn.115.227728
Valverde, M. E., Hernández-Pérez, T., & Paredes-López, O. (2015). Edible mushrooms: Improving human health and promoting quality life. International Journal of Microbiology, 2015 (Table I). https://doi.org/10.1155/2015/376387
Vega, O. A., Lucero, C. M. J., Araya, H. F., Jerez, S., Tapia, J. C., Antonelli, M., Salazar-Onfray, F., Las Heras, F., Thaler, R., Riester, S. M., Stein, G. S., van Wijnen, A. J., & Galindo, M. A. (2017). Wnt/β-Catenin Signaling Activates Expression of the Bone-Related Transcription Factor RUNX2 in Select Human Osteosarcoma Cell Types. Journal of Cellular Biochemistry, 118(11), 3662–3674. https://doi.org/10.1002/jcb.26011
Villares, A., Mateo-Vivaracho, L., García-Lafuente, A., & Guillamón, E. (2014). Storage temperature and UV-irradiation influence on the ergosterol content in edible mushrooms. Food Chemistry, 147, 252–256. https://doi.org/10.1016/j.foodchem.2013.09.144
Wu, W. J., & Ahn, B. Y. (2014). Statistical optimization of ultraviolet irradiate conditions for Vitamin D2 synthesis in oyster mushrooms (Pleurotus ostreatus) using response surface methodology. PLoS ONE, 9(4). https://doi.org/10.1371/journal.pone.0095359
Zhang, Y., Zhou, W. E., Yan, J. Q., Liu, M., Zhou, Y., Shen, X., Ma, Y. L., Feng, X. S., Yang, J., & Li, G. H. (2018). A review of the extraction and determination methods of thirteen essential vitamins to the human body: An update from 2010. Molecules, 23(6), 1–25. https://doi.org/10.3390/molecules23061484
Alshammaa, D. (2017). Phytochemical Investigation and Quantitative Comparison of Ergosterol Between Agaricus bisporus and Pleurotus ostreatus by HPLC and GC-MS methods. International Journal of Pharmaceutical Sciences Review and Research, 2(44), 215–220.
Berardi, S., Corrado, A., Maruotti, N., Cici, D., & Cantatore, F. P. (2021). Osteoblast role in the pathogenesis of rheumatoid arthritis. Molecular Biology Reports, 48(3), 2843–2852. https://doi.org/10.1007/s11033-021-06288-y
Bikle, D. D. (2014). Vitamin D metabolism, mechanism of action, and clinical applications. Chemistry and Biology, 21(3), 319–329. https://doi.org/10.1016/j.chembiol.2013.12.016
Briot, K., & Roux, C. (2015). Glucocorticoid-induced osteoporosis. RMD Open, 1(1). https://doi.org/10.1136/rmdopen-2014-000014
Calvo, M. S., Babu, U. S., Garthoff, L. H., Woods, T. O., Dreher, M., Hill, G., & Nagaraja, S. (2013). Vitamin D2 from light-exposed edible mushrooms is safe, bioavailable and effectively supports bone growth in rats. Osteoporosis International, 24(1), 197–207. https://doi.org/10.1007/s00198-012-1934-9
Canalis, E. (2003). Mechanisms of glucocorticoid-induced osteoporosis. Current Opinion in Rheumatology, 15(4), 454–457. https://doi.org/10.1097/00002281-200307000-00013
Cashman, K. D. (2020). Vitamin D Deficiency: Defining, Prevalence, Causes, and Strategies of Addressing. Calcified Tissue International, 106(1), 14–29. https://doi.org/10.1007/s00223-019-00559-4
Cashman, K. D., Dowling, K. G., Škrabáková, Z., Gonzalez-Gross, M., Valtueña, J., De Henauw, S., Moreno, L., Damsgaard, C. T., Michaelsen, K. F., Mølgaard, C., Jorde, R., Grimnes, G., Moschonis, G., Mavrogianni, C., Manios, Y., Thamm, M., Mensink, G. B. M., Rabenberg, M., Busch, M. A., … Kiely, M. (2016). Vitamin D deficiency in Europe: Pandemic? American Journal of Clinical Nutrition, 103(4), 1033–1044. https://doi.org/10.3945/ajcn.115.120873
Christakos, S., Dhawan, P., Verstuyf, A., Verlinden, L., & Carmeliet, G. (2015). Vitamin D: Metabolism, molecular mechanism of action, and pleiotropic effects. Physiological Reviews, 96(1), 365–408. https://doi.org/10.1152/physrev.00014.2015
Corrado, A., Maruotti, N., & Cantatore, F. P. (2017). Osteoblast role in rheumatic diseases. International Journal of Molecular Sciences, 18(6). https://doi.org/10.3390/ijms18061272
Felsenfeld, A. J., Levine, B. S., & Rodríguez, M. (2014). Serum calcium and bone: effect of PTH, phosphate, vitamin D and uremia. 34(5), 658–669. https://doi.org/10.3265/Nefrologia.pre2014.Jun.12379
Giustina, A., Adler, R. A., Binkley, N., Bouillon, R., Ebeling, P. R., Lazaretti-Castro, M., Marcocci, C., Rizzoli, R., Sempos, C. T., & Bilezikian, J. P. (2018). Controversies in Vitamin D: Summary Statement from an International Conference. Journal of Clinical Endocrinology and Metabolism, 104(2), 234–240. https://doi.org/10.1210/jc.2018-01414
Heo, T.-Y., Kim, Y.-N., Park, I. B., & Lee, D.-U. (2020). Amplification of Vitamin D2 in the White Button Mushroom (Agaricus bisporus) by UV-B Irradiation and Jet-Milling for Its Potential Use as a Functional Ingredient. Foods, 9(11), 1713. https://doi.org/10.3390/foods9111713
Holick, M. F. (1996). Vitamin D and bone health. Journal of Nutrition, 126(4 SUPPL.). https://doi.org/10.1093/jn/126.suppl_4.1159s
Iwaki, T., Iefuji, H., Hiraga, Y., Hosomi, A., Morita, T., Giga-Hama, Y., & Takegawa, K. (2008). Multiple functions of ergosterol in the fission yeast Schizosaccharomyces pombe. Microbiology, 154(3), 830–841. https://doi.org/10.1099/mic.0.2007/011155-0
Jasinghe, V. J., & Perera, C. O. (2005). Distribution of ergosterol in different tissues of mushrooms and its effect on the conversion of ergosterol to vitamin D2 by UV irradiation. Food Chemistry, 92(3), 541–546. https://doi.org/10.1016/j.foodchem.2004.08.022
Keflie, T. S., Nölle, N., Lambert, C., Nohr, D., & Biesalski, H. K. (2019). Impact of the natural resource of UVB on the content of vitamin D2 in oyster mushroom (Pleurotus ostreatus) under subtropical settings. Saudi Journal of Biological Sciences, 26(7), 1724–1730. https://doi.org/10.1016/j.sjbs.2018.07.014
Kim, M. Y., Lee, K., Shin, H. I., Lee, K. J., & Jeong, D. (2021). Metabolic activities affect femur and lumbar vertebrae remodeling, and anti-resorptive risedronate disturbs femoral cortical bone remodeling. Experimental and Molecular Medicine, 53(1), 103–114. https://doi.org/10.1038/s12276-020-00548-w
Koyyalamudi, S. R., Jeong, S. C., Song, C. H., Cho, K. Y., & Pang, G. (2009). Vitamin D2 formation and bioavailability from agaricus bisporus button mushrooms treated with ultraviolet irradiation. Journal of Agricultural and Food Chemistry, 57(8), 3351–3355. https://doi.org/10.1021/jf803908q
Krati Chauhan ; Mahsa Shahrokhi ; Martin R. Huecker. (2016). Vitamin D Vitamin D. Der Diabetologe, StatPearls, 4–7. https://doi.org/10.1007/978-1-60327-303-9
Kular, J., Tickner, J., Chim, S. M., & Xu, J. (2012). An overview of the regulation of bone remodelling at the cellular level. In Clinical Biochemistry (Vol. 45, Issue 12, pp. 863–873). Clin Biochem. https://doi.org/10.1016/j.clinbiochem.2012.03.021
Phillips, K. M., Ruggio, D. M., Horst, R. L., Minor, B., Simon, R. R., Feeney, M. J., Byrdwell, W. C., & Haytowitz, D. B. (2011). Vitamin D and sterol composition of 10 types of mushrooms from retail suppliers in the United States. Journal of Agricultural and Food Chemistry, 59(14), 7841–7853. https://doi.org/10.1021/jf104246z
Pike, J. W., Meyer, M. B., Lee, S. M., Onal, M., & Benkusky, N. A. (2017). The Vitamin D receptor: Contemporary genomic approaches reveal new basic and translational insights. Journal of Clinical Investigation, 127(4), 1146–1154. https://doi.org/10.1172/JCI88887
Prideaux, M., Findlay, D. M., & Atkins, G. J. (2016). Osteocytes: The master cells in bone remodelling. Current Opinion in Pharmacology, 28, 24–30. https://doi.org/10.1016/j.coph.2016.02.003
Roberts, J. S., Teichert, A., & McHugh, T. H. (2008). Vitamin D2 formation from post-harvest UV-B treatment of mushrooms (Agaricus bisporus) and retention during storage. Journal of Agricultural and Food Chemistry, 56(12), 4541–4544. https://doi.org/10.1021/jf0732511
Sánchez, C. (2017). Reactive oxygen species and antioxidant properties from mushrooms. Synthetic and Systems Biotechnology, 2(1), 13–22. https://doi.org/10.1016/j.synbio.2016.12.001
Sarafin, K., Durazo-Arvizu, R., Tian, L., Phinney, K. W., Tai, S., Camara, J. E., Merkel, J., Green, E., Sempos, C. T., & Brooks, S. P. J. (2015). Standardizing 25-hydroxyVitamin D values from the Canadian Health Measures Survey. American Journal of Clinical Nutrition, 102(5), 1044–1050. https://doi.org/10.3945/ajcn.114.103689
Schleicher, R. L., Sternberg, M. R., Looker, A. C., Yetley, E. A., Lacher, D. A., Sempos, C. T., Taylor, C. L., Durazo-Arvizu, R. A., Maw, K. L., Chaudhary-Webb, M., Johnson, C. L., & Pfeiffer, C. M. (2016). National estimates of serum total 25-hydroxyvitamin D and metabolite concentrations measured by liquid chromatography-tandem mass spectrometry in the US population during 2007-2010. Journal of Nutrition, 146(5), 1051–1061. https://doi.org/10.3945/jn.115.227728
Valverde, M. E., Hernández-Pérez, T., & Paredes-López, O. (2015). Edible mushrooms: Improving human health and promoting quality life. International Journal of Microbiology, 2015 (Table I). https://doi.org/10.1155/2015/376387
Vega, O. A., Lucero, C. M. J., Araya, H. F., Jerez, S., Tapia, J. C., Antonelli, M., Salazar-Onfray, F., Las Heras, F., Thaler, R., Riester, S. M., Stein, G. S., van Wijnen, A. J., & Galindo, M. A. (2017). Wnt/β-Catenin Signaling Activates Expression of the Bone-Related Transcription Factor RUNX2 in Select Human Osteosarcoma Cell Types. Journal of Cellular Biochemistry, 118(11), 3662–3674. https://doi.org/10.1002/jcb.26011
Villares, A., Mateo-Vivaracho, L., García-Lafuente, A., & Guillamón, E. (2014). Storage temperature and UV-irradiation influence on the ergosterol content in edible mushrooms. Food Chemistry, 147, 252–256. https://doi.org/10.1016/j.foodchem.2013.09.144
Wu, W. J., & Ahn, B. Y. (2014). Statistical optimization of ultraviolet irradiate conditions for Vitamin D2 synthesis in oyster mushrooms (Pleurotus ostreatus) using response surface methodology. PLoS ONE, 9(4). https://doi.org/10.1371/journal.pone.0095359
Zhang, Y., Zhou, W. E., Yan, J. Q., Liu, M., Zhou, Y., Shen, X., Ma, Y. L., Feng, X. S., Yang, J., & Li, G. H. (2018). A review of the extraction and determination methods of thirteen essential vitamins to the human body: An update from 2010. Molecules, 23(6), 1–25. https://doi.org/10.3390/molecules23061484
Published
2024-06-10
How to Cite
Hussaana, A., Revoni, F., Aulia, I., Dea, A., Pradana, D., Agustina, T., & Taufiq, H. (2024). Enhancement of Vitamin D2 Levels in Pleurotus ostreatus Using Ultraviolet Irradiation and Assessing Its Effect on Dexamethasone-Induced Osteoporosis in Mice. Indonesian Journal of Pharmacy, 35(2), 250-258. https://doi.org/10.22146/ijp.8252
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Research Article
