10-Hydroxydec-2-enoic acid enhances the erythrocyte membrane fluidity via interacting with phosphatidylcholine and phosphatidylethanolamine
Main Article Content
Keywords
10-hydroxydec-2-enoic acid, erythrocyte, membrane, fluidity
Abstract
10-Hydroxydec-2-enoic acid (10-HDA), the unique substance in the natural food royal jelly, is an unsaturated hydroxyl fatty acid with the bio-activity to guard against cell or tissue damages. However, the relevant mechanisms still remain largely unknown. Here, using a mouse erythrocyte model, whether the fluidity of plasma membrane is influenced by 10-HDA was investigated. 10-HDA was shown to enhance the erythrocyte membrane fluidity and to rescue the fluidity from •OH toxicity. In such occasions, 10-HDA promoted the dissolved O2 level in erythrocyte suspension thereof. The levels of β-actin and band 4.1 protein were not affected by 10-HDA in erythrocytes. In the framework of density functional theory, 10-HDA may interact with phosphatidylcholine and phosphatidylethanolamine, the major components of membrane lipid bilayer. This was evidenced by the fact that 10-HDA was detectable in erythrocytes after its addition to the erythrocyte suspension. Moreover, the fluorescent intensity of erythrocytes stained by the membrane probe DiIC18(5) increased with 10-HDA treatment. Hence, 10-HDA could regulate the erythrocyte membrane fluidity and the release of O2 from erythrocytes via targeting lipids rather than proteins. Our data cast light on the elucidation of the mechanism of 10-HDA modulating cell functionality and the utilization of 10-HDA in remedying the erythrocyte membrane fluidity-associated symptoms.
References
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Chen YF., Wang K., Zhang YZ., Zheng YF., and Hu FL. 2016. In vitro anti-inflammatory effects of three fatty acids from royal jelly. Mediators of Inflammation. 2016: 3583684. 10.1155/2016/3583684
Cooper RA., Durocher JR., and Leslie MH. 1977. Decreased fluidity of red cell membrane lipids in abetalipoproteinemia. Journal of Clinical Investigation. 60: 115–121. 10.1172/JCI108747
Dakroub H., Nowak M., Benoist JF., Noël B., Vedie B., Paul JL., et al. 2021. Eicosapentaenoic acid membrane incorporation stimulates ABCA1-mediated cholesterol efflux from human THP-1 macrophages. Biochimica et Biophysica Acta-Molecular and Cell Biology of Lipids, 1866: 159016. 10.1016/j.bbalip.2021.159016
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Fan P., Sha F., Ma C., Wei Q., Zhou Y., Shi J., et al. 2022. 10-Hydroxydec-2-enoic acid reduces hydroxyl free radical-induced damage to vascular smooth muscle cells by rescuing protein and energy metabolism. Frontiers in Nutrition. 9: 873892. 10.3389/fnut.2022.873892
Ferretti G., Simonetti O., Offidani AM., Messini L., Cinti B., Marshiseppe I. et al. 1993. Changes of plasma lipids and erythrocyte membrane fluidity in psoriatic children. Pediatric Research. 33: 506–509. 10.1203/00006450-199305000-00017
Filipič B., Gradišnik L., Rihar K., Šooš E., Pereyra A., and Potokar J. 2015. The influence of royal jelly and human interferon-alpha (HuIFN-αN3) on proliferation, glutathione level and lipid peroxidation in human colorectal adenocarcinoma cells in vitro. Arhiv za Higijenu Rada i Toksikologiju. 66: 269–274. 10.1515/aiht-2015-66-2632
Fonseca F., Pénicaud C., Tymczyszyn EE., Gómez-Zavaglia A., and Passot S. 2019. Factors influencing the membrane fluidity and the impact on production of lactic acid bacteria starters. Applied Microbiology and Biotechnology. 103: 6867–6883. 10.1007/s00253-019-10002-1
Fournier N., Sayet G., Vedie B., Nowak M., Allaoui F., Solgadi A., et al. 2017. Eicosapentaenoic acid membrane incorporation impairs cholesterol efflux from cholesterol-loaded human macrophages by reducing the cholesteryl ester mobilization from lipid droplets. Biochimica et Biophysica Acta-Molecular and Cell Biology of Lipids. 1862: 1079–1091. 10.1016/j.bbalip.2017.07.011
Fratini F., Cilia C., Mancini S., and Felicioli A. 2016. Royal jelly: an ancient remedy with remarkable antibacteria properties. Microbiological Research. 192: 130–141. 10.1016/j.micres.2016.06.007
Galván I. 2018. Evidence of evolutionary optimization of fatty acid length and unsaturation. Journal of Evolutionary Biology. 31: 172–176. 10.1111/jeb.13198
Grimme S., Ehrlich S., and Goerigk L. 2011. Effect of the damping function in dispersion corrected density functional theory. Journal of Computational Chemistry. 32: 1456–1465. 10.1002/jcc.21759
Humphrey W., Dalke A., and Schulten K. 1996. VMD: visual molecular dynamics. Journal of Molecular Graphics. 14: 33–38. 10.1016/0263-7855(96)00018-5
Johnson ER., Keinan S., Mori-Sánchez P., Contreras-García J., Cohen AJ., and Yang W. 2010. Revealing noncovalent interactions. Journal of the American Chemical Society. 132: 6498–6506. 10.1021/ja100936w
Lee C., Yang W., and Parr RG. 1988. Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density. Physical Review B: Condensed Matter and Materials Physics. 37: 785–789. 10.1103/PhysRevB.37.785
Lu T., and Chen F. 2012. Multiwfn: a multifunctional wavefunction analyzer. Journal of Computational Chemistry. 33: 580–592. 10.1002/jcc.22885
Marenich AV., Cramer CJ., and Truhlar DG. 2009. Universal solvation model based on solute electron density and on a continuum model of the solvent defined by the bulk dielectric constant and atomic surface tensions. Journal of Physical Chemistry B. 113: 6378–6396. 10.1021/jp810292n
Newell M., Baker K., Postovit LM., and Field CJ. 2017. A critical review on the effect of docosahexaenoic acid (DHA) on cancer cell cycle progression. International Journal of Molecular Sciences. 18: 1784. 10.3390/ijms18081784
Owen JS., Bruckdorfer KR., Day RC., and McIntyre N. 1982. Decreased erythrocyte membrane fluidity and altered lipid composition in human liver disease. Journal of Lipid Research. 23: 124–132. 10.1016/S0022-2275(20)38181-5
Richards SL., Wilkins KA., Swarbreck SM., Anderson AA., Habib N., Smith AG., et al. 2015. The hydroxyl radical in plants: from seed to seed. Journal of Experimental Botany. 66: 37–46. 10.1093/jxb/eru398
Schwartz RS., Chiu DT., and Lubin B. 1985. Plasma membrane phospholipid organization in human erythrocytes. Current Topics in Hematology. 5: 63–112.
Shin S., Ku Y., Babu N., and Singh M. 2007. Erythrocyte deformability and its variation in diabetes mellitus. Indian Journal of Experiemental Biology. 45: 121–128.
Sreekanth V., and Bajaj A. 2013. Number of free hydroxyl groups on bile acid phospholipids determines the fluidity and hydration of model membranes. Journal of Physical Chemistry B. 117: 12135–12144. 10.1021/jp406340y
Startek JB., Milici A., Naert R., Segal A., Alpizar YA., Voets T., et al. 2021. The agonist action of alkylphenols on TRPA1 relates to their effects on membrane lipid order: implications for TRPA1-mediated chemosensation. International Journal of Molecular Sciences. 22: 3368. 10.3390/ijms22073368
Staufenbiel M., and Lazarides E. 1986. Assembly of protein 4.1 during chicken erythroid differentiation. Journal of Cell Biology. 102: 1157–1163. 10.1083/jcb.102.4.1157
Sun K., and Xia Y. 2013. New insights into sickle cell disease: a disease of hypoxia. Current Opinion in Hematology. 20: 215–221. 10.1097/MOH.0b013e32835f55f9
Tsuda K., Kinoshita Y., Nishio I., and Masuyama Y. 2001. Hyperinsulinemia is a determinant of membrane fluidity of erythrocytes in essential hypertension. American Journal of Hypertension. 14: 419–423. 10.1016/S0895-7061(00)01247-4
Upchurch RG. 2008. Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. Biotechnology Letters. 30: 967–977. 10.1007/s10529-008-9639-z
Watanabe H., Kobayashi A., Yamamoto T., Suzuki S., Hayashi H., and Yamazaki N. 1990. Alterations of human erythrocyte membrane fluidity by oxygen-derived free radicals and calcium. Free Radical Biology & Medicine. 8: 507–514. 10.1016/0891-5849(90)90150-H
Weigend F. 2006. Accurate coulomb-fitting basis sets for H to Rn. Physical Chemistry Chemical Physics. 8: 1057–1065. 10.1039/b515623h
Wu D., and Yotnda P. 2011. Induction and testing of hypoxia in cell culture. Journal of Visualized Experiments, 2899. 10.3791/2899-v
Yang W., Tian Y., Han M., and Miao X. 2017. Longevity extension of worker honey bees (Apis mellifera) by royal jelly: optimal dose and active ingredient. Peer J. 5: e3118. 10.7717/peerj.3118
Yang YC., Chou WM., Widowati DA., Lin IP., and Peng CC. 2018. 10-hydroxy-2-decenoic acid of royal jelly exhibits bactericide and anti-inflammatory activity in human colon cancer cells. BMC Complementary and Alternative Medicine. 18: 202. 10.1186/s12906-018-2267-9
You M., Miao Z., Pan Y., and Hu F. 2019. Trans-10-hydroxy-2-decenoic acid alleviates LPS-induced blood-brain barrier dysfunction by activating the AMPK/PI3K/AKT pathway. European Journal of Pharmacology. 865: 172736. 10.1016/j.ejphar.2019.172736
You M., Miao Z., Tian J., and Hu F. 2020. Trans-10-hydroxy-2-decenoic acid protects against LPS-induced neuroinflammation through FOXO1-mediated activation of autophagy. European Journal of Nutrition. 59: 2875–2892. 10.1007/s00394-019-02128-9
Zheng J., Lai W., Zhu G., Wan M., Chen J., Tai Y., et al. 2013. 10-Hydroxy-2-decenoic acid prevents ultraviolet A-induced damage and matrix metalloproteinases expression in human dermal fibroblasts. Journal of the European Academy of Dermatology and Venereology. 27: 1269–1277. 10.1111/j.1468-3083.2012.04707.x
Aozaki S. Decreased membrane fluidity in erythrocytes from patients with Crohn’s disease. 1989. Gastroenterologica Japonica. 24: 246–254. 10.1007/BF02774321
Bader RFW. 1990. Atoms in Molecules: A Quantum Theory. Clarendon Press, Oxford, UK. 10.1093/oso/9780198551683.001.0001
Becatti M., Marcucci R., Gori AM., Mannini L., Grifoni E., Alessandrello LA., et al. 2016. Erythrocyte oxidative stress is associated with cell deformability in patients with retinal vein occlusion. Journal of Thrombosis and Haemostasis. 14: 2287–2297. 10.1111/jth.13482
Becke AD and Edgecombe KE. 1990. A simple measure of electron localization in atomic and molecular systems. Journal of Chemical Physics. 92: 5397–5403. 10.1063/1.458517
Becke AD. 1993. Density-functional thermochemistry. III. The role of exact exchange. Journal of Chemical Physics. 98: 5648–5652. 10.1063/1.464913
Chen YF., Wang K., Zhang YZ., Zheng YF., and Hu FL. 2016. In vitro anti-inflammatory effects of three fatty acids from royal jelly. Mediators of Inflammation. 2016: 3583684. 10.1155/2016/3583684
Cooper RA., Durocher JR., and Leslie MH. 1977. Decreased fluidity of red cell membrane lipids in abetalipoproteinemia. Journal of Clinical Investigation. 60: 115–121. 10.1172/JCI108747
Dakroub H., Nowak M., Benoist JF., Noël B., Vedie B., Paul JL., et al. 2021. Eicosapentaenoic acid membrane incorporation stimulates ABCA1-mediated cholesterol efflux from human THP-1 macrophages. Biochimica et Biophysica Acta-Molecular and Cell Biology of Lipids, 1866: 159016. 10.1016/j.bbalip.2021.159016
Diakowski W., Grzybek M., and Sikorski AF. 2006. Protein 4.1, a component of the erythrocyte membrane skeleton and its related homologue proteins forming the protein 4.1/FERM superfamily. Folia Histochemica et Cytobiologica. 44: 231–248.
Dumas D., Muller S., Gouin F., Baros F., Viriot ML., and Stoltz JF. 1997. Membrane fluidity and oxygen diffusion in cholesterol-enriched erythrocyte membrane. Archives of Biochemistry and Biophysics. 341: 34–39. 10.1006/abbi.1997.9936
Fan P., Han B., Hu H., Wei Q., Zhang X., Meng L., et al. 2020. Proteome of thymus and spleen reveals that 10-hydroxydec-2-enoic acid could enhance immunity in mice. Expert Opinion on Therapeutic Targets. 24: 267–279. 10.1080/14728222.2020.1733529
Fan P., Sha F., Ma C., Wei Q., Zhou Y., Shi J., et al. 2022. 10-Hydroxydec-2-enoic acid reduces hydroxyl free radical-induced damage to vascular smooth muscle cells by rescuing protein and energy metabolism. Frontiers in Nutrition. 9: 873892. 10.3389/fnut.2022.873892
Ferretti G., Simonetti O., Offidani AM., Messini L., Cinti B., Marshiseppe I. et al. 1993. Changes of plasma lipids and erythrocyte membrane fluidity in psoriatic children. Pediatric Research. 33: 506–509. 10.1203/00006450-199305000-00017
Filipič B., Gradišnik L., Rihar K., Šooš E., Pereyra A., and Potokar J. 2015. The influence of royal jelly and human interferon-alpha (HuIFN-αN3) on proliferation, glutathione level and lipid peroxidation in human colorectal adenocarcinoma cells in vitro. Arhiv za Higijenu Rada i Toksikologiju. 66: 269–274. 10.1515/aiht-2015-66-2632
Fonseca F., Pénicaud C., Tymczyszyn EE., Gómez-Zavaglia A., and Passot S. 2019. Factors influencing the membrane fluidity and the impact on production of lactic acid bacteria starters. Applied Microbiology and Biotechnology. 103: 6867–6883. 10.1007/s00253-019-10002-1
Fournier N., Sayet G., Vedie B., Nowak M., Allaoui F., Solgadi A., et al. 2017. Eicosapentaenoic acid membrane incorporation impairs cholesterol efflux from cholesterol-loaded human macrophages by reducing the cholesteryl ester mobilization from lipid droplets. Biochimica et Biophysica Acta-Molecular and Cell Biology of Lipids. 1862: 1079–1091. 10.1016/j.bbalip.2017.07.011
Fratini F., Cilia C., Mancini S., and Felicioli A. 2016. Royal jelly: an ancient remedy with remarkable antibacteria properties. Microbiological Research. 192: 130–141. 10.1016/j.micres.2016.06.007
Galván I. 2018. Evidence of evolutionary optimization of fatty acid length and unsaturation. Journal of Evolutionary Biology. 31: 172–176. 10.1111/jeb.13198
Grimme S., Ehrlich S., and Goerigk L. 2011. Effect of the damping function in dispersion corrected density functional theory. Journal of Computational Chemistry. 32: 1456–1465. 10.1002/jcc.21759
Humphrey W., Dalke A., and Schulten K. 1996. VMD: visual molecular dynamics. Journal of Molecular Graphics. 14: 33–38. 10.1016/0263-7855(96)00018-5
Johnson ER., Keinan S., Mori-Sánchez P., Contreras-García J., Cohen AJ., and Yang W. 2010. Revealing noncovalent interactions. Journal of the American Chemical Society. 132: 6498–6506. 10.1021/ja100936w
Lee C., Yang W., and Parr RG. 1988. Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density. Physical Review B: Condensed Matter and Materials Physics. 37: 785–789. 10.1103/PhysRevB.37.785
Lu T., and Chen F. 2012. Multiwfn: a multifunctional wavefunction analyzer. Journal of Computational Chemistry. 33: 580–592. 10.1002/jcc.22885
Marenich AV., Cramer CJ., and Truhlar DG. 2009. Universal solvation model based on solute electron density and on a continuum model of the solvent defined by the bulk dielectric constant and atomic surface tensions. Journal of Physical Chemistry B. 113: 6378–6396. 10.1021/jp810292n
Newell M., Baker K., Postovit LM., and Field CJ. 2017. A critical review on the effect of docosahexaenoic acid (DHA) on cancer cell cycle progression. International Journal of Molecular Sciences. 18: 1784. 10.3390/ijms18081784
Owen JS., Bruckdorfer KR., Day RC., and McIntyre N. 1982. Decreased erythrocyte membrane fluidity and altered lipid composition in human liver disease. Journal of Lipid Research. 23: 124–132. 10.1016/S0022-2275(20)38181-5
Richards SL., Wilkins KA., Swarbreck SM., Anderson AA., Habib N., Smith AG., et al. 2015. The hydroxyl radical in plants: from seed to seed. Journal of Experimental Botany. 66: 37–46. 10.1093/jxb/eru398
Schwartz RS., Chiu DT., and Lubin B. 1985. Plasma membrane phospholipid organization in human erythrocytes. Current Topics in Hematology. 5: 63–112.
Shin S., Ku Y., Babu N., and Singh M. 2007. Erythrocyte deformability and its variation in diabetes mellitus. Indian Journal of Experiemental Biology. 45: 121–128.
Sreekanth V., and Bajaj A. 2013. Number of free hydroxyl groups on bile acid phospholipids determines the fluidity and hydration of model membranes. Journal of Physical Chemistry B. 117: 12135–12144. 10.1021/jp406340y
Startek JB., Milici A., Naert R., Segal A., Alpizar YA., Voets T., et al. 2021. The agonist action of alkylphenols on TRPA1 relates to their effects on membrane lipid order: implications for TRPA1-mediated chemosensation. International Journal of Molecular Sciences. 22: 3368. 10.3390/ijms22073368
Staufenbiel M., and Lazarides E. 1986. Assembly of protein 4.1 during chicken erythroid differentiation. Journal of Cell Biology. 102: 1157–1163. 10.1083/jcb.102.4.1157
Sun K., and Xia Y. 2013. New insights into sickle cell disease: a disease of hypoxia. Current Opinion in Hematology. 20: 215–221. 10.1097/MOH.0b013e32835f55f9
Tsuda K., Kinoshita Y., Nishio I., and Masuyama Y. 2001. Hyperinsulinemia is a determinant of membrane fluidity of erythrocytes in essential hypertension. American Journal of Hypertension. 14: 419–423. 10.1016/S0895-7061(00)01247-4
Upchurch RG. 2008. Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. Biotechnology Letters. 30: 967–977. 10.1007/s10529-008-9639-z
Watanabe H., Kobayashi A., Yamamoto T., Suzuki S., Hayashi H., and Yamazaki N. 1990. Alterations of human erythrocyte membrane fluidity by oxygen-derived free radicals and calcium. Free Radical Biology & Medicine. 8: 507–514. 10.1016/0891-5849(90)90150-H
Weigend F. 2006. Accurate coulomb-fitting basis sets for H to Rn. Physical Chemistry Chemical Physics. 8: 1057–1065. 10.1039/b515623h
Wu D., and Yotnda P. 2011. Induction and testing of hypoxia in cell culture. Journal of Visualized Experiments, 2899. 10.3791/2899-v
Yang W., Tian Y., Han M., and Miao X. 2017. Longevity extension of worker honey bees (Apis mellifera) by royal jelly: optimal dose and active ingredient. Peer J. 5: e3118. 10.7717/peerj.3118
Yang YC., Chou WM., Widowati DA., Lin IP., and Peng CC. 2018. 10-hydroxy-2-decenoic acid of royal jelly exhibits bactericide and anti-inflammatory activity in human colon cancer cells. BMC Complementary and Alternative Medicine. 18: 202. 10.1186/s12906-018-2267-9
You M., Miao Z., Pan Y., and Hu F. 2019. Trans-10-hydroxy-2-decenoic acid alleviates LPS-induced blood-brain barrier dysfunction by activating the AMPK/PI3K/AKT pathway. European Journal of Pharmacology. 865: 172736. 10.1016/j.ejphar.2019.172736
You M., Miao Z., Tian J., and Hu F. 2020. Trans-10-hydroxy-2-decenoic acid protects against LPS-induced neuroinflammation through FOXO1-mediated activation of autophagy. European Journal of Nutrition. 59: 2875–2892. 10.1007/s00394-019-02128-9
Zheng J., Lai W., Zhu G., Wan M., Chen J., Tai Y., et al. 2013. 10-Hydroxy-2-decenoic acid prevents ultraviolet A-induced damage and matrix metalloproteinases expression in human dermal fibroblasts. Journal of the European Academy of Dermatology and Venereology. 27: 1269–1277. 10.1111/j.1468-3083.2012.04707.x
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Dec 7, 2023
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Sha, F., Yang, P., Wang, H., Ren, J., Li, Z., Zhang, L., & Fan, P. (2023). 10-Hydroxydec-2-enoic acid enhances the erythrocyte membrane fluidity via interacting with phosphatidylcholine and phosphatidylethanolamine. Italian Journal of Food Science, 35(4), 119-129. https://doi.org/10.15586/ijfs.v35i4.2358
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How to Cite
Sha, F., Yang, P., Wang, H., Ren, J., Li, Z., Zhang, L., & Fan, P. (2023). 10-Hydroxydec-2-enoic acid enhances the erythrocyte membrane fluidity via interacting with phosphatidylcholine and phosphatidylethanolamine. Italian Journal of Food Science, 35(4), 119-129. https://doi.org/10.15586/ijfs.v35i4.2358