Biomolecules & Therapeutics

The Korean Society of Applied Pharmacology (한국응용약물학회)
권호 표지
DOI QR코드

DOI QR Code

Anthocyanin Extracts from Black Soybean (Glycine max L.) Protect Human Glial Cells Against Oxygen-Glucose Deprivation by Promoting Autophagy

  • Kim, Yong-Kwan (Department of Biochemistry, The Catholic University of Korea College of Medicine) ;
  • Yoon, Hye-Hyeon (Department of Biochemistry, The Catholic University of Korea College of Medicine) ;
  • Lee, Young-Dae (Department of Biochemistry, The Catholic University of Korea College of Medicine) ;
  • Youn, Dong-Ye (Department of Biochemistry, The Catholic University of Korea College of Medicine) ;
  • Ha, Tae-Joung (Department of Functional Crop, National Institute of Crop Science (NICS), Rural Development Administration (RDA)) ;
  • Kim, Ho-Shik (Department of Biochemistry, The Catholic University of Korea College of Medicine) ;
  • Lee, Jeong-Hwa (Department of Biochemistry, The Catholic University of Korea College of Medicine)
  • Received : 2011.11.15
  • Accepted : 2011.12.01
  • Published : 2012.01.31
Download PDF
⟨ Previous Next ⟩

Abstract

Anthocyanins have received growing attention as dietary antioxidants for the prevention of oxidative damage. Astrocytes, which are specialized glial cells, exert numerous essential, complex functions in both healthy and diseased central nervous system (CNS) through a process known as reactive astrogilosis. Therefore, the maintenance of glial cell viability may be important because of its role as a key modulator of neuropathological events. The aim of this study was to investigate the effect of anthocyanin on the survival of glial cells exposed to oxidative stress. Our results demonstrated that anthocyanin extracts from black soybean increased survival of U87 glioma cells in a dose dependent manner upon oxygen-glucose deprivation (OGD), accompanied by decrease levels of reactive oxygen species (ROS). While treatment cells with anthocyanin extracts or OGD stress individually activated autophagy induction, the effect was signifi cantly augmented by pretreatment cells with anthocyanin extracts prior to OGD. The contribution of autophagy induction to the protective effects of anthocyanin was verifi ed by the observation that silencing the Atg5 expression, an essential regulator of autophagy induction, reversed the cytoprotective effect of anthocyanin extracts against OGD stress. Treatment of U87 cells with rapamycin, an autophagy inducer, increased cell survival upon OGD stress comparable to anthocyanin, indicating that autophagy functions as a survival mechanism against oxidative stress-induced cytotoxicity in glial cells. Our results, therefore, provide a rationale for the use of anthocyanin as a preventive agent for brain dysfunction caused by oxidative damage, such as a stroke.

Keywords

References

  1. Bonini, P., Cicconi, S., Cardinale, A., Vitale, C., Serafi no, A. L., Ciotti, M. T. and Marlier, L. N. (2004) Oxidative stress induces p53-mediated apoptosis in glia: p53 transcription-independent way to die. J. Neurosci. Res. 75. 83-95. https://doi.org/10.1002/jnr.10822
  2. Budd, S. L. and Lipton, S. A. (1998) Calcium tsunamis: do astrocytes transmit cell death messages via gap junctions during ischemia? Nat. Neurosci. 1, 431-432. https://doi.org/10.1038/2147
  3. Byun, Y. J., Kim, S. K., Kim, Y. M., Chae, G. T., Jeong, S. W. and Lee, S. B. (2009) Hydrogen peroxide induces autophagic cell death in C6 glioma cells via BNIP3-mediated suppression of the mTOR pathway. Neurosci. Lett. 461, 131-135. https://doi.org/10.1016/j.neulet.2009.06.011
  4. Casadesus, G., Shukitt-Hale, B., Stellwagen, H. M., Zhu, X., Lee, H. G., Smith, M. A. and Joseph, J. A. (2004) Modulation of hippocampal plasticity and cognitive behavior by short-term blueberry supplementation in aged rats. Nutr. Neurosci. 7, 309-316. https://doi.org/10.1080/10284150400020482
  5. Chen, Y., Vartiainen, N. E., Ying, W., Chan, P. H., Koistinaho, J. and Swanson, R. A. (2001) Astrocytes protect neurons from nitric oxide toxicity by a glutathione-dependent mechanism. J. Neurochem. 77, 1601-1610. https://doi.org/10.1046/j.1471-4159.2001.00374.x
  6. Chen, Y., McMillan-Ward, E., Kong, J., Israels, S. J. and Gibson, S. B. (2008) Oxidative stress induces autophagic cell death independent of apoptosis in transformed and cancer cells. Cell Death Differ. 15, 171-182. https://doi.org/10.1038/sj.cdd.4402233
  7. Clifford, M. N. (2004) Diet-derived phenols in plasma and tissues and their implications for health. Planta. Med. 70, 1103-1114. https://doi.org/10.1055/s-2004-835835
  8. Dringen, R., Pfeiffer, B. and Hamprecht, B. (1999) Synthesis of the antioxidant glutathione in neurons: supply by astrocytes of CysGly as precursor for neuronal glutathione. J. Neurosci. 19, 562-569.
  9. Feng, R., Wang, SY., Shi, Y. H., Fan, J. and Yin, X. M. (2010) Delphinidin Induces Necrosis in Hepatocellular Carcinoma Cells in the Presence of 3-Methyladenine, an Autophagy Inhibitor. J. Agric. Food Chem. 58, 3957-3964. https://doi.org/10.1021/jf9025458
  10. Galli, R. L., Bielinsky, D. F., Szprengiel. A., Shukitt-Hale, B. and Joseph, JA. (2006) Blueberry supplemented diet reverses age-related decline in hippocampal HSP70 neuroprotection. Neurobiology of Aging. 27, 344-350. https://doi.org/10.1016/j.neurobiolaging.2005.01.017
  11. Ha, T. J., Lee, J. H., Shin, S. O., Shin, S. H., Han, S. I., Kim, H. T., Ko, J. M., Lee, M. H. and Park, K. Y. (2009) Changes in anthocyanin and isofl avone concentrations in black seed-coated soybean at different planting locations. J. Crop Sci. Biotech. 12, 79-86. https://doi.org/10.1007/s12892-009-0093-9
  12. Hamby, M. E. and Sofroniew, M. V. (2010) Reactive astrocytes as therapeutic targets for CNS disorders. Neurotherapeutics. 7, 494-506. https://doi.org/10.1016/j.nurt.2010.07.003
  13. Hwang, J., Lee, S., Lee, J. T., Kwon, T. K., Kim, D. R., Kim, H., Park, H. C. and Suk, K. (2010) Gangliosides induce autophagic cell death in astrocytes. Br. J. Pharmacol. 159, 586-603. https://doi.org/10.1111/j.1476-5381.2009.00563.x
  14. Joseph, J. A., Shukitt-Hale, B., Denisova, N. A., Bielinski, D., Martin, A., McEwen, J. J. and Bickford, P. C. (1999) Reversals of agerelated declines in neuronal signal transduction, cognitive, and motor behavioral defi cits with blueberry, spinach, or strawberry dietary supplementation. J. Neurosci. 19, 8114-8121.
  15. Jung, S. E., Kim, Y. K., Youn, D. Y., Lim, M. H., Ko, J. H., Ahn, Y. S. and Lee, J. H. (2010) Down-modulation of Bis sensitizes cell death in C6 glioma cells induced by oxygen-glucose deprivation. Brain Res. 1349, 1-10. https://doi.org/10.1016/j.brainres.2010.06.043
  16. Kamei, H., Kojima, T., Hasegawa, M., Koide, T., Umeda, T., Yukawa, T. and Terabe, K. (1995) Suppression of tumor cell growth by anthocyanins in vitro. Cancer Invest. 13, 590-594. https://doi.org/10.3109/07357909509024927
  17. Kang, T. H., Hur, J. Y., Kim, H. B., Ryu, J. H. and Kim, S. Y. (2006) Neuroprotective effects of the cyanidin-3-O-beta-d-glucopyranoside isolated from mulberry fruit against cerebral ischemia. Neurosci. Lett. 391, 122-126. https://doi.org/10.1016/j.neulet.2005.08.053
  18. Klionsky, D. J. (2007) Autophagy:from phenomenology to molecular under-standing in less than a decade. Nat. Rev. Mol. Cell Biol. 8, 931-937. https://doi.org/10.1038/nrm2245
  19. Lee, J. H., Kang, N. S., Shin, S. O., Shin, S. H., Lim, S. G., Suh, D. Y., Baek, I. Y., Park, K. Y. and Ha, T. J. (2009a) Characterisation of anthocyanins in the black soybean (Glycine max L.) by HPLCDAD-ESI/MS analysis. Food Chemistry 112, 226-231. https://doi.org/10.1016/j.foodchem.2008.05.056
  20. Lee, S. H., Park, S. M., Park, S. M., Park, J. H., Shin, D. Y., Kim, G. Y., Ryu, C. H., Shin, S. C., Jung, J. M., Kang, H. S., Lee, W. S. and Choi, Y. H. (2009b) Induction of apoptosis in human leukemia U937 cells by anthocyanins through down-regulation of Bcl-2 and activation of caspases. Int. J. Oncol. 34, 1077-1083.
  21. Li, L., Lundkvist, A., Andersson, D., Wilhelmsson, U., Nagai, N., Pardo, A. C., Nodin, C., Ståhlberg, A., Aprico, K., Larsson, K., Yabe, T., Moons, L., Fotheringham, A., Davies, I., Carmeliet, P., Schwartz, J. P., Pekna, M., Kubista, M., Blomstrand, F., Maragakis, N., Nilsson, M. and Pekny, M. (2008) Protective role of reactive astrocytes in brain ischemia. J. Cereb. Blood Flow Metab. 28, 468-481. https://doi.org/10.1038/sj.jcbfm.9600546
  22. Lin, J. H., Weigel, H., Cotrina, M. L., Liu, S., Bueno, E., Hansen, A. J., Hansen, TW., Goldman, S. and Nedergaard, M. (1998) Gapjunction- mediated propagation and amplifi cation of cell injury. Nat. Neurosci. 1, 494-500. https://doi.org/10.1038/2210
  23. Longo, L., Platini, F., Scardino, A., Alabiso, O., Vasapollo, G. and Tessitore, L. (2008) Autophagy inhibition enhances anthocyanininduced apoptosis in hepatocellular carcinoma. Mol. Cancer Ther. 7, 2476-2485. https://doi.org/10.1158/1535-7163.MCT-08-0361
  24. Markiewicz, I. and Lukomska, B. (2006) The role of astrocytes in the physiology and pathology of the central nervous system. Acta. Neurobiol. Exp. 66, 343-358.
  25. Matsumoto, H., Nakamura, Y., Tachibanaki, S., Kawamura, S. and Hirayama, M. (2003) Stimulatory effect of cyanidin 3-glycosides on the regeneration of rhodopsin. J. Agric. Food Chem. 51, 3560-3563. https://doi.org/10.1021/jf034132y
  26. Mauray, A., Felgines, C., Morand, C., Mazur, A., Scalbert, A. and Milenkovic, D. (2010) Nutrigenomic analysis of the protective effects of bilberry anthocyanin-rich extract in apo E-deficient mice. Genes Nutr. 5, 343-353. https://doi.org/10.1007/s12263-010-0171-0
  27. McGhie, T. K. and Walton, M. C. (2007) The bioavailability and absorption of anthocyanins: towards a better understanding. Mol. Nutr. Food Res. 51, 702-713. https://doi.org/10.1002/mnfr.200700092
  28. Meijer, A. J. and Codogno, P. (2009) Autophagy: regulation and role in disease. Crit. Rev. Clin. Lab. Sci. 46, 210-240. https://doi.org/10.1080/10408360903044068
  29. Mizushima, N. (2007) Autophagy: process and function. Genes Dev. 21, 2861-2873. https://doi.org/10.1101/gad.1599207
  30. Paixao, J., Dinis, TC. and Almeida, L. M. (2011) Dietary anthocyanins protect endothelial cells against peroxynitrite-induced mitochondrial apoptosis pathway and Bax nuclear translocation: an in vitro approach. Apoptosis 16, 976-989. https://doi.org/10.1007/s10495-011-0632-y
  31. Papandreou, M. A., Dimakopoulou, A., Linardaki, Z. I., Cordopatis, P., Klimis-Zacas, D., Margarity, M. and Lamari, F. N. (2009) Effect of a polyphenol-rich wild blueberry extract on cognitive performance of mice, brain antioxidant markers and acetylcholinesterase activity. Behav. Brain Res. 198, 352-358. https://doi.org/10.1016/j.bbr.2008.11.013
  32. Poulletier de Gannes, F., Haro, E., Hurtier, A., Taxile, M., Ruffie, G., Billaudel, B., Veyret, B. and Lagroye, I. (2011) Effect of exposure to the edge signal on oxidative stress in brain cell models. Radiat. Res. 175, 225-230. https://doi.org/10.1667/RR2320.1
  33. Prior, R. L. and Wu, X. (2006) Anthocyanins: structural characteristics that result in unique metabolic patterns and biological activities. Free Radic. Res. 40, 1014-1028. https://doi.org/10.1080/10715760600758522
  34. Ramirez, M. R., Izquierdo, I., do Carmo Bassols, Raseira. M., Zuanazzi, J. A., Barros, D. and Henriques, AT. (2005) Effect of lyophilised Vaccinium berries on memory, anxiety and locomotion in adult rats. Pharmacol. Res. 52, 457-462. https://doi.org/10.1016/j.phrs.2005.07.003
  35. Ravikumar, B., Berger, Z., Vacher, C., O'Kane, C. J. and Rubinsztein, D. C. (2006) Rapamycin pre-treatment protects against apoptosis. Hum. Mol. Genet. 15, 1209-1216. https://doi.org/10.1093/hmg/ddl036
  36. Rossi, D. J., Brady, J. D. and Mohr, C. (2007) Astrocyte metabolism and signaling during brain ischemia. Nat. Neurosci. 11, 1377-1386.
  37. Roychowdhury, S., Wolf, G., Keilhoff, G., Bagchi, D. and Horn, T. (2001) Protection of primary glial cells by grape seed proanthocyanidin extract against nitrosative/ oxidative stress. Nitric. Oxide. 5, 137-149. https://doi.org/10.1006/niox.2001.0335
  38. Senger, D. L., Tudan, C., Guiot, M. C., Mazzoni, I. E., Molenkamp, G., LeBlanc, R., Antel, J., Olivier, A., Snipes, G. J. and Kaplan, D. R. (2002) Suppression of Rac activity induces apoptosis of human glioma cells but not normal human astrocytes. Cancer Res. 62, 2131-2140.
  39. Sick, E., Boukhari, A., Deramaudt, T., Rondé, P., Bucher, B., André, P., Gies, J. P. and Takeda, K. (2011) Activation of CD47 receptors causes proliferation of human astrocytoma but not normal astrocytes via an Akt-dependent pathway. Glia. 59, 308-319. https://doi.org/10.1002/glia.21102
  40. Sofroniew, M. V. and Vinters, H. V. (2010) Astrocytes: biology and pathology. Acta. Neuropathol. 119, 7-35. https://doi.org/10.1007/s00401-009-0619-8
  41. Takano, T., Oberheim, N., Cotrina, M. L. and Nedergaard, M. (2009) Astrocytes and ischemic injury. Stroke. 40, S8-12. https://doi.org/10.1161/STROKEAHA.108.533166
  42. Tanida, I., Ueno, T. and Kominami, E. (2004) LC3 conjugation system in mammalian autophagy. Int. J. Biochem. Cell Biol. 36, 2503-2518. https://doi.org/10.1016/j.biocel.2004.05.009
  43. Wang, H., Nair, M. G., Strasburg, G. M., Chang, Y. C., Booren, A. M., Gray, J. I. and DeWitt, D. L. (1999) Antioxidant and antiinfl ammatory activities of anthocyanins and their aglycon, cyanidin, from tart cherries. J. Nat. Prod. 62, 294-296. https://doi.org/10.1021/np980501m
  44. Xia, X., Ling, W., Ma, J., Xia, M., Hou, M., Wang, Q., Zhu, H. and Tang, Z. (2006) An anthocyanin-rich extract from black rice enhances atherosclerotic plaque stabilization in apolipoprotein E-deficient mice. J. Nutr. 136, 2220-2225.

Cited by

  1. A Critical Review on Polyphenols and Health Benefits of Black Soybeans vol.9, pp.5, 2017, https://doi.org/10.3390/nu9050455
  2. Time-Dependent Changes in Apoptosis Upon Autophagy Inhibition in Astrocytes Exposed to Oxygen and Glucose Deprivation vol.37, pp.2, 2017, https://doi.org/10.1007/s10571-016-0363-2
  3. Decreased vulnerability of hippocampal neurons after neonatal hypoxia-ischemia inbis-deficient mice vol.60, pp.12, 2012, https://doi.org/10.1002/glia.22407
  4. Anthocyanins in the black soybean (Glycine max L.) protect U2OS cells from apoptosis by inducing autophagy via the activation of adenosyl monophosphate-dependent protein kinase vol.28, pp.6, 2012, https://doi.org/10.3892/or.2012.2034
  5. Spectroscopic andin silicostudy of binding mechanism of cynidine-3-O-glucoside with human serum albumin and glycated human serum albumin vol.32, pp.4, 2017, https://doi.org/10.1002/bio.3233
  6. Protective effects of blueberry- and strawberry diets on neuronal stress following exposure to 56Fe particles vol.1593, 2014, https://doi.org/10.1016/j.brainres.2014.10.028
  7. Health benefits of anthocyanins and molecular mechanisms: Update from recent decade vol.57, pp.8, 2017, https://doi.org/10.1080/10408398.2015.1030064
  8. Neuroprotective properties of anthocyanidin glycosides against H 2 O 2 -induced glial cell death are modulated by their different stability and antioxidant activity in vitro vol.94, 2017, https://doi.org/10.1016/j.biopha.2017.07.077
  9. Radioprotective effects of delphinidin on normal human lung cells against proton beam exposure vol.12, pp.1, 2018, https://doi.org/10.4162/nrp.2018.12.1.41
  10. The Impact of O -Glycosylation on Cyanidin Interaction with RBCs and HMEC-1 Cells—Structure–Activity Relationships vol.20, pp.8, 2012, https://doi.org/10.3390/ijms20081928
  11. Dietary Anthocyanins and Stroke: A Review of Pharmacokinetic and Pharmacodynamic Studies vol.11, pp.7, 2019, https://doi.org/10.3390/nu11071479
  12. Anthocyanin fingerprinting and dynamics in differentially pigmented exotic soybean genotypes using modified HPLC-DAD method vol.14, pp.4, 2012, https://doi.org/10.1007/s11694-020-00443-y
  13. Total flavones of Dracocephalum moldavica L. protect astrocytes against H 2 O 2 -induced apoptosis through a mitochondria-dependent pathway vol.20, pp.None, 2012, https://doi.org/10.1186/s12906-020-2846-4
  14. Targeting autophagy in ischemic stroke: From molecular mechanisms to clinical therapeutics vol.225, pp.None, 2021, https://doi.org/10.1016/j.pharmthera.2021.107848