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Oxidative Medicine and Cellular Longevity
Volume 2017, Article ID 8519169, 16 pages
https://doi.org/10.1155/2017/8519169
Research Article

ROS-Dependent Activation of Autophagy through the PI3K/Akt/mTOR Pathway Is Induced by Hydroxysafflor Yellow A-Sonodynamic Therapy in THP-1 Macrophages

1Department of Pathophysiology, Key Laboratory of Cardiovascular Pathophysiology, Harbin Medical University, Harbin, China
2Division of Cardiology, The First Affiliated Hospital, Harbin Medical University, Harbin, China

Correspondence should be addressed to Liming Yang; moc.361@umhgnaygnimil

Received 29 October 2016; Revised 10 December 2016; Accepted 21 December 2016; Published 16 January 2017

Academic Editor: Jun Ren

Copyright © 2017 Yueqing Jiang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. L. A. Lotta, “Genome-wide association studies in atherothrombosis,” European Journal of Internal Medicine, vol. 21, no. 2, pp. 74–78, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. F. Wang, Q. Gao, S. Guo et al., “The sonodynamic effect of curcumin on THP-1 cell-derived macrophages,” BioMed Research International, vol. 2013, Article ID 737264, 9 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. P. Libby, P. M. Ridker, and G. K. Hansson, “Progress and challenges in translating the biology of atherosclerosis,” Nature, vol. 473, no. 7347, pp. 317–325, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. K. J. Moore and I. Tabas, “Macrophages in the pathogenesis of atherosclerosis,” Cell, vol. 145, no. 3, pp. 341–355, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. K. J. Moore, F. J. Sheedy, and E. A. Fisher, “Macrophages in atherosclerosis: a dynamic balance,” Nature Reviews Immunology, vol. 13, no. 10, pp. 709–721, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. Y. V. Bobryshev, E. A. Ivanova, D. A. Chistiakov, N. G. Nikiforov, and A. N. Orekhov, “Macrophages and their role in atherosclerosis: pathophysiology and transcriptome analysis,” BioMed Research International, vol. 2016, Article ID 9582430, 13 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  7. C. Zhai, J. Cheng, H. Mujahid et al., “Selective inhibition of PI3K/Akt/mTOR signaling pathway regulates autophagy of macrophage and vulnerability of atherosclerotic plaque,” PLoS ONE, vol. 9, no. 3, Article ID e90563, 2014. View at Publisher · View at Google Scholar · View at Scopus
  8. P. Boya, F. Reggiori, and P. Codogno, “Emerging regulation and functions of autophagy,” Nature Cell Biology, vol. 15, no. 7, pp. 713–720, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. M. E. Hubbi and G. L. Semenza, “An essential role for chaperone-mediated autophagy in cell cycle progression,” Autophagy, vol. 11, no. 5, pp. 850–851, 2015. View at Publisher · View at Google Scholar · View at Scopus
  10. D. M. Schrijvers, G. R. Y. De Meyer, and W. Martinet, “Autophagy in atherosclerosis: a potential drug target for plaque stabilization,” Arteriosclerosis, Thrombosis, & Vascular Biology, vol. 31, no. 12, pp. 2787–2791, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. W. Martinet, I. De Meyer, S. Verheye, D. M. Schrijvers, J.-P. Timmermans, and G. R. Y. De Meyer, “Drug-induced macrophage autophagy in atherosclerosis: for better or worse?” Basic Research in Cardiology, vol. 108, article no. 321, 2013. View at Publisher · View at Google Scholar · View at Scopus
  12. V. Deretic, T. Saitoh, and S. Akira, “Autophagy in infection, inflammation and immunity,” Nature Reviews Immunology, vol. 13, no. 10, pp. 722–737, 2013. View at Publisher · View at Google Scholar · View at Scopus
  13. Z. Zhong, E. Sanchez-Lopez, and M. Karin, “Autophagy, inflammation, and immunity: a troika governing cancer and its treatment,” Cell, vol. 166, no. 2, pp. 288–298, 2016. View at Publisher · View at Google Scholar · View at Scopus
  14. L. Yu, C. K. McPhee, L. Zheng et al., “Termination of autophagy and reformation of lysosomes regulated by mTOR,” Nature, vol. 465, no. 7300, pp. 942–946, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. Y.-T. Wu, H.-L. Tan, Q. Huang, C.-N. Ong, and H.-M. Shen, “Activation of the PI3K-Akt-mTOR signaling pathway promotes necrotic cell death via suppression of autophagy,” Autophagy, vol. 5, no. 6, pp. 824–834, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. S. Saiki, Y. Sasazawa, Y. Imamichi et al., “Caffeine induces apoptosis by enhancement of autophagy via PI3K/Akt/mTOR/p70S6K inhibition,” Autophagy, vol. 7, no. 2, pp. 176–187, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. S. G. Rockson, D. P. Lorenz, W.-F. Cheong, and K. W. Woodburn, “Photoangioplasty: an emerging clinical cardiovascular role for photodynamic therapy,” Circulation, vol. 102, no. 5, pp. 591–596, 2000. View at Publisher · View at Google Scholar · View at Scopus
  18. N. Yumita, R. Nishigaki, K. Umemura, and S.-I. Umemura, “Hematoporphyrin as a sensitizer of cell-damaging effect of ultrasound,” Japanese Journal of Cancer Research, vol. 80, no. 3, pp. 219–222, 1989. View at Publisher · View at Google Scholar · View at Scopus
  19. T. Inui, K. Makita, H. Miura et al., “Case report: a breast cancer patient treated with GcMAF, sonodynamic therapy and hormone therapy,” Anticancer Research, vol. 34, no. 8, pp. 4589–4594, 2014. View at Google Scholar · View at Scopus
  20. X. Li, L. Gao, L. Zheng et al., “The efficacy and mechanism of apoptosis induction by hypericin-mediated sonodynamic therapy in THP-1 macrophages,” International Journal of Nanomedicine, vol. 10, pp. 821–838, 2015. View at Publisher · View at Google Scholar · View at Scopus
  21. L. Zheng, X. Sun, X. Zhu et al., “Apoptosis of THP-1 derived macrophages induced by sonodynamic therapy using a new sonosensitizer hydroxyl acetylated curcumin,” PLoS ONE, vol. 9, no. 3, Article ID e93133, 2014. View at Publisher · View at Google Scholar · View at Scopus
  22. H. Wang, Y. Yang, H. Chen et al., “The predominant pathway of apoptosis in THP-1 macrophage-derived foam cells induced by 5-Aminolevulinic acid-mediated sonodynamic therapy is the mitochondria-caspase pathway despite the participation of endoplasmic reticulum stress,” Cellular Physiology and Biochemistry, vol. 33, no. 6, pp. 1789–1801, 2014. View at Publisher · View at Google Scholar · View at Scopus
  23. Z. Li, X. Sun, S. Guo et al., “Rapid stabilisation of atherosclerotic plaque with 5-aminolevulinic acid-mediated sonodynamic therapy,” Thrombosis & Haemostasis, vol. 114, no. 4, pp. 793–803, 2015. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Pallichankandy, A. Rahman, F. Thayyullathil, and S. Galadari, “ROS-dependent activation of autophagy is a critical mechanism for the induction of anti-glioma effect of sanguinarine,” Free Radical Biology & Medicine, vol. 89, pp. 708–720, 2015. View at Publisher · View at Google Scholar · View at Scopus
  25. N. Chu, G. Yao, Y. Liu, M. Cheng, and T. Ikejima, “Newly synthesized bis-benzimidazole compound 8 induces apoptosis, autophagy and reactive oxygen species generation in HeLa cells,” Bioorganic & Medicinal Chemistry Letters, vol. 26, no. 17, pp. 4367–4371, 2016. View at Publisher · View at Google Scholar · View at Scopus
  26. X. Su, X. Wang, Q. Liu, P. Wang, C. Xu, and A. W. Leung, “The role of Beclin 1 in SDT-induced apoptosis and autophagy in human leukemia cells,” International Journal of Radiation Biology, vol. 91, no. 6, pp. 472–479, 2015. View at Publisher · View at Google Scholar · View at Scopus
  27. Q. Li, Q. Liu, P. Wang, X. Feng, H. Wang, and X. Wang, “The effects of Ce6-mediated sono-photodynamic therapy on cell migration, apoptosis and autophagy in mouse mammary 4T1 cell line,” Ultrasonics, vol. 54, no. 4, pp. 981–989, 2014. View at Publisher · View at Google Scholar · View at Scopus
  28. X. Wang, Q. Liu, Z. Wang et al., “Role of autophagy in sonodynamic therapy-induced cytotoxicity in S180 cells,” Ultrasound in Medicine & Biology, vol. 36, no. 11, pp. 1933–1946, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. X. Zheng, J. Wu, Q. Shao et al., “Apoptosis of THP-1 macrophages induced by pseudohypericin-mediated sonodynamic therapy through the mitochondria-caspase pathway,” Cellular Physiology & Biochemistry, vol. 38, no. 2, pp. 545–557, 2016. View at Publisher · View at Google Scholar · View at Scopus
  30. Z.-M. Feng, J. He, J.-S. Jiang, Z. Chen, Y.-N. Yang, and P.-C. Zhang, “NMR solution structure study of the representative component hydroxysafflor yellow A and other quinochalcone C-glycosides from carthamus tinctorius,” Journal of Natural Products, vol. 76, no. 2, pp. 270–274, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. Z. Qi, F. Yan, W. Shi et al., “AKT-Related autophagy contributes to the neuroprotective efficacy of hydroxysafflor yellow A against ischemic stroke in rats,” Translational Stroke Research, vol. 5, no. 4, pp. 501–509, 2014. View at Publisher · View at Google Scholar · View at Scopus
  32. M. O. J. Grootaert, P. A. da Costa Martins, N. Bitsch et al., “Defective autophagy in vascular smooth muscle cells accelerates senescence and promotes neointima formation and atherogenesis,” Autophagy, vol. 11, no. 11, pp. 2014–2032, 2015. View at Publisher · View at Google Scholar · View at Scopus
  33. R. Kang, H. J. Zeh, M. T. Lotze, and D. Tang, “The Beclin 1 network regulates autophagy and apoptosis,” Cell Death & Differentiation, vol. 18, no. 4, pp. 571–580, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. R. Mathew, C. M. Karp, B. Beaudoin et al., “Autophagy suppresses tumorigenesis through elimination of p62,” Cell, vol. 137, no. 6, pp. 1062–1075, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. B. N. Singh, D. Kumar, S. Shankar, and R. K. Srivastava, “Rottlerin induces autophagy which leads to apoptotic cell death through inhibition of PI3K/Akt/mTOR pathway in human pancreatic cancer stem cells,” Biochemical Pharmacology, vol. 84, no. 9, pp. 1154–1163, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. Z.-W. Zhou, X.-X. Li, Z.-X. He et al., “Induction of apoptosis and autophagy via sirtuin1- and PI3K/Akt/mTOR-mediated pathways by plumbagin in human prostate cancer cells,” Drug Design, Development & Therapy, vol. 9, pp. 1511–1554, 2015. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Apostolakis and D. Spandidos, “Chemokines and atherosclerosis: focus on the CX3CL1/CX3CR1 pathway,” Acta Pharmacologica Sinica, vol. 34, no. 10, pp. 1251–1256, 2013. View at Publisher · View at Google Scholar · View at Scopus
  38. D. Costley, C. Mc Ewan, C. Fowley et al., “Treating cancer with sonodynamic therapy: a review,” International Journal of Hyperthermia, vol. 31, no. 2, pp. 107–117, 2015. View at Publisher · View at Google Scholar · View at Scopus
  39. K. Tachibana, L. B. Feril Jr., and Y. Ikeda-Dantsuji, “Sonodynamic therapy,” Ultrasonics, vol. 48, no. 4, pp. 253–259, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. I.-T. Lee and C.-M. Yang, “Role of NADPH oxidase/ROS in pro-inflammatory mediators-induced airway and pulmonary diseases,” Biochemical Pharmacology, vol. 84, no. 5, pp. 581–590, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. X. Su, P. Wang, S. Yang, K. Zhang, Q. Liu, and X. Wang, “Sonodynamic therapy induces the interplay between apoptosis and autophagy in K562 cells through ROS,” International Journal of Biochemistry & Cell Biology, vol. 60, pp. 82–92, 2015. View at Publisher · View at Google Scholar · View at Scopus
  42. J. Lopiccolo, G. M. Blumenthal, W. B. Bernstein, and P. A. Dennis, “Targeting the PI3K/Akt/mTOR pathway: effective combinations and clinical considerations,” Drug Resistance Updates: Reviews and Commentaries in Antimicrobial and Anticancer Chemotherapy, vol. 11, no. 1-2, pp. 32–50, 2008. View at Google Scholar
  43. H. Jiang, M. Westerterp, C. Wang, Y. Zhu, and D. Ai, “Macrophage mTORC1 disruption reduces inflammation and insulin resistance in obese mice,” Diabetologia, vol. 57, no. 11, pp. 2393–2404, 2014. View at Publisher · View at Google Scholar · View at Scopus
  44. H.-H. Chen, K. Keyhanian, X. Zhou et al., “IRF2BP2 reduces macrophage inflammation and susceptibility to atherosclerosis,” Circulation Research, vol. 117, no. 8, pp. 671–683, 2015. View at Publisher · View at Google Scholar · View at Scopus
  45. P. Libby, “Inflammation in atherosclerosis,” Nature, vol. 420, no. 6917, pp. 868–874, 2002. View at Publisher · View at Google Scholar · View at Scopus
  46. G. K. Hansson, A.-K. L. Robertson, and C. Söderberg-Nauclér, “Inflammation and atherosclerosis,” Annual Review of Pathology: Mechanisms of Disease, vol. 1, no. 1, pp. 297–329, 2006. View at Publisher · View at Google Scholar · View at Scopus