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References

  1. Mathias S, Holger B. 2007. Mitotic drug targets and the development of novel anti-mitotic anticancer drugs. Drug Resist. Updat. 10: 162-181.
    Pubmed CrossRef
  2. Ricci MS, Zong WX. 2006. Chemotherapeutic approaches for targeting cell death pathways. Oncologist 11: 342-357.
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  4. Mansilla S, Llovera L, Portugal J. 2012. Chemotherapeutic targeting of cell death pathways. Anticancer Agents Med. Chem. 12: 226-238.
    Pubmed CrossRef
  5. Dive C, Gregory CD, Phipps DJ, Evans DL, Milner AE, Wyllie AH. 1992. Analysis and discrimination of necrosis and apoptosis (programmed cell death) by multiparameter flow cytometry. Biochim. Biophys. Acta 1133: 275-285.
    CrossRef
  6. Bonfoco E, Krainc D, Ankarcrona M, Nicotera P, Lipton SA. 1995. Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-Daspartate or nitric oxide/superoxide in cortical cell cultures. Proc. Natl. Acad. Sci. USA 92: 7162-7166.
    Pubmed PMC CrossRef
  7. Hannun YA. 1997. Apoptosis and dilemma of cancer chemotherapy. Blood 89: 1845-1853.
    Pubmed
  8. Kaufman SH, Earnshaw WC. 2000. Induction of apoptosis by cancer chemotherapy. Exp. Cell Res. 256: 42-49.
    Pubmed CrossRef
  9. Jun DY, Kim JS, Park HS, Han CR, Fang Z, Woo MH, et al. 2007. Apoptogenic activity of auraptene of Zanthoxylum schinifolium toward human acute leukemia Jurkat T cells is associated with ER stress-mediated caspase-8 activation that stimulates mitochondria-dependent or -independent caspase cascade. Carcinogenesis 28: 1303-1313.
    Pubmed CrossRef
  10. Desagher S, Martinou JC. 2000. Mitochondria as the central control point of apoptosis. Trends Cell Biol. 10: 369-377.
    CrossRef
  11. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA, Yuan J. 2000. Caspase-12 mediates endoplasmic-reticulumspecific apoptosis and cytotoxicity by amyloid-beta. Nature 403: 98-103.
    Pubmed CrossRef
  12. Wallach D, Boldin M, Varfolomeev E, Beyaert R, Vandenabeele P, Fiers W. 1997. Cell death induction by receptors of the THF family: towards a molecular understanding. FEBS Lett. 410: 96-106.
    CrossRef
  13. Degenhardt K, Mathew R, Beaudoin B, Bray K, Anderson D, Chen G, et al. 2006. Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 10: 51-64.
    Pubmed PMC CrossRef
  14. Huang J, Klionsky DJ. 2007. Autophagy and human disease. Cell Cycle 6: 1837-1849.
    Pubmed CrossRef
  15. Yang ZJ, Chee CE, Huang S, Sinicrope FA. 2011. The role of autophagy in cancer: therapeutic implications. Mol. Cancer Ther. 10: 1533-1541.
    Pubmed PMC CrossRef
  16. Hsu Y L, K uo P L, Lin C C . 2004. Acacetin i nhibits the proliferation of Hep G2 by blocking cell cycle progression and inducing apoptosis. Biochem. Pharmacol. 67: 823-829.
    Pubmed CrossRef
  17. Pan MH, L ai C S, Hsu PC, Wang Y J. 2 005. Acacetin induces apoptosis in human gastric carcinoma cells accompanied by activation of caspase cascades and production of reactive oxygen species. J. Agric. Food Chem. 53: 620-630.
    Pubmed CrossRef
  18. Singh RP, Agrawal P, Yim D, Agarwal C, Agarwal R. 2005. Acacetin inhibits cell growth and cell cycle progression, and induces apoptosis in human prostate cancer cells: structure activity relationship with linarin and linarin acetate. Carcinogenesis 26: 845-854.
    Pubmed CrossRef
  19. Shim HY, Park JH, Paik HD, Nah SY, Kim DS, Han YS. 2007. Acacetin-induced apoptosis of human breast cancer MCF-7 cells involves caspase cascade, mitochondria-mediated death signaling and SAPK/JNK1/2-c-Jun activation. Mol. Cells 24: 95-104.
    Pubmed
  20. Watanabe K, Kanno S, Tomizawa A, Yomogida S, Ishikawa M. 2012. Acacetin induces apoptosis in human T cell leukemia Jurkat cells via activation of a caspase cascade. Oncol. Rep. 27: 204-209.
    Pubmed
  21. Han SJ, Kim AK. 2015. Effect of acacetin on the apoptosis induction of HeLa cells. Yakhak Hoeji 59: 17-22.
    CrossRef
  22. Park HS, Jun DY, Han CR, Woo HJ, Kim YH. 2011. Proteasome inhibitor MG132-induced apoptosis via ER stress-mediated apoptotic pathway and its potentiation by protein tyrosine kinase p56lck in human Jurkat T cells. Biochem. Pharmacol. 82: 1110-1125.
    Pubmed CrossRef
  23. Lee JW, Kim YH. 2011. Activation of pro-apoptotic multidomain Bcl-2 family member Bak and mitochondria-dependent caspase cascade are involved in p-coumaric acid-induced apoptosis of Jurkat T cells. J. Life Sci. 21: 1678-1688.
    CrossRef
  24. Paglin S, Hollister T, Delohery T, Hackett N, McMahill M, Sphicas E, et al. 2001. A novel response of cancer cells to radiation involves autophagy and formation of acidic vesicles. Cancer Res. 61: 439-444.
    Pubmed
  25. Okada H, Mak TW. 2004. Pathways of apoptotic and nonapoptotic death in tumor cells. Nat. Rev. Cancer 4: 592-603.
    Pubmed CrossRef
  26. Adams JM, Cory S. 2007. Bcl-2-regulated apoptosis: mechanism and therapeutic potential. Curr. Opin. Immunol. 19: 488-496.
    Pubmed PMC CrossRef
  27. Chipuk JE, Green DR. 2008. How do Bcl-2 proteins induce mitochondrial outer membrane permeabilization? Trends Cell Biol. 18: 157-164.
    Pubmed PMC CrossRef
  28. Czabotar PE, Colman PM, Huang DC. 2009. Bax activation by Bim? Cell Death Differ. 16: 1187-1191.
    Pubmed CrossRef
  29. Tada-Oikawa S, Oikawa S, Kawanishi S. 1998. Role of ultraviolet A-induced oxidative DNA damage in apoptosis via loss of mitochondrial membrane potential and caspase-3 activation. Biochem. Biophys. Res. Commun. 247: 693-696.
    Pubmed CrossRef
  30. Kroemer G, Reed JC. 2000. Mitochondrial control of cell death. Nat. Med. 6: 513-519.
    Pubmed CrossRef
  31. Kroemer G, Galluzzi L, Brenner C. 2007. Mitochondrial membrane permeabilization in cell death. Physiol. Rev. 87:99-163.
    Pubmed CrossRef
  32. Kanzawa T, Germano IM, Komata T, Ito H, Kondo Y, Kondo S. 2004. Role of autophagy in temozolomide-induced cytotoxicity for malignant glioma cells. Cell Death Differ. 11:448-457.
    Pubmed CrossRef
  33. Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD. 1997. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275: 1132-1136.
    Pubmed CrossRef
  34. Yang J, Liu X, Bhalla K, Kim CN, Ibrado AM, Cai J, et al. 1997. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275: 1129-1132.
    Pubmed CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2017; 27(1): 197-205

Published online January 28, 2017 https://doi.org/10.4014/jmb.1610.10055

Copyright © The Korean Society for Microbiology and Biotechnology.

Pharmacologic Inhibition of Autophagy Sensitizes Human Acute Leukemia Jurkat T Cells to Acacetin-Induced Apoptosis

Ji Young Lee 1, Do Youn Jun 1, Ki Yun Kim 1, Eun Ji Ha 1, Mi Hee Woo 2, Jee Youn Ko 3, Young Ho Yun 3, In-Seok Oh 3 and Young Ho Kim 1*

1Laboratory of Immunobiology, School of Life Science and Biotechnology, College of Natural Sciences, Kyungpook National University, Daegu 41566, Republic of Korea, 2College of Pharmacy, Catholic University of Daegu, Gyeongsan 38430, Republic of Korea, 3Upland Crop Breeding Research Division, Department of Southern Area Crop Science, RDA, Miryang 50424, Republic of Korea

Received: October 21, 2016; Accepted: October 31, 2016

Abstract

Exposure of Jurkat T cell clone (J/Neo cells) to acacetin (5,7-dihydroxy-4’-methoxyflavone),
which is present in barnyard millet (Echinochloa esculenta (A. Braun)) grains, caused
cytotoxicity, enhancement of apoptotic sub-G1 rate, Bak activation, loss of mitochondrial
membrane potential (Δψm), activation of caspase-9 and caspase-3, degradation of poly(ADPribose)
polymerase, and FITC-Annexin V-stainable phosphatidylserine exposure on the
external surface of the cytoplasmic membrane without accompanying necrosis. These
apoptotic responses were abrogated in Jurkat T cell clone (J/Bcl-xL) overexpressing Bcl-xL.
Under the same conditions, cellular autophagic responses, including suppression of the AktmTOR
pathway and p62/SQSTM1 down-regulation, were commonly detected in J/Neo and
J/Bcl-xL cells; however, formation of acridine orange-stainable acidic vascular organelles,
LC3-I/II conversion, and Beclin-1 phosphorylation (Ser-15) were detected only in J/Neo cells.
Correspondingly, concomitant treatment with the autophagy inhibitor (3-methyladenine or
LY294002) appeared to enhance acacetin-induced apoptotic responses, such as Bak activation,
Δψm loss, activation of caspase-9 and caspase-3, and apoptotic sub-G1 accumulation. This
indicated that acacetin could induce apoptosis and cytoprotective autophagy in Jurkat T cells
simultaneously. Together, these results demonstrate that acacetin induces not only apoptotic
cell death via activation of Bak, loss of Δψm, and activation of the mitochondrial caspase
cascade, but also cytoprotective autophagy resulting from suppression of the Akt-mTOR
pathway. Furthermore, pharmacologic inhibition of the autophagy pathway augments the
activation of Bak and resultant mitochondrial damage-mediated apoptosis in Jurkat T cells.

Keywords: Acacetin, Bak activation, cytoprotective autophagy, Echinochloa esculenta (A. Braun), Jurkat T cells, mitochondria-dependent apoptosis

References

  1. Mathias S, Holger B. 2007. Mitotic drug targets and the development of novel anti-mitotic anticancer drugs. Drug Resist. Updat. 10: 162-181.
    Pubmed CrossRef
  2. Ricci MS, Zong WX. 2006. Chemotherapeutic approaches for targeting cell death pathways. Oncologist 11: 342-357.
    Pubmed KoreaMed CrossRef
  3. Amaravadi RK, Thompson CB. 2007. The roles of therapyinduced autophagy and necrosis in cancer treatment. Clin. Cancer Res. 13: 7271-7279.
    Pubmed CrossRef
  4. Mansilla S, Llovera L, Portugal J. 2012. Chemotherapeutic targeting of cell death pathways. Anticancer Agents Med. Chem. 12: 226-238.
    Pubmed CrossRef
  5. Dive C, Gregory CD, Phipps DJ, Evans DL, Milner AE, Wyllie AH. 1992. Analysis and discrimination of necrosis and apoptosis (programmed cell death) by multiparameter flow cytometry. Biochim. Biophys. Acta 1133: 275-285.
    CrossRef
  6. Bonfoco E, Krainc D, Ankarcrona M, Nicotera P, Lipton SA. 1995. Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-Daspartate or nitric oxide/superoxide in cortical cell cultures. Proc. Natl. Acad. Sci. USA 92: 7162-7166.
    Pubmed KoreaMed CrossRef
  7. Hannun YA. 1997. Apoptosis and dilemma of cancer chemotherapy. Blood 89: 1845-1853.
    Pubmed
  8. Kaufman SH, Earnshaw WC. 2000. Induction of apoptosis by cancer chemotherapy. Exp. Cell Res. 256: 42-49.
    Pubmed CrossRef
  9. Jun DY, Kim JS, Park HS, Han CR, Fang Z, Woo MH, et al. 2007. Apoptogenic activity of auraptene of Zanthoxylum schinifolium toward human acute leukemia Jurkat T cells is associated with ER stress-mediated caspase-8 activation that stimulates mitochondria-dependent or -independent caspase cascade. Carcinogenesis 28: 1303-1313.
    Pubmed CrossRef
  10. Desagher S, Martinou JC. 2000. Mitochondria as the central control point of apoptosis. Trends Cell Biol. 10: 369-377.
    CrossRef
  11. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA, Yuan J. 2000. Caspase-12 mediates endoplasmic-reticulumspecific apoptosis and cytotoxicity by amyloid-beta. Nature 403: 98-103.
    Pubmed CrossRef
  12. Wallach D, Boldin M, Varfolomeev E, Beyaert R, Vandenabeele P, Fiers W. 1997. Cell death induction by receptors of the THF family: towards a molecular understanding. FEBS Lett. 410: 96-106.
    CrossRef
  13. Degenhardt K, Mathew R, Beaudoin B, Bray K, Anderson D, Chen G, et al. 2006. Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 10: 51-64.
    Pubmed KoreaMed CrossRef
  14. Huang J, Klionsky DJ. 2007. Autophagy and human disease. Cell Cycle 6: 1837-1849.
    Pubmed CrossRef
  15. Yang ZJ, Chee CE, Huang S, Sinicrope FA. 2011. The role of autophagy in cancer: therapeutic implications. Mol. Cancer Ther. 10: 1533-1541.
    Pubmed KoreaMed CrossRef
  16. Hsu Y L, K uo P L, Lin C C . 2004. Acacetin i nhibits the proliferation of Hep G2 by blocking cell cycle progression and inducing apoptosis. Biochem. Pharmacol. 67: 823-829.
    Pubmed CrossRef
  17. Pan MH, L ai C S, Hsu PC, Wang Y J. 2 005. Acacetin induces apoptosis in human gastric carcinoma cells accompanied by activation of caspase cascades and production of reactive oxygen species. J. Agric. Food Chem. 53: 620-630.
    Pubmed CrossRef
  18. Singh RP, Agrawal P, Yim D, Agarwal C, Agarwal R. 2005. Acacetin inhibits cell growth and cell cycle progression, and induces apoptosis in human prostate cancer cells: structure activity relationship with linarin and linarin acetate. Carcinogenesis 26: 845-854.
    Pubmed CrossRef
  19. Shim HY, Park JH, Paik HD, Nah SY, Kim DS, Han YS. 2007. Acacetin-induced apoptosis of human breast cancer MCF-7 cells involves caspase cascade, mitochondria-mediated death signaling and SAPK/JNK1/2-c-Jun activation. Mol. Cells 24: 95-104.
    Pubmed
  20. Watanabe K, Kanno S, Tomizawa A, Yomogida S, Ishikawa M. 2012. Acacetin induces apoptosis in human T cell leukemia Jurkat cells via activation of a caspase cascade. Oncol. Rep. 27: 204-209.
    Pubmed
  21. Han SJ, Kim AK. 2015. Effect of acacetin on the apoptosis induction of HeLa cells. Yakhak Hoeji 59: 17-22.
    CrossRef
  22. Park HS, Jun DY, Han CR, Woo HJ, Kim YH. 2011. Proteasome inhibitor MG132-induced apoptosis via ER stress-mediated apoptotic pathway and its potentiation by protein tyrosine kinase p56lck in human Jurkat T cells. Biochem. Pharmacol. 82: 1110-1125.
    Pubmed CrossRef
  23. Lee JW, Kim YH. 2011. Activation of pro-apoptotic multidomain Bcl-2 family member Bak and mitochondria-dependent caspase cascade are involved in p-coumaric acid-induced apoptosis of Jurkat T cells. J. Life Sci. 21: 1678-1688.
    CrossRef
  24. Paglin S, Hollister T, Delohery T, Hackett N, McMahill M, Sphicas E, et al. 2001. A novel response of cancer cells to radiation involves autophagy and formation of acidic vesicles. Cancer Res. 61: 439-444.
    Pubmed
  25. Okada H, Mak TW. 2004. Pathways of apoptotic and nonapoptotic death in tumor cells. Nat. Rev. Cancer 4: 592-603.
    Pubmed CrossRef
  26. Adams JM, Cory S. 2007. Bcl-2-regulated apoptosis: mechanism and therapeutic potential. Curr. Opin. Immunol. 19: 488-496.
    Pubmed KoreaMed CrossRef
  27. Chipuk JE, Green DR. 2008. How do Bcl-2 proteins induce mitochondrial outer membrane permeabilization? Trends Cell Biol. 18: 157-164.
    Pubmed KoreaMed CrossRef
  28. Czabotar PE, Colman PM, Huang DC. 2009. Bax activation by Bim? Cell Death Differ. 16: 1187-1191.
    Pubmed CrossRef
  29. Tada-Oikawa S, Oikawa S, Kawanishi S. 1998. Role of ultraviolet A-induced oxidative DNA damage in apoptosis via loss of mitochondrial membrane potential and caspase-3 activation. Biochem. Biophys. Res. Commun. 247: 693-696.
    Pubmed CrossRef
  30. Kroemer G, Reed JC. 2000. Mitochondrial control of cell death. Nat. Med. 6: 513-519.
    Pubmed CrossRef
  31. Kroemer G, Galluzzi L, Brenner C. 2007. Mitochondrial membrane permeabilization in cell death. Physiol. Rev. 87:99-163.
    Pubmed CrossRef
  32. Kanzawa T, Germano IM, Komata T, Ito H, Kondo Y, Kondo S. 2004. Role of autophagy in temozolomide-induced cytotoxicity for malignant glioma cells. Cell Death Differ. 11:448-457.
    Pubmed CrossRef
  33. Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD. 1997. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275: 1132-1136.
    Pubmed CrossRef
  34. Yang J, Liu X, Bhalla K, Kim CN, Ibrado AM, Cai J, et al. 1997. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275: 1129-1132.
    Pubmed CrossRef