Induction of endoplasmic reticulum stress-mediated apoptosis and non-canonical autophagy by luteolin in NCI-H460 lung carcinoma cells

Food and Chemical Toxicology

Volumn 56, Issue , 2013, Pages 100-109

  Park, Shin Hyung ^a   Park, Hyun Soo ^a   Lee, Jun Hyuk ^b   Chi, Gyoo Yong ^a   Kim, Gi Young ^c   Moon, Sung Kwon ^d   Chang, Young Chae ^e   Hyun, Jin Won ^c   Kim, Wun Jae ^f   Choi, Yung Hyun ^a  

^a Dong Eui University   (South Korea)

^b Korea Intellectual Property Office   (South Korea)

^c Jeju National University   (South Korea)

^d Chung Ang University   (South Korea)

^e Catholic University of Daegu   (South Korea)

^f Chungbuk National University College of Medicine   (South Korea)

Author keywords

Apoptosis; Autophagy; ER stress; Luteolin

Indexed keywords

BAFILOMYCIN A1; BECLIN 1; BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; CASPASE; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INITIATION FACTOR 2ALPHA; LIGHT CHAIN 3 II PROTEIN; LUTEOLIN; MICROTUBULE ASSOCIATED PROTEIN; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGY; CANCER CELL CULTURE; CANCER INHIBITION; CARCINOMA CELL; CELL STRAIN NCI H460; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; HUMAN; HUMAN CELL; LUNG CARCINOMA; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA INTERFERENCE;

AMINO ACID CHLOROMETHYL KETONES; ANTINEOPLASTIC AGENTS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; CCAAT-ENHANCER-BINDING PROTEINS; CELL LINE, TUMOR; DNA FRAGMENTATION; ENDOPLASMIC RETICULUM STRESS; EUKARYOTIC INITIATION FACTOR-2; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LUNG NEOPLASMS; LUTEOLIN; MACROLIDES; MEMBRANE PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; RNA, SMALL INTERFERING;

EID: 84874775471     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2013.02.022     Document Type: Article

References (76)

1. Bagli E., Stefaniotou M., Morbidelli L., Ziche M., Psillas K., Murphy C., Fotsis T. Luteolin inhibits vascular endothelial growth factor-induced angiogenesis; inhibition of endothelial cell survival and proliferation by targeting phosphatidylinositol 3'-kinase activity. Cancer Res. 2004, 64:7936-7946.
2. Birt D.F., Hendrich S., Wang W. Dietary agents in cancer prevention: flavonoids and isoflavonoids. Pharmacol. Ther. 2001, 90:157-177.
3. Cai X., Ye T., Liu C., Lu W., Lu M., Zhang J., Wang M., Cao P. Luteolin induced G2 phase cell cycle arrest and apoptosis on non-small cell lung cancer cells. Toxicol. In Vitro 2011, 25:1385-1391.
4. Chen Q., Liu S., Chen J., Zhang Q., Lin S., Chen Z., Jiang J. Luteolin induces mitochondria-dependent apoptosis in human lung adenocarcinoma cell. Nat. Prod. Commun. 2012, 7:29-32.
5. Choi A.Y., Choi J.H., Yoon H., Hwang K.Y., Noh M.H., Choe W., Yoon K.S., Ha J., Yeo E.J., Kang I. Luteolin induces apoptosis through endoplasmic reticulum stress and mitochondrial dysfunction in Neuro-2a mouse neuroblastoma cells. Eur. J. Pharmacol. 2011, 668:115-126.
6. Cory S., Adams J.M. The Bcl2 family: regulators of the cellular life-of-death switch. Nat. Rev. Cancer 2002, 2:647-656.
7. Esposti M.D. The roles of Bid. Apoptosis 2002, 7:433-440.
8. Fischer H., Koenig U., Eckhart L., Tschachler E. Human caspase 12 has acquired deleterious mutations. Biochem. Biophys. Res. Commun. 2002, 293:722-726.
9. Fotsis T., Pepper M.S., Aktas E., Breit S., Rasku S., Adlercreutz H., Wahala K., Montesano R., Schweigerer L. Flavonoids, dietary-derived inhibitors of cell proliferation and in vitro angiogenesis. Cancer Res. 1997, 57:2916-2921.
10. Gao P., Bauvy C., Souquère S., Tonelli G., Liu L., Zhu Y., Qiao Z., Bakula D., Proikas-Cezanne T., Pierron G., Codogno P., Chen Q., Mehrpour M. The Bcl-2 homology domain 3 mimetic gossypol induces both Beclin 1-dependent and Beclin 1-independent cytoprotective autophagy in cancer cells. J. Biol. Chem. 2010, 285:25570-25581.
11. Gill C., Dowling C., O'Neill A.J., Watson R.W. Effects of cIAP-1, cIAP-2 and XIAP triple knockdown on prostate cancer cell susceptibility to apoptosis, cell survival and proliferation. Mol. Cancer 2009, 8:39.
12. Gozuacik D., Bialik S., Raveh T., Mitou G., Shohat G., Sabanay H., Mizushima N., Yoshimori T., Kimchi A. DAP-kinase is a mediator of endoplasmic reticulum stress-induced caspase activation and autophagic cell death. Cell Death Differ. 2008, 15:1875-1886.
13. Gozuacik D., Kimchi A. Autophagy as a cell death and tumor suppressor mechanism. Oncogene 2004, 23:2891-2906.
14. Harding H.P., Zhang Y., Bertolotti A., Zeng H., Ron D. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol. Cell 2000, 5:897-904.
15. Horinaka M., Yoshida T., Shiraishi T., Nakata S., Wakada M., Nakanishi R., Nishino H., Matsui H., Sakai T. Luteolin induces apoptosis via death receptor 5 upregulation in human malignant tumor cells. Oncogene 2005, 24:7180-7189.
16. Huang H.C., Syu K.Y., Lin J.K. Chemical composition of Solanum nigrum Linn extract and induction of autophagy by leaf water extract and its major flavonoids in AU565 breast cancer cells. J. Agric. Food Chem. 2010, 58:8699-8708.
17. Huang Y.T., Hwang J.J., Lee P.P., Ke F.C., Huang J.H., Huang C.J., Kandaswami C., Middleton E., Lee M.T. Effects of luteolin and quercetin, inhibitors of tyrosine kinase, on cell growth and metastasis associated properties in A431 cells overexpressing epidermal growth factor receptor. Br. J. Pharmacol. 1999, 128:999-1010.
18. Igney F.H., Krammer P.H. Death and anti-death: tumour resistance to apoptosis. Nat. Rev. Cancer 2002, 2:277-288.
19. Ju W., Wang X., Shi H., Chen W., Belinsky S.A., Lin Y. A critical role of luteolin-induced reactive oxygen species in blockage of tumor necrosis factor-activated nuclear factor-kappaB pathway and sensitization of apoptosis in lung cancer cells. Mol. Pharmacol. 2007, 71:1381-1388.
20. Kabeya Y., Mizushima N., Ueno T., Yamamoto A., Kirisako T., Noda T., Kominami E., Ohsumi Y., Yoshimori T. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 2000, 19:5720-5728.
21. Kanzawa T., Germano I.M., Komata T., Ito H., Kondo Y., Kondo S. Role of autophagy in temozolomide-induced cytotoxicity for malignant glioma cells. Cell Death Differ. 2004, 11:448-457.
22. Kaufmann S.H., Desnoyers S., Ottaviano Y., Davidson N.E., Poirier G.G. Specific proteolytic cleavage of poly (ADP-ribose) polymerase: an early marker of chemotherapy-induced apoptosis. Cancer Res. 1993, 53:3976-3985.
23. Kauntz H., Bousserouel S., Gossé F., Raul F. Silibinin triggers apoptotic signaling pathways and autophagic survival response in human colon adenocarcinoma cells and their derived metastatic cells. Apoptosis 2011, 16:1042-1053.
24. Kim D.K., Yang J.S., Maiti K., Hwang J.I., Kim K., Seen D., Ahn Y., Lee C., Kang B.C., Kwon H.B., Cheon J., Seong J.Y. A gonadotropin-releasing hormone-II antagonist induces autophagy of prostate cancer cells. Cancer Res. 2009, 69:923-931.
25. Kim J.H., Lee E.O., Lee H.J., Ku J.S., Lee M.H., Yang D.C., Kim S.H. Caspase activation and extracellular signal-regulated kinase/Akt inhibition were involved in luteolin-induced apoptosis in Lewis lung carcinoma cells. Ann. N. Y. Acad. Sci. 2007, 1095:598-611.
26. Klionsky D.J. The correct way to monitor autophagy in higher eukaryotes. Autophagy 2005, 1:65.
27. Knowles L.M., Zigrossi D.A., Tauber R.A., Hightower C., Milner J.A. Flavonoids suppress androgenin dependent human prostate tumor proliferation. Nutr. Cancer 2000, 38:116-120.
28. Ko H., Kim Y.J., Amor E.C., Lee J.W., Kim H.C., Kim H.J., Yang H.O. Induction of autophagy by dimethyl cardamonin is associated with proliferative arrest in human colorectal carcinoma HCT116 and LOVO cells. J. Cell. Biochem. 2011, 112:2471-2479.
29. Leung H.W., Wu C.H., Lin C.H., Lee H.Z. Luteolin induced DNA damage leading to human lung squamous carcinoma CH27 cell apoptosis. Eur. J. Pharmacol. 2005, 508:77-83.
30. Li H., Wang P., Sun Q., Ding W.X., Yin X.M., Sobol R.W., Stolz D.B., Yu J., Zhang L. Following cytochrome c release, autophagy is inhibited during chemotherapy-induced apoptosis by caspase 8-mediated cleavage of Beclin 1. Cancer Res. 2011, 71:3625-3634.
31. Li H., Wang P., Yu J., Zhang L. Cleaving Beclin 1 to suppress autophagy in chemotherapy-induced apoptosis. Autophagy 2011, 7:1239-1241.
32. Li J., Ni M., Lee B., Barron E., Hinton D.R., Lee A.S. The unfolded protein response regulator GRP78/BiP is required for endoplasmic reticulum integrity and stress-induced autophagy in mammalian cells. Cell Death Differ. 2008, 15:1460-1471.
33. Lim D.Y., Jeong Y., Tyner A.L., Park J.H. Induction of cell cycle arrest and apoptosis in HT-29 human colon cancer cells by the dietary compound luteolin. Am. J. Physiol. Gastrointest. Liver Physiol. 2007, 292:G66-75.
34. Lin Y., Shi R., Wang X., Shen H.M. Luteolin, a flavonoid with potential for cancer prevention and therapy. Curr. Cancer Drug Targets 2008, 8:634-646.
35. Lockshin R.A., Zakeri Z. Caspase-independent cell deaths. Curr. Opin. Cell Biol. 2002, 14:727-733.
36. Malhotra J.D., Kaufman R.J. The endoplasmic reticulum and the unfolded protein response. Semin. Cell Dev. Biol. 2007, 18:716-731.
37. McCullough K.D., Martindale J.L., Klotz L.O., Aw T.Y., Holbrook N.J. Gadd153 sensitizes cells to endoplasmic reticulum stress by downregulating Bc12 and perturbing the cellular redox state. Mol. Cell. Biol. 2001, 21:1249-1259.
38. Mencherini T., Picerno P., Scesa C., Aquino R. Triterpene, antioxidant, and antimicrobial compounds from Melissa officinalis. J. Nat. Prod. 2007, 70:1889-1894.
39. Miean K.H., Mohamed S. Flavonoid (myricetin, quercetin, kaempferol, luteolin, and apigenin) content of edible tropical plants. J. Agric. Food Chem. 2001, 49:3106-3112.
40. Milani M., Rzymski T., Mellor H.R., Pike L., Bottini A., Generali D., Harris A.L. The role of ATF4 stabilization and autophagy in resistance of breast cancer cells treated with bortezomib. Cancer Res. 2009, 69:4415-4423.
41. Mizushima N., Levine B., Cuervo A.M., Klionsky D.J. Autophagy fights disease through cellular self-digestion. Nature 2008, 451:1069-1075.
42. Mizushima N., Yoshimori T. How to interpret LC3 immunoblotting. Autophagy 2007, 3:542-545.
43. Moretti L., Cha Y.I., Niermann K.J., Lu B. Switch between apoptosis and autophagy: radiation-induced endoplasmic reticulum stress?. Cell Cycle 2007, 6:793-798.
44. Nakagawa T., Zhu H., Morishima N., Li E., Xu J., Yankner B.A., Yuan J. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 2000, 403:98-103.
45. Neuhouser M.L. Dietary flavonoids and cancer risk: evidence from human population studies. Nutr. Cancer 2004, 50:1-7.
46. Nishitoh H., Matsuzawa A., Tobiume K., Saegusa K., Takeda K., Inoue K., Hori S., Kakizuka A., Ichijo H. ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev. 2002, 16:1345-1355.
47. Ogata M., Hino S., Saito A., Morikawa K., Kondo S., Kanemoto S., Murakami T., Taniguchi M., Tanii I., Yoshinaga K., Shiosaka S., Hammarback J.A., Urano F., Imaizumi K. Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol. Cell. Biol. 2006, 26:9220-9231.
48. Pattingre S., Tassa A., Qu X., Garuti R., Liang X.H., Mizushima N., Packer M., Schneider M.D., Levine B. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 2005, 122:927-939.
49. Pyo J.O., Nah J., Jung Y.K. Molecules and their functions in autophagy. Exp. Mol. Med. 2012, 44:73-80.
50. Quan W., Lim Y.M., Lee M.S. Role of autophagy in diabetes and endoplasmic reticulum stress of pancreatic β-cells. Exp. Mol. Med. 2012, 44:81-88.
51. Ron D., Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 2007, 8:519-529.
52. Rubinsztein D.C., Cuervo A.M., Ravikumar B., Sarkar S., Korolchuk V., Kaushik S., Klionsky D.J. In search of an "autophagomometer". Autophagy 2009, 5:585-589.
53. Sakahira H., Enari M., Nahata S. Cleavage of CAD inhibitor in CAD activation and DNA degradation during apoptosis. Nature 1998, 391:96-99.
54. Sakaki K., Wu J., Kaufman R.J. Protein kinase C theta is required for autophagy in response to stress in the endoplasmic reticulum. J. Biol. Chem. 2008, 283:15370-15380.
55. Scarlatti F., Maffei R., Beau I., Codogno P., Ghidoni R. Role of non-canonical Beclin 1-independent autophagy in cell death induced by resveratrol in human breast cancer cells. Cell Death Differ. 2008, 15:1318-1329.
56. Schroder M. Endoplasmic reticulum stress responses. Cell. Mol. Life Sci. 2008, 65:862-894.
57. Schröder M., Kaufman R.J. The mammalian unfolded protein response. Annu. Rev. Biochem. 2005, 74:739-789.
58. Selvendiran K., Koga H., Ueno T., Yoshida T., Maeyama M., Torimura T., Yano H., Kojiro M., Sata M. Luteolin promotes degradation in signal transducer and activator of transcription 3 in human hepatoma cells: an implication for the antitumor potential of flavonoids. Cancer Res. 2006, 66:4826-4834.
59. Shimizu S., Kanaseki T., Mizushima N., Mizuta T., Arakawa-Kobayashi S., Thompson C.B., Tsujimoto Y. Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nat. Cell Biol. 2004, 6:1221-1228.
60. Strasser A., O'Connor L., Dixit V.M. Apoptosis signaling. Annu. Rev. Biochem. 2000, 69:217-245.
61. Suh Y., Afaq F., Khan N., Johnson J.J., Khusro F.H., Mukhtar H. Fisetin induces autophagic cell death through suppression of mTOR signaling pathway in prostate cancer cells. Carcinogenesis 2010, 31:1424-1433.
62. Tak J.K., Lee J.H., Park J.W. Resveratrol and piperine enhance radiosensitivity of tumor cells. BMB Rep. 2012, 45:242-246.
63. Tanida I., Minematsu-Ikeguchi N., Ueno T., Kominami E. Lysosomal turnover, but not a cellular level, of endogenous LC3 is a marker for autophagy just by observing the increased LC3II expression. Autophagy 2005, 1:84-91.
64. Urano F., Wang X., Bertolotti A., Zhang Y., Chung P., Harding H.P., Ron D. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 2000, 287:664-666.
65. Vandenabeele P., Vanden Berghe T., Festjens N. Caspase inhibitors promote alternative cell death pathways. Sci. STKE 2006, pe44.
66. Wang K., Liu R., Li J., Mao J., Lei Y., Wu J., Zeng J., Zhang T., Wu H., Chen L., Huang C., Wei Y. Quercetin induces protective autophagy in gastric cancer cells: involvement of Akt-mTOR- and hypoxia-induced factor 1α-mediated signaling. Autophagy 2011, 7:966-978.
67. Wang X.Z., Lawson B., Brewer J.W., Zinszner H., Sanjay A., Mi L.J., Boorstein R., Kreibich G., Hendershot L.M., Ron D. Signals from the stressed endoplasmic reticulum induce C/EBP-homologous protein (CHOP/GADD153). Mol. Cell. Biol. 1996, 16:4273-4280.
68. Wirawan E., Vande Walle L., Kersse K., Cornelis S., Claerhout S., Vanoverberghe I., Roelandt R., De Rycke R., Verspurten J., Declercq W., Agostinis P., Vanden Berghe T., Lippens S., Vandenabeele P. Caspase-mediated cleavage of Beclin-1 inactivates Beclin-1-induced autophagy and enhances apoptosis by promoting the release of proapoptotic factors from mitochondria. Cell Death Dis. 2010, 1:e18.
69. Wolf B.B., Green D.R. Suicidal tendencies: apoptotic cell death by caspase family proteinases. J. Biol. Chem. 1999, 274:20049-20052.
70. Wu B., Zhang Q., Shen W., Zhu J. Anti-proliferative and chemosensitizing effects of luteolin on human gastric cancer AGS cell line. Mol. Cell. Biochem. 2008, 313:125-132.
71. Yan J., Wang Q., Zheng X., Sun H., Zhou Y., Li D., Lin Y., Wang X. Luteolin enhances TNF-related apoptosis-inducing ligand's anticancer activity in a lung cancer xenograft mouse model. Biochem. Biophys. Res. Commun. 2012, 417:842-846.
72. Yano K., Hattori M., Moriyasu Y. A novel type of autophagy occurs together with vacuole genesis in miniprotoplasts prepared from tobacco culture cells. Autophagy 2007, 3:215-221.
73. Yorimitsu T., Nair U., Yang Z., Klionsky D.J. Endoplasmic reticulum stress triggers autophagy. J. Biol. Chem. 2006, 281:30299-30304.
74. Yoshimori T. Autophagy: a regulated bulk degradation process inside cells. Biochem. Biophys. Res. Commun. 2004, 313:453-458.
75. Zhu Y., Zhao L., Liu L., Gao P., Tian W., Wang X., Jin H., Xu H., Chen Q. Beclin 1 cleavage by caspase-3 inactivates autophagy and promotes apoptosis. Protein Cell 2010, 1:468-477.
76. Zinszner H., Kuroda M., Wang X., Batchvarova N., Lightfoot R.T., Remotti H., Stevens J.L., Ron D. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev. 1998, 12:982-995.