Gypenoside L, Isolated from Gynostemma pentaphyllum, Induces Cytoplasmic Vacuolation Death in Hepatocellular Carcinoma Cells through Reactive-Oxygen-Species-Mediated Unfolded Protein Response

Journal of Agricultural and Food Chemistry

Volumn 64, Issue 8, 2016, Pages 1702-1711

  Zheng, Kai ^a,c   Liao, Chenghui ^a   Li, Yan ^d   Fan, Xinmin ^a   Fan, Long ^a   Xu, Hong ^b   Kang, Qiangrong ^a   Zeng, Yong ^d   Wu, Xuli ^a   Wu, Haiqiang ^a   Liu, Lizhong ^a   Xiao, Xiaohua ^b   Zhang, Jian ^a   Wang, Yifei ^c   He, Zhendan ^a  

^a Shenzhen University   (China)

^b SHENZHEN UNIVERSITY   (China)

^c JINAN UNIVERSITY   (China)

^d KUNMING MEDICAL UNIVERSITY   (China)

Author keywords

calcium release; gypenoside L; ROS; unfolded protein response; vacuolation death

Indexed keywords

BIOSYNTHESIS; CALCIUM; CELL DEATH; CELLS; CYTOLOGY; GYPSUM; PROTEINS;

CALCIUM RELEASE; GYNOSTEMMA PENTAPHYLLUM; GYPENOSIDE L; HEPATOCELLULAR CARCINOMA CELL; HUMAN HEPATOCELLULAR CARCINOMA (HCC); REACTIVE OXYGEN SPECIES; UNFOLDED PROTEIN RESPONSE; VACUOLATION DEATH;

CELL SIGNALING;

GYPENOSIDE; PLANT EXTRACT; REACTIVE OXYGEN METABOLITE;

APOPTOSIS; CARCINOMA, HEPATOCELLULAR; CELL VACUOLE; CHEMISTRY; DRUG EFFECTS; GYNOSTEMMA; HUMAN; ISOLATION AND PURIFICATION; LIVER NEOPLASMS; METABOLISM; PATHOPHYSIOLOGY; TUMOR CELL LINE; UNFOLDED PROTEIN RESPONSE;

APOPTOSIS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; GYNOSTEMMA; HUMANS; LIVER NEOPLASMS; PLANT EXTRACTS; REACTIVE OXYGEN SPECIES; UNFOLDED PROTEIN RESPONSE; VACUOLES;

EID: 84960153577     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.5b05668     Document Type: Article

References (43)

1. Siegel, R.; Naishadham, D.; Jemal, A. Cancer statistics, 2012 Ca-Cancer J. Clin. 2012, 62, 10-29 10.3322/caac.20138
2. Attwa, M. H.; El-Etreby, S. A. Guide for diagnosis and treatment of hepatocellular carcinoma World J. Hepatol. 2015, 7, 1632-1651 10.4254/wjh.v7.i12.1632
3. Chen, C.; Wang, G. Mechanisms of hepatocellular carcinoma and challenges and opportunities for molecular targeted therapy World J. Hepatol. 2015, 7, 1964-1970 10.4254/wjh.v7.i15.1964
4. Mohammad, R. M.; Muqbil, I.; Lowe, L.; Yedjou, C.; Hsu, H. Y.; Lin, L. T.; Siegelin, M. D.; Fimognari, C.; Kumar, N. B.; Dou, Q. P.; Yang, H.; Samadi, A. K.; Russo, G. L.; Spagnuolo, C.; Ray, S. K.; Chakrabarti, M.; Morre, J. D.; Coley, H. M.; Honoki, K.; Fujii, H.; Georgakilas, A. G.; Amedei, A.; Niccolai, E.; Amin, A.; Ashraf, S. S.; Helferich, W. G.; Yang, X.; Boosani, C. S.; Guha, G.; Bhakta, D.; Ciriolo, M. R.; Aquilano, K.; Chen, S.; Mohammed, S. I.; Keith, W. N.; Bilsland, A.; Halicka, D.; Nowsheen, S.; Azmi, A. S. Broad targeting of resistance to apoptosis in cancer Semin. Cancer Biol. 2015, 35, S78-S103 10.1016/j.semcancer.2015.03.001
5. Chen, M. C.; Lee, N. H.; Hsu, H. H.; Ho, T. J.; Tu, C. C.; Hsieh, D. J.; Lin, Y. M.; Chen, L. M.; Kuo, W. W.; Huang, C. Y. Thymoquinone induces caspase-independent, autophagic cell death in CPT-11-resistant lovo colon cancer via mitochondrial dysfunction and activation of JNK and p38 J. Agric. Food Chem. 2015, 63, 1540-1546 10.1021/jf5054063
6. Chao, A. C.; Hsu, Y. L.; Liu, C. K.; Kuo, P. L. α-Mangostin, a dietary xanthone, induces autophagic cell death by activating the AMP-activated protein kinase pathway in glioblastoma cells J. Agric. Food Chem. 2011, 59, 2086-2096 10.1021/jf1042757
7. Hung, J. Y.; Hsu, Y. L.; Li, C. T.; Ko, Y. C.; Ni, W. C.; Huang, M. S.; Kuo, P. L. 6-Shogaol, an active constituent of dietary ginger, induces autophagy by inhibiting the AKT/mTOR pathway in human non-small cell lung cancer A549 cells J. Agric. Food Chem. 2009, 57, 9809-9816 10.1021/jf902315e
8. Feng, R.; Wang, S. Y.; Shi, Y. H.; Fan, J.; Yin, X. M. Delphinidin induces necrosis in hepatocellular carcinoma cells in the presence of 3-methyladenine, an autophagy inhibitor J. Agric. Food Chem. 2010, 58, 3957-3964 10.1021/jf9025458
9. Weerasinghe, P.; Buja, L. M. Oncosis: an important non-apoptotic mode of cell death Exp. Mol. Pathol. 2012, 93, 302-308 10.1016/j.yexmp.2012.09.018
10. Su, Z.; Yang, Z.; Xu, Y.; Chen, Y.; Yu, Q. Apoptosis, autophagy, necroptosis, and cancer metastasis Mol. Cancer 2015, 14, 48 10.1186/s12943-015-0321-5
11. Overholtzer, M.; Mailleux, A. A.; Mouneimne, G.; Normand, G.; Schnitt, S. J.; King, R. W.; Cibas, E. S.; Brugge, J. S. A nonapoptotic cell death process, entosis, that occurs by cell-in-cell invasion Cell 2007, 131, 966-979 10.1016/j.cell.2007.10.040
12. Sperandio, S.; Poksay, K.; de Belle, I.; Lafuente, M. J.; Liu, B.; Nasir, J.; Bredesen, D. E. Paraptosis: mediation by MAP kinases and inhibition by AIP-1/Alix Cell Death Differ. 2004, 11, 1066-1075 10.1038/sj.cdd.4401465
13. Henics, T.; Wheatley, D. N. Cytoplasmic vacuolation, adaptation and cell death: a view on new perspectives and features Biol. Cell 1999, 91, 485-498 10.1016/S0248-4900(00)88205-2
14. Kar, R.; Singha, P. K.; Venkatachalam, M. A.; Saikumar, P. A novel role for MAP1 LC3 in nonautophagic cytoplasmic vacuolation death of cancer cells Oncogene 2009, 28, 2556-2568 10.1038/onc.2009.118
15. Wasik, A. M.; Almestrand, S.; Wang, X.; Hultenby, K.; Dackland, Å.L.; Andersson, P.; Kimby, E.; Christensson, B.; Sander, B. WIN55,212-2 induces cytoplasmic vacuolation in apoptosis-resistant MCL cells Cell Death Dis. 2011, 2, e225 10.1038/cddis.2011.106
16. Singha, P. K.; Pandeswara, S.; Venkatachalam, M. A.; Saikumar, P. Manumycin A inhibits triple-negative breast cancer growth through LC3-mediated cytoplasmic vacuolation death Cell Death Dis. 2013, 4, e457 10.1038/cddis.2012.192
17. Lee, W. J.; Chien, M. H.; Chow, J. M.; Chang, J. L.; Wen, Y. C.; Lin, Y. W.; Cheng, C. W.; Lai, G. M.; Hsiao, M.; Lee, L. M. Nonautophagic cytoplasmic vacuolation death induction in human PC-3M prostate cancer by curcumin through reactive oxygen species -mediated endoplasmic reticulum stress Sci. Rep. 2015, 5, 10420 10.1038/srep10420
18. Shi, L.; Pi, Y.; Luo, C.; Zhang, C.; Tan, D.; Meng, X. In vitro inhibitory activities of six gypenosides on human liver cancer cell line HepG2 and possible role of HIF-1α pathway in them Chem.-Biol. Interact. 2015, 238, 48-54 10.1016/j.cbi.2015.06.004
19. Liu, J. S.; Chiang, T. H.; Wang, J. S.; Lin, L. J.; Chao, W. C.; Inbaraj, B. S.; Lu, J. F.; Chen, B. H. Induction of p53-independent growth inhibition in lung carcinoma cell A549 by gypenosides J. Cell Mol. Med. 2015, 19, 1697-1709 10.1111/jcmm.12546
20. Yan, H.; Wang, X.; Niu, J.; Wang, Y.; Wang, P.; Liu, Q. Anti-cancer effect and the underlying mechanisms of gypenosides on human colorectal cancer SW-480 cells PLoS One 2014, 9, e95609 10.1371/journal.pone.0095609
21. Cheng, T. C.; Lu, J. F.; Wang, J. S.; Lin, L. J.; Kuo, H. I.; Chen, B. H. Antiproliferation effect and apoptosis mechanism of prostate cancer cell PC-3 by flavonoids and saponins prepared from Gynostemma pentaphyllum J. Agric. Food Chem. 2011, 59, 11319-11329 10.1021/jf2018758
22. Xie, Z. H.; Liu, W.; Huang, H.; Slavin, M.; Zhao, Y.; Whent, M.; Blackford, J.; Lutterodt, H.; Zhou, H. P.; Chen, P.; Wang, T. T. Y.; Wang, S.; Yu, L. Chemical Composition of Five Commercial Gynostemma pentaphyllum Samples and Their Radical Scavenging, Antiproliferative, and Anti-inflammatory Properties J. Agric. Food Chem. 2010, 58, 11243-11249 10.1021/jf1026372
23. Piao, X. L.; Wu, Q.; Yang, J.; Park, S. Y.; Chen, D. J.; Liu, H. M. Dammarane-type saponins from heat-processed Gynostemma pentaphyllum show fortified activity against A549 cells Arch. Pharmacal Res. 2013, 36, 874-879 10.1007/s12272-013-0086-6
24. Nguyen, P. H.; Gauhar, R.; Hwang, S. L.; Dao, T. T.; Park, D. C.; Kim, J. E.; Song, H.; Huh, T. L.; Oh, W. K. New dammarane-type glucosides as potential activators of AMP-activated protein kinase (AMPK) from Gynostemma pentaphyllum Bioorg. Med. Chem. 2011, 19, 6254-6260 10.1016/j.bmc.2011.09.013
25. Wu, Q.; Jang, M.; Piao, X. L. Determination by UPLC-MS of four dammarane-type saponins from heat-processed Gynostemma pentaphyllum Biosci., Biotechnol., Biochem. 2014, 78, 311-316 10.1080/09168451.2014.882751
26. Ron, D.; Bertolotti, A.; Zhang, Y.; Hendershot, L. M.; Harding, H. P. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response Nat. Cell Biol. 2000, 2, 326-332 10.1038/35014014
27. Mimnaugh, E. G.; Xu, W.; Vos, M.; Yuan, X.; Isaacs, J. S.; Bisht, K. S.; Gius, D.; Neckers, L. Simultaneous inhibition of hsp 90 and the proteasome promotes protein ubiquitination, causes endoplasmic reticulum-derived cytosolic vacuolization, and enhances antitumor activity Mol. Cancer Ther. 2004, 3, 551-566
28. Mimnaugh, E. G.; Xu, W.; Vos, M.; Yuan, X.; Neckers, L. Endoplasmic reticulum vacuolization and valosincontaining protein relocalization result from simultaneous hsp90 inhibition by geldanamycin and proteasome inhibition by velcade Mol. Cancer Res. 2006, 4, 667-681 10.1158/1541-7786.MCR-06-0019
29. Avivar-Valderas, A.; Salas, E.; Bobrovnikova-Marjon, E.; Diehl, J. A.; Nagi, C.; Debnath, J.; Aguirre-Ghiso, J. A. PERK integrates autophagy and oxidative stress responses to promote survival during extracellular matrix detachment Mol. Cell. Biol. 2011, 31, 3616-3629 10.1128/MCB.05164-11
30. Verfaillie, T.; Rubio, N.; Garg, A. D.; Bultynck, G.; Rizzuto, R.; Decuypere, J. P.; Piette, J.; Linehan, C.; Gupta, S.; Samali, A.; Agostinis, P. PERK is required at the ER-mitochondrial contact sites to convey apoptosis after ROS-based ER stress Cell Death Differ. 2012, 19, 1880-1891 10.1038/cdd.2012.74
31. Liu, Z. W.; Zhu, H. T.; Chen, K. L.; Dong, X.; Wei, J.; Qiu, C.; Xue, J. H. Protein kinase RNA-like endoplasmic reticulum kinase (PERK) signaling pathway plays a major role in reactive oxygen species (ROS)-mediated endoplasmic reticulum stress-induced apoptosis in diabetic cardiomyopathy Cardiovasc. Diabetol. 2013, 12, 158 10.1186/1475-2840-12-158
32. He, C.; Li, B.; Song, W.; Ding, Z.; Wang, S.; Shan, Y. Sulforaphane attenuates homocysteine-induced endoplasmic reticulum stress through Nrf-2-driven enzymes in immortalized human hepatocytes J. Agric. Food Chem. 2014, 62, 7477-7485 10.1021/jf501944u
33. Zhivotovsky, B.; Orrenius, S. Calcium and cell death mechanisms: a perspective from the cell death community Cell Calcium 2011, 50, 211-221 10.1016/j.ceca.2011.03.003
34. Hakimuddin, F.; Paliyath, G.; Meckling, K. Treatment of mcf-7 breast cancer cells with a red grape wine polyphenol fraction results in disruption of calcium homeostasis and cell cycle arrest causing selective cytotoxicity J. Agric. Food Chem. 2006, 54, 7912-7923 10.1021/jf060834m
35. 2+ from the endoplasmic reticulum and its subsequent influx into mitochondria trigger celastrol-induced paraptosis in cancer cells Oncotarget 2014, 5, 6816-6831 10.18632/oncotarget.2256
36. Jeong, S. A.; Kim, I. Y.; Lee, A. R.; Yoon, M. J.; Cho, H.; Lee, J. S.; Choi, K. S. Ca2+ influx-mediated dilation of the endoplasmic reticulum and c-FLIPL downregulation trigger CDDO-Me-induced apoptosis in breast cancer cells Oncotarget 2015, 6, 21173-21192 10.18632/oncotarget.4065
37. Yoon, M. J.; Kim, E. H.; Kwon, T. K.; Park, S. A.; Choi, K. S. Simultaneous mitochondrial Ca(2+) overload and proteasomal inhibition are responsible for the induction of paraptosis in malignant breast cancer cells Cancer Lett. 2012, 324, 197-209 10.1016/j.canlet.2012.05.018
38. Bury, M.; Girault, A.; Mégalizzi, V.; Spiegl-Kreinecker, S.; Mathieu, V.; Berger, W.; Evidente, A.; Kornienko, A.; Gailly, P.; Vandier, C.; Kiss, R. Ophiobolin A induces paraptosis-like cell death in human glioblastoma cells by decreasing BKCa channel activity Cell Death Dis. 2013, 4, e561 10.1038/cddis.2013.85
39. Yu, C. T.; Li, J. H.; Lee, T. C.; Lin, L. F. Characterization of cocaine-elicited cell vacuolation: the involvement of calcium/calmodulin in organelle deregulation J. Biomed. Sci. 2008, 15, 215-226 10.1007/s11373-007-9213-z
40. Cao, Q.; Zhong, X. Z.; Zou, Y.; Murrell-Lagnado, R.; Zhu, M. X.; Dong, X. P. Calcium release through P2 × 4 activates calmodulin to promote endolysosomal membrane fusion J. Cell Biol. 2015, 209, 879-894 10.1083/jcb.201409071
41. Brostrom, M. A.; Brostrom, C. O. Calcium dynamics and endoplasmic reticular function in the regulation of protein synthesis: implications for cell growth and adaptability Cell Calcium 2003, 34, 345-363 10.1016/S0143-4160(03)00127-1
42. 2+ requirement for alpha1antitrypsin processing and transport competence Biochem. J. 1997, 325, 601-608 10.1042/bj3250601
43. 2+ signaling and calcium binding chaperones of the endoplasmic reticulum Cell Calcium 2002, 32, 269-278 10.1016/S0143416002001884