Oleanolic acid induces autophagic death in human gastric cancer cells in vitro and in vivo
Oleanolic acid (OA), a plant‐derived pentacyclic terpenoid, is known to have hepatoprotective effects. In this study, we found that OA induced autophagic cell death in multiple human gastric cancer cell lines. Moreover, OA‐induced autophagy was shown for the first time in human gastric cancer cells,...
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| Published in | Cell biology international Vol. 40; no. 7; pp. 770 - 778 |
|---|---|
| Main Authors | , , , |
| Format | Journal Article |
| Language | English |
| Published |
England
Blackwell Publishing Ltd
01.07.2016
Wiley Subscription Services, Inc |
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| Abstract | Oleanolic acid (OA), a plant‐derived pentacyclic terpenoid, is known to have hepatoprotective effects. In this study, we found that OA induced autophagic cell death in multiple human gastric cancer cell lines. Moreover, OA‐induced autophagy was shown for the first time in human gastric cancer cells, evidenced by the formation of GFP‐RFP‐LC3 puncta and autophagosomes. OA suppressed phospho‐mTOR through inhibition of the PI3 K/AKT and ERK/p38 MAPK signalling pathways and through activation of the AMPK signalling pathway. Furthermore, we found that OA‐induced cytotoxicity and autophagy could be blocked by the autophagy inhibitor 3‐methyladenine or via siRNA targeting Beclin‐1. Our in vivo research showed that OA delayed the formation of MGC‐803 tumours in an autophagy‐dependent manner. These results reveal a novel mechanism for OA in gastric cancer cells and suggest that OA could be a novel agent in the treatment of gastric cancer. |
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| AbstractList | Oleanolic acid (OA), a plant-derived pentacyclic terpenoid, is known to have hepatoprotective effects. In this study, we found that OA induced autophagic cell death in multiple human gastric cancer cell lines. Moreover, OA-induced autophagy was shown for the first time in human gastric cancer cells, evidenced by the formation of GFP-RFP-LC3 puncta and autophagosomes. OA suppressed phospho-mTOR through inhibition of the PI3 K/AKT and ERK/p38 MAPK signalling pathways and through activation of the AMPK signalling pathway. Furthermore, we found that OA-induced cytotoxicity and autophagy could be blocked by the autophagy inhibitor 3-methyladenine or via siRNA targeting Beclin-1. Our in vivo research showed that OA delayed the formation of MGC-803 tumours in an autophagy-dependent manner. These results reveal a novel mechanism for OA in gastric cancer cells and suggest that OA could be a novel agent in the treatment of gastric cancer.Oleanolic acid (OA), a plant-derived pentacyclic terpenoid, is known to have hepatoprotective effects. In this study, we found that OA induced autophagic cell death in multiple human gastric cancer cell lines. Moreover, OA-induced autophagy was shown for the first time in human gastric cancer cells, evidenced by the formation of GFP-RFP-LC3 puncta and autophagosomes. OA suppressed phospho-mTOR through inhibition of the PI3 K/AKT and ERK/p38 MAPK signalling pathways and through activation of the AMPK signalling pathway. Furthermore, we found that OA-induced cytotoxicity and autophagy could be blocked by the autophagy inhibitor 3-methyladenine or via siRNA targeting Beclin-1. Our in vivo research showed that OA delayed the formation of MGC-803 tumours in an autophagy-dependent manner. These results reveal a novel mechanism for OA in gastric cancer cells and suggest that OA could be a novel agent in the treatment of gastric cancer. Oleanolic acid (OA), a plant-derived pentacyclic terpenoid, is known to have hepatoprotective effects. In this study, we found that OA induced autophagic cell death in multiple human gastric cancer cell lines. Moreover, OA-induced autophagy was shown for the first time in human gastric cancer cells, evidenced by the formation of GFP-RFP-LC3 puncta and autophagosomes. OA suppressed phospho-mTOR through inhibition of the PI3K/AKT and ERK/p38 MAPK signalling pathways and through activation of the AMPK signalling pathway. Furthermore, we found that OA-induced cytotoxicity and autophagy could be blocked by the autophagy inhibitor 3-methyladenine or via siRNA targeting Beclin-1. Our in vivo research showed that OA delayed the formation of MGC-803 tumours in an autophagy-dependent manner. These results reveal a novel mechanism for OA in gastric cancer cells and suggest that OA could be a novel agent in the treatment of gastric cancer. Oleanolic acid (OA), a plant‐derived pentacyclic terpenoid, is known to have hepatoprotective effects. In this study, we found that OA induced autophagic cell death in multiple human gastric cancer cell lines. Moreover, OA‐induced autophagy was shown for the first time in human gastric cancer cells, evidenced by the formation of GFP‐RFP‐LC3 puncta and autophagosomes. OA suppressed phospho‐mTOR through inhibition of the PI3 K/AKT and ERK/p38 MAPK signalling pathways and through activation of the AMPK signalling pathway. Furthermore, we found that OA‐induced cytotoxicity and autophagy could be blocked by the autophagy inhibitor 3‐methyladenine or via siRNA targeting Beclin‐1. Our in vivo research showed that OA delayed the formation of MGC‐803 tumours in an autophagy‐dependent manner. These results reveal a novel mechanism for OA in gastric cancer cells and suggest that OA could be a novel agent in the treatment of gastric cancer. |
| Author | Qin, Yong Wang, Yu Nie, Hao Gong, Xing-Guo |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/27079177$$D View this record in MEDLINE/PubMed |
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| References | Cheng KG, Su CH, Yang LD, Liu J, Chen ZF ( 2015) Synthesis of oleanolic acid dimers linked at C-28 and evaluation of anti-tumor activity. Eur J Med Chem 89: 480-9. Sun MX, Huang L, Wang R, Yu YL, Li C, Li PP, Hu XC, Hao HP, Ishag HA, Mao X ( 2012) Porcine reproductive and respiratory syndrome virus induces autophagy to promote virus replication. Autophagy 8: 1434-47. Takemura M, Endo S, Matsunaga T, Soda M, Zhao HT, El-Kabbani O, Tajima K, Iinuma M, Hara A ( 2011) Selective inhibition of the tumor marker aldo-keto reductase family member 1B10 by oleanolic acid. J Nat Prod 74: 1201-6. Furtado RA, Rodrigues EP, Araujo FR, Oliveira WL, Furtado MA, Castro MB, Cunha WR, Tavares DC ( 2008) Ursolic acid and oleanolic acid suppress preneoplastic lesions induced by 1,2-dimethylhydrazine in rat colon. Toxicol Pathol 36: 576-80. Shanmugam MK, Dai X, Kumar AP, Tan BK, Sethi G, Bishayee A ( 2014) Oleanolic acid and its synthetic derivatives for the prevention and therapy of cancer: preclinical and clinical evidence. Cancer Lett 346: 206-16. Aryal P, Kim K, Park PH, Ham S, Cho J, Song K ( 2014) Baicalein induces autophagic cell death through AMPK/ULK1 activation and downregulation of mTORC1 complex components in human cancer cells. FEBS J 281: 4644-58. Park SJ, Lee Y, Oh HK, Lee HE, Lee Y, Ko SY, Kim B, Cheong JH, Shin CY, Ryu JH ( 2014) Oleanolic acid attenuates MK-801-induced schizophrenia-like behaviors in mice. Neuropharmacology 86: 49-56. Macintosh RL, Ryan KM ( 2013) Autophagy in tumour cell death. Semin Cancer Biol 23: 344-51. Shaw RJ ( 2006) Glucose metabolism and cancer. Curr Opin Cell Biol, 18: 598-608. Shaw RJ, Cantley LC ( 2006) Ras, PI(3)K and mTOR signalling controls tumour cell growth. Nature 441: 424-30. Marino ML, Pellegrini P, Di Lernia G, Djavaheri-Mergny M, Brnjic S, Zhang X, Hagg M, Linder S, Fais S, Codogno P, De Milito A ( 2012) Autophagy is a protective mechanism for human melanoma cells under acidic stress. J Biol Chem 287: 30664-76. Degenhardt K, Mathew R, Beaudoin B, Bray K, Anderson D, Chen G, Mukherjee C, Shi Y, Gelinas C, Fan Y, Nelson DA, Jin S, White E ( 2006) Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 10: 51-64. Akl MR, Elsayed HE, Ebrahim HY, Haggag EG, Kamal AM, El Sayed KA ( 2014) 3-O-[N-(p-fluorobenzenesulfonyl)-carbamoyl]-oleanolic acid, a semisynthetic analog of oleanolic acid, induces apoptosis in breast cancer cells. Eur J Pharmacol 740: 209-17. Cairns RA, Harris IS, Mak TW ( 2011) Regulation of cancer cell metabolism. Nat Rev Cancer 11: 85-95. Shimobayashi M, Hall MN ( 2014) Making new contacts: the mTOR network in metabolism and signalling crosstalk. Nat Rev Mol Cell Biol 15: 155-62. Dunlop EA, Tee AR ( 2014) MTOR and autophagy: a dynamic relationship governed by nutrients and energy. Semin Cell Dev Biol 36: 121-9. Salminen A, Kaarniranta K, Kauppinen A, Ojala J, Haapasalo A, Soininen H, Hiltunen M ( 2013) Impaired autophagy and APP processing in Alzheimer's disease: the potential role of Beclin 1 interactome. Prog Neurobiol 106: 33-54. Meschini S, Condello M, Calcabrini A, Marra M, Formisano G, Lista P, De Milito A, Federici E, Arancia G ( 2008) The plant alkaloid voacamine induces apoptosis-independent autophagic cell death on both sensitive and multidrug resistant human osteosarcoma cells. Autophagy 4: 1020-33. Speranza G, Gutierrez ME, Kummar S, Strong JM, Parker RJ, Collins J, Yu Y, Cao L, Murgo AJ, Doroshow JH, Chen A ( 2012) Phase I study of the synthetic triterpenoid, 2-cyano-3, 12-dioxoolean-1, 9-dien-28-oic acid (CDDO), in advanced solid tumors. Cancer Chemother Pharmacol 69: 431-8. Shyu MH, Kao TC, Yen GC ( 2010) Oleanolic acid and ursolic acid induce apoptosis in HuH7 human hepatocellular carcinoma cells through a mitochondrial-dependent pathway and downregulation of XIAP. J Agric Food Chem 58: 6110-8. Cuervo AM, Macian F ( 2012) Autophagy, nutrition and immunology. Mol Aspects Med 33: 2-13. Ng YP, Chen Y, Hu Y, Ip FC, Ip NY ( 2013) Olean-12-eno[2,3-c] [1,2,5]oxadiazol-28-oic acid (OEOA) induces G1 cell cycle arrest and differentiation in human leukemia cell lines. PLoS ONE 8: e63580. Galluzzi L, Pietrocola F, Levine B, Kroemer G ( 2014) Metabolic control of autophagy. Cell 159: 1263-76. Meijer AJ, Codogno P ( 2009) Autophagy: regulation and role in disease. Crit Rev Clin Lab Sci 46: 210-40. Mizushima N, Komatsu M ( 2011) Autophagy: renovation of cells and tissues. Cell 147: 728-41. Orvedahl A, Levine B ( 2009) Eating the enemy within: autophagy in infectious diseases. Cell Death Differ 16: 57-69. 2009; 46 2012; 287 2010; 58 2006; 10 2013; 23 2013; 106 2008; 36 2011; 74 2011; 11 2006; 18 2008; 4 2013; 8 2012; 33 2014; 159 2014; 86 2015; 89 2011; 147 2014; 15 2014; 36 2014; 281 2012; 69 2009; 16 2014; 346 2006; 441 2012; 8 2014; 740 e_1_2_8_24_1 e_1_2_8_25_1 e_1_2_8_26_1 e_1_2_8_27_1 e_1_2_8_3_1 e_1_2_8_2_1 e_1_2_8_5_1 e_1_2_8_4_1 e_1_2_8_7_1 e_1_2_8_6_1 e_1_2_8_9_1 e_1_2_8_8_1 e_1_2_8_20_1 e_1_2_8_21_1 e_1_2_8_22_1 e_1_2_8_23_1 e_1_2_8_17_1 e_1_2_8_18_1 e_1_2_8_19_1 e_1_2_8_13_1 e_1_2_8_14_1 e_1_2_8_15_1 e_1_2_8_16_1 e_1_2_8_10_1 e_1_2_8_11_1 e_1_2_8_12_1 |
| References_xml | – reference: Sun MX, Huang L, Wang R, Yu YL, Li C, Li PP, Hu XC, Hao HP, Ishag HA, Mao X ( 2012) Porcine reproductive and respiratory syndrome virus induces autophagy to promote virus replication. Autophagy 8: 1434-47. – reference: Takemura M, Endo S, Matsunaga T, Soda M, Zhao HT, El-Kabbani O, Tajima K, Iinuma M, Hara A ( 2011) Selective inhibition of the tumor marker aldo-keto reductase family member 1B10 by oleanolic acid. J Nat Prod 74: 1201-6. – reference: Meschini S, Condello M, Calcabrini A, Marra M, Formisano G, Lista P, De Milito A, Federici E, Arancia G ( 2008) The plant alkaloid voacamine induces apoptosis-independent autophagic cell death on both sensitive and multidrug resistant human osteosarcoma cells. Autophagy 4: 1020-33. – reference: Shanmugam MK, Dai X, Kumar AP, Tan BK, Sethi G, Bishayee A ( 2014) Oleanolic acid and its synthetic derivatives for the prevention and therapy of cancer: preclinical and clinical evidence. Cancer Lett 346: 206-16. – reference: Shaw RJ ( 2006) Glucose metabolism and cancer. Curr Opin Cell Biol, 18: 598-608. – reference: Cheng KG, Su CH, Yang LD, Liu J, Chen ZF ( 2015) Synthesis of oleanolic acid dimers linked at C-28 and evaluation of anti-tumor activity. Eur J Med Chem 89: 480-9. – reference: Park SJ, Lee Y, Oh HK, Lee HE, Lee Y, Ko SY, Kim B, Cheong JH, Shin CY, Ryu JH ( 2014) Oleanolic acid attenuates MK-801-induced schizophrenia-like behaviors in mice. Neuropharmacology 86: 49-56. – reference: Degenhardt K, Mathew R, Beaudoin B, Bray K, Anderson D, Chen G, Mukherjee C, Shi Y, Gelinas C, Fan Y, Nelson DA, Jin S, White E ( 2006) Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 10: 51-64. – reference: Shimobayashi M, Hall MN ( 2014) Making new contacts: the mTOR network in metabolism and signalling crosstalk. Nat Rev Mol Cell Biol 15: 155-62. – reference: Ng YP, Chen Y, Hu Y, Ip FC, Ip NY ( 2013) Olean-12-eno[2,3-c] [1,2,5]oxadiazol-28-oic acid (OEOA) induces G1 cell cycle arrest and differentiation in human leukemia cell lines. PLoS ONE 8: e63580. – reference: Orvedahl A, Levine B ( 2009) Eating the enemy within: autophagy in infectious diseases. Cell Death Differ 16: 57-69. – reference: Aryal P, Kim K, Park PH, Ham S, Cho J, Song K ( 2014) Baicalein induces autophagic cell death through AMPK/ULK1 activation and downregulation of mTORC1 complex components in human cancer cells. FEBS J 281: 4644-58. – reference: Mizushima N, Komatsu M ( 2011) Autophagy: renovation of cells and tissues. Cell 147: 728-41. – reference: Speranza G, Gutierrez ME, Kummar S, Strong JM, Parker RJ, Collins J, Yu Y, Cao L, Murgo AJ, Doroshow JH, Chen A ( 2012) Phase I study of the synthetic triterpenoid, 2-cyano-3, 12-dioxoolean-1, 9-dien-28-oic acid (CDDO), in advanced solid tumors. Cancer Chemother Pharmacol 69: 431-8. – reference: Galluzzi L, Pietrocola F, Levine B, Kroemer G ( 2014) Metabolic control of autophagy. Cell 159: 1263-76. – reference: Dunlop EA, Tee AR ( 2014) MTOR and autophagy: a dynamic relationship governed by nutrients and energy. Semin Cell Dev Biol 36: 121-9. – reference: Furtado RA, Rodrigues EP, Araujo FR, Oliveira WL, Furtado MA, Castro MB, Cunha WR, Tavares DC ( 2008) Ursolic acid and oleanolic acid suppress preneoplastic lesions induced by 1,2-dimethylhydrazine in rat colon. Toxicol Pathol 36: 576-80. – reference: Meijer AJ, Codogno P ( 2009) Autophagy: regulation and role in disease. Crit Rev Clin Lab Sci 46: 210-40. – reference: Marino ML, Pellegrini P, Di Lernia G, Djavaheri-Mergny M, Brnjic S, Zhang X, Hagg M, Linder S, Fais S, Codogno P, De Milito A ( 2012) Autophagy is a protective mechanism for human melanoma cells under acidic stress. 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Eur J Pharmacol 740: 209-17. – reference: Salminen A, Kaarniranta K, Kauppinen A, Ojala J, Haapasalo A, Soininen H, Hiltunen M ( 2013) Impaired autophagy and APP processing in Alzheimer's disease: the potential role of Beclin 1 interactome. Prog Neurobiol 106: 33-54. – reference: Shaw RJ, Cantley LC ( 2006) Ras, PI(3)K and mTOR signalling controls tumour cell growth. 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| Snippet | Oleanolic acid (OA), a plant‐derived pentacyclic terpenoid, is known to have hepatoprotective effects. In this study, we found that OA induced autophagic cell... Oleanolic acid (OA), a plant-derived pentacyclic terpenoid, is known to have hepatoprotective effects. In this study, we found that OA induced autophagic cell... |
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| SubjectTerms | Animals Apoptosis - drug effects Apoptosis Regulatory Proteins - metabolism autophagic death Autophagy Autophagy - drug effects Beclin-1 - genetics Cell Line, Tumor Female Gastric cancer Humans in vivo MAP Kinase Signaling System - drug effects Mice Mice, Inbred BALB C Mice, Nude mTOR oleanolic acid Oleanolic Acid - pharmacology Proto-Oncogene Proteins c-akt - metabolism Random Allocation RNA, Small Interfering - administration & dosage RNA, Small Interfering - genetics Signal Transduction - drug effects Stomach Neoplasms - drug therapy Stomach Neoplasms - metabolism Stomach Neoplasms - pathology TOR Serine-Threonine Kinases - metabolism Transfection Xenograft Model Antitumor Assays |
| Title | Oleanolic acid induces autophagic death in human gastric cancer cells in vitro and in vivo |
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