Sensitization of lung cancer cells to cisplatin by β-elemene is mediated through blockade of cell cycle progression: Antitumor efficacies of β-elemene and its synthetic analogs

Medical Oncology

Volumn 30, Issue 1, 2013, Pages

  Li, Q Quentin ^a,c   Wang, Gangduo ^a   Huang, Furong ^a   Li, Jueli M ^b   Cuff, Christopher F ^a   Reed, Eddie ^a,c  

^a WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF PHARMACY   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Elemene; Cell cycle arrest; Chinese medicine; Cisplatin resistance; Lung cancer; Synthetic analogs

Indexed keywords

BETA ELEMENAL; BETA ELEMENE; BETA ELEMENE FLUORIDE; BETA ELEMENOL; CELL CYCLE PROTEIN; CHECKPOINT KINASE 2; CISPLATIN; CYCLIN B1; CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 1B; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; PROTEIN CDC25C; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; BETA-ELEMENE; CDC2 PROTEIN, HUMAN; CYCLIN B; PROTEIN SERINE THREONINE KINASE; SESQUITERPENE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CELL CYCLE PROGRESSION; CELL PROLIFERATION; CYTOTOXICITY; DRUG EFFICACY; DRUG POTENTIATION; DRUG SENSITIZATION; DRUG STRUCTURE; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; G2 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; LUNG NON SMALL CELL CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION; CELL CYCLE; DRUG EFFECT; LUNG TUMOR; METABOLISM; PATHOLOGY; PHOSPHORYLATION; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; CARCINOMA, NON-SMALL-CELL LUNG; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; CISPLATIN; CYCLIN B; G2 PHASE CELL CYCLE CHECKPOINTS; HUMANS; LUNG NEOPLASMS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; SESQUITERPENES;

EID: 84873391545     PISSN: 13570560     EISSN: 1559131X     Source Type: Journal    
DOI: 10.1007/s12032-013-0488-9     Document Type: Article

References (56)

1. McAuliffe SM, Morgan SL, Wyant GA, Tran LT, Muto KW, Chen YS, Chin KT, Partridge JC, Poole BB, Cheng KH, Daggett J, Cullen K, Kantoff E, Hasselbatt K, Berkowitz J, Muto MG, Berkowitz RS, Aster JC, Matulonis UA, Dinulescu DM. Targeting Notch, a key pathway for ovarian cancer stem cells, sensitizes tumors to platinum therapy. Proc Natl Acad Sci USA. 2012;109:2939-48.
2. Sanchez-Perez I, Murguia JR, Perona R. Cisplatin induces a persistent activation of JNK that is related to cell death. Oncogene. 1998;16:533-40.
3. Benhar M, Dalyot I, Engelberg D, Levitzki A. Enhanced ROS production in oncogenically transformed cells potentiates c-Jun N-terminal kinase and p38 mitogen-activated protein kinase activation and sensitization to genotoxic stress. Mol Cell Biol. 2001;21:6913-26.
4. Verbon EH, Post JA, Boonstra J. The influence of reactive oxygen species on cell cycle progression in mammalian cells. Gene. 2012;511:1-6.
5. Kip2 CDK inhibitors. Cell Cycle. 2010;9:2342-52.
6. Lacy ER, Wang Y, Post J, Nourse A, Webb W, Mapelli M, Musacchio A, Siuzdak G, Kriwacki RW. Molecular basis for the specificity of p27 toward cyclin-dependent kinases that regulate cell division. J Mol Biol. 2005;349:764-73.
7. Hu X, Moscinski LC. Cdc2: a monopotent or pluripotent CDK? Cell Prolif. 2011;44:205-11.
8. 2/M cell cycle transitions: pRb is a critical determinant in blocking DNA replication and in preventing endoreduplication. Mol Cell Biol. 1998;18:629-43.
9. 2-phase DNA-damage checkpoint. Trends Cell Biol. 2000;10:296-303.
10. Brezak MC, Quaranta M, Mondesert O, Galcera MO, Lavergne O, Alby F, Cazales M, Baldin V, Thurieau C, Harnett J, Lanco C, Kasprzyk PG, Prevost GP, Ducommun B. A novel synthetic inhibitor of CDC25 phosphatases: BN82002. Cancer Res. 2004;64:3320-5.
11. Sanchez Y, Wong C, Thoma RS, Richman R, Wu Z, Piwnica-Worms H, Elledge SJ. Conservation of the Chk1 checkpoint pathway in mammals: linkage of DNA damage to Cdk regulation through Cdc25. Science. 1997;277:1497-501.
12. Han SJ, Conti M. New pathways from PKA to the Cdc2/cyclin B complex in oocytes: Wee1B as a potential PKA substrate. Cell Cycle. 2006;5:227-31.
13. 2/M transition. Cell Cycle. 2004;3:733-7.
14. Watanabe N, Broome M, Hunter T. Regulation of the human WEE1Hu CDK tyrosine 15-kinase during the cell cycle. EMBO J. 1995;14:1878-91.
15. Parker LL, Sylvestre PJ, Byrnes MJ, Liu F, Piwnica-Worms H. Identification of a 95-kDa WEE1-like tyrosine kinase in HeLa cells. Proc Natl Acad Sci USA. 1995;92:9638-42.
16. Mueller PR, Coleman TR, Kumagai A, Dunphy WG. Myt1: a membrane-associated inhibitory kinase that phosphorylates Cdc2 on both threonine-14 and tyrosine-15. Science. 1995;270:86-90.
17. Ruiz EJ, Vilar M, Nebreda AR. A two-step inactivation mechanism of Myt1 ensures CDK1/cyclin B activation and meiosis I entry. Curr Biol. 2010;20:717-23.
18. The Non-Small Cell Lung Cancer Collaborative Group. Chemotherapy in non-small cell lung cancer: a meta-analysis using updated data on individual patients from 52 randomized clinical trials. BMJ. 1995;311:899-909.
19. Boni C, Tiseo M, Boni L, Baldini E, Recchia F, Barone C. Triplets versus doublets, with or without cisplatin, in the first-line treatment of stage IIIB-IV non-small cell lung cancer (NSCLC) patients: a multicenter randomised factorial trial (FAST). Br J Cancer. 2012;106:658-65.
20. Stephens R, Fairlamb N, Gower N. The big lung trial (BLT): determining the value of cisplatin-based chemotherapy for all patients with non-small cell lung cancer (NSCLC). Preliminary results in the supportive care setting. Proc Am Soc Clin Oncol. 2002;21:291a.
21. Roszkowski K, Pluzanska A, Krzakowski M. A multicenter, randomized phase III study of docetaxel plus best supportive care versus best supportive care in chemotherapy-naïve patients with metastatic or non-resectable localized non-small cell lung cancer (NSCLC). Lung Cancer. 2000;27:145-57.
22. Johnson DH. Evolution of cisplatin-based chemotherapy in non-small cell lung cancer: a historical perspective and the eastern cooperative oncology group experience. Chest. 2000;117(S1):133S-7S.
23. Wang G, Reed E, Li QQ. Molecular basis of cellular response to cisplatin chemotherapy in non-small cell lung cancer. Oncol Rep. 2004;12:955-65.
24. Thongprasert S, Sanuganmitra P, Juthapan N. Relationship between quality of life and clinical outcomes in advanced non-small cell lung cancer: best supportive care (BSc) versus BSC plus chemotherapy. Lung Cancer. 1999;24:17-24.
25. Azzoli CG, Baker S Jr, Temin S, Pao W, Aliff T, Brahmer J, Johnson DH, Laskin JL, Masters G, Milton D, Nordquist L, Pfister DG, Piantadosi S, Schiller JH, Smith R, Smith TJ, Strawn JR, Trent D, Giaccone G. American Society of Clinical Oncology Clinical Practice Guideline update on chemotherapy for stage IV non-small-cell lung cancer. J Clin Oncol. 2009;27:6251-66.
26. Qian J, Qin S. Pharmacological and clinical studies of elemene, a new anticancer drug (Chinese). Chin Clin Cancer. 1999;26:1-3.
27. Zheng S, Yang H, Zhang S, Wang X, Yu L, Lu J, Li J. Initial study on naturally occurring products from traditional Chinese herbs and vegetables for chemoprevention. J Cell Biochem Suppl. 1997;27:106-12.
28. Yuan J, Gu ZL, Chou WH, Kwok CY. Elemene induces apoptosis and regulates expression of bcl-2 protein in human leukemia K562 cells (Chinese). Zhongguo Yao Li Xue Bao. 1999;20:103-6.
29. Zhou H, Shen J, Hou J, Qiu Y, Luo Q. Experimental study on apoptosis induced by elemene in glioma cells (Chinese). Ai Zheng. 2003;22:959-63.
30. Wang G, Li X, Huang X, Zhao J, Ding H, Cunningham C, Coad J, Flynn D, Reed E, Li QQ. Antitumor effect of β-elemene in non-small cell lung cancer cells is mediated via induction of cell cycle arrest and apoptotic cell death. Cell Mol Life Sci. 2005;62:881-93.
31. 2-M phase. Cell Mol Life Sci. 2005;62:894-904.
32. Li QQ, Wang G, Zhang M, Cuff CF, Huang L, Reed E. β-Elemene, a novel plant-derived antineoplastic agent, increases cisplatin chemosensitivity of lung tumor cells by triggering apoptosis. Oncol Rep. 2009;22:161-70.
33. Li QQ, Wang G, Reed E, Huang L, Cuff CF. Evaluation of cisplatin in combination with β-elemene as a regimen for prostate cancer chemotherapy. Basic Clin Pharmacol Toxicol. 2010;107:868-76.
34. Li QQ, Wang G, Huang F, Banda M, Reed E. Antineoplastic effect of β-elemene on prostate cancer cells and other types of solid tumour cells. J Pharm Pharmacol. 2010;62:1018-27.
35. Lee RX, Li QQ, Reed E. β-Elemene effectively suppresses the growth and survival of both platinum-sensitive and -resistant ovarian tumor cells. Anticancer Res. 2012;32:3103-13.
36. Zhao J, Li QQ, Zou B, Wang G, Li X, Kim JE, Cuff CF, Huang L, Reed E, Gardner K. In vitro combination characterization of the new anticancer plant drug β-elemene with taxanes against human lung carcinoma. Int J Oncol. 2007;31:241-52.
37. Li QQ, Lee RX, Liang H, Zhong Y. Anticancer activity of β-elemene and its synthetic analogs in human malignant brain tumor cells. Anticancer Res. 2013;33:65-76.
38. Li QQ, Lee RX, Liang H, Zhong Y, Reed E. Enhancement of cisplatin-induced apoptosis by β-elemene in resistant human ovarian cancer cells. Med Oncol. 2013;30:424-35.
39. Zou B, Li QQ, Zhao J, Cuff CF, Reed E. β-Elemene and taxanes synergistically induce cytotoxicity and inhibit proliferation in ovarian cancer and other tumor cells. Anticancer Res. 2013 (in press).
40. Wang B, Guo J, Di J, Shi Q. The experimental study of association between elemene and tumor multidrug-resistance (Chinese). Chin Clin Cancer. 1999;26:10-3.
41. Wang H, Quan T, He T, Franke T, Voorhees J, Fisher G. Epidermal growth factor receptor-dependent, NF-κB-independent activation of the phosphatidylinositol 3-kinase/Akt pathway inhibits ultraviolet irradiation-induced caspases-3, -8, and -9 in human keratinocytes. J Biol Chem. 2003;278:45737-45.
42. Mashour GA, Ratner N, Khan GA, Wang HL, Martuza RL, Kurtz A. The angiogenic factor midkine is aberrantly expressed in NF1-deficient Schwann cells and is a mitogen for neurofibroma-derived cells. Oncogene. 2001;20:97-105.
43. Wang HL, Kurtz A. Breast cancer growth inhibition by delivery of the MDGI-derived peptide P108. Oncogene. 2000;19:2455-60.
44. Ramalingam S, Belani CP. State-of-the-art chemotherapy for advanced non-small cell lung cancer. Semin Oncol. 2004;31:68-74.
45. Eastman A. Cell cycle checkpoints and their impact on anticancer therapeutic strategies. J Cell Biochem. 2004;91:223-31.
46. Sherr C. Cancer cell cycles. Science. 1996;274:1672-7.
47. Dynlacht B. Regulation of transcription by proteins that control the cell cycle. Nature. 1997;389:149-52.
48. 2/M arrest by the isoflavone genistein in human prostate carcinoma cells. Jpn J Cancer Res. 2000;91:164-73.
49. 2 arrest in mammalian cells and exhibits tumoricidal activity in vivo. Cancer Res. 2001;61:5499-504.
50. 2/M arrest. J Biol Chem. 1996;271:29556-60.
51. 2 DNA damage checkpoint. J Biol Chem. 2000;275:30638-43.
52. Fornace AJ, Alamo I, Hollander MC. DNA damage-inducible transcripts in mammalian cells. Proc Natl Acad Sci USA. 1988;85:8800-4.
53. Cip1. Oncogene. 1995;11:1675-83.
54. 2/M cell cycle checkpoint. Proc Natl Acad Sci USA. 1999;96:3706-11.
55. 2 phase and cell death induced by cisplatin. J Natl Cancer Inst. 1990;82:749-55.
56. waf1/cip1 and Wee1. Biochem Pharmacol. 2004;67:717-26.