Flavonoids isolated from Citrus platymamma induced G2/M cell cycle arrest and apoptosis in A549 human lung cancer cells

Oncology Letters

Volumn 12, Issue 2, 2016, Pages 1394-1402

  Nagappan, Arulkumar ^a   Lee, Ho Jeong ^b   Saralamma, Venu Venkatarame Gowda ^b   Park, Hyeon Soo ^b   Hong, Gyeong Eun ^b   Yumnam, Silvia ^b   Raha, Suchismita ^b   Charles, Shobana Nancy ^a   Shin, Sung Chul ^c   Kim, Eun Hee ^d   Lee, Won Sup ^a   Kim, Gon Sup ^b  

^a Gyeongsang National University School of Medicine   (South Korea)

^b Research Institute of Life Science and College of Veterinary Medicine   (South Korea)

^c Gyeongsang National University   (South Korea)

^d International University of Korea   (South Korea)

Author keywords

A549 cells; Apoptosis; Cell cycle; Citrus platymamma; Flavonoids; Lung cancer

Indexed keywords

4',6 DIAMIDINO 2 PHENYLINDOLE; AURANTIIN; CASPASE 3; CASPASE 6; CASPASE 8; CASPASE 9; CELL CYCLE PROTEIN; CYCLIN B1; CYCLIN DEPENDENT KINASE 1; FLAVONOID; HEPTAMETHOXYFLAVONE; HESPERIDIN; HYDROXYPENTAMETHOXYFLAVONE; ISOSINENSETIN; NEOERIOCITRIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NOBILETIN; SINENSETIN; TANGERETIN; TETRAMETHOXYFLAVONE; TETRAMETHYL O ISOSCUTELLAREIN; UNCLASSIFIED DRUG;

A549 CELL LINE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL PROLIFERATION; CELL VIABILITY; CITRUS; CITRUS PLATYMAMMA; CONTROLLED STUDY; DOWN REGULATION; ELECTROPHORESIS; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IC50; IMMUNOBLOTTING; LUNG CANCER; MASS SPECTROMETRY; MTT ASSAY; WESTERN BLOTTING;

EID: 84977125787     PISSN: 17921074     EISSN: 17921082     Source Type: Journal    
DOI: 10.3892/ol.2016.4793     Document Type: Article

References (45)

1. Siegel R, Naishadham D and Jemal A: Cancer statistics, 2013. CA Cancer J Clin 63: 11-30, 2013.
2. Jung KW, Won YJ, Kong HJ, Oh CM, Seo HG and Lee JS: Prediction of cancer incidence and mortality in Korea, 2013. Cancer Res Treat 45: 15-21, 2013.
3. Meoni G, Cecere FL, Lucherini E and Di Costanzo F: Medical treatment of advanced non-small cell lung cancer in elderly patients: A review of the role of chemotherapy and targeted agents. J Geriatr Oncol 4: 282-290, 2013.
4. Park KI, Park HS, Kang SR, Nagappan A, Lee DH, Kim JA, Han DY and Kim GS: Korean Scutellaria baicalensis water extract inhibits cell cycle G1/S transition by suppressing cyclin D1 expression and matrix-metalloproteinase-2 activity in human lung cancer cells. J Ethnopharmacol 133: 634-641, 2011.
5. Molina JR, Yang P, Cassivi SD, Schild SE and Adjei AA: Non-small cell lung cancer: epidemiology, risk factors, treatment, and survivorship. Mayo Clin Proc 83: 584-594, 2008.
6. Jemal A, Siegel R, Xu J and Ward E: Cancer statistics, 2010. CA Cancer J Clin 60: 277-300, 2010.
7. Liang XJ, Chen C, Zhao Y and Wang PC: Circumventing tumor resistance to chemotherapy by nanotechnology. Methods Mol Biol 596: 467-488, 2010.
8. Hyun HB, Lee WS, Go SI, Nagappan A, Park C, Han MH, Hong SH, Kim G, Kim GY, Cheong J, et al: The flavonoid morin from Moraceae induces apoptosis by modulation of Bcl-2 family members and Fas receptor in HCT 116 cells. Int J Oncol 46: 2670-2678, 2015.
9. Jeong JW, Lee WS, Go SI, Nagappan A, Baek JY, Lee JD, Lee SJ, Park C, Kim GY, Kim HJ, et al: Pachymic Acid Induces Apoptosis of EJ Bladder Cancer Cells by DR5 Up-Regulation, ROS Generation, Modulation of Bcl-2 and IAP Family Members. Phytother Res 29: 1516-1524, 2015.
10. Zamzami N, Susin SA, Marchetti P, Hirsch T, Gómez-Monterrey I, Castedo M and Kroemer G: Mitochondrial control of nuclear apoptosis. J Exp Med 183: 1533-1544, 1996.
11. Hengartner MO: The biochemistry of apoptosis. Nature 407: 770-776, 2000.
12. Cregan SP, Dawson VL and Slack RS: Role of AIF in caspase-dependent and caspase-independent cell death. Oncogene 23: 2785-2796, 2004.
13. Findley HW, Gu L, Yeager AM and Zhou M: Expression and regulation of Bcl-2, Bcl-xl, and Bax correlate with p53 status and sensitivity to apoptosis in childhood acute lymphoblastic leukemia. Blood 89: 2986-2993, 1997.
14. DiPaola RS: To arrest or not to G(2)-M Cell-cycle arrest: Commentary re: A. K. Tyagi et al., Silibinin strongly synergizes human prostate carcinoma DU145 cells to doxorubicin-induced growth inhibition, G(2)-M arrest, and apoptosis. Clin. cancer res., 8: 3512-3519, 2002. Clin Cancer Res 8: 3311-3314, 2002.
15. Adams JM: Ways of dying: multiple pathways to apoptosis. Genes Dev 17: 2481-2495, 2003.
16. Gibbs WW: Untangling the roots of cancer. Sci Am 289: 56-65, 2003.
17. Lee HJ, Nagappan A, Park HS, Hong GE, Yumnam S, Raha S, Saralamma VV, Lee WS, Kim EH and Kim GS: Flavonoids isolated from Citrus platymamma induce mitochondrial-dependent apoptosis in AGS cells by modulation of the PI3K/AKT and MAPK pathways. Oncol Rep 34: 1517-1525, 2015.
18. Liu BL, Zhang X, Zhang W and Zhen HN: New enlightenment of French Paradox: Resveratrol's potential for cancer chemoprevention and anti-cancer therapy. Cancer Biol Ther 6: 1833-1836, 2007.
19. Hatcher H, Planalp R, Cho J, Torti FM and Torti SV: Curcumin: From ancient medicine to current clinical trials. Cell Mol Life Sci 65: 1631-1652, 2008.
20. Nogata Y, Sakamoto K, Shiratsuchi H, Ishii T, Yano M and Ohta H: Flavonoid composition of fruit tissues of citrus species. Biosci Biotechnol Biochem 70: 178-192, 2006.
21. Benavente-Garcia O and Castillo J: Update on uses and properties of citrus flavonoids: New findings in anticancer, cardiovascular and anti-inflammatory activity. J Agric Food Chem 56: 6185-6205, 2008.
22. Luo G, Guan X and Zhou L: Apoptotic effect of citrus fruit extract nobiletin on lung cancer cell line A549 in vitro and in vivo. Cancer Biol Ther 7: 966-973, 2008.
23. Lai CS, Li S, Miyauchi Y, Suzawa M, Ho CT and Pan MH: Potent anti-cancer effects of citrus peel flavonoids in human prostate xenograft tumors. Food Funct 4: 944-949, 2013.
24. Park KI, Park HS, Nagappan A, Hong GE, Lee do H, Kang SR, Kim JA, Zhang J, Kim EH, Lee WS, et al: Induction of the cell cycle arrest and apoptosis by flavonoids isolated from Korean Citrus aurantium L. Food Chem 135: 2728-2735, 2012.
25. Donzelli M and Draetta GF: Regulating mammalian checkpoints through Cdc25 inactivation. EMBO Rep 4: 671-677, 2003.
26. Parrish AB, Freel CD and Kornbluth S: Cellular mechanisms controlling caspase activation and function. Cold Spring Harb Perspect Biol 5: a008672, 2013.
27. Slee EA, Adrain C and Martin SJ: Serial killers: ordering caspase activation events in apoptosis. Cell Death Differ 6: 1067-1074, 1999.
28. Wang GH, Mitsui K, Kotliarova S, Yamashita A, Nagao Y, Tokuhiro S, Iwatsubo T, Kanazawa I and Nukina N: Caspase activation during apoptotic cell death induced by expanded polyglutamine in N2a cells. Neuroreport 10: 2435-2438, 1999.
29. Harapu CD, Miron A, Cuciureanu M and Cuciureanu R: Flavonoids-bioactive compounds in fruits juice. Rev Med Chir Soc Med Nat Iasi 114: 1209-1214, 2010 (In Romanian).
30. Lee DH, Park KI, Park HS, Kang SR, Nagappan A, Kim JA, Kim EH, Lee WS, Hah YS, Chung HJ, et al: Flavonoids isolated from Korea Citrus aurantium L. Induce G2/M phase arrest and apoptosis in human gastric cancer AGS Cells. Evid Based Complement Alternat Med 2012: 515901, 2012.
31. Kim JA, Park HS, Park KI, Hong GE, Nagappan A, Zhang J, Han DY, Shin SC, Won CG, Kim EH and Kim GS: Proteome analysis of the anti-inflammatory response of flavonoids isolated from Korean Citrus aurantium L. In lipopolysaccharide-induced L6 rat skeletal muscle cells. Am J Chin Med 41: 901-912, 2013.
32. Kim DI, Lee SJ, Lee SB, Park K, Kim WJ and Moon SK: Requirement for Ras/Raf/ERK pathway in naringin-induced G1-cell-cycle arrest via p21WAF1 expression. Carcinogenesis 29: 1701-1709, 2008.
33. Boonstra J and Post JA: Molecular events associated with reactive oxygen species and cell cycle progression in mammalian cells. Gene 337: 1-13, 2004.
34. Nicolini F, Burmistrova O, Marrero MT, Torres F, Hernández C, Quintana J and Estévez F: Induction of G2/M phase arrest and apoptosis by the flavonoid tamarixetin on human leukemia cells. Mol Carcinog 53: 939-950, 2014.
35. Li Y, Duan S, Jia H, Bai C, Zhang L and Wang Z: Flavonoids from tartary buckwheat induce G2/M cell cycle arrest and apoptosis in human hepatoma HepG2 cells. Acta Biochim Biophys Sin (Shanghai) 46: 460-470, 2014.
36. Tao L, Fu R, Wang X, Yao J, Zhou Y, Dai Q, Li Z, Lu N and Wang W: LL-202, a newly synthesized flavonoid, inhibits tumor growth via inducing G(2)/M phase arrest and cell apoptosis in MCF-7 human breast cancer cells in vitro and in vivo. Toxicol Lett 228: 1-12, 2014.
37. Majno G and Joris I: Apoptosis, oncosis and necrosis. An overview of cell death. Am J Pathol 146: 3-15, 1995.
38. Mao WP, Ye JL, Guan ZB, Zhao JM, Zhang C, Zhang NN, Jiang P and Tian T: Cadmium induces apoptosis in human embryonic kidney (HEK) 293 cells by caspase-dependent and-independent pathways acting on mitochondria. Toxicol In Vitro 21: 343-354, 2007.
39. Lazebnik YA, Kaufmann SH, Desnoyers S, Poirier GG and Earnshaw WC: Cleavage of poly (ADP-ribose) polymerase by a proteinase with properties like ICE. Nature 371: 346-347, 1994.
40. Debatin KM: Apoptosis pathways in cancer and cancer therapy. Cancer Immunol Immunother 53: 153-159, 2004.
41. MacKenzie SH and Clark AC: Targeting cell death in tumors by activating caspases. Curr Cancer Drug Targets 8: 98-109, 2008.
42. Wong WW and Puthalakath H: Bcl-2 family proteins: The sentinels of the mitochondrial apoptosis pathway. IUBMB Life 60: 390-397, 2008.
43. Cai J, Yang J and Jones DP: Mitochondrial control of apoptosis: the role of cytochrome c. Biochim Biophys Acta 1366: 139-149, 1998.
44. Liu X, Kim CN, Yang J, Jemmerson R and Wang X: Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86: 147-157, 1996.
45. Shin DY, Ryu CH, Lee WS, Kim DC, Kim SH, Hah YS, Lee SJ, Shin SC, Kang HS and Choi YH: Induction of apoptosis and inhibition of invasion in human hepatoma cells by anthocyanins from meoru. Ann N Y Acad Sci 1171: 137-148, 2009.