The apoptotic effect of hesperetin on human cervical cancer cells is mediated through cell cycle arrest, death receptor, and mitochondrial pathways

Fundamental and Clinical Pharmacology

Volumn 27, Issue 6, 2013, Pages 581-592

  Alshatwi, Ali A ^a   Ramesh, E ^a   Periasamy, V S ^a   Subash Babu, P ^a  

^a KING SAUD UNIVERSITY   (Saudi Arabia)

Author keywords

Apoptosis; Cell cycle; Cervical cancer; Death receptor; Hesperetin; Mitochondria

Indexed keywords

3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; ACRIDINE ORANGE; CASPASE 3; CASPASE 8; CASPASE 9; CYANINE DYE 3; ETHIDIUM BROMIDE; FAS ANTIGEN; FAS ASSOCIATED DEATH DOMAIN PROTEIN; FLAVONOID; HESPERETIN; LIPOCORTIN 5; PROPIDIUM IODIDE; PROTEIN BAX; PROTEIN P53;

ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IC 50; IN VITRO STUDY; MARKER GENE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; NICK END LABELING; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; UTERINE CERVIX CANCER;

APOPTOSIS; CELL CYCLE; CERVICAL CANCER; DEATH RECEPTOR; HESPERETIN; MITOCHONDRIA;

ANTIGENS, CD95; ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; FLOW CYTOMETRY; HESPERIDIN; HUMANS; IN SITU NICK-END LABELING; INHIBITORY CONCENTRATION 50; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; REAL-TIME POLYMERASE CHAIN REACTION; TIME FACTORS; UTERINE CERVICAL NEOPLASMS;

EID: 84886597627     PISSN: 07673981     EISSN: 14728206     Source Type: Journal    
DOI: 10.1111/j.1472-8206.2012.01061.x     Document Type: Article

References (61)

1. WHO/ICO. Summary report on HPV and cervical cancer statistics in Saudi Arabia. (2007) 4 3-12.
2. Shukla S., Bharti A.C., Mahata S. et al. Infection of human papillomaviruses in cancers of different human organ sites. Indian J. Med. Res. (2009) 130 222-233.
3. Kerkar S.C., Latta S., Salvi V., Mania-Pramanik J. Human Papillomavirus infection in asymptomatic population. Sex Reprod. Healthc (2011) 2 7-11.
4. Bosch F.X., Lorincz A., Munoz N., Meijer C.J., Shah K.V. The causal relation between human papillomavirus and cervical cancer. J. Clin. Pathol. (2002) 55 244-265.
5. Pillai R.M., Babu J.M., Jissa V.T. et al. Region-wise distribution of high-risk human papillomavirus types in squamous cell carcinomas of the cervix in India. Int. J. Gynecol. Cancer (2010) 20 1046-1051.
6. Munoz N., Bosch F.X., de Sanjose S. et al. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N. Engl. J. Med. (2003) 348 518-527.
7. Smith J.S., Herrero R., Bosetti C. et al. Herpes simplex virus-2 as a human papillomavirus cofactor in the etiology of invasive cervical cancer. J. Natl Cancer Inst. (2002) 94 1604-1613.
8. Smith J.S., Bosetti C., Munoz N. et al. Chlamydia trachomatis and invasive cervical cancer: a pooled analysis of the IARC multicentric case-control study. Int. J. Cancer (2004) 111 431-439.
9. Thomas G.M. Improved treatment for cervical cancer-concurrent chemotherapy and radiotherapy. N. Engl. J. Med. (1999) 340 1198-1200.
10. Ren G., Zhao Y.P., Yang L., Fu C.X. Anti-proliferative effect of clitocine from the mushroom Leucopaxillus giganteus on human cervical cancer HeLa cells by inducing apoptosis. Cancer Lett. (2008) 262 190-200.
11. Jacobson M.D., Weil M., Raff M.C. Programmed cell death in animal development. Cell (1997) 88 347-354.
12. Thompson C.B. Apoptosis in the pathogenesis and treatment of disease. Science (1995) 267 1456-1462.
13. Leist M., Jaattela M. Four deaths and a funeral: from caspases to alternative mechanisms. Nat. Rev. Mol. Cell Biol. (2001) 2 589-598.
14. Rudner J., Lepple-Wienhues A., Budach W. et al. Wild-type, mitochondrial and ER-restricted Bcl-2 inhibit DNA damageinduced apoptosis but do not affect death receptor-induced apoptosis. J. Cell Sci. (2001) 114 4161-4172.
15. Castedo M., Ferri K., Roumier T., Métivier D., Zamzami N., Kroemer G. Quantitation of mitochondrial alterations associated with apoptosis. J. Immunol. Methods (2002) 265 39-47.
16. Nencioni A., Lauber K., Grünebach F. et al. Cyclopentenone prostaglandins induce lymphocyte apoptosis by activating the mitochondrial apoptosis pathway independent of external death receptor signaling. J. Immunol. (2003) 171 5148-5156.
17. Salvesen G.S., Dixit V.M. Caspase activation: the induced proximity model. Proc. Natl. Acad. Sci. USA (1999) 96 10964-11067.
18. Chan S.W., Hegyi L., Scott S., Cary N.R., Weissberg P.L., Bennett M.R. Sensitivity to Fas-mediated apoptosis is determined below receptor level in human vascular smooth muscle cells. Circ. Res. (2000) 86 1038-1046.
19. Chinnaiyan A.M., O'Rourke K., Tewari M., Dixit V.M. FADD, a novel death domain-containing protein, interacts with the death domain of Fas and initiates apoptosis. Cell (1995) 81 505-512.
20. LeBlanc H.N., Ashkenazi A. Apo2L/TRAIL and its death and decoy receptors. Cell Death Differ. (2003) 10 66-75.
21. Huang Y., Sheikh M.S. TRAIL death receptors and cancer therapeutics. Toxicol. Appl. Pharmacol. (2007) 224 284-289.
22. Khan N., Adhami V.M., Mukhtar H. Apoptosis by dietary agents for prevention and treatment of cancer. Biochem. Pharmacol. (2008) 76 1333-1339.
23. Boffetta P., Couto E., Wichmann J. et al. Fruit and vegetable intake and overall cancer risk in the European prospective investigation into cancer and nutrition (EPIC). J. Natl Cancer Inst. (2010) 102 529-537.
24. Slattery M.L., Edwards S.L., Ma K.N., Friedman G.D. Colon cancer screening, lifestyle, and risk of colon cancer. Cancer Causes Control (2000) 11 555-563.
25. Kroon P., Williamson G. Polyphenols: dietary components with established benefits to health? J. Sci. Food Agric. (2005) 85 1239-1240.
26. Letchoumy P.V., Mohan K.V., Prathiba D., Hara Y., Nagini S. Comparative evaluation of antiproliferative, antiangiogenic and apoptosis inducing potential of black tea polyphenols in the hamster buccal pouch carcinogenesis model. J. Carcinog. (2007) 6 19.
27. Chakraborty P.K., Mustafi S.B., Ganguly S., Chatterjee M., Raha S. Resveratrol induces apoptosis in K562 (chronic myelogenous leukemia) cells by targeting a key survival protein, heat shock protein 70. Cancer Sci. (2008) 99 1109-1116.
28. Kim S.H., Kim S.H., Lee S.C., Song Y.S. Involvement of both extrinsic and intrinsic apoptotic pathways in apoptosis induced by genistein in human cervical cancer cells. Ann. N. Y. Acad. Sci. (2009) 1171 196-201.
29. Watson J.L., Greenshields A., Hill R., Hilchie A., Lee P.W., Giacomantonio C.A. Curcumin-induced apoptosis in ovarian carcinoma cells is p53-independent and involves p38 mitogen-activated protein kinase activation and downregulation of Bcl-2 and survivin expression and Akt signaling. Mol. Carcinog. (2010) 49 13-24.
30. Gil-Izquierdo A., Gil M.I., Ferreres F., Tomás-Barberán F.A. In vitro availability of flavonoids and other phenolics in orange juice. J. Agric. Food Chem. (2001) 49 1035-1041.
31. Galati E.M., Trovato A., Kirjavainen S., Forestieri A.M., Rossitto A., Monforte M.T. Biological effects of hesperidin, a citrus flavonoid. (Note III). Antihypertensive and diuretic activity in rat. Farmaco (1996) 51 219-221.
32. Garg A., Garg S., Zaneveld L.J., Singla A.K.Chemistry and pharmacology of the citrus bioflavonoid hesperidin. Phytother. Res. (2001) 15 655-669.
33. Choi E.J. Hesperetin induced G1-phase cell cycle arrest in human breast cancer MCF-7 cells: involvement of CDK4 and p21. Nutr. Cancer (2007) 59 115-119.
34. Cai Y.Z., Luo Q., Sun M., Corke H. Antioxidant activity and phenolic compounds of 112 traditional. Life Sci. (2004) 74 2157-2184.
35. Guthrie N., Carroll K.K. Inhibition of mammary cancer by citrus flavonoids. Adv. Exp. Med. Biol. (1998) 439 227-236.
36. Aranganathan S., Selvam J.P., Nalini N. Effect of hesperetin, a citrus flavonoid, on bacterial enzymes and carcinogen-induced aberrant crypt foci in colon cancer rats: a dose-dependent study. J. Pharm. Pharmacol. (2008) 60 1385-1392.
37. Choi E.J., Ahn W.S. Neuroprotective effects of chronic hesperetin administration in mice. Arch. Pharm. Res. (2008) 31 1457-1462.
38. Scholz E.P., Zitron E., Kiesecker C., Thomas D., Kathofer S., Kreuzer J. Orange flavonoid hesperetin modulates cardiac hERG potassium channel via binding to amino acids F656. Nutr. Metab. Cardiovasc. Dis. (2006) 17 666-675.
39. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods (1983) 65 55-63.
40. Smiley S.T., Reers M., Mollola-Hartsorn C., Lin M., Chen A., Smith T.W. Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1. Proc. Natl. Acad. Sci. USA (1991) 88 671-675.
41. Leite M., Quinta-Costa M., Leite P.S., Guimarães J.E. Critical evaluation of techniques to detect and measure cell death-study in a model of UV radiation of the leukaemic cell line HL60. Anal. Cell. Pathol. (1999) 19 139-151.
42. Grassi G., Scaggiante B., Farra R., Dapas B., Agostini F., Baiz D. The expression levels of the translational factors eEF1A 1/2 correlate with cell growth but not apoptosis in hepatocellular carcinoma cell lines with different differentiation grade. Biochimie (2007) 89 1544-1552.
43. Yuan J.S., Reed A., Chen F., Stewart C.N. Jr Statistical analysis of real-time PCR data. BMC Bioinformatics (2006) 7 85.
44. Knekt P., Kumpulainen J., Jarvinen R., Rissanen H., Heliovaara M., Reunanen A. Flavonoid intake and risk of chronic diseases. Am. J. Clin. Nutr. (2002) 76 560-568.
45. Le M.L., Murphy S.P., Hankin J., Wilkens L.R., Kolonel L.N. Intake of flavonoids and lung cancer. J. Natl Cancer Inst. (2000) 92 154-160.
46. Alshatwi A.A., Shafi G., Hasan T.N., Al-Hazzani A., Alsaif M.A., Alfawaz M.A. Apoptosis-mediated inhibition on human breast cancer cell proliferation by lemon citrus extract. Asian Pac. J. Cancer Prev. (2011) 12 1583-1587.
47. Kurowska E.M., Spence J.D., Jordan J., Wetmore S., Freeman D.J., Piche L.A. HDL-cholesterol-raising effect of orange juice in subjects with hypercholesterolemia. Am. J. Clin. Nutr. (2000) 72 1095-1100.
48. Choi E.J., Kim G.D., Chee K.M., Kim G.H. The effects of hesperetin on vessel structure formation in mouse embryonic stem (mES) cells. Nutrition (2006) 22 947-951.
49. Rodriguez M., Schaper J. Apoptosis: measurement and technical issues. J. Mol. Cell. Cardiol. (2005) 38 15-20.
50. Nakazato T., Ito K., Ikeda Y., Kizaki M. Green tea component, catechin, induces apoptosis of human malignant B cells via production of reactive oxygen species. Clin. Cancer Res. (2005) 11 6040-6049.
51. Mattivi F., Guzzon R., Vrhovsek U., Stefanini M., Velasco R. Metabolite profiling of grape: flavonols and anthocyanins. J. Agric. Food Chem. (2006) 54 7692-7702.
52. Castillo-Munoz N., Gómez-Alonso S., García-Romero E., Hermosín-Gutiérrez I. Flavonol profiles of Vitis vinifera red grapes and their single-cultivar wines. J. Agric. Food Chem. (2007) 55 992-1002.
53. Shan B.E., Wang M.X., Li R.G. Quercetin inhibit human sw480 colon cancer growth in association with inhibition of cyclin d1 and surviving expression through wnt/b-catenin signaling pathway. Cancer Invest. (2009) 27 604-612.
54. Wang W., Heideman L., Chung C.S., Pelling J.C., Koehler K.J., Birt D.F. Cell-cycle arrest at G2/M and growth inhibition by apigenin in human colon carcinoma cell lines. Mol. Carcinog. (2000) 28 102-110.
55. Alshatwi A.A. Catechin hydrate suppresses MCF-7 proliferation through TP53/Caspase-mediated apoptosis. J. Exp. Clin. Cancer Res. (2010) 29 167.
56. Al-Hazzani A.A., Alshatwi A.A. Catechin hydrate inhibits proliferation and mediates apoptosis of SiHa human cervical cancer cells. Food Chem. Toxicol. (2011) 49 3281-3286.
57. Ahmeda K., Weia Z., Zhaoa Q., Nakajimab N., Matsunagac T., Ogasawarac M. Role of fatty acid chain length on the induction of apoptosis by newly synthesized catechin derivatives. Chem. Biol. Interact. (2010) 185 182-188.
58. Earnshaw W.C., Martins L.M., Kaufmann S.H. Mammalian caspases structure, activation, substrates, and functions during apoptosis. Annu. Rev. Biochem. (1999) 68 383-424.
59. Riedl S.J., Shi Y. Molecular mechanisms of caspase regulation during apoptosis. Nat. Rev. Mol. Cell Biol. (2004) 5 897-907.
60. Pommier Y., Sordet O., Antony S., Haywrd R.L., Kohn K.W. Apoptosis defects and chemotherapy resistance: molecular interaction maps and networks. Oncogene (2004) 23 2934-2949.
61. Bernard B., Fest T., Prétet J.L., Mougin C. Staurosporine-induced apoptosis of HPV positive and negative human cervical cancer cells from different points in the cell cycle. Cell Death Differ. (2001) 8 234-244.