A polysaccharide from pomegranate peels induces the apoptosis of human osteosarcoma cells via the mitochondrial apoptotic pathway

Tumor Biology

Volumn 35, Issue 8, 2014, Pages 7475-7482

  Li, Jun ^a   Zhang, Fujun ^b,c   Wang, Shaohua ^d  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^c Orthopedic Department Kunlun Hospital   (China)

^d Zhengzhou Orthopaedics Hospital   (China)

Author keywords

Anticancer activity; Apoptosis; Osteosarcoma; Polysaccharide; Pomegranate (Punica granatum L.)

Indexed keywords

BAX PROTEIN, HUMAN; CASPASE; POLYSACCHARIDE; PROTEIN BAX; PROTEIN BCL 2;

APOPTOSIS; CELL CYCLE; CELL PROLIFERATION; CHEMISTRY; DOSE RESPONSE; DRUG EFFECTS; HUMAN; ISOLATION AND PURIFICATION; LYTHRACEAE; MITOCHONDRION; OSTEOSARCOMA; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CASPASES; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; MITOCHONDRIA; OSTEOSARCOMA; POLYSACCHARIDES; PROTO-ONCOGENE PROTEINS C-BCL-2; PUNICACEAE;

EID: 84922391936     PISSN: 10104283     EISSN: None     Source Type: Journal    
DOI: 10.1007/s13277-014-1983-0     Document Type: Article

References (54)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, et al. Cancer statistics, 2008. CA Cancer J Clin. 2008;58:71–96.
2. Ferrari S, Palmerini E. Adjuvant and neoadjuvant combination chemotherapy for osteogenic sarcoma. Curr Opin Oncol. 2007;19:341–6.
3. Dass CR, Ek ET, Contreras KG, Choong PF. A novel orthotopic murine model provides insights into cellular and molecular characteristics contributing to human osteosarcoma. Clin Exp Metastasis. 2006;23:367–80.
4. Bielack S, Carrle D, Casali PG. ESMO Guidelines Working Group. Osteosarcoma: ESMO clinical recommendations for diagnosis, treatment and follow-up. Ann Oncol. 2009;20:137–9.
5. Akiyama T, Dass CR, Choong PF. Novel therapeutic strategy for osteosarcoma targeting osteoclast differentiation, bone-resorbing activity, and apoptosis pathway. Mol Cancer Ther. 2008;7:3461–9.
6. Liu SY, Song SX, Lin L, Liu X. Molecular mechanism of cell apoptosis by paclitaxel and pirarubicin in a human osteosarcoma cell line. Chemotherapy. 2010;56:101–7.
7. Shapovalov Y, Benavidez D, Zuch D, Eliseev RA. Proteasome inhibition with bortezomib suppresses growth and induces apoptosis in osteosarcoma. Int J Cancer. 2010;127:67–76.
8. Cheng AC, Lee MF, Tsai ML, Lai CS, Lee JH, Ho CT, et al. Rosmanol potently induces apoptosis through both the mitochondrial apoptotic pathway and death receptor pathway in human colon adenocarcinoma COLO 205 cells. Food Chem Toxicol. 2011;49:485–93.
9. Wang F, Ma R, Yu L. Role of mitochondria and mitochondrial cytochrome c in tubeimoside I-mediated apoptosis of human cervical carcinoma HeLa cell line. Cancer Chemother Pharmacol. 2006;57:389–99.
10. Lansky EP, Newman RA. Punica granatum (pomegranate) and its potential for prevention and treatment of inflammation and cancer. J Ethnopharmacol. 2007;109:117–206.
11. Li Y, Guo C, Yang J, Wei J, Xu J, Cheng S. Evaluation of antioxidant properties of pomegranate peel extract in comparison with pomegranate pulp extract. Food Chem. 2006;96:254–60.
12. Valadares MC, Pereira ERT, Benfica PL, Paula JR. Assessment of mutagenic and antimutagenic effects of Punica granatum in mice. Braz J Pharm Sci. 2010;46:121–7.
13. Zhu C, Liu X. Optimization of extraction process of crude polysaccharides from Pomegranate peel by response surface methodology. Carbohydr Polym. 2013;92:1197–202.
14. Joseph MM, Aravind SR, Varghese S, Mini S, Sreelekha TT. Evaluation of antioxidant, antitumor and immunomodulatory properties of polysaccharide isolated from fruit rind of Punica granatum. Mol Med Rep. 2012;5:489–96.
15. Joseph MM, Aravind SR, George SK, Varghese S, Sreelekha TT. A galactomannan polysaccharide from Punica granatum imparts in vitro and in vivo anticancer activity. Carbohydr Polym. 2013;98:1466–75.
16. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F. Colorimetric method for determination of sugars and related substances. Anal Chem. 1956;28:350–6.
17. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein binding. Anal Biochem. 1976;72:248–54.
18. Filisetti-Cozzi TMCC, Carpita NC. Measurement of uronic acids without interference from neutral sugars. Anal Biochem. 1991;197:157–62.
19. Moalic S, Liagre B, Labrousse F, Beneytout JL. Enhanced apoptosis in retrovirally transfected osteosarcoma cells after exposure to sodium butyrate. Int J Oncol. 2000;16:695–700.
20. van Engeland M, Nieland LJ, Ramaekers FC, Schutte B, Reutelingsperger CP. Annexin V-affinity assay: a review on an apoptosis detection system based on phosphatidylserine exposure. Cytometry. 1998;31:1–9.
21. Moalic S, Liagre B, Le Bail JC, Beneytout JL. Dose-dependent modulation of apoptosis and cyclooxygenase-2 expression in human 1547 osteosarcoma cells by NS-398, a selective cyclooxygenase-2 inhibitor. Int J Oncol. 2001;18:533–40.
22. Cao J, Liu Y, Jia L, Zhou HM, Kong Y, Yang G, et al. Curcumin induces apoptosis through mitochondrial hyperpolarization and mtDNA damage in human hepatoma G2 cells. Free Radic Biol Med. 2007;43:968–75.
23. Johnson LV, Walsh ML, Bockus BJ, Chen LB. Monitoring of relative mitochondrial membrane potential in living cells by fluorescence microscopy. J Cell Biol. 1981;88:526–35.
24. Von Ahsen O, Waterhouse NJ, Kuwana T, Newmeyer DD, Green DR. The ‘harmless’ release of cytochrome c. Cell Death Differ. 2000;7:1192–9.
25. Skulachev VP. Cytochrome c in the apoptotic and antioxidant cascades. FEBS Lett. 1998;423:275–80.
26. Green DR, Reed JC. Mitochondria and apoptosis. Science. 1998;281:1309–12.
27. Schafer ZT, Kornbluth S. The apoptosome: physiological, developmental, and pathological modes of regulation. Dev Cell. 2006;10:549–61.
28. Nouri K, Yazdanparast R. Proliferation inhibition, cell cycle arrest and apoptosis induced in HL-60 cells by a natural diterpene ester from Daphne mucronata. Daru. 2011;19:145–53.
29. Farnebo M, Bykov VJ, Wiman KG. The p53 tumor suppressor: a master regulator of diverse cellular processes and therapeutic target in cancer. Biochem Biophys Res Commun. 2010;396:85–9.
30. Tian Z, Liu YM, Chen SB, Yang JS, Xiao PG, Wang L, et al. Cytotoxicity of two triterpenoids from Nigella glandulifera. Molecules. 2006;11:693–9.
31. Huh JE, Lee EO, Kim MS, Kang KS, Kim CH, Cha BC, et al. Penta-O-galloyl-beta-d-glucose suppresses tumor growth via inhibition of angiogenesis and stimulation of apoptosis: roles of cyclooxygenase-2 and mitogen-activated protein kinase pathways. Carcinogenesis. 2005;26:1436–45.
32. Taraphdar AK, Roy M, Bhattacharya RK. Natural products as inducers of apoptosis: implication for cancer therapy and prevention. Curr Sci. 2001;80:1387–96.
33. Mehta R, Lansky EP. Breast cancer chemopreventive properties of pomegranate (Punica granatum) fruit extracts in a mouse mammary organ culture. Eur J Cancer Prev. 2004;13:345–8.
34. Kim ND, Mehta R, Yu W, Neeman I, Livney T, Amichay A, et al. Chemopreventive and adjuvant therapeutic potential of pomegranate (Punica granatum) for human breast cancer. Breast Cancer Res Treat. 2002;71:203–17.
35. Kawaii S, Lansky EP. Differentiation-promoting activity of pomegranate (Punica granatum) fruit extracts in HL-60 human promyelocytic leukemia cells. J Med Food. 2004;7:13–8.
36. Rettig MB, Heber D, An J, Seeram NP, Rao JY, Liu H, et al. Pomegranate extract inhibits androgen-independent prostate cancer growth through a nuclear factor-kappaB-dependent mechanism. Mol Cancer Ther. 2008;7:2662–71.
37. Ming DS, Pham S, Deb S, Chin MY, Kharmate G, Adomat H, et al. Pomegranate extracts impact the androgen biosynthesis pathways in prostate cancer models in vitro and in vivo. J Steroid Biochem Mol Biol. 2014;143C:19–28.
38. Dikmen M, Ozturk N, Ozturk Y. The antioxidant potency of Punica granatum L. Fruit peel reduces cell proliferation and induces apoptosis on breast cancer. J Med Food. 2011;14:1638–46.
39. Qi F, Li A, Zhao L, Xu H, Inagaki Y, Wang D, et al. Cinobufacini, an aqueous extract from Bufo bufo gargarizans Cantor, induces apoptosis through a mitochondria-mediated pathway in human hepatocellular carcinoma cells. J Ethnopharmacol. 2010;128:654–61.
40. Kroemer G, Galluzzi L, Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol Rev. 2007;87:99–163.
41. Han J, Goldstein LA, Gastman BR, Rabinowich H. Interrelated roles for Mcl-1 and BIM in regulation of TRAIL-mediated mitochondrial apoptosis. J Biol Chem. 2006;281:10153–63.
42. Fu YR, Yi ZJ, Yan YR, Qiu ZY. Hydroxycamptothecin-induced apoptosis in hepatoma SMMC-7721 cells and the role of mitochondrial pathway. Mitochondrion. 2006;6:211–7.
43. Green DR, Evan GI. A matter of life and death. Cancer Cell. 2002;1:19–30.
44. Walesnky LD. BCL-2 in the crosshairs: tipping the balance of life and death. Cell Death Differ. 2006;13:1339–50.
45. Raisova M, Hossini AM, Eberle J, Riebeling C, Wieder T, Sturm I, et al. The Bax/Bcl-2 ratio determines the susceptibility of human melanoma cells to CD95/Fas-mediated apoptosis. J Invest Dermatol. 2001;117:333–40.
46. Hui K, Kanungo A, Elia A, Henderson J. Caspase-3 deficiency reveals a physiologic role for Smac/DIABLO in regulating programmed cell death. Cell Death Differ. 2011;18:1780–90.
47. Chang HY, Yang X. Proteases for cell suicide: functions and regulation of caspases. Microbiol Mol Biol Rev. 2000;64:821–46.
48. Stennicke HR, Salvesen GS. Properties of the caspases. Biochim Biophys Acta. 1998;1387:17–31.
49. Cain K, Brown DG, Langlais C, Cohen GM. Caspase activation involves the formation of the aposome, a large (approximately 700 kDa) caspase-activating complex. J Biol Chem. 1999;274:22686–92.
50. Sun XM, MacFarlane M, Zhuang J, Wolf BB, Green DR, Cohen GM. Distinct caspase cascades are initiated in receptor-mediated and chemical-induced apoptosis. J Biol Chem. 1999;274:5053–60.
51. Tang XL, Yang XY, Jung HJ, Kim SY, Jung SY, Choi DY, et al. Asiatic acid induces colon cancer cell growth inhibition and apoptosis through mitochondrial death cascade. Biol Pharm Bull. 2009;32:1399–405.
52. Zou H, Li Y, Liu X, Wang X. An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J Biol Chem. 1999;274:11549–56.
53. Debatin KM, Krammer PH. Death receptors in chemotherapy and cancer. Oncogene. 2004;23:2950–66.
54. Fulda S, Debatin KM. Extrinsic versus intrinsic apoptosis pathways in anticancer chemotherapy. Oncogene. 2006;25:4798–811.