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Original Articles

Antiproliferative Effect of Vine Stem Extract from Spatholobus Suberectus Dunn on Rat C6 Glioma Cells Through Regulation of ROS, Mitochondrial Depolarization, and P21 Protein Expression

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Pages 605-619 | Received 19 Mar 2017, Accepted 03 Feb 2018, Published online: 18 Apr 2018

References

  • Ostrom QT, Gittleman H, Fulop J, Liu M, Blanda R, et al.: CBTRUS statistical report: Primary brain and central nervous system tumors diagnosed in the United States in 2008–2012. Neuro Oncol 17(Suppl 4), iv1–iv62, 2015. doi:10.1093/neuonc/nov189.
  • Siegel RL, Miller KD, and Jemal A: Cancer statistics, 2015. CA Cancer J Clin 65, 5–29, 2015. doi:10.3322/caac.21254.
  • Huang R, Ke W, Han L, Li J, Liu S, et al.: Targeted delivery of chlorotoxin-modified DNA-loaded nanoparticles to glioma via intravenous administration. Biomaterials 32, 2399–2406, 2011. doi:10.1016/j.biomaterials.2010.11.079.
  • Simon HU, Haj-Yehia A, and Levi-Schaffer F: Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 5, 415–418, 2000. doi:10.1023/A:1009616228304.
  • Schumacker PT: Reactive oxygen species in cancer cells: live by the sword, die by the sword. Cancer Cell 10, 175–176, 2006. doi:10.1016/j.ccr.2006.08.015.
  • Wiseman H and Halliwell B: Damage to DNA by reactive oxygen and nitrogen species: role in inflammatory disease and progression to cancer. Biochem J 313(Pt 1), 17–29, 1996. doi:10.1042/bj3130017.
  • Clerkin JS, Naughton R, Quiney C, and Cotter TG: Mechanisms of ROS modulated cell survival during carcinogenesis. Cancer Lett 266, 30–36, 2008. doi:10.1016/j.canlet.2008.02.029 .
  • Pelicano H, Carney D, and Huang P: ROS stress in cancer cells and therapeutic implications. Drug Resist Updat 7, 97–110, 2004. doi:10.1016/j.drup.2004.01.004.
  • Ray PD, Huang BW, and Tsuji Y: Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 24, 981–990, 2012. doi:10.1016/j.cellsig.2012.01.008.
  • Yakes FM and Van Houten B: Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc Natl Acad Sci U S A 94, 514–519, 1997. doi:10.1073/pnas.94.2.514.
  • Ziech D, Franco R, Pappa A, and Panayiotidis MI: Reactive oxygen species (ROS)–induced genetic and epigenetic alterations in human carcinogenesis. Mutat Res 711, 167–173, 2011. doi:10.1016/j.mrfmmm.2011.02.015.
  • Forcados GE, James DB, Sallau AB, Muhammad A, and Mabeta P: Oxidative stress and carcinogenesis: potential of phytochemicals in Breast Cancer Therapy. Nutr Cancer 69, 365–374, 2017. doi.org/10.1080/01635581.2017.1267777.
  • Owen RW, Giacosa A, Hull WE, Haubner R, Spiegelhalder B, et al.: The antioxidant/anticancer potential of phenolic compounds isolated from olive oil. Eur J Cancer 36, 1235–1247, 2000. doi:10.1016/S0959-8049(00)00103-9.
  • Trachootham D, Alexandre J, and Huang P: Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat Rev Drug Discov 8, 579–591, 2009. doi:10.1038/nrd2803.
  • Wang J and Yi J: Cancer cell killing via ROS: to increase or decrease, that is the question. Cancer Biol Ther 7, 1875–1884, 2008. doi:10.4161/cbt.7.12.7067.
  • Liu B, Tan X, Liang J, Wu S, Liu J, et al.: A reduction in reactive oxygen species contributes to dihydromyricetin-induced apoptosis in human hepatocellular carcinoma cells. Sci Rep 4, 7041, 2014. doi:10.1038/srep07041.
  • Jeong CH and Joo SH: Downregulation of reactive oxygen species in apoptosis. J Cancer Prev 21, 13–20, 2016. doi:10.15430/JCP.2016.21.1.13.
  • Kim SJ, Hwang E, Yi SS, Song KD, Lee HK, et al.: Sea Buckthorn Leaf extract inhibits glioma cell growth by reducing reactive oxygen species and promoting apoptosis. Appl Biochem Biotechnol 182, 1663–1674, 2017. doi.org/10.1007/s12010-017-2425-4.
  • Pimm SL and Joppa LN: How many plant species are there, where are they, and at what rate are they going extinct? Annals of the Missouri Botanical Garden 100, 170–176, 2015. doi:10.3417/2012018.
  • Nobili S, Lippi D, Witort E, Donnini M, Bausi L, et al.: Natural compounds for cancer treatment and prevention. Pharmacol Res 59, 365–378, 2009. doi:10.1016/j.phrs.2009.01.017.
  • Reddy L, Odhav B, and Bhoola KD: Natural products for cancer prevention: a global perspective. Pharmacol Ther 99, 1–13, 2003. doi:10.1016/S0163-7258(03)00042-1.
  • Jeong JC, Jang SW, Kim TH, Kwon CH, and Kim YK: Mulberry fruit (Moris fructus) extracts induce human glioma cell death in vitro through ROS-dependent mitochondrial pathway and inhibits glioma tumor growth in vivo. Nutr Cancer 62, 402–412, 2010. doi:10.1080/01635580903441287.
  • Li RW, David Lin G, Myers SP, and Leach DN: Anti-inflammatory activity of Chinese medicinal vine plants. J Ethnopharmacol 85, 61–67, 2003. doi:10.1016/S0378-8741(02)00339-2.
  • Pang J, Guo JP, Jin M, Chen ZQ, Wang XW, et al.: Antiviral effects of aqueous extract from Spatholobus suberectus Dunn. Against coxsackievirus B3 in mice. Chin J Integr Med 17, 764–769, 2011. doi:10.1007/s11655-011-0642-1.
  • Wang DX, Liu P, Chen YH, Chen RY, Guo DH, et al.: Stimulating effect of catechin, an active component of Spatholobus suberectus Dunn, on bioactivity of hematopoietic growth factor. Chin Med J (Engl) 121, 752–755, 2008.
  • Chen SR, Wang AQ, Lin LG, Qiu HC, Wang YT, et al.: In vitro study on anti-hepatitis C virus activity of Spatholobus suberectus Dunn. Molecules 21, 1367, 2016. doi:10.3390/molecules21101367.
  • Zhang R, Liu C, Liu X, Guo Y: Protective effect of Spatholobus suberectus on brain tissues in cerebral ischemia. Am J Transl Res 8, 3963–3969, 2016.
  • Fu Q, Tang Y, Luo X, Yang G, He W, et al.: Anti-tumor activity and mechanism with SSCE of Spatholobus suberctus. Zhongguo Zhong Yao Za Zhi 34, 1570–1573, 2009.
  • Peng F, Meng CW, Zhou QM, Chen JP, and Xiong L: Cytotoxic evaluation against breast cancer cells of Isoliquiritigenin analogues from spatholobus suberectus and their synthetic derivatives. J Nat Prod 79, 248–251, 2016. doi:10.1021/acs.jnatprod.5b00774.
  • Wang ZY, Wang DM, Loo TY, Cheng Y, Chen LL, et al.: Spatholobus suberectus inhibits cancer cell growth by inducing apoptosis and arresting cell cycle at G2/M checkpoint. J Ethnopharmacol 133, 751–758, 2011. doi:10.1016/j.jep.2010.11.004.
  • Tang Y, Fu Q, He W, Sun YK, Wang YZ, et al.: Non-apoptotic programmed cell death induced by extract of Spatholobus suberctus in human lung cancer A549 cells. Zhongguo Zhong Yao Za Zhi 33, 2040–2044, 2008.
  • Cui YJ, Liu P, and Chen RY: Studies on the chemical constituents of Spatholobus suberectus Dunn. Yao Xue Xue Bao 37, 784–787, 2002.
  • Yoon JS, Sung SH, Park JH, and Kim YC: Flavonoids from Spatholobus suberectus. Arch Pharm Res 27, 589–592, 2004. doi:10.1007/BF02980154.
  • Tang RN, Qu XB, Guan SH, Xu PP, Shi YY, et al.: Chemical constituents of Spatholobus suberectus. Chin J Nat Med 10, 32–35, 2012. doi:10.1016/S1875-5364(12)60007-7 doi.org/10.3724/SP.J.1009.2012.00032.
  • Deeken JF and Loscher W: The blood-brain barrier and cancer: transporters, treatment, and Trojan horses. Clin Cancer Res 13, 1663–1674, 2007. doi:10.1158/1078-0432.CCR-06-2854.
  • Liu Y, Ran R, Chen J, Kuang Q, Tang J, et al.: Paclitaxel loaded liposomes decorated with a multifunctional tandem peptide for glioma targeting. Biomaterials 35, 4835–4847, 2014. doi:10.1016/j.biomaterials.2014.02.031.
  • Rong Y, Durden DL, Van Meir EG, and Brat DJ: ‘Pseudopalisading’ necrosis in glioblastoma: A familiar morphologic feature that links vascular pathology, hypoxia, and angiogenesis. J Neuropathol Exp Neurol 65, 529–539, 2006. doi:10.1097/00005072-200606000-00001.
  • Hassas-Roudsari M, Chang PR, Pegg RB, and Tyler RT: Antioxidant capacity of bioactives extracted from canola meal by subcritical water, ethanolic and hot water extraction. Food Chem 114, 717–726, 2009. doi:10.1016/j.foodchem.2008.09.097.
  • Dudonne S, Vitrac X, Coutiere P, Woillez M, and Merillon JM: Comparative study of antioxidant properties and total phenolic content of 30 plant extracts of industrial interest using DPPH, ABTS, FRAP, SOD, and ORAC assays. J Agric Food Chem 57, 1768–1774, 2009. doi:10.1021/jf803011r.
  • He Q, Yao K, Jia D, Fan H, Liao X, et al.: Determination of total catechins in tea extracts by HPLC and spectrophotometry. Nat Prod Res 23, 93–100, 2009. doi:10.1080/14786410801886682.
  • Miyake JA, Benadiba M, and Colquhoun A: Gamma-linolenic acid inhibits both tumour cell cycle progression and angiogenesis in the orthotopic C6 glioma model through changes in VEGF, Flt1, ERK1/2, MMP2, cyclin D1, pRb, p53 and p27 protein expression. Lipids Health Dis 8, 8, 2009. doi:10.1186/1476-511X-8-8.
  • Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402–408, 2001. doi:10.1006/meth.2001.1262.
  • Hong M, Song KD, Lee HK, Yi S, Lee YS, et al.: Fibrates inhibit the apoptosis of Batten disease lymphoblast cells via autophagy recovery and regulation of mitochondrial membrane potential. In Vitro Cell Dev Biol-Anim 52, 349–355, 2016. doi:10.1007/s11626-015-9979-7.
  • Cai Y, Luo Q, Sun M, and Corke H: Antioxidant activity and phenolic compounds of 112 traditional Chinese medicinal plants associated with anticancer. Life Sci 74, 2157–2184, 2004. doi:10.1016/j.lfs.2003.09.047.
  • Vistica DT, Skehan P, Scudiero D, Monks A, Pittman A, et al.: Tetrazolium-based assays for cellular viability: a critical examination of selected parameters affecting formazan production. Cancer Res 51, 2515–2520, 1991.
  • Ren Y, Zhou X, Mei M, Yuan XB, Han L, et al.: MicroRNA-21 inhibitor sensitizes human glioblastoma cells U251 (PTEN-mutant) and LN229 (PTEN-wild type) to taxol. BMC Cancer 10, 27, 2010. doi:10.1186/1471-2407-10-27.
  • Kondo Y, Kondo S, Tanaka Y, Haqqi T, Barna BP, et al.: Inhibition of telomerase increases the susceptibility of human malignant glioblastoma cells to cisplatin-induced apoptosis. Oncogene 16, 2243–2248, 1998. doi:10.1038/sj.onc.1201754.
  • Sanchez-Perez I and Perona R: Lack of c-Jun activity increases survival to cisplatin. FEBS Lett 453, 151–158, 1999. doi:10.1016/S0014-5793(99)00690-0.
  • Evan GI and Vousden KH: Proliferation, cell cycle and apoptosis in cancer. Nature 411, 342–348, 2001. doi:10.1038/35077213.
  • Waldman T, Zhang Y, Dillehay L, Yu J, Kinzler K, et al.: Cell-cycle arrest versus cell death in cancer therapy. Nat Med 3, 1034–1036, 1997. doi:10.1038/nm0997-1034.
  • Gomes A, Fernandes E, and Lima JLFC: Fluorescence probes used for detection of reactive oxygen species. J Biochem Biophys Methods 65, 45–80, 2005. doi:10.1016/j.jbbm.2005.10.003.
  • Salvioli S, Ardizzoni A, Franceschi C, and Cossarizza A: JC-1, but not DiOC6(3) or rhodamine 123, is a reliable fluorescent probe to assess delta psi changes in intact cells: implications for studies on mitochondrial functionality during apoptosis. FEBS Lett 411, 77–82, 1997. doi:10.1016/S0014-5793(97)00669-8.
  • Guo YF, Xiao P, Lei SF, Deng FY, Xiao GG, et al.: How is mRNA expression predictive for protein expression? A correlation study on human circulating monocytes. Acta Biochimica Et Biophysica Sinica 40, 426–436, 2008. doi:10.1111/j.1745-7270.2008.00418.x.
  • Ruch RJ, Cheng SJ, and Klaunig JE: Prevention of cytotoxicity and inhibition of intercellular communication by antioxidant catechins isolated from Chinese green tea. Carcinogenesis 10, 1003–1008, 1989. doi:10.1093/carcin/10.6.1003.
  • Galati G and O'Brien PJ: Potential toxicity of flavonoids and other dietary phenolics: significance for their chemopreventive and anticancer properties. Free Radic Biol Med 37, 287–303, 2004. doi:10.1016/j.freeradbiomed.2004.04.034.
  • Havsteen BH: The biochemistry and medical significance of the flavonoids. Pharmacol Ther 96, 67–202, 2002. doi:10.1016/S0163-7258(02)00298-X.
  • Middleton E, Jr., Kandaswami C, and Theoharides TC: The effects of plant flavonoids on mammalian cells: implications for inflammation, heart disease, and cancer. Pharmacol Rev 52, 673–751, 2000.
  • Kumar S and Pandey AK: Chemistry and biological activities of flavonoids: an overview. Sci World J 2013, 162750, 2013. doi:10.1155/2013/162750.
  • Normen L, Johnsson M, Andersson H, van Gameren Y, and Dutta P: Plant sterols in vegetables and fruits commonly consumed in Sweden. Eur J Nutr 38, 84–89, 1999. doi:10.1007/s003940050048.
  • Hrabovski N, Sinadinovic-Fiser S, Nikolovski B, Sovilj M, and Borota O: Phytosterols in pumpkin seed oil extracted by organic solvents and supercritical CO2. Eur J Lipid Sci Technol 114, 1204–1211, 2012. doi:10.1002/ejlt.201200009.
  • Kimura ET, Ebert DM, and Dodge PW: Acute toxicity and limits of solvent residue for sixteen organic solvents. Toxicol Appl Pharmacol 19, 699–704, 1971. doi:10.1016/0041-008X(71)90301-2.
  • Ling WH, and Jones PJ: Dietary phytosterols: a review of metabolism, benefits and side effects. Life Sci 57, 195–206, 1995. doi:10.1016/0024-3205(95)00263-6.
  • Woyengo TA, Ramprasath VR, and Jones PJ: Anticancer effects of phytosterols. Eur J Clin Nutr 63, 813–820, 2009. doi:10.1038/ejcn.2009.29.
  • Lindley C, McCune JS, Thomason TE, Lauder D, Sauls A, et al.: Perception of chemotherapy side effects cancer versus noncancer patients. Cancer Pract 7, 59–65, 1999. doi:10.1046/j.1523-5394.1999.07205.x.
  • Taixiang W, Munro AJ, and Guanjian L: Chinese medical herbs for chemotherapy side effects in colorectal cancer patients. Cochrane Database Syst Rev 25, CD004540, 2005. doi:10.1002/14651858.CD004540.pub2.
  • Shu X, McCulloch M, Xiao H, Broffman M, and Gao J: Chinese herbal medicine and chemotherapy in the treatment of hepatocellular carcinoma: a meta-analysis of randomized controlled trials. Integr Cancer Ther 4, 219–229, 2005. doi:10.1177/1534735405279927 doi.org/10.1177/1534735405279927.
  • Qi F, Li A, Inagaki Y, Gao J, Li J, et al.: Chinese herbal medicines as adjuvant treatment during chemo- or radio-therapy for cancer. Biosci Trends 4, 297–307, 2010.
  • Fleischer T, Chang TT, Chiang JH, Sun MF, and Yen HR: Improved survival with integration of Chinese herbal medicine therapy in patients with acute Myeloid Leukemia: a nationwide population-based cohort study. Integr Cancer Ther 16, 156–164, 2016. doi:10.1177/1534735416664171.
  • Porter AG and Janicke RU: Emerging roles of caspase-3 in apoptosis. Cell Death Differ 6, 99–104, 1999. doi:10.1038/sj.cdd.4400476.
  • Valko M, Rhodes CJ, Moncol J, Izakovic M, and Mazur M: Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact 160, 1–40, 2006. doi:10.1016/j.cbi.2005.12.009.
  • Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, et al.: Respiratory burst oxidases: the engines of ROS signaling. Curr Opin Plant Biol 14, 691–699, 2011. doi:10.1016/j.pbi.2011.07.014.
  • Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, et al.: ROS signaling: the new wave? Trends Plant Sci 16, 300–309, 2011. doi:10.1016/j.tplants.2011.03.007.
  • Gupta S: Molecular signaling in death receptor and mitochondrial pathways of apoptosis (Review). Int J Oncol 22, 15–20, 2003.
  • Zamzami N, Marchetti P, Castedo M, Decaudin D, Macho A, et al.: Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J Exp Med 182, 367–377, 1995. doi:10.1084/jem.182.2.367.
  • Heiskanen KM, Bhat MB, Wang HW, Ma J, and Nieminen AL: Mitochondrial depolarization accompanies cytochrome c release during apoptosis in PC6 cells. J Biol Chem 274, 5654–5658, 1999. doi:10.1074/jbc.274.9.5654.
  • Yang J, Liu X, Bhalla K, Kim CN, Ibrado AM, et al.: Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275, 1129–1132, 1997. doi:10.1126/science.275.5303.1129.
  • Wang G, Wang JJ, Chen XL, Du SM, Li DS, et al.: The JAK2/STAT3 and mitochondrial pathways are essential for quercetin nanoliposome-induced C6 glioma cell death. Cell Death Dis 4, e746, 2013. doi:10.1038/cddis.2013.242.
  • Twig G, Hyde B, and Shirihai OS: Mitochondrial fusion, fission and autophagy as a quality control axis: the bioenergetic view. Biochim Biophys Acta 1777, 1092–1097, 2008. doi:10.1016/j.bbabio.2008.05.001.
  • Twig G, Elorza A, Molina AJ, Mohamed H, Wikstrom JD, et al.: Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J 27, 433–446, 2008. doi:10.1038/sj.emboj.7601963.
  • Macleod KF, Sherry N, Hannon G, Beach D, Tokino T, et al.: p53-dependent and independent expression of p21 during cell growth, differentiation, and DNA damage. Genes Dev 9, 935–944, 1995. doi:10.1101/gad.9.8.935.
  • Abbas T and Dutta A: p21 in cancer: intricate networks and multiple activities. Nat Rev Cancer 9, 400–414, 2009. doi:10.1038/nrc2657.
  • Frankel RH, Bayona W, Koslow M, and Newcomb EW: p53 mutations in human malignant gliomas: comparison of loss of heterozygosity with mutation frequency. Cancer Res 52, 1427–1433, 1992.
  • Muller PA and Vousden KH: p53 mutations in cancer. Nat Cell Biol 15, 2–8, 2013. doi:10.1038/ncb2641.
  • Polager S and Ginsberg D: p53 and E2f: partners in life and death. Nat Rev Cancer 9, 738–748, 2009. doi:10.1038/nrc2718.
  • Wu X and Levine AJ: p53 and E2F-1 cooperate to mediate apoptosis. Proc Natl Acad Sci U S A 91, 3602–3606, 1994. doi:10.1073/pnas.91.9.3602.
  • Hickman ES, Moroni MC, and Helin K: The role of p53 and pRB in apoptosis and cancer. Curr Opin Genet Dev 12, 60–66, 2002. doi:10.1016/S0959-437X(01)00265-9.
  • Zhu H, Zhang L, Wu S, Teraishi F, Davis JJ, et al.: Induction of S-phase arrest and p21 overexpression by a small molecule 2[[3-(2,3-dichlorophenoxy)propyl] amino]ethanol in correlation with activation of ERK. Oncogene 23, 4984–4992, 2004. doi:10.1038/sj.onc.1207645.
  • Prentice RL: A generalization of the probit and logit methods for dose response curves. Biometrics 32, 761–768, 1976. doi:10.2307/2529262.
  • Kalish LA: Efficient design for estimation of median lethal dose and quantal dose-response curves. Biometrics 46, 737–48, 1990. doi:10.2307/2532092.
  • Turner PV, Brabb T, Pekow C, and Vasbinder MA: Administration of substances to laboratory animals: routes of administration and factors to consider. J Am Assoc Lab Anim Sci 50, 600–613, 2011.
  • Chen L, Lee MJ, Li H, and Yang CS: Absorption, distribution, elimination of tea polyphenols in rats. Drug Metab Dispos 25, 1045–1050, 1997.
  • Miyazawa T: Absorption, metabolism and antioxidative effects of tea catechin in humans. Biofactors 13, 55–59, 2000. doi:10.1002/biof.5520130110.
  • Scalbert A, Morand C, Manach C, and Remesy C: Absorption and metabolism of polyphenols in the gut and impact on health. Biomed Pharmacother 56, 276–282, 2002. doi:10.1016/S0753-3322(02)00205-6.
  • Nair AB and Jacob S: A simple practice guide for dose conversion between animals and human. J Basic Clin Pharm 7, 27–31, 2016. doi:10.4103/0976-0105.177703.
  • Barnard R and Gurevich KG: In vitro bioassay as a predictor of in vivo response. Theor Biol Med Model 2, 3, 2005. doi:10.1186/1742-4682-2-3.
  • Spielmann H, Genschow E, Liebsch M, and Halle W: Determination of the starting dose for Acute Oral Toxicity (LD50) testing in the up and down procedure (UDP) from Cytotoxicity data. Altern Lab Anim 27, 957–966, 1999.

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