174
Views
30
CrossRef citations to date
0
Altmetric
Original Research

Apoptosis and oxidative stress as relevant mechanisms of antitumor activity and genotoxicity of ZnO-NPs alone and in combination with N-acetyl cysteine in tumor-bearing mice

, , &
Pages 3911-3928 | Published online: 27 May 2019

References

  • Laurenti M, Cauda V. ZnO nanostructures for tissue engineering applications. Nanomaterials (Basel). 2017;7:11. doi:10.3390/nano7120458
  • Saptarshi SR, Feltis BN, Wright PF, Lopata AL. Investigating the immunomodulatory nature of zinc oxide nanoparticles at sub-cytotoxic levels in vitro and after intranasal instillation in vivo. J Nanobiotechnology. 2015;13:6. doi:10.1186/s12951-015-0067-725645871
  • Kalpana V, Devi Rajeswari V. A review on green synthesis, biomedical applications, and toxicity studies of ZnO NPs. Bioinorg Chem Appl. 2018;2018:3569758.
  • Rokbani H, Daigle F, Ajji A. Combined Effect Of Ultrasound Stimulations And Autoclaving On The Enhancement Of Antibacterial Activity Of ZnO and SiO(2)/ZnO Nanoparticles. Nanomaterials (Basel). 2018;8:3. doi:10.3390/nano8030129
  • Youssef AM, El-Nahrawy AM, Abou Hammad AB. Sol-gel synthesis and characterizations of hybrid chitosan-PEG/calcium silicate nanocomposite modified with ZnO-NPs and (E102) for optical and antibacterial applications. Int J Biol Macromol. 2017;97:561–567. doi:10.1016/j.ijbiomac.2017.01.05928108409
  • Hassan HFH, Mansour AM, Abo‐Youssef AMH, Elsadek BE, Messiha BAS. Zinc oxide nanoparticles as a novel anticancer approach; in vitro and in vivo evidence. Clin Exp Pharmacol Physiol. 2017;44(2):235–243. doi:10.1111/1440-1681.1268127718258
  • Palanikumar L, Ramasamy S, Balachandran C. Antibacterial and cytotoxic response of nano zinc oxide in gram negative bacteria and colo 320 human adenocarcinoma cancer cells. Curr Nanosci. 2013;9(4):469–478. doi:10.2174/1573413711309040009
  • Namvar F, Rahman HS, Mohamad R, et al. Cytotoxic effects of biosynthesized zinc oxide nanoparticles on murine cell lines. Evid Based Complement Alternat Med. 2015;2015:593014.
  • Wahab R, Siddiqui MA, Saquib Q, et al. ZnO nanoparticles induced oxidative stress and apoptosis in HepG2 and MCF-7 cancer cells and their antibacterial activity. Colloids Surf B Biointerfaces. 2014;117:267–276. doi:10.1016/j.colsurfb.2014.02.03824657613
  • Wahab R, Kaushik NK, Verma AK, et al. Fabrication and growth mechanism of ZnO nanostructures and their cytotoxic effect on human brain tumor U87, cervical cancer HeLa, and normal HEK cells. J Biol Inorg Chem. 2011;16(3):431–442. doi:10.1007/s00775-010-0740-021140179
  • Selvakumari D, Deepa R, Mahalakshmi V, Subhashini P, Lakshminarayan N. Anti cancer activity of ZnO nanoparticles on MCF7 (breast cancer cell) and A549 (lung cancer cell). Asian Res Pub Net J Eng Appl Sci. 2015;10:5418–5421.
  • Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–674. doi:10.1016/j.cell.2011.02.01321376230
  • Sherr CJ. Principles of tumor suppression. Cell. 2004;116(2):235–246.14744434
  • Ahamed M, Karns M, Goodson M, et al. DNA damage response to different surface chemistry of silver nanoparticles in mammalian cells. Toxicol Appl Pharmacol. 2008;233(3):404–410. doi:10.1016/j.taap.2008.09.01518930072
  • 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(1):85–89. doi:10.1016/j.bbrc.2010.02.15220494116
  • Chougule M, Patel AR, Sachdeva P, Jackson T, Singh M. Anticancer activity of Noscapine, an opioid alkaloid in combination with Cisplatin in human non-small cell lung cancer. Lung Cancer. 2011;71(3):271–282. doi:10.1016/j.lungcan.2010.06.00220674069
  • Deng X, Gao F, Flagg T, Anderson J, May WS. Bcl2’s flexible loop domain regulates p53 binding and survival. Mol Cell Biol. 2006;26(12):4421–4434. doi:10.1128/MCB.01647-0516738310
  • Landsiedel R, Ma-Hock L, Van Ravenzwaay B, et al. Gene toxicity studies on titanium dioxide and zinc oxide nanomaterials used for UV-protection in cosmetic formulations. Nanotoxicology. 2010;4(4):364–381. doi:10.3109/17435390.2010.50669420925445
  • Li C-H, Shen -C-C, Cheng Y-W, et al. Organ biodistribution, clearance, and genotoxicity of orally administered zinc oxide nanoparticles in mice. Nanotoxicology. 2012;6(7):746–756. doi:10.3109/17435390.2011.62071721950449
  • Wang B, Feng W, Wang M, et al. Acute toxicological impact of nano-and submicro-scaled zinc oxide powder on healthy adult mice. J Nanopart Res. 2008;10(2):263–276. doi:10.1007/s11051-007-9245-3
  • Surekha P, Kishore AS, Srinivas A, et al. Repeated dose dermal toxicity study of nano zinc oxide with Sprague-Dawley rats. Cutan Ocul Toxicol. 2012;31(1):26–32. doi:10.3109/15569527.2011.59575021830917
  • Millea PJ. N-acetylcysteine: multiple clinical applications. Am Fam Physician. 2009;80:3.
  • Agarwal A, Munoz-Nájar U, Klueh U, Shih S-C, Claffey KP. N-acetyl-cysteine promotes angiostatin production and vascular collapse in an orthotopic model of breast cancer. Am J Pathol. 2004;164(5):1683–1696. doi:10.1016/S0002-9440(10)63727-315111315
  • Albini A, Morini M, D’Agostini F, et al. Inhibition of angiogenesis-driven Kaposi’s sarcoma tumor growth in nude mice by oral N-acetylcysteine. Cancer Res. 2001;61(22):8171–8178.11719447
  • Spagnuolo G, D’Antò V, Cosentino C, Schmalz G, Schweikl H, Rengo S. Effect of N-acetyl-L-cysteine on ROS production and cell death caused by HEMA in human primary gingival fibroblasts. Biomaterials. 2006;27(9):1803–1809. doi:10.1016/j.biomaterials.2005.10.02216289659
  • Fu A-L, Dong Z-H, Sun M-J. Protective effect of N-acetyl-L-cysteine on amyloid β-peptide-induced learning and memory deficits in mice. Brain Res. 2006;1109(1):201–206. doi:10.1016/j.brainres.2006.06.04216872586
  • Fukami G, Hashimoto K, Koike K, Okamura N, Shimizu E, Iyo M. Effect of antioxidant N-acetyl-L-cysteine on behavioral changes and neurotoxicity in rats after administration of methamphetamine. Brain Res. 2004;1016(1):90–95. doi:10.1016/j.brainres.2004.04.07215234256
  • Kim JH, Jeong MS, Kim DY, Her S, Wie MB. Zinc oxide nanoparticles induce lipoxygenase-mediated apoptosis and necrosis in human neuroblastoma SH-SY5Y cells. Neurochem Int. 2015;90:204–214. doi:10.1016/j.neuint.2015.09.00226364578
  • Albini A, D’Agostini F, Giunciuglio D, Paglieri I, Balansky R, De Flora S. Inhibition of invasion, gelatinase activity, tumor take and metastasis of malignant cells by N-acetylcysteine. Int J Cancer. 1995;61(1):121–129.7705924
  • Singh R, Shah R, Turner C, Regueira O, Vasylyeva TL. N-acetylcysteine renoprotection in methotrexate induced nephrotoxicity and its effects on B-cell lymphoma. Indian J Med Paediatr Oncol. 2015;36(4):243–248. doi:10.4103/0971-5851.17154526811594
  • Kozak YS, PanchuK R, Skorokhyd N, Lehka L, StoIka R. Impact of N-acetylcysteine on antitumor activity of doxorubIcin and landomycin in NK/ly lymphoma-bearing mIce. Ukrainian Biochem J. 2018;90(2):46–54. doi:10.15407/ubj90.02.046
  • Nargi JL, Ratan RR, Griffin D E. p53-independent inhibition of proliferation and p21(WAF1/Cip1)-modulated induction of cell death by the antioxidants N-acetylcysteine and vitamin E. Neoplasia. 1999;1(6):544–556.10935502
  • Kawakami S, Kageyama Y, Fujii Y, Kihara K, Oshima H. Inhibitory effect of N-acetylcysteine on invasion and MMP-9 production of T24 human bladder cancer cells. Anticancer Res. 2001;21(1a):213–219.11299737
  • Supabphol A, Muangman V, Chavasiri W, Supabphol R, Gritsanapan W. N-acetylcysteine inhibits proliferation, adhesion, migration and invasion of human bladder cancer cells. J Med Assoc Thai. 2009;92(9):1171–1177.19772176
  • Lee YJ, Lee DM, Lee CH, et al. Suppression of human prostate cancer PC-3 cell growth by N-acetylcysteine involves over-expression of Cyr61. Toxicol In Vitro. 2011;25(1):199–205. doi:10.1016/j.tiv.2010.10.02021055460
  • Lee MF, Chan CY, Hung HC, Chou IT, Yee AS, Huang CY. N-acetylcysteine (NAC) inhibits cell growth by mediating the EGFR/Akt/HMG box-containing protein 1 (HBP1) signaling pathway in invasive oral cancer. Oral Oncol. 2013;49(2):129–135. doi:10.1016/j.oraloncology.2012.08.00322944050
  • Hann SS, Zheng F, Zhao S. Targeting 3-phosphoinositide-dependent protein kinase 1 by N-acetyl-cysteine through activation of peroxisome proliferators activated receptor alpha in human lung cancer cells, the role of p53 and p65. J Exp Clin Cancer Res. 2013;32:43. doi:10.1186/1756-9966-32-4323867003
  • Muldoon LL, Wu YJ, Pagel MA, Neuwelt EA. N-acetylcysteine chemoprotection without decreased cisplatin antitumor efficacy in pediatric tumor models. J Neurooncol. 2015;121(3):433–440. doi:10.1007/s11060-014-1657-125411097
  • Sharma R. Kinetic measurements from in situ TEM observations. Microsc Res Tech. 2009;72(3):144–152. doi:10.1002/jemt.2066719130611
  • Tice RR, Shelby MD. International workshop on standardisation of genotoxicity test procedures. Report of in vivo subgroup. Mutat Res. 1994;312(3):287–292.7514740
  • Sanceau J, Poupon MF, Delattre O, Sastre-Garau X, Wietzerbin J. Strong inhibition of Ewing tumor xenograft growth by combination of human interferon-alpha or interferon-beta with ifosfamide. Oncogene. 2002;21(50):7700–7709. doi:10.1038/sj.onc.120588112400012
  • Mayer AG, Tortugas T. Florida, as a station for research in biology. Science. 1903;17(422):190–192. doi:10.1126/science.17.422.19017818040
  • Habig WH, Pabst MJ, Jakoby WB. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem. 1974;249(22):7130–7139.4436300
  • Aebi H. Catalase in vitro. Methods Enzymol. 1984;105:121–126.6727660
  • Tice RR, Agurell E, Anderson D, et al. Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing. Environ Mol Mutagen. 2000;35(3):206–221.10737956
  • Krishna PG, Ananthaswamy PP, Yadavalli T, Mutta NB, Sannaiah A, Shivanna Y. ZnO nanopellets have selective anticancer activity. Mater Sci Eng C. 2016;62:919–926. doi:10.1016/j.msec.2016.02.039
  • Degen A, Kosec M. Effect of pH and impurities on the surface charge of zinc oxide in aqueous solution. J Eur Ceram Soc. 2000;20(6):667–673. doi:10.1016/S0955-2219(99)00203-4
  • Rasmussen JW, Martinez E, Louka P, Wingett DG. Zinc oxide nanoparticles for selective destruction of tumor cells and potential for drug delivery applications. Expert Opin Drug Deliv. 2010;7(9):1063–1077. doi:10.1517/17425247.2010.50256020716019
  • Papo N, Shahar M, Eisenbach L, Shai Y. A novel lytic peptide composed of DL-amino acids selectively kills cancer cells in culture and in mice. J Biol Chem. 2003;278(23):21018–21023. doi:10.1074/jbc.M21120420012646578
  • Peetla C, Vijayaraghavalu S, Labhasetwar V. Biophysics of cell membrane lipids in cancer drug resistance: implications for drug transport and drug delivery with nanoparticles. Adv Drug Deliv Rev. 2013;65(13–14):1686–1698. doi:10.1016/j.addr.2013.09.00424055719
  • Moos PJ, Chung K, Woessner D, Honeggar M, Cutler NS, Veranth JM. ZnO particulate matter requires cell contact for toxicity in human colon cancer cells. Chem Res Toxicol. 2010;23(4):733–739. doi:10.1021/tx900203v20155942
  • Bisht G, Rayamajhi S. ZnO nanoparticles: a promising anticancer agent. Nanobiomed. 2016;3(Godište 2016):3–9. doi:10.5772/63437
  • Carmody RJ, Cotter TG. Signalling apoptosis: a radical approach. Redox Rep. 2001;6(2):77–90. doi:10.1179/13510000110153608511450987
  • Guan R, Kang T, Lu F, Zhang Z, Shen H, Liu M. Cytotoxicity, oxidative stress, and genotoxicity in human hepatocyte and embryonic kidney cells exposed to ZnO nanoparticles. Nanoscale Res Lett. 2012;7(1):602. doi:10.1186/1556-276X-7-60223110934
  • Zijno A, De Angelis I, De Berardis B, et al. Different mechanisms are involved in oxidative DNA damage and genotoxicity induction by ZnO and TiO2 nanoparticles in human colon carcinoma cells. Toxicol In Vitro. 2015;29(7):1503–1512. doi:10.1016/j.tiv.2015.06.00926079941
  • Pryor WA. Cancer and free radicals. Basic Life Sci. 1986;39:45–59.3767848
  • Kang DH. Oxidative stress, DNA damage, and breast cancer. AACN Clin Issues. 2002;13(4):540–549.12473916
  • Sharma V, Anderson D, Dhawan A. Zinc oxide nanoparticles induce oxidative stress and genotoxicity in human liver cells (HepG2). J Biomed Nanotechnol. 2011;7(1):98–99.21485822
  • Hackenberg S, Scherzed A, Technau A, et al. Cytotoxic, genotoxic and pro-inflammatory effects of zinc oxide nanoparticles in human nasal mucosa cells in vitro. Toxicol In Vitro. 2011;25(3):657–663. doi:10.1016/j.tiv.2011.01.00321232592
  • Sharma V, Anderson D, Dhawan A. Zinc oxide nanoparticles induce oxidative DNA damage and ROS-triggered mitochondria mediated apoptosis in human liver cells (HepG2). Apoptosis. 2012;17(8):852–870. doi:10.1007/s10495-012-0705-622395444
  • Pandurangan M, Enkhtaivan G, Kim DH. Anticancer studies of synthesized ZnO nanoparticles against human cervical carcinoma cells. J Photochem Photobiol B. 2016;158:206–211. doi:10.1016/j.jphotobiol.2016.03.00226985734
  • Bai Aswathanarayan J, Rai Vittal R, Muddegowda U. Anticancer activity of metal nanoparticles and their peptide conjugates against human colon adenorectal carcinoma cells. Artif Cells Nanomed Biotechnol. 2018;46(7):1444–1451. doi:10.1080/21691401.2017.137365528884587
  • Gao F, Ma N, Zhou H, et al. Zinc oxide nanoparticles-induced epigenetic change and G2/M arrest are associated with apoptosis in human epidermal keratinocytes. Int J Nanomedicine. 2016;11:3859–3874. doi:10.2147/IJN.S10702127570453
  • Boroumand Moghaddam A, Moniri M, Azizi S, et al. Eco-friendly formulated zinc oxide nanoparticles: induction of cell cycle arrest and apoptosis in the MCF-7 cancer cell line. Genes (Basel). 2017;8:10. doi:10.3390/genes8100281
  • Rajeshkumar S, Kumar SV, Ramaiah A, Agarwal H, Lakshmi T, Roopan SM. Biosynthesis of zinc oxide nanoparticles usingMangifera indica leaves and evaluation of their antioxidant and cytotoxic properties in lung cancer (A549) cells. Enzyme Microb Technol. 2018;117:91–95. doi:10.1016/j.enzmictec.2018.06.00930037558
  • Othman BA, Greenwood C, Abuelela AF, et al. Targeted cancer therapy: correlative light-electron microscopy shows RGD-targeted ZnO nanoparticles dissolve in the intracellular environment of triple negative breast cancer cells and cause apoptosis with intratumor heterogeneity (Adv. Healthcare Mater. 11/2016). Adv Healthc Mater. 2016;5(11):1248. doi:10.1002/adhm.20167005327275627
  • Chen N, Hanly L, Rieder M, Yeger H, Koren G. The effect of N-acetylcysteine on the antitumor activity of ifosfamide. Can J Physiol Pharmacol. 2011;89(5):335–343. doi:10.1139/y11-02821609276
  • Hanly L, Figueredo R, Rieder M, Koropatnick J, Koren G. The effects of N-acetylcysteine on ifosfamide efficacy in a mouse xenograft model. Anticancer Res. 2012;32(9):3791–3798.22993321
  • Vimala K, Sundarraj S, Paulpandi M, Vengatesan S, Kannan S. Green synthesized doxorubicin loaded zinc oxide nanoparticles regulates the Bax and Bcl-2 expression in breast and colon carcinoma. Process Biochem. 2014;49(1):160–172. doi:10.1016/j.procbio.2013.10.007
  • Adamcakova-Dodd A, Stebounova LV, Kim JS, et al. Toxicity assessment of zinc oxide nanoparticles using sub-acute and sub-chronic murine inhalation models. Part Fibre Toxicol. 2014;11(1):15. doi:10.1186/1743-8977-11-1524684892
  • Esmaeillou M, Moharamnejad M, Hsankhani R, Tehrani AA, Maadi H. Toxicity of ZnO nanoparticles in healthy adult mice. Environ Toxicol Pharmacol. 2013;35(1):67–71. doi:10.1016/j.etap.2012.11.00323262039
  • Chen N, Aleksa K, Woodland C, Rieder M, Koren G. N-Acetylcysteine prevents ifosfamide-induced nephrotoxicity in rats. Br J Pharmacol. 2008;153(7):1364–1372. doi:10.1038/bjp.2008.1518278066
  • Pati R, Das I, Mehta RK, Sahu R, Sonawane A. Zinc-oxide nanoparticles exhibit genotoxic, clastogenic, cytotoxic and actin depolymerization effects by inducing oxidative stress responses in macrophages and adult mice. Toxicol Sci. 2016;150(2):454–472. doi:10.1093/toxsci/kfw01026794139
  • Arora-Kuruganti P, Lucchesi PA, Wurster RD. Proliferation of cultured human astrocytoma cells in response to an oxidant and antioxidant. J Neurooncol. 1999;44(3):213–221.10720201
  • Kurata S-I. Selective activation of p38 MAPK cascade and mitotic arrest caused by low level oxidative stress. J Biol Chem. 2000;275(31):23413–23416. doi:10.1074/jbc.C00030820010856288
  • Liu M, Wikonkal NM, Brash D E. Induction of cyclin-dependent kinase inhibitors and G(1) prolongation by the chemopreventive agent N-acetylcysteine. Carcinogenesis. 1999;20(9):1869–1872.10469636
  • Havre PA, O’Reilly S, McCormick JJ, Brash D E. Transformed and tumor-derived human cells exhibit preferential sensitivity to the thiol antioxidants, N-acetyl cysteine and penicillamine. Cancer Res. 2002;62(5):1443–1449.11888918