Generic placeholder image

Anti-Infective Agents

Editor-in-Chief

ISSN (Print): 2211-3525
ISSN (Online): 2211-3533

Research Article

The Cytotoxic and Immunomodulatory Effects of Titanium Dioxide Nanoparticles and Sargassum oligocystum on Toxoplasma gondii In Vitro and In Vivo

Author(s): Negar Asadi, Shahram Khademvatan*, Habib Mohammadzadeh Hajipirloo, Behnam Heshmatiyan, Sadegh Asghari and Masoud Foroutan

Volume 19, Issue 3, 2021

Published on: 16 December, 2020

Page: [317 - 324] Pages: 8

DOI: 10.2174/2211352518999201216095713

Price: $65

Abstract

Objective: This study was undertaken to evaluate the effect of titanium dioxide (TiO2) nanoparticles (NPs) and methanolic extract of Persian Gulf brown algae (Sargassum oligocystum) on the growth and cell death of T. gondii tachyzoites in vitro and in vivo.

Methods: Six- to eight-week-old female BALB/c mice (n = 28) were used for the treatment experiment and infected with 105 T. gondii tachyzoites. Four days after treatment, IFN-γ and the levels of splenic lymphocyte proliferation were measured. All the groups were challenged with T. gondii, and the survival rate of experimental mice was assessed. The effects of TiO2NPs and S. oligocystum on the proliferation of T. gondii were evaluated by MTT and annexin V staining in vitro.

Results: Based on the results, the combination of S. oligocystum extract and TiO2NPs exhibited a more cytotoxic effect compared to their use separately. The results of the challenge test also revealed that mice which received combined treatment had the highest life time expectancy than those receiving the treatment alone.

Conclusion: The simultaneous use of immunomodulatory compounds for the stimulation of the immune system as well as S. oligocystum and TiO2NPs with antiparasitic activity can be promising to develop an effective drug for the treatment of toxoplasmosis.

Keywords: Toxoplasma gondii, Sargassum oligocystum, titanium dioxide, BALB/c, immunomodulatory, nanoparticles.

Graphical Abstract

[1]
Dubey, J.P. History of the discovery of the life cycle of Toxoplasma gondii. Int. J. Parasitol., 2009, 39(8), 877-882.
[http://dx.doi.org/10.1016/j.ijpara.2009.01.005] [PMID: 19630138]
[2]
Rostami, A.; Riahi, S.M.; Fakhri, Y.; Saber, V.; Hanifehpour, H.; Valizadeh, S.; Gholizadeh, M.; Pouya, R.H.; Gamble, H.R. The global seroprevalence of Toxoplasma gondii among wild boars: A systematic review and meta-analysis. Vet. Parasitol., 2017, 244, 12-20.
[http://dx.doi.org/10.1016/j.vetpar.2017.07.013] [PMID: 28917302]
[3]
Foroutan, M.; Fakhri, Y.; Riahi, S.M.; Ebrahimpour, S.; Namroodi, S.; Taghipour, A.; Spotin, A.; Gamble, H.R.; Rostami, A. The global seroprevalence of Toxoplasma gondii in pigs: A systematic review and meta-analysis. Vet. Parasitol., 2019, 269, 42-52.
[http://dx.doi.org/10.1016/j.vetpar.2019.04.012] [PMID: 31079827]
[4]
Khademvatan, S.; Foroutan, M.; Hazrati-Tappeh, K.; Dalvand, S.; Khalkhali, H.; Masoumifard, S.; Hedayati-Rad, F. Toxoplasmosis in rodents: A systematic review and meta-analysis in Iran. J. Infect. Public Health, 2017, 10(5), 487-493.
[http://dx.doi.org/10.1016/j.jiph.2017.01.021] [PMID: 28237696]
[5]
Wang, Z.D.; Liu, H.H.; Ma, Z.X.; Ma, H.Y.; Li, Z.Y.; Yang, Z.B.; Zhu, X.Q.; Xu, B.; Wei, F.; Liu, Q. Toxoplasma gondii infection in immunocompromised patients: a systematic review and meta-analysis. Front. Microbiol., 2017, 8, 389.
[http://dx.doi.org/10.3389/fmicb.2017.00389] [PMID: 28337191]
[6]
Rostami, A.; Riahi, S.M.; Gamble, H.R.; Fakhri, Y.; Nourollahpour Shiadeh, M.; Danesh, M.; Behniafar, H.; Paktinat, S.; Foroutan, M.; Mokdad, A.H.; Hotez, P.J.; Gasser, R.B. Global prevalence of latent toxoplasmosis in pregnant women: a systematic review and meta-analysis. Clin. Microbiol. Infect., 2020, 26(6), 673-683.
[http://dx.doi.org/10.1016/j.cmi.2020.01.008] [PMID: 31972316]
[7]
Foroutan-Rad, M.; Majidiani, H.; Dalvand, S.; Daryani, A.; Kooti, W.; Saki, J.; Hedayati-Rad, F.; Ahmadpour, E. Toxoplasmosis in blood donors: a systematic review and meta-analysis. Transfus. Med. Rev., 2016, 30(3), 116-122.
[http://dx.doi.org/10.1016/j.tmrv.2016.03.002] [PMID: 27145927]
[8]
Fallahi, S.; Rostami, A.; Nourollahpour Shiadeh, M.; Behniafar, H.; Paktinat, S. An updated literature review on maternal-fetal and reproductive disorders of Toxoplasma gondii infection. J. Gynecol. Obstet. Hum. Reprod., 2018, 47(3), 133-140.
[http://dx.doi.org/10.1016/j.jogoh.2017.12.003] [PMID: 29229361]
[9]
Rostami, A.; Riahi, S.M.; Contopoulos-Ioannidis, D.G.; Gamble, H.R.; Fakhri, Y.; Shiadeh, M.N.; Foroutan, M.; Behniafar, H.; Taghipour, A.; Maldonado, Y.A.; Mokdad, A.H.; Gasser, R.B. Acute Toxoplasma infection in pregnant women worldwide: A systematic review and meta-analysis. PLoS Negl. Trop. Dis., 2019, 13(10), e0007807.
[http://dx.doi.org/10.1371/journal.pntd.0007807] [PMID: 31609966]
[10]
Antczak, M.; Dzitko, K.; Długońska, H. Human toxoplasmosis-Searching for novel chemotherapeutics. Biomed. Pharmacother., 2016, 82, 677-684.
[http://dx.doi.org/10.1016/j.biopha.2016.05.041] [PMID: 27470411]
[11]
Montazeri, M.; Sharif, M.; Sarvi, S.; Mehrzadi, S.; Ahmadpour, E.; Daryani, A. A systematic review of in vitro and in vivo activities of anti-Toxoplasma drugs and compounds (2006–2016). Front. Microbiol., 2017, 8, 25.
[http://dx.doi.org/10.3389/fmicb.2017.00025] [PMID: 28163699]
[12]
Sharif, M.; Sarvi, S.; Pagheh, A.S.; Asfaram, S.; Rahimi, M.T.; Mehrzadi, S.; Ahmadpour, E.; Gholami, S.; Daryani, A. The efficacy of herbal medicines against Toxoplasma gondii during the last 3 decades: a systematic review. Can. J. Physiol. Pharmacol., 2016, 94(12), 1237-1248.
[http://dx.doi.org/10.1139/cjpp-2016-0039] [PMID: 27564395]
[13]
Organization, W.H. A report of the consultation meeting on traditional and modern medicine: harmonizing two approaches, 22–26 November 1999; West Pacific Region: Beijing, China, 2000.
[14]
Masoumifard, S.; Mohammadzadeh Hajipirloo, H.; Khezri, P.; Heshmatiayan, B.; Manafpour, N.; Khademvatan, S. The effect of the Persian Gulf brown algae extract (Sargassum Oligocystum) on Leishmania major (MRHO/IR/75/ER) in vitro. Indian J. Med. Microbiol., 2017, 11, 75-82.
[15]
Bolaños, J.M.; Baleta, F.N.; Cairel, J.D. Antimicrobial Properties of Sargassum spp.(Phaeophyceae) against Selected Aquaculture pathogens. Int. J. Curr. Microbiol. Appl. Sci., 2017, 6, 1024-1037.
[http://dx.doi.org/10.20546/ijcmas.2017.602.115]
[16]
Kuda, T.; Tsunekawa, M.; Goto, H.; Araki, Y. Antioxidant properties of four edible algae harvested in the Noto Peninsula, Japan. J. Food Compos. Anal., 2005, 18, 625-633.
[http://dx.doi.org/10.1016/j.jfca.2004.06.015]
[17]
Mohebali, M.; Rezayat, M.; Gilani, K.; Sarkar, S.; Akhoundi, B.; Esmaeili, J. Nanosilver in the treatment of localized cutaneous leishmaniasis caused by Leishmania major (MRHO/IR/75/ER): an in vitro and in vivo study. Daru, 2009, 17(4), 285-289.
[18]
Allahverdiyev, A.M.; Abamor, E.S.; Bagirova, M.; Baydar, S.Y.; Ates, S.C.; Kaya, F.; Kaya, C.; Rafailovich, M. Investigation of antileishmanial activities of Tio2@Ag nanoparticles on biological properties of L. tropica and L. infantum parasites, in vitro. Exp. Parasitol., 2013, 135(1), 55-63.
[http://dx.doi.org/10.1016/j.exppara.2013.06.001] [PMID: 23792003]
[19]
Schanen, B.C.; Das, S.; Reilly, C.M.; Warren, W.L.; Self, W.T.; Seal, S.; Drake, D.R., III Immunomodulation and T helper TH₁/TH₂ response polarization by CeO₂ and TiO₂ nanoparticles. PLoS One, 2013, 8(5), e62816.
[http://dx.doi.org/10.1371/journal.pone.0062816] [PMID: 23667525]
[20]
Gaafar, M.R.; Mady, R.F.; Diab, R.G.; Shalaby, T.I. Chitosan and silver nanoparticles: promising anti-toxoplasma agents. Exp. Parasitol., 2014, 143, 30-38.
[http://dx.doi.org/10.1016/j.exppara.2014.05.005] [PMID: 24852215]
[21]
Fujita, K.; Horie, M.; Kato, H.; Endoh, S.; Suzuki, M.; Nakamura, A.; Miyauchi, A.; Yamamoto, K.; Kinugasa, S.; Nishio, K.; Yoshida, Y.; Iwahashi, H.; Nakanishi, J. Effects of ultrafine TiO2 particles on gene expression profile in human keratinocytes without illumination: involvement of extracellular matrix and cell adhesion. Toxicol. Lett., 2009, 191(2-3), 109-117.
[http://dx.doi.org/10.1016/j.toxlet.2009.08.011] [PMID: 19695317]
[22]
van der Ven, A.J.; Schoondermark-van de Ven, E.M.; Camps, W.; Melchers, W.J.; Koopmans, P.P.; van der Meer, J.W.; Galama, J.M. Anti-toxoplasma effect of pyrimethamine, trimethoprim and sulphonamides alone and in combination: implications for therapy. J. Antimicrob. Chemother., 1996, 38(1), 75-80.
[http://dx.doi.org/10.1093/jac/38.1.75] [PMID: 8858459]
[23]
Jamali, A.; Mahdavi, M.; Shahabi, S.; Hassan, Z.M.; Sabahi, F.; Javan, M.; Farsani, M.J.; Parsania, M.; Bamdad, T. Naloxone, an opioid receptor antagonist, enhances induction of protective immunity against HSV-1 infection in BALB/c mice. Microb. Pathog., 2007, 43(5-6), 217-223.
[http://dx.doi.org/10.1016/j.micpath.2007.06.001] [PMID: 17669616]
[24]
Foroutan-Rad, M.; Khademvatan, S.; Saki, J.; Hashemitabar, M. Holothuria leucospilota Extract Induces Apoptosis in Leishmania major Promastigotes. Iran. J. Parasitol., 2016, 11(3), 339-349.
[PMID: 28127339]
[25]
Tavakoli, P.; Ghaffarifar, F.; Delavari, H.; Shahpari, N. Efficacy of manganese oxide (Mn2O3) nanoparticles against Leishmania major in vitro and in vivo. J. Trace Elem. Med. Biol., 2019, 56, 162-168.
[http://dx.doi.org/10.1016/j.jtemb.2019.08.003] [PMID: 31473559]
[26]
Tajbakhsh, S.; Pouyan, M.; Zandi, K.; Bahramian, P.; Sartavi, K.; Fouladvand, M.; Asayesh, G.; Barazesh, A. in vitro study of antibacterial activity of the alga Sargassum oligocystum from the Persian Gulf. Eur. Rev. Med. Pharmacol. Sci., 2011, 15(3), 293-298.
[PMID: 21528775]
[27]
Gong, P.; Li, H.; He, X.; Wang, K.; Hu, J.; Tan, W. Preparation and antibacterial activity of Fe3O4@ Ag nanoparticles. Nanotechnology, 2007, 18, 285604.
[http://dx.doi.org/10.1088/0957-4484/18/28/285604]
[28]
Telles, C.B.S.; Mendes-Aguiar, C.; Fidelis, G.P.; Frasson, A.P.; Pereira, W.O.; Scortecci, K.C. Immunomodulatory effects and antimicrobial activity of heterofucans from Sargassum filipendula. J. Appl. Phycol., 2018, 30, 569-578.
[http://dx.doi.org/10.1007/s10811-017-1218-z]
[29]
Latha, T.S.; Reddy, M.C.; R Durbaka, P.V.; Muthukonda, S.V.; Lomada, D. Immunomodulatory properties of titanium dioxide nanostructural materials. Indian J. Pharmacol., 2017, 49(6), 458-464.
[http://dx.doi.org/10.4103/ijp.IJP_536_16] [PMID: 29674801]
[30]
Mehdinezhad, N.; Ghannadi, A.; Yegdaneh, A. Phytochemical and biological evaluation of some Sargassum species from Persian Gulf. Res. Pharm. Sci., 2016, 11(3), 243-249.
[PMID: 27499794]
[31]
McNeil, S.E. Nanotechnology for the biologist. J. Leukoc. Biol., 2005, 78(3), 585-594.
[http://dx.doi.org/10.1189/jlb.0205074] [PMID: 15923216]
[32]
Deng, Z.J.; Liang, M.; Monteiro, M.; Toth, I.; Minchin, R.F. Nanoparticle-induced unfolding of fibrinogen promotes Mac-1 receptor activation and inflammation. Nat. Nanotechnol., 2011, 6(1), 39-44.
[http://dx.doi.org/10.1038/nnano.2010.250] [PMID: 21170037]
[33]
Thevenot, P.; Cho, J.; Wavhal, D.; Timmons, R.B.; Tang, L. Surface chemistry influences cancer killing effect of TiO2 nanoparticles. Nanomedicine (Lond.), 2008, 4(3), 226-236.
[http://dx.doi.org/10.1016/j.nano.2008.04.001] [PMID: 18502186]
[34]
Sun, Q.; Tan, D.; Zhou, Q.; Liu, X.; Cheng, Z.; Liu, G.; Zhu, M.; Sang, X.; Gui, S.; Cheng, J.; Hu, R.; Tang, M.; Hong, F. Oxidative damage of lung and its protective mechanism in mice caused by long-term exposure to titanium dioxide nanoparticles. J. Biomed. Mater. Res. A, 2012, 100(10), 2554-2562.
[http://dx.doi.org/10.1002/jbm.a.34190] [PMID: 22528760]
[35]
Gonçalves, D.M.; Chiasson, S.; Girard, D. Activation of human neutrophils by titanium dioxide (TiO2) nanoparticles. Toxicol. in vitro, 2010, 24(3), 1002-1008.
[http://dx.doi.org/10.1016/j.tiv.2009.12.007] [PMID: 20005940]
[36]
Mikaeiloo, H.; Ghaffarifar, F.; Dalimi, A.; Sharifi, Z.; Hassan, Z.M. Apoptotic activity and anti-Toxoplasma effects of artemether on the tachyzoites and experimental infected Vero and J774 cell lines by Toxoplasma gondii. Indian J. Pharmacol., 2016, 48(2), 179-185.
[http://dx.doi.org/10.4103/0253-7613.178838] [PMID: 27127321]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy