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Review Article

Effects of nano-titanium dioxide on calcium homeostasis in vivo and in vitro: a systematic review and meta-analysis

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Pages 249-259 | Received 17 Jun 2022, Accepted 30 Aug 2022, Published online: 19 Sep 2022

References

  • Abiko LA, Vitale PM, Favaro DC, Hauk P, Li DW, Yuan JQ, Bruschweiler-Li L, Salinas RK, Bruschweiler R. 2016. Model for the allosteric regulation of the Na+/Ca2+ exchanger NCX. Proteins Struct Funct Bioinform. 84(5):580–590.
  • Alena K, Magdalena B, Marta S, Martina D, Katarina V, Maria D. 2019. Titanium dioxide nanoparticles tested for genotoxicity with the comet and micronucleus assays in vitro, ex vivo and in vivo. Mutat Res Genet Toxicol Environ Mutagen. 843:57–65.
  • Attia HF, Soliman MM, Hassan G, Abdel R, Mohamed AN, Shimaa AI, Mona F, Solcan C. 2013. Hepatoprotective effect of N-acetylcystiene on the toxic hazards of titanium dioxide nanoparticles. Am J Pharmacol Toxicol. 8(4):141–147.
  • Aulestia FJ, Groeling J, Bomfim GHS, Costiniti V, Manikandan V, Chaloemtoem A, Concepcion AR, Li Y, Wagner LE, Idaghdour Y, et al. 2020. Fluoride exposure alters Ca2+ signaling and mitochondrial function in enamel cells. Sci Signal. 13(619):eaay0086.
  • Bergin IL, Witzmann FA. 2013. Nanoparticle toxicity by the gastrointestinal route: evidence and knowledge gaps. IJBNN. 3(1/2):163–162.
  • Berridge MJ, Bootman MD, Roderick HL. 2003. Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol. 4(7):517–529.
  • Brini M, Cali T, Ottolini D, Carafoli E. 2013. Intracellular calcium homeostasis and signaling. In: Banci L, editor. Metallomics and the cell. Metal ions in life sciences. Vol. 12. Dordrecht: Springer; p. 119–168.
  • Brini M. 2009. Plasma membrane Ca2+-ATPase: from a housekeeping function to a versatile signaling role. Pflugers Arch. 457(3):657–664.
  • Burgoyne RD, Helassa N, Mccue HV, Haynes LP. 2019. Calcium sensors in neuronal function and dysfunction. Cold Spring Harb Perspect Biol. 11(5):a035154.
  • Bhullar S, Goyal N, Gupta S. 2021. Rapid green-synthesis of TiO2 nanoparticles for therapeutic applications. RSC Adv. 11(48):30343–30352.
  • Bae JE, Huh MI, Ryu BK, Do JY, Jin SU, Moon JJ, Jung JC, Chang Y, Kim E, Chi SG, et al. 2011. The effect of static magnetic fields on the aggregation and cytotoxicity of magnetic nanoparticles. Biomaterials. 32(35):9401–9414.
  • Chen EYT, Garnica M, Wang YC, Chen CS, Chin WC. 2011. Mucin secretion induced by titanium dioxide nanoparticles. PLoS One. 6(1):e16198.
  • Chen EY, Garnica M, Wang YC, Alexander JM, Chen CS, Wei CC. 2012. A mixture of anatase and rutile TiO2 nanoparticles induces histamine secretion in mast cells. Part Fibre Toxicol. 9:2–2.
  • Chowdhury I, Cwiertny DM, Walker SL. 2012. Combined factors influencing the aggregation and deposition of nano-TiO2 in the presence of humic acid and bacteria. Environ Sci Technol. 46(13):6968–6976.
  • Carmo TLL, Azevedo VC, Siqueira PR, Galvão TD, Santos FA, Martinez CBR, Appoloni CR, Fernandes MN. 2018. Mitochondria-rich cells adjustments and ionic balance in the Neotropical fish Prochilodus lineatus exposed to titanium dioxide nanoparticles. Aquat Toxicol. 200:168–177.
  • Delamere NA, Paterson CA, Borchman D, King KL, Cawood SA. 1991. Calcium transport, Ca2+-ATPase, and lipid order in rabbit ocular lens membranes. Am J Physiol. 260(4 Pt 1):C731–C737.
  • Deng YX, Meng XJ, Ling CM, Lu TJ, Chang HM, Li L, Yang YQ, Song GL, Ding YS. 2022. Nanosized titanium dioxide induced apoptosis and abnormal expression of blood-testis barrier junction proteins through Jnk signaling pathway in TM4 cells. Biol Trace Elem Res. doi:10.1007/s12011-022-03099-5.
  • Dong T, Ni J, Ke W, Xiao L, Tu B. 2015. Effects of benzo(a)pyrene exposure on the ATPase activity and content of Ca in the hippocampus of neonatal Sd rats. J Central South Univ. 4:356.
  • Feng DD, Wang WB, Li CL, An LH, Zhang FM, Li J, Li GZ. 2014. Effects of nano-titanium dioxide exposure on intracellular calcium ion concentration and calpain 1 expression in rat brain cortex. J Environ Health. 4:302–305.
  • Ferris CD, Huganir RL, Snyder SH. 1990. Calcium flux mediated by purified inositol 1,4,5-trisphosphate receptor in reconstituted lipid vesicles is allosterically regulated by adenine nucleotides. Proc Natl Acad Sci U S A. 87(6):2147–2151.
  • Fill M, Gillespie D. 2021. Simulating cardiac Ca2+ release units: effects of Ryr cluster size and Ca2+ buffers on diastolic Ca2+ leak. Pflugers Arch. 473(3):435–446.
  • Foskett JK, White C, Cheung KH, Mak DOD. 2007. Inositol trisphosphate receptor Ca2+ release channels. Physiol Rev. 87(2):593–658.
  • Gao GD. 2013. Reproductive toxicity and gene expression changes in mice induced by nano-titanium dioxide exposure [dissertation]. Suzhou University.
  • Gong DS, Chi XM, Wei JH, Zhou GW, Huang GXY, Zhang L, Wang RW, Lei JL, Chen SRW, Yan N. 2019. Modulation of cardiac ryanodine receptor 2 by calmodulin. Nature. 572(7769):347–351.
  • Gui SX, Sang XZ, Zheng L, Ze YG, Zhao XY, Sheng L, Sun QQ, Cheng Z, Cheng J, Hu RP, et al. 2013. Intragastric exposure to titanium dioxide nanoparticles induced nephrotoxicity in mice, assessed by physiological and gene expression modifications. Part Fibre Toxicol. 10:4.
  • Guo CY, Luo G. 2020. Research progress of calcium homeostasis in neurodegenerative diseases. J Practi Med. 36:263–267.
  • Guo DD, Bi HS, Liu B, Wu QX, Wang DG, Cui Y. 2013. Reactive oxygen species-induced cytotoxic effects of zinc oxide nanoparticles in rat retinal ganglion cells. Toxicol in Vitro. 27(2):731–738.
  • Gitrowski C, Al-Jubory AR, Handy RD. 2014. Uptake of different crystal structures of TiO2 nanoparticles by Caco-2 intestinal cells. Toxicol Lett. 226(3):264–276.
  • Harper AGS, Sage SO. 2016. Trp-Na+/Ca2+ exchanger coupling. In: JA. Rosado, editor. Calcium entry pathways in non-excitable cells: advances in experimental medicine and biology. Vol. 898. p. 67–85. UK: Springer.
  • Hong FS, Sheng L, Ze YG, Hong J, Zhou YJ, Wang L, Liu D, Yu XH, Xu BQ, Zhao XY, et al. 2015. Suppression of neurite outgrowth of primary cultured hippocampal neurons is involved in impairment of glutamate metabolism and NMDA receptor function caused by nanoparticulate TiO2. Biomaterials. 53:76–85.
  • Hong FS, Yu XH, Wu N, Zhang YQ. 2017. Progress of in vivo studies on the systemic toxicities induced by titanium dioxide nanoparticles. Toxicol Res (Camb). 6(2):115–133.
  • Hong FS, Zhou YJ, Zhao XY, Sheng L, Wang L. 2017. Maternal exposure to nanosized titanium dioxide suppresses embryonic development in mice. Int J Nanomed. 12:6197–6204.
  • Hooijmans CR, Rovers MM, De Vries RBM, Leenaars M, Ritskes-Hoitinga M, Langendam MW. 2014. Syrcle’s risk of bias tool for animal studies. BMC Med Res Methodol. 14:43.
  • Hu R, Gong X, Duan Y, Li N, Che Y, Cui Y, Zhou M, Liu C, Wang H, Hong FS. 2010. Neurotoxicological effects and the impairment of spatial recognition memory in mice caused by exposure to TiO2 nanoparticles. Biomaterials. 31(31):8043–8050.
  • Jacobson KH, Gunsolus IL, Kuech TR, Troiano JM, Melby ES, Lohse SE, Hu D, Chrisler WB, Murphy CJ, Orr G, et al. 2015. Lipopolysaccharide density and structure govern the extent and distance of nanoparticle interaction with actual and model bacterial outer membranes. Environ Sci Technol. 49(17):10642–10650.
  • Jaeger A, Weiss DG, Jonas L, Kriehuber R. 2012. Oxidative stress-induced cytotoxic and genotoxic effects of nano-sized titanium dioxide particles in human HaCat keratinocytes. Toxicology. 296(1–3):27–36.
  • Jafarnejad M, Cromer WE, Kaunas RR, Zhang SL, Zawieja DC, Moore JE. 2015. Measurement of shear stress-mediated intracellular calcium dynamics in human dermal lymphatic endothelial cells. Am J Physiol Heart Circ Physiol. 308(7):H697–H706.
  • Jin H, Heller DA, Sharma R, Strano MS. 2009. Size-dependent cellular uptake and expulsion of single-walled carbon nanotubes: single particle tracking and a generic uptake model for nanoparticles. ACS Nano. 3(1):149–158.
  • Johnston H, Brown DM, Kanase N, Euston M, Gaiser BK, Robb CT, Dyrynda E, Rossi AG, Brown ER, Stone V. 2015. Mechanism of neutrophil activation and toxicity elicited by engineered nanomaterials. Toxicol in Vitro. 29(5):1172–1184.
  • Kaplan P, Babusikova E, Lehotsky J, Dobrota D. 2003. Free radical-induced protein modification and inhibition of Ca2+-ATPase of cardiac sarcoplasmic reticulum. Mol Cell Biochem. 248(1-2):41–47.
  • Kawaai K, Hisatsune C, Kuroda Y, Mizutani A, Tashiro T, Mikoshiba K. 2009. 80k-H interacts with inositol 1,4,5-trisphosphate (IP3) receptors and regulates IP3-induced calcium release activity. J Biol Chem. 284(1):372–380.
  • Kelly CV, Leroueil PR, Orr BG, Holl MMB, Andricioaei I. 2008. Poly (amidoamine) dendrimers on lipid bilayers II: effects of bilayer phase and dendrimer termination. J Phys Chem B. 112(31):9346–9353.
  • Kim BG, Park MK, Lee PH, Lee SH, Hong J, Aung MMM, Moe KT, Han NY, Jang AS. 2020. Effects of nanoparticles on neuroinflammation in a mouse model of asthma. Respir Physiol Neurobiol. 271:103292.
  • Li Z, Pan XB, Wang TL, Wang PN, Chen JY, Mi L. 2013. Comparison of the killing effects between nitrogen-doped and pure TiO2 on hela cells with visible light irradiation. Nanoscale Res Lett. 8(1):96.
  • Long TC, Tajuba J, Sama P, Saleh N, Swartz C, Parker J, Hester S, Lowry GV, Veronesi B. 2007. Nanosize titanium dioxide stimulates reactive oxygen species in brain microglia and damages neurons in vitro. Environ Health Perspect. 115(11):1631–1637.
  • Long T, Saleh N, Tilton R, Lowry G, Veronesi BJ. 2006. Titanium dioxide (P25) produces reactive oxygen species in immortalized brain microglia (Bv2): implications for nanoparticle neurotoxicity. Environ Sci Technol. 40(14):4346–4352.
  • Maeda N, Kawasaki T, Nakade S, Yokota N, Taguchi T, Kasai M, Mikoshiba K. 1991. Structural and functional characterization of inositol 1,4,5-trisphosphate receptor channel from mouse cerebellum. J Biol Chem Sci. 266(2):1109–1116.
  • Meng HP, Li D, YZ Y. 2010. Calcium and human health. Stud Trace Elem Health. 27:65–67.
  • Mikoshiba K. 2007. IP3 receptor/Ca2+ channel: from discovery to new signaling concepts. J Neurochem. 102(5):1426–1446.
  • Mikoshiba K. 2015. Role of IP3 receptor signaling in cell functions and diseases. Adv Biol Regul. 57:217–227.
  • Mu YH. 2013. Regulation of Ryr2-Ca2+ release on Sk channel function in mouse cardiomyocytes [dissertation]. Zhengzhou (China): Zhengzhou University.
  • Rose CR, Ziemens D, Verkhratsky A. 2020. On the special role of NCX in astrocytes: translating Na+-transients into intracellular Ca2+ signals. Cell Calcium. 86:102154.
  • Sagawa T, Honda A, Ishikawa R, Miyasaka N, Nagao M, Akaji S, Kida T, Tsujikawa T, Yoshida T, Kawahito Y, et al. 2021. Role of necroptosis of alveolar macrophages in acute lung inflammation of mice exposed to titanium dioxide nanoparticles. Nanotoxicology. 15(10):1312–1330.
  • Sahoo SK, Parveen S, Panda JJ. 2007. The present and future of nanotechnology in human health care. Nanomed Nanotechnol Biol Med. 3(1):20–31.
  • Schneider K, Schwarz M, Burkholder I, Kopp-Schneider A, Edler L, Kinsner-Ovaskainen A, Hartung T, Hoffmann S. 2009. Toxrtool, a new tool to assess the reliability of toxicological data. Toxicol Lett. 189(2):138–144.
  • Shahin NN, Mohamed MM. 2017. Nano-sized titanium dioxide toxicity in rat prostate and testis: possible ameliorative effect of morin. Toxicol Appl Pharmacol. 334:129–141.
  • Shakeel M, Jabeen F, Shabbir S, Asghar MS, Khan MS, Chaudhry AS. 2016. Toxicity of nano-titanium dioxide (TiO2-NP) through various routes of exposure: a review. Biol Trace Elem Res. 172(1):1–36.
  • Shattock MJ, Ottolia M, Bers DM, Blaustein MP, Boguslavskyi A, Bossuyt J, Bridge JHB, Chen-Izu Y, Clancy CE, Edwards A, et al. 2015. Na+/Ca2+ exchange and Na+/K+-ATPase in the heart. J Physiol. 593(6):1361–1382.
  • Sheng L, Wang X, Sang X, Ze Y, Zhao X, Liu D, Gui S, Sun Q, Cheng J, Cheng Z, et al. 2013. Cardiac oxidative damage in mice following exposure to nanoparticulate titanium dioxide. J Biomed Mater Res A. 101(11):3238–3246.
  • Tang D, Dean WL, Borchman D, Paterson CA. 2006. The influence of membrane lipid structure on plasma membrane Ca2+-ATPase activity. Cell Calcium. 39(3):209–216.
  • Vasantharaja D, Ramalingam V. 2018. Neurotoxic effect of titanium dioxide nanoparticles: biochemical and pathological approach in male Wistar rats. Int J App Pharm. 10(4):74.
  • Wang MH, Tan J, Miao YY, Li MM, Zhang Q. 2018. Role of Ca2+ and ion channels in the regulation of apoptosis under hypoxia. Histol Histopathol. 33:11918.
  • Wang WB. 2014. The effect of nanometer titanium dioxide on the central nervous system of rats and its mechanism [dissertation]. Jinan (China): Shandong University.
  • Wang ZJ, Tiruppathi C, Minshall RD, Malik AB. 2009. Size and dynamics of caveolae studied using nanoparticles in living endothelial cells. ACS Nano. 3(12):4110–4116.
  • Windhorst S, Minge D, Bahring R, Huser S, Schob C, Blechner C, Lin HY, Mayr GW, Kindler S. 2012. Inositol-1,4,5-trisphosphate 3-kinase a regulates dendritic morphology and shapes synaptic Ca2+ transients. Cell Signal. 24(3):750–757.
  • Wu QX, Guo DD, Du YX, Liu DM, Wang DG, Bi HS. 2014. UVB irradiation enhances TiO2 nanoparticle-induced disruption of calcium homeostasis in human lens epithelial cells. Photochem Photobiol. 90(6):1324–1331.
  • Xiao AY, Wei L, Xia SL, Rothman S, Yu SP. 2002. Ionic mechanism of ouabain-induced concurrent apoptosis and necrosis in individual cultured cortical neurons. J Neurosci. 22(4):1350–1362.
  • Xiong SJ, George S, Yu HY, Damoiseaux R, France B, Ng KW, Loo JSC. 2013. size influences the cytotoxicity of poly (lactic-co-glycolic acid) (Plga) and titanium dioxide (TiO2) nanoparticles. Arch Toxicol. 87(6):1075–1086.
  • Xu B, Li J, Hu SJ. 2007. 1,4,5-Inositol triphosphate receptor and cardiovascular disease. Int J Internal Med. 34:253–256.
  • Xue CB, Wu JH, Lan FL, Liu W, Yang XL, Zeng FD, Xu HB. 2010. Nano titanium dioxide induces the generation of ros and potential damage in hacat cells under UVA irradiation. J Nanosci Nanotech. 10(12):8500–8507.
  • Yaghi A, Zaman A, Dolovich M. 2010. Primary human bronchial epithelial cells grown from explants. JoVE. 26(37):1789.
  • Yu XH, Hong FS, Zhang YQ. 2016. Cardiac inflammation involving in PKCε or ERK1/2-activated NF-κB signalling pathway in mice following exposure to titanium dioxide nanoparticles. J Hazard Mater. 313:68–77.
  • Yu Q, Sun X, Zhao J, Zhao L, Chen Y, Fan L, Li Z, Sun Y, Wang M, Wang F. 2019. The effects of zinc deficiency on homeostasis of twelve minerals and trace elements in the serum, feces, urine and liver of rats. Nutr Metab (Lond). 16:73.
  • Zaidi A, Fernandes D, Bean JL, Michaelis ML. 2009. Effects of paraquat-induced oxidative stress on the neuronal plasma membrane Ca2+-ATPase. Free Radic Biol Med. 47(10):1507–1514.
  • Zaidi A, Michaelis ML. 1999. Effects of reactive oxygen species on brain synaptic plasma membrane Ca2+-ATPase. Free Radic Biol Med. 27(7–8):810–821.
  • Zhang L, Qiao H. 2019. The regulatory mechanism of calcium homeostasis in vascular endothelial cells. Chin J Cardiovasc Rehabil Med. 28:688–690.
  • Zhang S, Li J, Lykotrafitis G, Bao G, Suresh S. 2009. Size-dependent endocytosis of nanoparticles. Adv Mater. 21:419–424.
  • Zhao JF, Li N, Wang SS, Zhao XY, Wang J, Yan JY, Ruan J, Wang H, Hong FS. 2010. The mechanism of oxidative damage in the nephrotoxicity of mice caused by nano-anatase TiO2. J Exp Nanosci. 5(5):447–462.
  • Zhou YH, Wang K, Wang BS, Pu YP, Zhang J. 2020. Occupational benzene exposure and the risk of genetic damage: a systematic review and meta-analysis. BMC Public Health. 20(1):1113.

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