Molecular mechanisms underlying titanium dioxide nanoparticles (TiO₂NP) induced autophagy in mesenchymal stem cells (MSC)

References

• Alaraby, M., B. Annangi, R. Marcos, and A. Hernandez. 2016. Drosophila melanogaster as a suitable in vivo model to determine potential side effects of nanomaterials: A review. J. Toxicol. Environ. Health B 19:65–104. doi:10.1080/10937404.2016.1166466.
   PubMed Web of Science ®Google Scholar
• Arthur, C. R., J. T. Gupton, G. E. Kellogg, W. A. Yeudall, M. C. Cabot, I. F. Newsham, and D. A. Gewirtz. 2007. Autophagic cell death, polyploidy and senescence induced in breast tumor cells by the substituted pyrrole jg-03-14, a novel microtubule poison. Biochem. Pharmacol. 74:981–91. doi:10.1016/j.bcp.2007.07.003.
   PubMed Web of Science ®Google Scholar
• Azad, M. B., Y. Chen, and S. B. Gibson. 2009. Regulation of autophagy by reactive oxygen species (ROS): Implications for cancer progression and treatment. Antioxid. Redox. Signal 11:777–90. doi:10.1089/ARS.2008.2270.
   PubMed Web of Science ®Google Scholar
• Bakand, S., A. Hayes, and F. Dechsakulthorn. 2012. Nanoparticles: A review of particle toxicology following inhalation exposure. Inhal. Toxicol. 24:125–35. doi:10.3109/08958378.2010.642021.
   PubMed Web of Science ®Google Scholar
• Cheng, Y., F. Qiu, S. Tashiro, S. Onodera, and T. Ikejima. 2008. ERK and JNK mediate TNF alpha-induced p53 activation in apoptotic and autophagic l929 cell death . Biochem. Biophys. Res. Commun. 376:483–88. doi:10.1016/j.bbrc.2008.09.018.
   PubMed Web of Science ®Google Scholar
• Chuang, S. M., I. C. Wang, and J. L. Yang. 2000. Roles of JNK, p38 and ERK mitogen-activated protein kinases in the growth inhibition and apoptosis induced by cadmium. Carcinogenesis 21:1423–32. doi:10.1093/carcin/21.7.1423.
   PubMed Web of Science ®Google Scholar
• Crane, F. L., and H. Low. 2008. Reactive oxygen species generation at the plasma membrane for antibody control. Autoimmun Rev 7:518–522. doi: 10.1016/j.autrev.2008.04.004.
   Google Scholar
• Crosera, M., M. Bovenzi, G. Maina, G. Adami, C. Zanette, C. Florio, and F. Filon Larese. 2009. Nanoparticle dermal absorption and toxicity: A review of the literature. Int. Arch. Occup. Environ. Health 82:1043–55. doi:10.1007/s00420-009-0458-x.
   PubMed Web of Science ®Google Scholar
• Dhupal, M., J. M. Oh, D. R. Tripathy, S. K. Kim, S. B. Koh, and K. S. Park. 2018. Immunotoxicity of titanium dioxide nanoparticles via simultaneous induction of apoptosis and multiple toll-like receptors signaling through ros-dependent SAPK/JNK and p38 MAPK activation. Int. J. Nanomed. 13:6735–50. doi:10.2147/ijn.S176087.
   PubMed Web of Science ®Google Scholar
• Dobrzyńska, M. M., A. Gajowik, J. Radzikowska, A. Lankoff, M. Dušinská, and M. Kruszewski. 2014. Genotoxicity of silver and titanium dioxide nanoparticles in bone marrow cells of rats in vivo. Toxicology. 315:86–91. doi:10.1016/j.tox.2013.11.012.
   PubMed Web of Science ®Google Scholar
• Freitas, G. P., H. B. Lopes, A. L. G. Almeida, R. P. F. Abuna, R. Gimenes, L. E. B. Souza, D. T. Covas, M. M. Beloti, and A. L. Rosa. 2017. Potential of osteoblastic cells derived from bone marrow and adipose tissue associated with a polymer/ceramic composite to repair bone tissue. Calcif. Tissue Int. 101:312–20. doi:10.1007/s00223-017-0282-3.
   PubMed Web of Science ®Google Scholar
• Ghavami, S., M. Eshragi, S. R. Ande, W. J. Chazin, T. Klonisch, A. J. Halayko, K. D. McNeill, M. Hashemi, C. Kerkhoff, and M. Los. 2010. S100a8/a9 induces autophagy and apoptosis via ROS-mediated cross-talk between mitochondria and lysosomes that involves BNIP3. Cell Res. 20:314–31. doi:10.1038/cr.2009.129.
   PubMed Web of Science ®Google Scholar
• Goncalves, D. M., S. Chiasson, and D. Girard. 2010. Activation of human neutrophils by titanium dioxide (TiO2) nanoparticles. Toxicol In Vitro 24:1002–08. doi:10.1016/j.tiv.2009.12.007.
   PubMed Web of Science ®Google Scholar
• Gurr, J. R., A. S. Wang, C. H. Chen, and K. Y. Jan. 2005. Ultrafine titanium dioxide particles in the absence of photoactivation can induce oxidative damage to human bronchial epithelial cells. Toxicology 213:66–73. doi:10.1016/j.tox.2005.05.007.
   PubMed Web of Science ®Google Scholar
• He, C., and D. J. Klionsky. 2009. Regulation mechanisms and signaling pathways of autophagy. Annu. Rev. Genet. 43:67–93. doi:10.1146/annurev-genet-102808-114910.
   PubMed Web of Science ®Google Scholar
• Hugo, H., M. L. Ackland, T. Blick, M. G. Lawrence, J. A. Clements, E. D. Williams, and E. W. Thompson. 2007. Epithelial–Mesenchymal and mesenchymal–Epithelial transitions in carcinoma progression. J. Cell. Physiol. 213:374–83. doi:10.1002/jcp.21223.
   PubMed Web of Science ®Google Scholar
• Jiang, Y., B. N. Jahagirdar, R. L. Reinhardt, R. E. Schwartz, C. D. Keene, X. R. Ortiz-Gonzalez, M. Reyes, T. Lenvik, T. Lund, M. Blackstad, et al. 2002. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418:41–49. doi:10.1038/nature00870.
   PubMed Web of Science ®Google Scholar
• Jin, C. Y., B. S. Zhu, X. F. Wang, and Q. H. Lu. 2008. Cytotoxicity of titanium dioxide nanoparticles in mouse fibroblast cells. Chem. Res. Toxicol. 21:1871–77. doi:10.1021/tx800179f.
   PubMed Web of Science ®Google Scholar
• Kang, S. J., B. M. Kim, Y. J. Lee, and H. W. Chung. 2008. Titanium dioxide nanoparticles trigger p53-mediated damage response in peripheral blood lymphocytes. Environ. Mol. Mutagen. 49:399–405. doi:10.1002/em.20399.
   PubMed Web of Science ®Google Scholar
• Kang, S. J., B. M. Kim, Y. J. Lee, S. H. Hong, and H. W. Chung. 2009. Titanium dioxide nanoparticles induce apoptosis through the JNK/p38-caspase-8-Bid pathway in phytohemagglutinin-stimulated human lymphocytes. Biochem. Biophys. Res. Commun. 386:682–87. doi:10.1016/j.bbrc.2009.06.097.
   PubMed Web of Science ®Google Scholar
• Kermanizadeh, A., I. Gosens, L. MacCalman, H. Johnston, P. H. Danielsen, N. R. Jacobsen, A. G. Lenz, T. Fernandes, R. P. Schins, F. R. Cassee, et al. 2016. A multilaboratory toxicological assessment of a panel of 10 engineered nanomaterials to human health–ENPRA project–The highlights, limitations, and current and future challenges. J. Toxicol. Environ. Health B 19:1–28. doi:10.1080/10937404.2015.1126210.
   PubMed Web of Science ®Google Scholar
• Lamouille, S., J. Xu, and R. Derynck. 2014. Molecular mechanisms of epithelial–Mesenchymal transition. Nat. Rev. Mol. Cell Biol. 15:178–96. doi:10.1038/nrm3758.
   PubMed Web of Science ®Google Scholar
• Li, M., F. Luan, Y. Zhao, H. Hao, Y. Zhou, W. Han, and X. Fu. 2016. Epithelial-mesenchymal transition: An emerging target in tissue fibrosis. Exp. Biol. Med. 241:1–13. doi:10.1177/1535370215597194.
   Web of Science ®Google Scholar
• Liu, B., Y. Cheng, B. Zhang, H. J. Bian, and J. K. Bao. 2009. Polygonatum cyrtonema lectin induces apoptosis and autophagy in human melanoma A 375 cells through a mitochondria-mediated ROS-p38-p53 pathway. Cancer Lett. 275:54–60. doi:10.1016/j.canlet.2008.09.042.
   PubMed Web of Science ®Google Scholar
• Mackey, A. M., N. Sanvicens, G. Groeger, F. Doonan, D. Wallace, and T. G. Cotter. 2008. Redox survival signalling in retina-derived 661W cells. Cell Death Differ. 15:1291–303. doi:10.1038/cdd.2008.43.
   PubMed Web of Science ®Google Scholar
• Martins, A. D. C., L. F. Azevedo, C. C. de Souza Rocha, M. F. H. Carneiro, V. P. Venancio, M. R. de Almeida, L. M. G. Antunes, R. de Carvalho Hott, J. L. Rodrigues, A. T. Ogunjimi, et al. 2017. Evaluation of distribution, redox parameters, and genotoxicity in Wistar rats co-exposed to silver and titanium dioxide nanoparticles. J. Toxicol. Environ. Health Part A 80:1156–65. doi:10.1080/15287394.2017.1357376.
   PubMed Web of Science ®Google Scholar
• Meena, R., M. Rani, R. Pal, and P. Rajamani. 2012. Nano-TiO2-induced apoptosis by oxidative stress-mediated DNA damage and activation of p53 in human embryonic kidney cells. Appl. Biochem. Biotechnol. 167:791–808. doi:10.1007/s12010-012-9699-3.
   PubMed Web of Science ®Google Scholar
• Meirelles, L. S., and N. B. Nardi. 2009. Methodology, biology, and clinical applications of mesenchymal stem cells. Front. Biosci. 14:4281–98. doi:10.2741/3528.
   Web of Science ®Google Scholar
• Mueller, L. P., J. Luetzkendorf, T. Mueller, K. Reichelt, H. Simon, and H. J. Schmoll. 2006. Presence of mesenchymal stem cells in human bone marrow after exposure to chemotherapy: Evidence of resistance to apoptosis induction. Stem Cells 24:2753–65. doi:10.1634/stemcells.2006-0108.
   PubMed Web of Science ®Google Scholar
• Ng, F., S. Boucher, S. Koh, K. S. Sastry, L. Chase, U. Lakshmipathy, C. Choong, Z. Yang, M. C. Vemuri, M. S. Rao, et al. 2008. PDGF, TGF-beta, and FGF signaling is important for differentiation and growth of mesenchymal stem cells (MSCs): Transcriptional profiling can identify markers and signaling pathways important in differentiation of MSCs into adipogenic, chondrogenic, and osteogenic lineages. Blood 112:295–307. doi:10.1182/blood-2007-07-103697.
   PubMed Web of Science ®Google Scholar
• Oh, S. H., and S. C. Lim. 2009. Endoplasmic reticulum stress-mediated autophagy/apoptosis induced by capsaicin (8-methyl-N-vanillyl-6-nonenamide) and dihydrocapsaicin is regulated by the extent of c-Jun NH2-terminal kinase/extracellular signal-regulated kinase activation in WI38 lung epithelial fibroblast cells. J. Pharmacol. Exp. Ther. 329:112–22. doi:10.1124/jpet.108.144113.
   PubMed Web of Science ®Google Scholar
• Ortiz, L. A., F. Gambelli, C. McBride, D. Gaupp, M. Baddoo, N. Kaminski, and D. G. Phinney. 2003. Mesenchymal stem cell engraftment in lung is enhanced in response to bleomycin exposure and ameliorates its fibrotic effects. Proc. Natl. Acad. Sci. U S A 100:8407–11. doi:10.1073/pnas.1432929100.
   PubMed Web of Science ®Google Scholar
• Oswald, J., S. Boxberger, B. Jorgensen, S. Feldmann, G. Ehninger, M. Bornhauser, and C. Werner. 2004. Mesenchymal stem cells can be differentiated into endothelial cells in vitro. Stem Cells 22:377–84. doi:10.1634/stemcells.22-3-377.
   PubMed Web of Science ®Google Scholar
• Pujalté, I., D. Dieme, S. Haddad, A. M. Serventi, and M. Bouchard. 2017. Toxicokinetics of titanium dioxide (TiO2) nanoparticles after inhalation in rats. Toxicol. Lett. 265:77–85. doi:10.1016/j.toxlet.2016.11.014.
   PubMed Web of Science ®Google Scholar
• Rahman, Q., J. Norwood, and G. Hatch. 1997. Evidence that exposure of particulate air pollutants to human and rat alveolar macrophages leads to differential oxidative response. Biochem. Biophys. Res. Commun. 240:669–72. doi:10.1006/bbrc.1997.7373..
   PubMed Web of Science ®Google Scholar
• Raman, M., W. Chen, and M. H. Cobb. 2007. Differential regulation and properties of MAPKs. Oncogene 26:3100–12. doi:10.1038/sj.onc.1210392.
   PubMed Web of Science ®Google Scholar
• Sanchez, C. G., P. Penfornis, A. Z. Oskowitz, A. G. Boonjindasup, D. Z. Cai, S. S. Dhule, B. G. Rowan, A. Kelekar, D. S. Krause, and R. R. Pochampally. 2011. Activation of autophagy in mesenchymal stem cells provides tumor stromal support. Carcinogenesis 32:964–72. doi:10.1093/carcin/bgr029.
   PubMed Web of Science ®Google Scholar
• Shakeel, M., F. Jabeen, S. Shabbir, M. S. Asghar, M. S. Khan, and A. S. Chaudhry. 2016. Toxicity of nano-titanium dioxide (TiO2-NP) through various routes of exposure: A review. Biol. Trace Elem. Res. 172:1–36. doi:10.1007/s12011-015-0550-x.
   PubMed Web of Science ®Google Scholar
• Shi, H., R. Magaye, V. Castranova, and J. Zhao. 2013. Titanium dioxide nanoparticles: A review of current toxicological data. Part Fibre Toxicol. 10:15. doi:10.1186/1743-8977-10-15.
   PubMed Web of Science ®Google Scholar
• Shi, Y., F. Wang, J. He, S. Yadav, and H. Wang. 2010. Titanium dioxide nanoparticles cause apoptosis in BEAS-2b cells through the caspase 8/t-Bid-independent mitochondrial pathway. Toxicol. Lett. 196:21–27. doi:10.1016/j.toxlet.2010.03.014.
   PubMed Web of Science ®Google Scholar
• Shukla, R. K., A. Kumar, D. Gurbani, A. K. Pandey, S. Singh, and A. Dhawan. 2013. TiO(2) nanoparticles induce oxidative DNA damage and apoptosis in human liver cells. Nanotoxicology 7:48–60. doi:10.3109/17435390.2011.629747.
   PubMed Web of Science ®Google Scholar
• Streeter, A., F. M. Menzies, and D. C. Rubinsztein. 2016. LC3-II tagging and western blotting for monitoring autophagic activity in mammalian cells. Meth. Mol. Biol. 1303:161–70. doi:10.1007/978-1-4939-2627-5_8.
   PubMedGoogle Scholar
• Tassinari, R., F. Cubadda, G. Moracci, F. Aureli, M. D’Amato, M. Valeri, B. De Berardis, A. Raggi, A. Mantovani, D. Passeri, et al. 2014. Oral, short-term exposure to titanium dioxide nanoparticles in Sprague-Dawley rat: Focus on reproductive and endocrine systems and spleen. Nanotoxicology 8:654–62. doi:10.3109/17435390.2013.822114.
   PubMed Web of Science ®Google Scholar
• Toma, C., M. F. Pittenger, K. S. Cahill, B. J. Byrne, and P. D. Kessler. 2002. Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation 105:93–98. doi:10.1161/hc0102.101442.
   PubMed Web of Science ®Google Scholar
• Trouiller, B., R. Reliene, A. Westbrook, P. Solaimani, and R. H. Schiestl. 2009. Titanium dioxide nanoparticles induce DNA damage and genetic instability in vivo in mice. Cancer Res. 69:8784–89. doi:10.1158/0008-5472.CAN-09-2496.
   PubMed Web of Science ®Google Scholar
• Wang, J. J., B. J. Sanderson, and H. Wang. 2007. Cyto- and genotoxicity of ultrafine TiO2 particles in cultured human lymphoblastoid cells. Mutat. Res. 628:99–106. doi:10.1016/j.mrgentox.2006.12.003.
   PubMed Web of Science ®Google Scholar
• Wang, M. L., R. Tuli, P. A. Manner, P. F. Sharkey, D. J. Hall, and R. S. Tuan. 2003. Direct and indirect induction of apoptosis in human mesenchymal stem cells in response to titanium particles. J. Orthop. Res. 21:697–707. doi:10.1016/S0736-0266(02)00241-3.
   PubMed Web of Science ®Google Scholar
• Wang, X., J. L. Martindale, Y. Liu, and N. J. Holbrook. 1998. The cellular response to oxidative stress: Influences of mitogen-activated protein kinase signalling pathways on cell survival. Biochem. J. 333:291–300. doi:10.1042/bj3330291.
   PubMed Web of Science ®Google Scholar
• Wei, H., Z. Li, S. Hu, X. Chen, and X. Cong. 2010. Apoptosis of mesenchymal stem cells induced by hydrogen peroxide concerns both endoplasmic reticulum stress and mitochondrial death pathway through regulation of caspases, p38 and JNK. J. Cell. Biochem. 111:967–78. doi:10.1002/jcb.22785.
   PubMed Web of Science ®Google Scholar
• Xiong, Y., A. L. Contento, P. Q. Nguyen, and D. C. Bassham. 2007. Degradation of oxidized proteins by autophagy during oxidative stress in arabidopsis. Plant Physiol. 143:291–99. doi:10.1104/pp.106.092106.
   PubMed Web of Science ®Google Scholar
• Yadav, S., Y. Shi, F. Wang, and H. Wang. 2010. Arsenite induces apoptosis in human mesenchymal stem cells by altering Bcl-2 family proteins and by activating intrinsic pathway. Toxicol. Appl. Pharmacol. 244:263–72. doi:10.1016/j.taap.2010.01.001.
   PubMed Web of Science ®Google Scholar
• Yang, C., V. Kaushal, S. V. Shah, and G. P. Kaushal. 2008. Autophagy is associated with apoptosis in cisplatin injury to renal tubular epithelial cells. Am. J. Physiol. Renal. Physiol. 294:F777–F787. doi:10.1152/ajprenal.00590.2007.
   PubMed Web of Science ®Google Scholar
• Yin, Z. F., L. Wu, H. G. Yang, and Y. H. Su. 2013. Recent progress in biomedical applications of titanium dioxide. Phys. Chem. Chem. Phys. 15:4844–58. doi:10.1039/c3cp43938k.
   PubMed Web of Science ®Google Scholar
• Yoo, K. C., C. H. Yoon, D. Kwon, K. H. Hyun, S. J. Woo, R. K. Kim, E. J. Lim, Y. Suh, M. J. Kim, T. H. Yoon, et al. 2012. Titanium dioxide induces apoptotic cell death through reactive oxygen species-mediated Fas upregulation and Bax activation. Int. J. Nanomed. 7:1203–14. doi:10.2147/ijn.s28647.
   PubMed Web of Science ®Google Scholar
• Yu, J. X., and T. H. Li. 2011. Distinct biological effects of different nanoparticles commonly used in cosmetics and medicine coatings. Cell Biosci. 1:19. doi:10.1186/2045-3701-1-19.
   PubMed Web of Science ®Google Scholar
• Zhu, W., J. Chen, X. Cong, S. Hu, and X. Chen. 2006. Hypoxia and serum deprivation-induced apoptosis in mesenchymal stem cells. Stem Cells 24:416–25. doi:10.1634/stemcells.2005-0121.
   PubMed Web of Science ®Google Scholar