Exposure to TiO2 Nanoparticles Induces Immunological Dysfunction in Mouse Testitis

Journal of Agricultural and Food Chemistry

Volumn 64, Issue 1, 2016, Pages 346-355

  Hong, Fashui ^a   Wang, Yajing ^a   Zhou, Yingjun ^a   Zhang, Qi ^a   Ge, Yushuang ^a   Chen, Ming ^a   Hong, Jie ^b   Wang, Ling ^c  

^a HUAIYIN NORMAL UNIVERSITY   (China)

^b MEDICAL COLLEGE OF SOOCHOW UNIVERSITY   (China)

^c SOOCHOW UNIVERSITY   (China)

Author keywords

immune dysfunction; reproductive toxicity; TAM TLRs signal pathway; testitis; titanium dioxide nanoparticles

Indexed keywords

ANIMALS; CELL DEATH; GLYCOPROTEINS; HEALTH RISKS; INTERFERONS; MAMMALS; NANOPARTICLES; TOXICITY;

IMMUNE DYSFUNCTION; REPRODUCTIVE TOXICITIES; SIGNAL PATHWAYS; TESTITIS; TITANIUM DIOXIDE NANOPARTICLES;

TITANIUM DIOXIDE;

AXL RECEPTOR TYROSINE KINASE; NANOPARTICLE; ONCOPROTEIN; PROTEIN TYROSINE KINASE; SOCS1 PROTEIN, MOUSE; SUPPRESSOR OF CYTOKINE SIGNALING; TITANIUM; TITANIUM DIOXIDE; TYRO3 PROTEIN, MOUSE;

ANIMAL; DRUG EFFECTS; GENETICS; HUMAN; IMMUNOLOGY; INSTITUTE FOR CANCER RESEARCH MOUSE; MALE; MOUSE; ORCHITIS; TESTIS;

ANIMALS; HUMANS; MALE; MICE; MICE, INBRED ICR; NANOPARTICLES; ORCHITIS; PROTO-ONCOGENE PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TESTIS; TITANIUM;

EID: 84954323889     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.5b05262     Document Type: Article

References (78)

1. Kaida, T.; Kobayashi, K.; Adachi, M.; Suzuki, F. Optical characteristics of titanium oxide interference film and the film laminated with oxides and their application for cosmetics J. Cosmet. Sci. 2004, 55 (2) 219-220
2. 3 composite membranes for environmental applications Appl. Catal., B 2006, 63, 60-67 10.1016/j.apcatb.2005.09.012
3. Skocaj, M.; Filipic, M.; Petkovic, J.; Novak, S. Titanium dioxide in our everyday life; is it safe? Radiol. Oncol. 2011, 45, 227-247 10.2478/v10019-011-0037-0
4. 2 J. Southeast Univ. (Med. Sci. Edi.) 2011, 30 (6) 945-952 (in Chinese)
5. Weir, A.; Westerhoff, P.; Fabricius, L.; Hristovski, K.; von Goetz, N. Titanium dioxide nanoparticles in food and personal care products Environ. Sci. Technol. 2012, 46, 2242-2250 10.1021/es204168d
6. Lindenschmidt, R. C.; Driscoll, K. E.; Perkins, M. A.; Higgins, J. M.; Maurer, J. K.; Belfiore, K. A. The comparison of a fibrogenic and two nonfibrogenic dusts by bronchoalveolar lavage Toxicol. Appl. Pharmacol. 1990, 102, 268-281 10.1016/0041-008X(90)90026-Q
7. Iavicoli, I.; Leso, V.; Bergamaschi, A. Toxicological effects of titanium dioxide nanoparticles: a review of in vivo studies J. Nanomater. 2012, 2012, 1-36 10.1155/2012/964381
8. Shi, H. B.; Magaye, R.; Castranova, V.; Zhao, J. S. Titanium dioxide nanoparticles: a review of current toxicological data Part. Fibre Toxicol. 2013, 10, 15 10.1186/1743-8977-10-15
9. 2 NP-induced hepatic inflammation J. Agric. Food Chem. 2014, 62, 6871-6878 10.1021/jf501428w
10. Gui, S. X.; Li, B. Y.; Zhao, X. Y.; Sheng, L.; Hong, J.; Yu, X. H.; Sang, X. Z.; Sun, Q. Q.; Ze, Y. G.; Wang, L.; Hong, F. S. Renal injury and Nrf2 modulation in mouse kidney following exposure to titanium dioxide nanoparticles J. Agric. Food Chem. 2013, 61, 8959-8968 10.1021/jf402387e
11. Sang, X. Z.; Li, B.; Ze, Y. G.; Hong, J.; Ze, X.; Gui, S. X.; Sun, Q. Q.; Liu, H. T.; Zhao, X. Y.; Sheng, L.; Liu, D.; Yu, X. H.; Hong, F. S. Toxicological effects of nanosized titanium dioxide-induced spleen injury in mice J. Agric. Food Chem. 2013, 61 (23) 5590-5599 10.1021/jf3035989
12. 2 causes renal fibrosis involving activation of the Wnt pathway in mouse kidney J. Agric. Food Chem. 2015, 63 (5) 1639-1647 10.1021/jf5034834
13. 2 Inhalation Toxicol. 2007, 19 (Suppl. 1) 205-212 10.1080/08958370701497754
14. IARC. Carbon Black, Titanium Dioxide and Talc; IARC Monographs on the Evaluation of Carcinogenic Risks to Humans 93; International Agency for Research on Cancer: Lyon, France, 2006.
15. Lan, Z.; Yang, W. X. Nanoparticles and spermatogenesis: how do nanoparticles affect spermatogenesis and penetrate the blood-testis barrier Nanomedicine 2012, 7 (4) 579-596 10.2217/nnm.12.20
16. Iavicoli, I.; Fontana, L.; Leso, V.; Bergamaschi, A. The effects of nanomaterials as endocrine disruptors Int. J. Mol. Sci. 2013, 14, 16732-16801 10.3390/ijms140816732
17. De Jong, W. H.; Hagens, W. I.; Krystek, P.; Burger, M. C.; Sips, A. J.; Geertsma, R. E. Particle sizedependent organ distribution of gold nanoparticles after intravenous administration Biomaterials 2008, 29, 1912-1919 10.1016/j.biomaterials.2007.12.037
18. Lankveld, D. P.; Oomen, A. G.; Krystek, P.; Neigh, A.; Troost-de Jong, A.; Noorlander, C. W.; Van Eijkeren, J. C.; Geertsma, R. E.; De Jong, W. H. The kinetics of the tissue distribution of silver nanoparticles of different sizes Biomaterials 2010, 31, 8350-8361 10.1016/j.biomaterials.2010.07.045
19. Yoshida, S.; Ono, N.; Tsukue, N.; Oshio, S.; Umeda, T.; Takano, H.; Takeda, K. In utero exposure to diesel exhaust increased accessory reproductive gland weight and serum testosterone concentration in male mice Environ. Sci. 2006, 13, 139-147
20. Asare, N.; Instanesa, C.; Sandberga, W. J.; Refsnesa, M.; Schwarzea, P.; Kruszewskib, M.; Brunborg, G. Cytotoxic and genotoxic effects of silver nanoparticles in testicular cells Toxicology 2012, 291, 65-72 10.1016/j.tox.2011.10.022
21. Takeda, K.; Suzuki, K.; Ishihara, A.; Kubo-Irie, M.; Fujimoto, R.; Tabata, M.; Oshio, S.; Nihei, Y.; Ihara, T.; Sugamata, M. Nanoparticles transferred from pregnant mice to their offspring can damage the genital and cranial nerve systems J. Health Sci. 2009, 55, 95-102 10.1248/jhs.55.95
22. Kubo-Irie, M.; Uchida, H.; Mastuzawa, S.; Yoshida, Y.; Shinkai, Y.; Suzuki, K.; Yokota, S.; Oshio, S.; Takeda, K. Dose-dependent biodistribution of prenatal exposureto rutile-type titanium dioxide nanoparticles on mouse testis J. Nanopart. Res. 2014, 16, 2284 10.1007/s11051-014-2284-7
23. Guo, L. L.; Liu, X. H.; Qin, D. X.; Gao, L.; Zhang, H. M.; Liu, J. Y.; Cui, Y. G. Effects of nanosized titanium dioxide on the reproductive system of male mice Zhonghua Nan Ke Xue 2009, 15, 517-522 (abstract in English)
24. Wang, Y.; Ge, S. Q.; Yang, H. L.; Zhang, W. W.; Cao, H. C.; Chen, Z. G. Effects of nanoparticulate titanium dioxide on male reproduction in mice J. Environ. Health 2011, 28, 262-264 (in Chinese)
25. Gao, G. D.; Ze, Y. G.; Zhao, X. Y.; Sang, X. Z.; Zheng, L.; Ze, X.; Gui, S. X.; Sheng, L.; Sun, Q. Q.; Hong, J.; Yu, X. H.; Wang, L.; Hong, F. S.; Zhang, X. G. Titanium dioxide nanoparticle-induced testicular damage, spermatogenesis suppression, and gene expression alterations in male mice J. Hazard. Mater. 2013, 258, 133-143 10.1016/j.jhazmat.2013.04.046
26. 2 exposure J. Hazard. Mater. 2015, 300, 718-728 10.1016/j.jhazmat.2015.08.010
27. 2 nanoparticle exposure decreases spermatogenesis via biochemical dysfunctions in the testis of male mice J. Agric. Food Chem. 2015, 63, 7084-7092 10.1021/acs.jafc.5b02652
28. Orazizadeh, M.; Khorsandi, L.; Absalan, F.; Hashemitabar, M.; Daneshi, E. Effect of beta-carotene on titanium oxide nanoparticles-induced testicular toxicity in mice J. Assist. Reprod. Genet. 2014, 31, 561-568 10.1007/s10815-014-0184-5
29. Ramovatar, M.; Kumari, K.; Paulraj, R. Cytotoxic and genotoxic effects of titanium dioxide nanoparticles in testicular cells of male Wistar rat Appl. Biochem. Biotechnol. 2015, 175, 825-840 10.1007/s12010-014-1299-y
30. 2 nanoparticles induced apoptosis of primary cultured Sertoli cells of mice J. Biomed. Mater. Res., Part A 2016, 104A, 124-135 10.1002/jbm.a.35548
31. Hedger, M. P. Toll-like receptors and signalling in spermatogenesis and testicular responses to inflammation-a perspective J. Reprod. Immunol. 2011, 88, 130-141 10.1016/j.jri.2011.01.010
32. Sun, B.; Qi, N.; Shang, T.; Wu, H.; Deng, T. T.; Han, D. S. Sertoli cell-initiated testicular innate immune response through Toll-like receptor-3 activation is negatively regulated by Tyro3, Axl, and Mer receptors Endocrinology 2010, 151, 2886-2897 10.1210/en.2009-1498
33. Li, N.; Wang, T.; Han, D. S. Structural, cellular and molecular aspects of immune privilege in the testis Front. Immunol. 2012, 3, 152 10.3389/fimmu.2012.00152
34. Wu, H.; Wang, H.; Xiong, W.; Chen, S.; Tang, H.; Han, D. Expression patterns and functions of toll-like receptors in mouse Sertoli cells Endocrinology 2008, 149, 4402-4412 10.1210/en.2007-1776
35. Riccioli, A.; Starace, D.; Galli, R.; Fuso, A.; Scarpa, S.; Palombi, F.; De Cesaris, P.; Ziparo, E.; Filippini, A. Sertoli cells initiate testicular innate immune responses through TLR activation J. Immunol. 2006, 177, 7122-7130 10.4049/jimmunol.177.10.7122
36. Starace, D.; Galli, R.; Paone, A.; De Cesaris, P.; Filippini, A.; Ziparo, E.; Riccioli, A. Toll-like receptor 3 activation induces antiviral immune responses in mouse Sertoli cells Biol. Reprod. 2008, 79, 766-775 10.1095/biolreprod.108.068619
37. 3+ ions for photocatalysis Mater. Lett. 2002, 57, 794-801 10.1016/S0167-577X(02)00875-3
38. Hu, R. P.; Zheng, L.; Zhang, T.; Cui, Y. L.; Gao, G. D.; Cheng, Z.; Cheng, J.; Tang, M.; Hong, F. S. Molecular mechanism of hippocampal apoptosis of mice following exposure to titanium dioxide nanoparticles J. Hazard. Mater. 2011, 191, 32-40 10.1016/j.jhazmat.2011.04.027
39. AshaRani, P. V.; Mun, G. L. K.; Hande, M. P.; Valiyaveettil, S. Cytotoxicity and genotoxicity of silver nanoparticles in human cells ACS Nano 2009, 3, 279-290 10.1021/nn800596w
40. Bustin, S. A.; Benes, V.; Garson, J. A.; Hellemans, J.; Huggett, J.; Kubista, M.; Mueller, R.; Nolan, T.; Pfaffl, M. W.; Shipley, G. L.; Vandesompele, J.; Wittwer, C. T. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments Clin. Chem. 2009, 55 (4) 611-622 10.1373/clinchem.2008.112797
41. Schefe, J. H.; Lehmann, K. E.; Buschmann, I. R.; Unger, T.; Funke-Kaiser, H. Quantitative real-time RT-PCR data analysis: current concepts and the novel "gene expressions CT difference" formula J. Mol. Med. 2006, 84, 901-910 10.1007/s00109-006-0097-6
42. Gao, G. D.; Ze, Y. G.; Li, B.; Zhao, X. Y.; Liu, X. R.; Sheng, L.; Hu, R. P.; Gui, S. X.; Sang, X. Z.; Sun, Q. Q.; Cheng, J.; Cheng, Z.; Wang, L.; Tang, M.; Hong, F. S. The ovarian dysfunction and its gene-expressed characteristics of female mice caused by long-term exposure to titanium dioxide nanoparticles J. Hazard. Mater. 2012, 243, 19-27 10.1016/j.jhazmat.2012.08.049
43. 2-induced reproductive system dysfunction and its mechanism in female mice PLoS One 2013, 8 (4) e59378 10.1371/journal.pone.0059378
44. Kaur, G.; Mital, P.; Dufour, J. M. Testis immune privilege-assumptions versus facts Anim. Reprod. 2013, 10, 3-15
45. Maeda, T.; Goto, A.; Kobayashi, D.; Tamai, I. Transport of organic cations across the blood-testis barrier Mol. Pharmaceutics 2007, 4, 600-607 10.1021/mp070023l
46. Meng, J.; Greenlee, A. R.; Taub, C. J.; Braun, R. E. Sertoli cell-specific deletion of the androgen receptor compromises testicular immune privilege in mice Biol. Reprod. 2011, 85, 254-260 10.1095/biolreprod.110.090621
47. Palladino, M. A.; Johnson, T. A.; Gupta, R.; Chapman, J. L.; Ojha, P. Members of the Toll-like receptor family of innate immunity pattern-recognition receptors are abundant in the male reproductive tract Biol. Reprod. 2007, 76, 958-964 10.1095/biolreprod.106.059410
48. Bhushan, S.; Tchatalbachev, S.; Klug, J.; Fijak, M.; Pineau, C.; Chakraborty, T.; Meinhardt, A. Uropathogenic Escherichia coli block MyD88-dependent and activate MyD88-independet signalling pathways in rat testicular cells J. Immunol. 2008, 180, 5537-5547 10.4049/jimmunol.180.8.5537
49. Wang, T.; Zhang, X. Y.; Chen, Q. Y.; Deng, T. T.; Zhang, Y.; Li, N.; Shang, T.; Chen, Y. M.; Han, D. S. Toll-like receptor 3-initiated antiviral responses in mouse male germ cells in vitro Biol. Reprod. 2012, 86, 106 10.1095/biolreprod.111.096719
50. Hedger, M. P. Toll-like receptors and signalling in spermatogenesis and testicular responses to inflammation - a perspective J. Reprod. Immunol. 2011, 88, 130-141 10.1016/j.jri.2011.01.010
51. Wang, H.; Chen, Y.; Ge, Y.; Ma, P.; Ma, Q.; Ma, J.; Xue, S.; Han, D. Immunoexpression of Tyro 3 family receptors-Tyro 3, Axl, and Mer-and their ligand Gas6 in postnatal developing mouse testis J. Histochem. Cytochem. 2005, 53, 1355-1364 10.1369/jhc.5A6637.2005
52. Rothlin, C. V.; Ghosh, S.; Zuniga, E. I.; Oldstone, M. B.; Lemke, G. TAM receptors are pleiotropic inhibitors of the innate immune response Cell 2007, 131, 1124-1136 10.1016/j.cell.2007.10.034
53. Xiong, W.; Chen, Y.; Wang, H.; Wu, H.; Lu, Q.; Han, D. Gas6 and the Tyro 3 receptor tyrosine kinase subfamily regulate the phagocytic function of Sertoli cells Reproduction 2008, 135, 77-87 10.1530/REP-07-0287
54. Shang, T.; Zhang, X.; Wang, T.; Sun, B.; Deng, T.; Han, D. Toll-like receptor-initiated testicular innate immune responses in mouse Leydig cells Endocrinology 2011, 152, 2827-2836 10.1210/en.2011-0031
55. Lemke, G.; Rothlin, C. V. Immunobiology of the TAM receptors Nat. Rev. Immunol. 2008, 8, 327-336 10.1038/nri2303
56. Ghosh, S.; May, M. J.; Kopp, E. B. NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses Annu. Rev. Immunol. 1998, 16, 225 10.1146/annurev.immunol.16.1.225
57. Vives-Pi, M.; Somoza, N.; Fernandez-Alvarez, J.; Vargas, F.; Caro, P.; Alba, A.; Gomis, R.; Labeta, M. O.; Pujol-Borrell, R. Evidence of expression of endotoxin receptors CD14. Toll-like receptors TLR4 and TLR2 and associated molecule MD-2 and of sensitivity to endotoxin (LPS) in islet beta cells Clin. Exp. Immunol. 2003, 133, 208-218 10.1046/j.1365-2249.2003.02211.x
58. Iwasaki, A.; Medzhitov, R. Toll-like receptor control of adaptive immune responses Nat. Immunol. 2004, 5, 987-995 10.1038/ni1112
59. Jones, B. W.; Means, T. K.; Heldwein, K. A.; Keen, M. A.; Hill, P. J.; Belisle, J. T.; Fenton, M. J. Different Toll-like receptor agonists induce distinct macrophage responses J. Leukoc. Biol. 2001, 69, 1036-1044
60. Fan, H.; Peck, O. M.; Tempel, G. E.; Halushka, P. V.; Cook, J. A. Toll-like receptor 4 coupled GI protein signaling pathways regulate extracellular signal-regulated kinase phosphorylation and AP-1 activation independent of NF kappaB activation Shock 2004, 22, 57-62 10.1097/01.shk.0000129759.58490.d6
61. Li, Q.; Verma, I. M. NF-κB regulation in the immune system Nat. Rev. Immunol. 2002, 2, 725-734 10.1038/nri910
62. Liew, F. Y.; Xu, D.; Brint, E. K.; ONeill, L. A. Negative regulation of toll-like receptor-mediated immune responses Nat. Rev. Immunol. 2005, 5, 446-458 10.1038/nri1630
63. 2 Nanoscale Res. Lett. 2009, 4, 1275-1285 10.1007/s11671-009-9393-8
64. 2 nanoparticles J. Biomed. Mater. Res., Part A 2011, 96, 221-229 10.1002/jbm.a.32976
65. Gui, S. X.; Zhang, Z. L.; Zheng, L.; Cui, Y. L.; Liu, X. R.; Li, N.; Sang, X. Z.; Sun, Q. Q.; Gao, G. D.; Cheng, Z.; Cheng, J.; Wang, L.; Tang, M.; Hong, F. S. Molecular mechanism of kidney injury of mice caused by exposure to titanium dioxide nanoparticles J. Hazard. Mater. 2011, 195, 365-370 10.1016/j.jhazmat.2011.08.055
66. Sun, Q. Q.; Tan, D. L.; Ze, Y. G.; Sang, X. Z.; Liu, X. R.; Gui, S. X.; Cheng, Z.; Cheng, J.; Hu, R. P.; Gao, G. D.; Liu, G.; Zhu, M.; Zhao, X. Y.; Sheng, L.; Wang, L.; Tang, M.; Hong, F. S. Pulmotoxicological effects caused by long-term titanium dioxide nanoparticles exposure in mice J. Hazard. Mater. 2012, 235-236, 47-53 10.1016/j.jhazmat.2012.05.072
67. 2 nanoparticles induced hippocampal neuroinflammation in mice PLoS One 2014, 9 (3) e92230 10.1371/journal.pone.0092230
68. Cook, D. N.; Pisetsky, D. S.; Schwartz, D. A. Toll-like receptors in the pathogenesis of human disease Nat. Immunol. 2004, 5, 975-979 10.1038/ni1116
69. Wormald, S.; Hilton, D. J. The negative regulatory roles of suppressor of cytokine signaling proteins in myeloid signaling pathways Curr. Opin. Hematol. 2007, 14, 9-15 10.1097/00062752-200701000-00004
70. Liu, S. C.; Xu, L. J.; Zhang, T.; Ren, G. G.; Yang, Z. Oxidative stress and apoptosis induced by nanosized titanium dioxide in PC12 cells Toxicology 2010, 267, 172-177 10.1016/j.tox.2009.11.012
71. Wu, J.; Sun, J.; Xue, Y. Involvement of JNK and P53 activation in G2/M cell cycle arrest and apoptosis induced by titanium dioxide nanoparticles in neuron cells Toxicol. Lett. 2010, 199, 269-276 10.1016/j.toxlet.2010.09.009
72. Sayes, C. M.; Wahi, R.; Kurian, P. A.; Liu, Y.; West, J. L.; Ausman, K. D.; Warheit, D. B.; Colvin, V. L. Correlating nanoscale titania structure with toxicity: a cytotoxicity and inflammatory response study with human dermal fibroblasts and human lung epithelial cells Toxicol. Sci. 2006, 92, 174-185 10.1093/toxsci/kfj197
73. Sabokbar, A.; Pandey, R.; Athanasou, N. A. The effect of particle size and electrical charge on macrophage-osteoclast differentiation and bone resorption J. Mater. Sci.: Mater. Med. 2003, 14, 731-738 10.1023/A:1025088418878
74. Long, T. C.; Saleh, N.; Tilton, R. D.; Lowry, G.; Veronesi, B. Titanium dioxide (P25) produces reactive oxygen species in immortalized brain microglia (BV2): implications for nanoparticle neurotoxicity Environ. Sci. Technol. 2006, 40, 4346-4352 10.1021/es060589n
75. Long, T. C.; Tajuba, J.; Sama, P.; Saleh, N.; Swartz, C.; Parker, J.; Hester, S.; Lowry, G. V.; Veronesi, B. Nanosize titanium dioxide stimulates reactive oxygen species in brain microglia and damages neurons in vitro Environ. Health Perspect. 2007, 115 (11) 1631-1637 10.1289/ehp.10216
76. Nel, A.; Madler, L.; Velegol, D.; Xia, T. M. V.; Hoek, E.; Somasundaran, P.; Klaessig, F.; Castranova, V.; Thompson, M. Understanding biophysicochemical interactions at nano-bio interface Nat. Mater. 2009, 8, 543-556 10.1038/nmat2442
77. Domingos, R.; Baaloush, M.; Yonju-Nam, M.; Reid, M.; Tufenkji, N.; Lead, J.; Leppard, G.; Wilkinson, K. Characterizing manufactured nanoparticles in the environment: multimethod determinationof particle sizes Environ. Sci. Technol. 2009, 43, 7277-7284 10.1021/es900249m
78. Gentile, F.; Ferrari, M.; Decuzzi, P. The transport of nanoparticles in blood vessels: the effect of vessel permeability and blood rheology Ann. Biomed. Eng. 2008, 36 (2) 254-261 10.1007/s10439-007-9423-6