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TiO2 nanoparticles induce omphalocele in chicken embryo by disrupting Wnt signaling pathway

Patel, Shweta, Jana, Sarmita, Chetty, Rajlakshmi, Thakore, Sonal, Singh, Man, Devkar, Ranjitsinh·2018·Scientific Reports
DOI 10.1038/s41598-018-23215-7PMC PMC5859020
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Abstract

Titanium dioxide nanoparticles (TiO 2 NPs) are among abundantly used metal oxide NPs but their interactions with biomolecules and subsequent embryonic toxicity in higher vertebrates is not extensively reported. Physicochemical interactions of TiO 2 NPs with egg albumen reveals that lower doses of TiO 2 NPs (10 and 25 µg/ml) accounted for higher friccohesity and activation energy but an increment in molecular radii was recorded at higher doses (50 and 100 µg/ml). FTIR analysis revealed conformational changes in secondary structure of egg albumen as a result of electrostratic interactions between egg albumen and TiO 2 NPs. The morphometric data of chicken embryo recorded a reduction at all the doses of TiO 2 NPs, but toxicity and developmental deformity (omphalocele and flexed limbs) were recorded at lower doses only. Inductively coupled plasma optical emission spectrometry (ICP-OES) confirmed presence of Ti in chicken embryos. mRNA levels of genes involved in canonical and non-canonical Wnt signaling were lowered following TiO 2 NPs treatment resulting in free radical mediated disruption of lateral plate mesoderm and somite myogenesis. Conformational changes in egg albumen and subsequent developmental deformity in chicken embryo following TiO 2 NPs treatment warrants detailed studies of NP toxicity at lower doses prior to their biomedical applications.

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Figure 1 Physicochemical analysis of titanium dioxide nanoparticles and their interaction with egg albumen. Density, Viscosity, Surface tension, Friccohesity, Activation energy and Molecular radii of TiO2 NPs in albumen (a–f) respectively.
Figure 1 Physicochemical analysis of titanium dioxide nanoparticles and their interaction with egg albumen. Density, Viscosity, Surface tension, Friccohesity, Activation energy and Molecular radii of TiO2 NPs in albumen (a–f) respectively.CC BY · PubMed Central
Figure 2 FTIR spectra of native egg albumen and TiO2 NPs + Albumen. (a) Entire spectral range from 400–4000 cm−1; (b–d) Gaussian curve fitting of secondary derivative of Native Albumen and TiO2 NPs + Albumen with Comparative Secondary structure elements from FTIR spectra.
Figure 2 FTIR spectra of native egg albumen and TiO2 NPs + Albumen. (a) Entire spectral range from 400–4000 cm−1; (b–d) Gaussian curve fitting of secondary derivative of Native Albumen and TiO2 NPs + Albumen with Comparative Secondary structure elements from FTIR spectra.CC BY · PubMed Central
Figure 3 TiO2 NPs induces developmental deformities in chicken embryo. (a) Percentages of living normal, dead and malformed embryos in 19-day-old chick embryos. (b) Mean body weight (g) and lengths (cm) of living 19-day-old chick embryos in control and treated groups. (c) Concentrations of Ti in embryos of control and TiO2 NPs-treated group (4 day old) by ICP-OES. (d) Chicken-embryo development after 19 days of incubation, control (i), 10–100 µg/ml TiO2 NPs-treated groups (ii,iii,iv), 10 µg/ml TiO2 Bulk (v) and 10 µg/ml cadmium chloride (vi), (Scale bar: 1 cm). Embryos treated with 10 µg/ml TiO2 NPs (ii) exhibits omphalocele (red arrow) & flexed limbs (white arrow). (e) Photographs showing endoskeleton (bone and cartilage) of 19-day-old chick embryos, control (i) and TiO2 NPs–treated (ii) stained with Alizarin red S and alcian blue staining. TiO2 NPs treated (10 µg/ml) embryos exhibits flexed digits (arrow). The data are expressed as Mean ± SD. Statistical analysis was done by one way ANOVA, *p ≤ 0.05, **p < 0.01, ***p < 0.001, ns- not significant, C- control, P-placebo, B- TiO2 Bulk (10 µg/ml), Cd- cadmium chloride (10 µg/ml).
Figure 3 TiO2 NPs induces developmental deformities in chicken embryo. (a) Percentages of living normal, dead and malformed embryos in 19-day-old chick embryos. (b) Mean body weight (g) and lengths (cm) of living 19-day-old chick embryos in control and treated groups. (c) Concentrations of Ti in embryos of control and TiO2 NPs-treated group (4 day old) by ICP-OES. (d) Chicken-embryo development after 19 days of incubation, control (i), 10–100 µg/ml TiO2 NPs-treated groups (ii,iii,iv), 10 µg/ml TiO2 Bulk (v) and 10 µg/ml cadmium chloride (vi), (Scale bar: 1 cm). Embryos treated with 10 µg/ml TiO2 NPs (ii) exhibits omphalocele (red arrow) & flexed limbs (white arrow). (e) Photographs showing endoskeleton (bone and cartilage) of 19-day-old chick embryos, control (i) and TiO2 NPs–treated (ii) stained with Alizarin red S and alcian blue staining. TiO2 NPs treated (10 µg/ml) embryos exhibits flexed digits (arrow). The data are expressed as Mean ± SD. Statistical analysis was done by one way ANOVA, *p ≤ 0.05, **p < 0.01, ***p < 0.001, ns- not significant, C- control, P-placebo, B- TiO2 Bulk (10 µg/ml), Cd- cadmium chloride (10 µg/ml).CC BY · PubMed Central
Figure 4 Expression of Wnt signaling pathway-related genes in TiO2 NPs-treated chicken embryos. The expression of Wnt signaling pathway-related genes (a–h) including CTNNB1, PITX2, LEF1, WNT11, PRKCA, CAMK2D, ROCK1 and ROCK2 and (i) limb development gene HOXD13 was analyzed using reverse transcription polymerase chain reaction (RT-PCR) in control and TiO2 NPs-treated embryos (n = 3), 4 h after treatment in shell-less culture at 60 h. All the Wnt signaling pathway related genes and limb development gene were downregulated in TiO2 NPs-treated embryos compared to those of control embryos. *p < 0.05, **p < 0.01, ***p < 0.001, ns = not significant. (j) Somite numbers in control and TiO2 NPs-treated embryos 24 h after treatment in shell-less culture (HH-23). There is a reduction in the number of somites in TiO2 NPs-treated embryos as compared to the control embryos. The data are expressed as Mean ± SD. Statistical analysis was done by one way ANOVA followed by Dunnett’s test. *p < 0.05, **p < 0.01, ***p < 0.001, ns = not significant.
Figure 4 Expression of Wnt signaling pathway-related genes in TiO2 NPs-treated chicken embryos. The expression of Wnt signaling pathway-related genes (a–h) including CTNNB1, PITX2, LEF1, WNT11, PRKCA, CAMK2D, ROCK1 and ROCK2 and (i) limb development gene HOXD13 was analyzed using reverse transcription polymerase chain reaction (RT-PCR) in control and TiO2 NPs-treated embryos (n = 3), 4 h after treatment in shell-less culture at 60 h. All the Wnt signaling pathway related genes and limb development gene were downregulated in TiO2 NPs-treated embryos compared to those of control embryos. *p < 0.05, **p < 0.01, ***p < 0.001, ns = not significant. (j) Somite numbers in control and TiO2 NPs-treated embryos 24 h after treatment in shell-less culture (HH-23). There is a reduction in the number of somites in TiO2 NPs-treated embryos as compared to the control embryos. The data are expressed as Mean ± SD. Statistical analysis was done by one way ANOVA followed by Dunnett’s test. *p < 0.05, **p < 0.01, ***p < 0.001, ns = not significant.CC BY · PubMed Central

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Research works printed but not linked: 50

  1. Oberdörster, G., Oberdörster, E. & Oberdörster, J. Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environmental health perspectives 113, 823 (2005). · DOI · Paper page
  2. Nel, A., Xia, T., Mädler, L. & Li, N. Toxic potential of materials at the nanolevel. science 311, 622–627 (2006). · DOI · Paper page
  3. Vance, M. E. et al. Nanotechnology in the real world: Redeveloping the nanomaterial consumer products inventory. Beilstein journal of nanotechnology 6, 1769 (2015). · DOI · Paper page
  4. Dalai, S., Pakrashi, S., Chandrasekaran, N. & Mukherjee, A. Acute toxicity of TiO2 nanoparticles to Ceriodaphnia dubia under visible light and dark conditions in a freshwater system. PLoS One 8, e62970 (2013). · DOI
  5. Maurer-Jones, M. A., Gunsolus, I. L., Murphy, C. J. & Haynes, C. L. Toxicity of engineered nanoparticles in the environment. Analytical chemistry 85, 3036–3049 (2013). · DOI
  6. Shukla, R. K. et al. TiO2 nanoparticles induce oxidative DNA damage and apoptosis in human liver cells. Nanotoxicology 7, 48–60 (2013). · DOI
  7. Lai, J. C. et al. Exposure to titanium dioxide and other metallic oxide nanoparticles induces cytotoxicity on human neural cells and fibroblasts. International journal of nanomedicine 3, 533 (2008).
  8. Hussain, S., Hess, K., Gearhart, J., Geiss, K. & Schlager, J. In vitro toxicity of nanoparticles in BRL 3A rat liver cells. Toxicology in vitro 19, 975–983 (2005). · DOI
  9. Li, Y. et al. Molecular control of TiO2-NPs toxicity formation at predicted environmental relevant concentrations by Mn-SODs proteins. PLoS One 7, e44688 (2012). · DOI
  10. Hu, C. et al. Toxicological effects of TiO 2 and ZnO nanoparticles in soil on earthworm Eisenia fetida. Soil Biology and Biochemistry 42, 586–591 (2010). · DOI
  11. Gupta, G. S., Kumar, A., Shanker, R. & Dhawan, A. Assessment of agglomeration, co-sedimentation and trophic transfer of titanium dioxide nanoparticles in a laboratory-scale predator-prey model system. Scientific reports 6, 31422 (2016). · DOI
  12. Clemente, Z., Castro, V., Moura, M., Jonsson, C. & Fraceto, L. Toxicity assessment of TiO 2 nanoparticles in zebrafish embryos under different exposure conditions. Aquatic toxicology 147, 129–139 (2014). · DOI
  13. Linhua, H., Zhenyu, W. & Baoshan, X. Effect of sub-acute exposure to TiO2 nanoparticles on oxidative stress and histopathological changes in Juvenile Carp (Cyprinus carpio). Journal of Environmental Sciences 21, 1459–1466 (2009). · DOI
  14. Zhu, X., Zhou, J. & Cai, Z. TiO2 nanoparticles in the marine environment: Impact on the toxicity of tributyltin to abalone (Haliotis diversicolor supertexta) embryos. Environmental science & technology 45, 3753–3758 (2011). · DOI
  15. Mohammadipour, A. et al. Maternal exposure to titanium dioxide nanoparticles during pregnancy; impaired memory and decreased hippocampal cell proliferation in rat offspring. Environmental toxicology and pharmacology 37, 617–625 (2014). · DOI
  16. Wierzbicki, M., Sawosz, E. & Grodzik, M. Caveolin-1 localization in chicken embryo chorioallantoic membrane treated with diamond and graphite nanoparticles. Brzozowski m., głogowski r., grzeszczak-pytlak a. Reproduc-tive efficiency of mink females, selected for weaned litter size after first season of repro-duction 5, 133 (2012).
  17. Pineda, L., Sawosz, E., Vadalasetty, K. & Chwalibog, A. Effect of copper nanoparticles on metabolic rate and development of chicken embryos. Animal feed science and technology 186, 125–129 (2013). · DOI
  18. Wierzbicki, M. et al. Carbon nanoparticles downregulate expression of basic fibroblast growth factor in the heart during embryogenesis. International journal of nanomedicine 8, 3427 (2013).
  19. Prasek, M. et al. Influence of nanoparticles of platinum on chicken embryo development and brain morphology. Nanoscale research letters 8, 251 (2013). · DOI
  20. Szmidt, M. et al. Toxicity of different forms of graphene in a chicken embryo model. Environmental Science and Pollution Research 23, 19940–19948 (2016). · DOI
  21. Hotowy, A. et al. Silver nanoparticles administered to chicken affect VEGFA and FGF2 gene expression in breast muscle and heart. Nanoscale research letters 7, 418 (2012). · DOI
  22. Patel, S. et al. DNA binding and dispersion activities of titanium dioxide nanoparticles with UV/vis spectrophotometry, fluorescence spectroscopy and physicochemical analysis at physiological temperature. Journal of Molecular Liquids 213, 304–311 (2016). · DOI
  23. Willems, E., Decuypere, E., Buyse, J. & Everaert, N. Importance of albumen during embryonic development in avian species, with emphasis on domestic chicken. World’s poultry science journal 70, 503–518 (2014). · DOI
  24. Singh, M. Study of apparent molal volume and viscosity of mutual citric acid and disodium hydrogen orthophosphate aqueous systems. Journal of Chemical Sciences 118, 269–274 (2006). · DOI
  25. Venyaminov, S. Y. & Kalnin, N. Quantitative IR spectrophotometry of peptide compounds in water (H2O) solutions. II. Amide absorption bands of polypeptides and fibrous proteins in α‐, β‐, and random coil conformations. Biopolymers 30, 1259–1271 (1990). · DOI
  26. Brosnan, J. T. & Brosnan, M. E. Glutamate: a truly functional amino acid. Amino acids 45, 413–418 (2013). · DOI
  27. Rollerova, E. et al. Titanium dioxide nanoparticles: some aspects of toxicity/focus on the development. Endocrine regulations 49, 97–112 (2015). · DOI
  28. Doi, T., Puri, P., Bannigan, J. & Thompson, J. Altered PITX2 and LEF1 gene expression in the cadmium-induced omphalocele in the chick model. Pediatric Surgery International 27, 495–499 (2011). · DOI
  29. Thompson, J. M. & Bannigan, J. G. Omphalocele induction in the chick embryo by administration of cadmium. Journal of pediatric surgery 42, 1703–1709 (2007). · DOI
  30. Pampfer, S. & Streffer, C. Prenatal death and malformations after irradiation of mouse zygotes with neutrons or X‐rays. Teratology 37, 599–607 (1988). · DOI
  31. Wangikar, P., Dwivedi, P. & Sinha, N. Effect in rats of simultaneous prenatal exposure to ochratoxin A and aflatoxin B1. I. Maternal toxicity and fetal malformations. Birth defects research Part B: Developmental and reproductive toxicology 71, 343–351 (2004). · DOI
  32. Doi, T., Puri, P., Bannigan, J. & Thompson, J. Disruption of noncanonical Wnt/CA 2+ pathway in the cadmium-induced omphalocele in the chick model. Journal of pediatric surgery 45, 1645–1649 (2010). · DOI
  33. Kioussi, C. et al. Identification of a Wnt/Dvl/β-Catenin → Pitx2 pathway mediating cell-type-specific proliferation during development. Cell 111, 673–685 (2002). · DOI
  34. Vadlamudi, U. et al. PITX2, β-catenin and LEF-1 interact to synergistically regulate the LEF-1 promoter. Journal of cell science 118, 1129–1137 (2005). · DOI
  35. Burke, A. C. & Nowicki, J. A new view of patterning domains in the vertebrate mesoderm. Developmental cell 4, 159–165 (2003). · DOI
  36. Shih, H. P., Gross, M. K. & Kioussi, C. Cranial muscle defects of Pitx2 mutants result from specification defects in the first branchial arch. Proceedings of the National Academy of Sciences 104, 5907–5912 (2007). · DOI
  37. Geetha-Loganathan, P., Nimmagadda, S., Huang, R., Christ, B. & Scaal, M. Regulation of ectodermal Wnt6 expression by the neural tube is transduced by dermomyotomal Wnt11: a mechanism of dermomyotomal lip sustainment. Development 133, 2897–2904 (2006). · DOI
  38. Ozaki, M., Ogita, H. & Takai, Y. Involvement of integrin‐induced activation of protein kinase C in the formation of adherens junctions. Genes to Cells 12, 651–662 (2007). · DOI
  39. Shi, J. & Wei, L. Rho kinase in the regulation of cell death and survival. Archivum immunologiae et therapiae experimentalis 55, 61–75 (2007). · DOI · Paper page
  40. Shimizu, Y. et al. ROCK-I regulates closure of the eyelids and ventral body wall by inducing assembly of actomyosin bundles. J Cell Biol 168, 941–953 (2005). · DOI
  41. Matsumaru, D. et al. Genetic analysis of Hedgehog signaling in ventral body wall development and the onset of omphalocele formation. PloS one 6, e16260 (2011). · DOI
  42. Goff, D. J. & Tabin, C. J. Analysis of Hoxd-13 and Hoxd-11 misexpression in chick limb buds reveals that Hox genes affect both bone condensation and growth. Development 124, 627–636 (1997). · DOI
  43. Wu, S., Weng, Z., Liu, X., Yeung, K. & Chu, P. Functionalized TiO2 based nanomaterials for biomedical applications. Advanced Functional Materials 24, 5464–5481 (2014). · DOI
  44. Yin, Z. F., Wu, L., Yang, H. G. & Su, Y. H. Recent progress in biomedical applications of titanium dioxide. Physical Chemistry Chemical Physics 15, 4844–4858 (2013). · DOI
  45. Chandra, A., Patidar, V., Singh, M. & Kale, R. Physicochemical and friccohesity study of glycine, L-alanine and L-phenylalanine with aqueous methyltrioctylammonium and cetylpyridinium chloride from T = (293.15 to 308.15) K. The Journal of Chemical Thermodynamics 65, 18–28 (2013). · DOI
  46. Hamburger, V. & Hamilton, H. L. A series of normal stages in the development of the chick embryo. Journal of morphology 88, 49–92 (1951). · DOI
  47. Lamb, K. J. et al. Diverse range of fixed positional deformities and bone growth restraint provoked by flaccid paralysis in embryonic chicks. International journal of experimental pathology 84, 191–199 (2003). · DOI
  48. Bryszewska, M. A., Hannam, S. E., Olivas, R. M. & Camara, C. Direct arsenic determination in exposed embryos of zebrafish (Danio rerio) with Zeeman electrothermal atomic absorption spectrophotometry. Spectroscopy Letters 42, 363–369 (2009). · DOI
  49. Dugan, J. D., Lawton, M. T., Glaser, B. & Brem, H. A new technique for explantation and in vitro cultivation of chicken embryos. The Anatomical Record 229, 125–128 (1991). · DOI
  50. Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. methods 25, 402–408 (2001). · DOI · Paper page

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Authors
Patel, S., Jana, S., Chetty, R., Thakore, S., Singh, M., & Devkar, R.
Venue
Scientific Reports
Publisher
Springer Science and Business Media LLC
Published
2018-03-19
Volume
8
Issue
1
ISSN
2045-2322
DOI
10.1038/s41598-018-23215-7
PMC
PMC5859020
Cited by
23
References
1
Language
en
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