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Ecotoxicol Environ Saf
2024 Mar 15;273:116119. doi: 10.1016/j.ecoenv.2024.116119.
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Cadmium induces physiological and behavioral changes associated with 180 kDa NCAM lower expression and higher polysialic acid, in the African clawed Xenopus laevis tadpoles.
Marchand G
,
Fliniaux I
,
Titran P
,
Takeda Uchimura Y
,
Bodart JF
,
Harduin Lepers A
,
Cailliau K
,
Marin M
.
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Heavy metals are released into the environment in increasing amounts from different natural and anthropogenic sources. Among them, cadmium contaminates aquatic habitats and represents a threat to Amphibians. To assess the risks of exposure to cadmium in the aquatic environment, we studied the survival rate of early tadpoles of Xenopus laevis under exposure to CdCl2 for 6 days in the concentration range between 0.15 and 150 µM of Cd2+. Tadpoles survived and reached stage 45 before feeding at all concentrations tested except 150 µM Cd2+, which significantly induced death. With an exposure of 15 µM Cd2+, tadpoles' mean body length decreased, heart rate increased, fastest swimming speed decreased, and distance traveled was greater compared to unexposed controls. Additionally, a witness of neuronal normal development, the neural cell adhesion molecules (NCAM) expression, was decreased. Moreover, this cell-surface glycoprotein exhibited higher polysialylation, a post-translational modification capable to reduce cell adhesion properties and to affect organ development. Our study highlights the effects of Cd2+ on a series of parameters including morphology, physiology, and behavior. They emphasize the deregulation of molecular NCAM suggesting this effector is an interesting biomarker to detect cadmic toxicity in early tadpoles.
Fig. 1. Survival after 6 days of continuous exposure to Cd2+. Surviving embryos 6 days after fertilization (Stage 45) unexposed (white) or exposed to contaminated medium (increasing concentrations of Cd2+ 0.15 µM (yellow), 1.5 µM (orange), 15 µM (red), and 150 µM (purple)). Statistical analysis was performed with the Kruskal-Wallis test and post-hoc: pairwise multiple comparison (*: p < 0.05, nf = 5, n=100).
Fig. 2. Biometry, heart rate, and morphology of tadpoles continuously exposed to increasing concentrations of Cd2+ for 6 days. Fertilized and embryos were exposed to increasing concentrations of Cd2+: 0 µM (white), 0.15 µM (yellow), 1.5 µM (orange), and 15 µM (red). A Length of tadpoles in mm. B Eye gap measurements in mm. C Heart rate (heartbeat/min) of tadpoles measured without stimuli. D Whole distance in cm covered by tadpoles was recorded during 5 minutes. E fastest swimming speed (cm/sec) of tadpoles was recorded during 5 minutes. Data are presented as boxplots. Statistical analyses are performed A, B with Kruskal-Wallis test and post-hoc: pairwise multiple comparisons (**: p < 0.01; ***: p < 0.001; nf=5, n=50); C with generalized linear mixed-effects models (***: p < 0.001; nf=8, 58<n<81) D, E with generalized linear mixed-effects models (***: p < 0.001; nf=9, 75<n<99). F Typical pictures of tadpoles at stage 45, stained with alcian blue. Up, control tadpoles, down, Cd-treated tadpoles (lateral view on the left and ventral view on the right).
Fig. 3. Cadmium induces a decrease in NCAM expression and an enrichment in polysialic acid content in 6 days treated tadpoles. A Western blots were performed on Xenopus adult brains and stage 45 tadpoles using anti-NCAM and anti-β-actin antibodies. B Tadpoles at stage 1 and stage 45 were untreated or treated with 15 µM Cd2+ before electrophoresis and Western blot analysis with anti-NCAM or anti-β−actin antibodies. The upper part depicts a typical result of NCAM, the middle part the expression profiles of β−actin, and the lower part an analysis by Image J® normalized with respective β-actin values. C Stage 45 tadpole extracts were treated or not with endoneuraminidase-N (0.7 U) before Western blots using anti-PSA and anti-β-actin antibodies. D Stage 45 tadpoles were treated or not with 15 µM Cd2+ and immunoprecipitated with an anti-NCAM antibody before Western blot analysis with anti-PSA antibody. The upper part shows representative results of PSA, the middle part the same membranes reblotted with anti-NCAM antibody, and the lower part the analysis of the expression profiles of PSA by Image J® normalized with respective values of immunoprecipitated NCAM. Data are presented as mean +/- standard deviation. The significance of the results was assessed by an ANOVA two-factors and a Tukey post-hoc test (*** p < 0.001).
