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Hydroxylated polychlorinated biphenyls may affect the thyroid hormone-induced brain development during metamorphosis of Xenopus laevis by disturbing the expression of matrix metalloproteinases

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Abstract

Background

Thyroid hormones are primarily responsible for the brain development in perinatal mammals. However, this process can be inhibited by external factors such as environmental chemicals. Perinatal mammals are viviparous, which makes direct fetal examination difficult.

Methods

We used metamorphic amphibians, which exhibit many similarities to perinatal mammals, as an experimental system. Therefore, using metamorphic amphibians, we characterized the gene expression of matrix metalloproteinases, which play an important role in brain development.

Results

The expression of many matrix metalloproteinases (mmps) was characteristically induced during metamorphosis. We also found that the expression of many mmps was induced by T3 and markedly inhibited by hydroxylated polychlorinated biphenyls (PCBs).

Conclusion

Overall, our findings suggest that hydroxylated PCBs disrupt normal brain development by disturbing the gene expression of mmps.

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Data availability

All data generated or analyzed during this study are included in this manuscript.

Abbreviations

ANOVA:

Analysis of variance

DMSO:

Dimethyl sulfoxide

EDCs:

Endocrine-disrupting chemicals

FETAX:

Frog embryo teratogenesis assay Xenopus

MMPs:

Matrix metalloproteinases

PCBs:

Polychlorinated biphenyls

PCR:

Polymerase chain reaction

T3 :

3,3′,5-Triiodo-L-thyronine

THs:

Thyroid hormones

References

  1. Braun JM (2017) Early-life exposure to EDCs: role in childhood obesity and neurodevelopment. Nat Rev Endocrinol 13:161–173. https://doi.org/10.1038/nrendo.2016.186

    Article  CAS  PubMed  Google Scholar 

  2. Miodovnik A, Engel SM, Zhu C et al (2011) Endocrine disruptors and childhood social impairment. Neurotoxicology 32:261–267. https://doi.org/10.1016/j.neuro.2010.12.009

    Article  CAS  PubMed  Google Scholar 

  3. Roze E, Meijer L, Bakker A et al (2009) Prenatal exposure to organohalogens, including brominated flame retardants, influences motor, cognitive, and behavioral performance at school age. Environ Health Perspect 117:1953–1958. https://doi.org/10.1289/ehp.0901015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Braun JM, Kalkbrenner AE, Calafat AM et al (2011) Impact of early-life bisphenol A exposure on behavior and executive function in children. Pediatrics 128:873–882. https://doi.org/10.1542/peds.2011-1335

    Article  PubMed  PubMed Central  Google Scholar 

  5. Almazroo OA, Miah MK, Venkataramanan R (2017) Drug Metabolism in the Liver. Clin Liver Dis 21:1–20. https://doi.org/10.1016/j.cld.2016.08.001

    Article  PubMed  Google Scholar 

  6. Shi Y-B (1999) Amphibian Metamorphosis: From Morphology to Molecular Biology, 1st edn. Wiley-Liss

    Google Scholar 

  7. Tata JR (1996) Metamorphosis: an exquisite model for hormonal regulation of post-embryonic development. Biochem Soc Symp 62:123–136

    CAS  PubMed  Google Scholar 

  8. Niu Y, Zhu M, Dong M et al (2021) Bisphenols disrupt thyroid hormone (TH) signaling in the brain and affect TH-dependent brain development in Xenopus laevis. Aquat Toxicol 237:105902. https://doi.org/10.1016/j.aquatox.2021.105902

    Article  CAS  PubMed  Google Scholar 

  9. Dong M, Li Y, Zhu M et al (2021) Tetrabromobisphenol a disturbs brain development in both thyroid hormone-dependent and -independent manners in Xenopus laevis. Molecules. https://doi.org/10.3390/molecules27010249

    Article  PubMed  PubMed Central  Google Scholar 

  10. Ishihara A, Makita Y, Yamauchi K (2011) Gene expression profiling to examine the thyroid hormone-disrupting activity of hydroxylated polychlorinated biphenyls in metamorphosing amphibian tadpole. J Biochem Mol Toxicol 25:303–311. https://doi.org/10.1002/jbt.20390

    Article  CAS  PubMed  Google Scholar 

  11. Nagase H, Visse R, Murphy G (2006) Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res 69:562–573. https://doi.org/10.1016/j.cardiores.2005.12.002

    Article  CAS  PubMed  Google Scholar 

  12. Bassiouni W, Ali MAM, Schulz R (2021) Multifunctional intracellular matrix metalloproteinases: implications in disease. FEBS J 288:7162–7182. https://doi.org/10.1111/febs.15701

    Article  CAS  PubMed  Google Scholar 

  13. Fu L, Hasebe T, Ishizuya-Oka A, Shi Y-B (2007) Roles of Matrix Metalloproteinases and ECM Remodeling during Thyroid Hormone-Dependent Intestinal Metamorphosis in Xenopus laevis. Organogenesis 3:14–19

    Article  PubMed  PubMed Central  Google Scholar 

  14. Nieuwkoop PD, Faber J (1994) Normal Table of Xenopus laevis (Daudin) Garland Publishing. New York 252

  15. Dumont JN, Schultz TW, Buchanan MV, Kao GL (1983) Frog Embryo Teratogenesis Assay: Xenopus (FETAX) — A Short-Term Assay Applicable to Complex Environmental Mixtures. In: Waters MD, Sandhu SS, Lewtas J et al (eds) Short-Term Bioassays in the Analysis of Complex Environmental Mixtures III. Springer, US, Boston, MA, pp 393–405

    Chapter  Google Scholar 

  16. Tamaoki K, Okada R, Ishihara A et al (2016) Morphological, biochemical, transcriptional and epigenetic responses to fasting and refeeding in intestine of Xenopus laevis. Cell Biosci 6:2. https://doi.org/10.1186/s13578-016-0067-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Mathew S, Fu L, Hasebe T et al (2010) Tissue-dependent induction of apoptosis by matrix metalloproteinase stromelysin-3 during amphibian metamorphosis. Birth Defects Res C Embryo Today 90:55–66. https://doi.org/10.1002/bdrc.20170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Leloup J (1977) La triiodothyronine, hormone de la metamorphose des amphibiens. CR Acad Sci Paris, D 284:2261–2263

    CAS  Google Scholar 

  20. Krain LP, Denver RJ (2004) Developmental expression and hormonal regulation of glucocorticoid and thyroid hormone receptors during metamorphosis in Xenopus laevis. J Endocrinol 181:91–104. https://doi.org/10.1677/joe.0.1810091

    Article  CAS  PubMed  Google Scholar 

  21. Fujimoto K, Nakajima K, Yaoita Y (2006) One of the duplicated matrix metalloproteinase-9 genes is expressed in regressing tail during anuran metamorphosis. Dev Growth Differ 48:223–241. https://doi.org/10.1111/j.1440-169X.2006.00859.x

    Article  CAS  PubMed  Google Scholar 

  22. Wang Z, Brown DD (1993) Thyroid hormone-induced gene expression program for amphibian tail resorption. J Biol Chem 268:16270–16278

    Article  CAS  PubMed  Google Scholar 

  23. Larsen PH, DaSilva AG, Conant K, Yong VW (2006) Myelin formation during development of the CNS is delayed in matrix metalloproteinase-9 and -12 null mice. J Neurosci 26:2207–2214. https://doi.org/10.1523/JNEUROSCI.1880-05.2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Verslegers M, Van Hove I, Dekeyster E et al (2015) MMP-2 mediates Purkinje cell morphogenesis and spine development in the mouse cerebellum. Brain Struct Funct 220:1601–1617. https://doi.org/10.1007/s00429-014-0747-3

    Article  CAS  PubMed  Google Scholar 

  25. McKenna M, Shackelford D, Ferreira Pontes H et al (2021) Multiple particle tracking detects changes in brain extracellular matrix and predicts neurodevelopmental age. ACS Nano 15:8559–8573. https://doi.org/10.1021/acsnano.1c00394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Ethell IM, Ethell DW (2007) Matrix metalloproteinases in brain development and remodeling: synaptic functions and targets. J Neurosci Res 85:2813–2823. https://doi.org/10.1002/jnr.21273

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Editage (https://www.editage.jp/) for the thorough and critical reading and revision of the manuscript.

Funding

This work was supported in part by JSPS KAKENHI (Grant Number 22K06312).

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Authors and Affiliations

  1. Department of Biological Science, Faculty of Science, Shizuoka University, Shizuoka, 422-8529, Japan

    Akinori Ishihara

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  1. Akinori Ishihara
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Material preparation, data collection and analysis, and the first draft of the manuscript was prepared by Akinori Ishihara.

Corresponding author

Correspondence to Akinori Ishihara.

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The authors declare no conflicts of interest.

Research involving human/animal participants

All breeding and experimental procedures were approved by the Shizuoka University Animal Experiment Committee (permits #2019F-10 and #2020F-11) under the International Guidelines on Welfare and Management of Animals (Ministry of the Environment).

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Ishihara, A. Hydroxylated polychlorinated biphenyls may affect the thyroid hormone-induced brain development during metamorphosis of Xenopus laevis by disturbing the expression of matrix metalloproteinases. Mol Biol Rep 51, 624 (2024). https://doi.org/10.1007/s11033-024-09555-w

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