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Expression Patterns and Biological Roles of Micall2a during Zebrafish Vascular Development

  • DEVELOPMENTAL BIOLOGY
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Abstract

MICAL-like 2 belongs to a multi-domain protein family and involves in a series of biological processes. However, the expression patterns and biological functions of this gene during embryonic development have not been well characterized. Here, the model organism zebrafish (Danio rerio) is utilized to examine the gene expression and its roles in vascular development. Whole-mount in situ hybridization analysis demonstrates that zebrafish micall2a is a maternal gene that commences to express at the zygote stage, and continues to larval stage. Moreover, micall2a is dynamically expressed in zebrafish developing vascular system during a time window encompassing many key steps in embryonic vasculogenesis and angiogenesis. Loss-of-function of micall2a in zebrafish embryos leads to deficiency in caudal vein plexus (CVP) formation, while the dorsal aorta (DA), posterior cardinal vein (PCV), and intersegmental vessels (ISVs) are not influenced. Our study suggests a role of MICALL2 in vascular development and offers a potential therapeutic target for vascular associated diseases.

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REFERENCES

  1. Barravecchia, I., Mariotti, S., Pucci, A., Scebba, F., De Cesari, C., Bicciato, S., Tagliafico, E., Tenedini, E., Vindigni, C., Cecchini, M., Berti, G., Vitiello, M., Poliseno, L., Mazzanti, C.M., and Angeloni, D., MICAL2 is expressed in cancer associated neo-angiogenic capillary endothelia and it is required for endothelial cell viability, motility and VEGF response, Biochim. Biophys. Acta, Mol. Basis Dis., 2019, vol. 1865, pp. 2111–2124. https://doi.org/10.1016/j.bbadis.2019.04.008

    Article  CAS  Google Scholar 

  2. Cai, Y., Lu, J., and Tang, F., Overexpression of MICAL2, a novel tumor-promoting factor, accelerates tumor progression through regulating cell proliferation and EMT, J. Cancer, 2018, vol. 9, pp. 521–527. https://doi.org/10.7150/jca.22355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Chi, N.C., Shaw, R.M., Val, S.D., Kang, G., Jan, L.Y., Black, B.L., and Stainier, D.Y.R., Foxn4 directly regulates tbx2b expression and atrioventricular canal formation, Genes Dev., 2008, vol. 22, pp. 734–739. https://doi.org/10.1101/gad.1629408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Gore, A.V., Monzo, K., Cha, Y.R., Pan, W., and Weinstein, B.M., Vascular development in the zebrafish, Cold Spring Harb. Perspect. Med. 2012, vol. 2, pp. 1–21. https://doi.org/10.1101/cshperspect.a006684

    Article  CAS  Google Scholar 

  5. Gu, H., Li, Y., Cui, X., Cao, H., Hou, Z., Ti, Y., Liu, D., Gao, J., Wang, Y., and Wen, P., MICAL1 inhibits colorectal cancer cell migration and proliferation by regulating the EGR1/β-catenin signaling pathway, Biochem. Pharmacol., 2022, vol. 195, p. 114870. https://doi.org/10.1016/j.bcp.2021.114870

    Article  CAS  PubMed  Google Scholar 

  6. Ioannou, M.S., Bell, E.S., Girard, M., Chaineau, M., Hamlin, J.N.R., Daubaras, M., Monast, A., Park, M., Hodgson, L., and McPherson, P.S., DENND2B activates Rab13 at the leading edge of migrating cells and promotes metastatic behavior, J. Cell Biol., 2015, vol. 208, pp. 629–648. https://doi.org/10.1083/jcb.201407068

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Krueger, J., Liu, D., Scholz, K., Zimmer, A., Shi, Y., Klein, C., Siekmann, A., Schulte-Merker, S., Cudmore, M., Ahmed, A., and Noble, F., Flt1 acts as a negative regulator of tip cell formation and branching morphogenesis in the zebrafish embryo, Development, 2011, vol. 138, no. 10, pp. 2111–2120. https://doi.org/10.1242/dev.063933

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Min, P., Zhao, S., Liu, L., Zhang, Y., Ma, Y., Zhao, X., Wang, Y., Song, Y., Zhu, C., Jiang, H., Gu, L., and Du, J., MICAL-L2 potentiates Cdc42-dependent EGFR stability and promotes gastric cancer cell migration, J. Cell Mol. Med., 2019, vol. 23, pp. 4475–4488. https://doi.org/10.1111/jcmm.14353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Risau, W. and Flamme, I., Vasculogenesis, Annu. Rev. Cell Dev. Biol., 1995, vol. 11, pp. 73–91. https://doi.org/10.1146/annurev.cb.11.110195.000445

    Article  CAS  PubMed  Google Scholar 

  10. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J.-Y., White, D.J., Hartenstein, V., Eliceiri, K., Tomancak, P., and Cardona, A., Fiji: an open-source platform for biological-image analysis, Nat. Methods, 2012, vol. 9, pp. 676–682. https://doi.org/10.1038/nmeth.2019

    Article  CAS  PubMed  Google Scholar 

  11. Suzuki, T., Nakamoto, T., Ogawa, S., Seo, S., Matsumura, T., Tachibana, K., Morimoto, C., and Hirai, H., MICAL, a novel CasL interacting molecule, associates with vimentin, J. Biol. Chem., 2002, vol. 277, pp. 14933–14941. https://doi.org/10.1074/jbc.M111842200

    Article  CAS  PubMed  Google Scholar 

  12. Terai, T., Nishimura, N., Kanda, I., Yasui, N., and Sasaki, T., JRAB/MICAL-L2 is a junctional Rab13-binding protein mediating the endocytic recycling of occludin, Mol. Biol. Cell, 2006, vol. 17, pp. 2465–2475. https://doi.org/10.1091/mbc.e05-09-0826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Wang, X., Ling, C.C., Li, L., Qin, Y., Qi, J., Liu, X., You, B., Shi, Y., Zhang, J., Jiang, Q., Xu, H., Sun, C., You, Y., Chai, R., and Liu, D., MicroRNA-10a/10b represses a novel target gene mib1 to regulate angiogenesis, Cardiovasc. Res., 2016, vol. 1, pp. 140–150. https://doi.org/10.1093/cvr/cvw023

    Article  CAS  Google Scholar 

  14. Wang, F., Chen, X., Cheng, H., Song, L., Liu, J., Caplan, S., Zhu, L., and Wu, J.Y., MICAL2PV suppresses the formation of tunneling nanotubes and modulates mitochondrial trafficking, EMBO Rep., 2021, vol. 22, p. e52006. https://doi.org/10.15252/embr.202052006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Wang, X., Ge, X., Qin, Y., Liu, D., and Chen, C., Ifi30 is required for sprouting angiogenesis during caudal vein plexus formation in zebrafish, Front. Physiol., 2022, vol. 13, p. 919579. https://doi.org/10.3389/fphys.2022.919579

    Article  PubMed  PubMed Central  Google Scholar 

  16. Wen, P., Wang, H., Li, Y., Sui, X., Hou, Z., Guo, X., Xue, W., Liu, D., Wang, Y., and Gao, J., MICALL2 as a substrate of ubiquitinase TRIM21 regulates tumorigenesis of colorectal cancer, Cell Commun. Signal., 2022, vol. 20, p. 170. https://doi.org/10.1186/s12964-022-00984-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Xue, Y., Kuok, C., Xiao, A., Zhu, Z., Lin, S., and Zhang, B., Identification and expression analysis of mical family genes in zebrafish, J. Genet. Genomics, 2010, vol. 37, pp. 685–693. https://doi.org/10.1016/S1673-8527(09)60086-2

    Article  CAS  PubMed  Google Scholar 

  18. Yang, L., Chang, S., Lu, Q., Zhang, Y., Wu, Z., Sun, X., Cao, Q., Qian, Y., Jia, T., Xu, B., Duan, Q., Li, Y., Zhang, K., Schumann, G., Liu, D., Wang, J., Wang, Y., and Lu, L., A new locus regulating MICALL2 expression was identified for association with executive inhibition in children with attention deficit hyperactivity disorder, Mol. Psychiatry, 2018, vol. 23, pp. 1014–1020. https://doi.org/10.1038/mp.2017.74

    Article  CAS  PubMed  Google Scholar 

  19. Yang, Y., Ye, F., Xia, T., Wang, Q., Zhang, Y., and Du, J., High MICAL-L2 expression and its role in the prognosis of colon adenocarcinoma, BMC Cancer, 2022, vol. 22, p. 487. https://doi.org/10.1186/s12885-022-09614-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Zhou, Y., Gunput, R.-A.F., Adolfs, Y., and Pasterkamp, R.J., MICALs in control of the cytoskeleton, exocytosis, and cell death, Cell Mol. Life Sci., 2011, vol. 68, pp. 4033–4044. https://doi.org/10.1007/s00018-011-0787-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Zhu, L.-Y., Zhang, W.-M., Yang, X.-M., Cui, L., Li, J., Zhang, Y.-L., Wang, Y.-H., Ao, J.-P., Ma, M.-Z., Lu, H., Ren, Y., Xu, S.-H., Yang, G.-D., Song, W.-W., Wang, J.-H., Zhang, X.-D., Zhang, R., and Zhang, Z.-G., Silencing of MICAL-L2 suppresses malignancy of ovarian cancer by inducing mesenchymal–epithelial transition, Cancer Lett., 2015, vol. 363, pp. 71–82. https://doi.org/10.1016/j.canlet.2015.04.002

    Article  CAS  PubMed  Google Scholar 

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Funding

This study was supported by grants from the National Natural Science Foundation of China (82000458).

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Authors and Affiliations

  1. School of Life Sciences, Nantong University, 226019, Nantong, China

    Wei Liu, Dongxu Fu, Dong Liu & Changsheng Chen

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  1. Wei Liu
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  2. Dongxu Fu
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  3. Dong Liu
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Contributions

Wei Liu and Dongxu Fu contributed equally to this work. Changsheng Chen and Dong Liu supervised and designed this project. Changsheng Chen wrote the manuscript. Wei Liu and Dongxu Fu performed the experiments. Wei Liu, Dongxu Fu and Changsheng Chen analyzed the data.

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Correspondence to Changsheng Chen.

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Conflict of interest. The authors declare that they have no conflicts of interest. The authors declare that they have no conflicts of interest.

Statement on the welfare of animals. Animal-related experiments were carried out following the NIH Guidelines for the care and use of laboratory animals (http://oacu.od.nih.gov/regs/index.htm), and animal protocols were ethically approved by the Administration Committee of Experimental Animals of Nantong University, Jiangsu Province, China (Approval ID: SYXK(SU) 20200711–001 of January 30, 2021).

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Wei Liu, Fu, D., Liu, D. et al. Expression Patterns and Biological Roles of Micall2a during Zebrafish Vascular Development. Biol Bull Russ Acad Sci 50, 1106–1114 (2023). https://doi.org/10.1134/S1062359023600885

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  • DOI: https://doi.org/10.1134/S1062359023600885

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