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Effect of retinoids on Post2 Нох gene expression in nereid polychaetes

Russian Journal of Developmental Biology volume 48, pages 211–218 (2017)Cite this article

Abstract

Retinoic acid (RA) plays an important role in vertebrate development and regeneration. RA signalling directly regulates the expression of Hox genes, being in this way involved in the patterning of the anterior-posterior (AP) axis of vertebrate embryos. So far the relationship between retinoic acid signalling and Hox genes has been shown only for chordates. In this study we incubated juvenile worms and regenerating worms of two polychaete species from the family Nereididae, Alitta virens and Platynereis dumerilii, with all-trans-retinal, the precursor of retinoic acid. Under the influence of all-trans-retinal the anterior expression boundary of Post2 Нох gene shifted towards the anterior end both in intact and in regenerating worms of both species. Our data indicate the existence of a relationship between RA signalling and Нох genes in Protostomia.

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References

  • Ahn, Y., Mullan, H.E., and Krumlauf, R., Long-range regulation by shared retinoic acid response elements modulates dynamic expression of posterior Hoxb genes in CNS development, Dev. Biol., 2014, vol. 388, pp. 134–144.

    Article  CAS  PubMed  Google Scholar 

  • Albalat, R., The retinoic acid machinery in invertebrates: ancestral elements and vertebrate innovations, Mol. Cell Endocrinol., 2009, vol. 313, pp. 23–35.

    Article  CAS  PubMed  Google Scholar 

  • Bakalenko, N.I., Novikova, E.L., Nesterenko, A.Y., and Kulakova, M.A., Hox gene expression during postlarval development of the polychaete Alitta virens, EvoDevo, 2013, vol. 4, p. 13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bel-Vialar, S., Itasaki, N., and Krumlauf, R., Initiating Hox gene expression: in the early chick neural tube differential sensitivity to FGF and RA signaling subdivides the HoxB genes in two distinct groups, Development, 2002, vol. 129, pp. 5103–5115.

    CAS  PubMed  Google Scholar 

  • Brade, T., Kumar, S., Cunningham, T.J., Chatzi, C., Zhao, X., Cavallero, S., Li, P., Sucov, H.M., Ruiz-Lozano, P., and Duester, G., Retinoic acid stimulates myocardial expansion by induction of hepatic erythropoietin which activates epicardial Igf2, Development, 2011, vol. 138, pp. 139–148.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bui-Gobbels, K., Quintela, R.M., Braunig, P., et al., Is retinoic acid a signal for nerve regeneration in insects?, Neural Regener. Res., 2015, vol. 10, no. 6, pp. 901–903.

    Article  Google Scholar 

  • Campo-Paysaa, F., Marletaz, F., Laudet, V., and Schubert, M., Retinoic acid signaling in development: tissue-specific functions and evolutionary origins, Genesis, 2008, vol. 46, pp. 640–656.

    Article  CAS  PubMed  Google Scholar 

  • Canestro, C., Postlethwait, J.H., Gonzalez-Duarte, R., and Albalat, R., Is retinoic acid genetic machinery a chordate innovation?, Evol. Dev., 2006, vol. 8, no. 5, pp. 394–406.

    Article  CAS  PubMed  Google Scholar 

  • Chang, J., Skromne, I., and Ho, R.K., Cdx4 and retinoic acid interact to position the hindbrain-spinal cord transition, Dev. Biol., 2016, vol. 410, no. 2, pp. 178–189.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cunningham, T.J. and Duester, G., Mechanisms of retinoic acid signaling and its roles in organ and limb development, Nat. Rev. Mol. Cell Biol., 2015. doi 10.1038/nrm3932

    Google Scholar 

  • Ermakova, O.N., Ermakov, A.M., Tiras, Kh.P., and Lednev, V.V., Retinoic acid as a regulator of planarian morphogenesis, Russ. J. Dev. Biol., 2009, vol. 40, no. 6, pp. 367–372.

    Article  CAS  Google Scholar 

  • Farrar, N.R., Dmetrichuk, J.M., Carlone, R.L., and Spencer, G.E., A novel, nongenomic mechanism underlies retinoic acid-induced growth cone turning, J. Neurosci., 2009, vol. 29, pp. 14136–14142.

    Article  CAS  PubMed  Google Scholar 

  • Fröbius, A.C., Matus, D.Q., and Seaver, E.C., Genomic organization and expression demonstrate spatial and temporal Hox gene collinearity in the lophotrochozoan Capitella sp., PLoS One, 2008, vol. 3, p. e4004.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gudas, L.J., Emerging roles for retinoids in regeneration and differentiation in normal and disease states, Biochem. Biophys. Acta, 2012, vol. 1821, no. 1, pp. 213–221.

    CAS  PubMed  Google Scholar 

  • Hernandez, R.E., Putzke, A.P., Myers, J.P., Margaretha, L., and Moens, C.B., Cyp26 enzymes generate the retinoic acid response pattern necessary for hindbrain development, Development, 2007, vol. 134, pp. 177–187.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Houle, M., Prinos, P., Iulianella, A., Bouchard, N., and Lohnes, D., Retinoic acid regulation of Cdx1: an indirect mechanism for retinoids and vertebral specification, Mol. Cell Biol., 2000, vol. 20, no. 17, pp. 6579–6586.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Katsuyama, Y., Wada, S., Yasugi, S., and Saiga, H., Expression of the labial group Hox gene HrHox-1 and its alteration induced by retinoic acid in development of the ascidian Halocynthia roretzi, Development, 1995, vol. 121, pp. 3197–3205.

    CAS  PubMed  Google Scholar 

  • Kulakova, M., Bakalenko, N., Novikova, E., Cook, C.E., Eliseeva, E., Steinmetz, P.R., Kostyuchenko, R.P., Dondua, A., Arendt, D., Akam, M., and Andreeva, T., Hox gene expression in larval development of the polychaetes Nereis virens and Platynereis dumerilii (Annelida, Lophotrochozoa), Dev. Genes Evol., 2007, vol. 217, pp. 39–54.

    Article  CAS  PubMed  Google Scholar 

  • Kumar, S. and Duester, G., Retinoic acid signaling in perioptic mesenchyme represses Wnt signaling via induction of Pitx2 and Dkk2, Dev. Biol., 2010, vol. 340, pp. 67–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar, S., Cunningham, T.J., and Duester, G., Resolving molecular events in the regulation of meiosis in male and female germ cells, Sci. Signal., 2013, vol. 6, p. e25.

    Article  Google Scholar 

  • Linville, A., Gumusaneli, E., Chandraratna, R.A., and Schilling, T.F., Independent roles for retinoic acid in segmentation and neuronal differentiation in the zebrafish hindbrain, Dev. Biol., 2004, vol. 270, pp. 186–199.

    Article  CAS  PubMed  Google Scholar 

  • Maden, M., Vitamin A and pattern formation in the regenerating limb, Nature, 1982, vol. 295, pp. 672–675.

    Article  CAS  PubMed  Google Scholar 

  • Maden, M. and Hind, M., Retinoic acid, a regenerationinducing molecule, Dev. Dynam., 2003, vol. 226, pp. 237–244.

    Article  CAS  Google Scholar 

  • Mainguy, G., In der Rieden, P.M.J., Berezikov, E., Woltering, J.M., Plasterk, R.H.A., and Durston, A.J., A position-dependent organisation of retinoid response elements is conserved in the vertebrate Hox clusters, Trends Genet., 2003, vol. 19, no. 9, pp. 476–479.

    Article  CAS  PubMed  Google Scholar 

  • Marletaz, F., Holland, L.Z., Laudet, V., and Schubert, M., Retinoic acid signaling and the evolution of chordates, Int. J. Biol. Sci., 2006, vol. 2, no. 2, pp. 38–47.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maves, L. and Kimmel, C.B., Dynamic and sequential patterning of the zebrafish posterior hindbrain by retinoic acid, Dev. Biol., 2005, vol. 285, pp. 593–605.

    Article  CAS  PubMed  Google Scholar 

  • Molotkova, N., Molotkov, A., and Duester, G., Role of retinoic acid during forebrain development begins late when Raldh3 generates retinoic acid in the ventral subventricular zone, Dev. Biol., 2007, vol. 303, pp. 601–610.

    Article  CAS  PubMed  Google Scholar 

  • Nagatomo, K., Ishibashi, T., Satou, Y., Satoh, N., and Fujiwara, S., Retinoic acid affects gene expression and morphogenesis without upregulating the retinoic acid receptor in the ascidian Ciona intestinalis, Mech. Dev., 2003, vol. 120, pp. 363–372.

    Article  CAS  PubMed  Google Scholar 

  • Niazi, I.A. and Saxena, S., Abnormal hind limb regeneration in tadpoles of the toad, Bufo andersoni, exposed to excess vitamin, Folia Biol. (Krakow), 1978, vol. 26, pp. 3–8.

    CAS  Google Scholar 

  • Niederreither, K., Vermot, J., Schuhbaur, B., Chambon, P., and Dollé, P., Retinoic acid synthesis and hindbrain patterning in the mouse embryo, Development, 2000, vol. 127, pp. 75–85.

    CAS  PubMed  Google Scholar 

  • Nowickyj, S.M., Chithalen, J.V., Cameron, D., Tyshenko, M.G., Petkovich, M., Wyatt, G.R., Jones, G., and Walker, V.K., Locust retinoid X receptors: 9-cisretinoic acid in embryos from a primitive insect, Proc. Natl. Acad. Sci. U. S. A., 2008, vol. 105, pp. 9540–9545.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oosterveen, T., Niederreither, K., Dolle, P., Chambon, P., Meijlink, F., and Deschamps, J., Retinoids regulate the anterior expression boundaries of 5' HoxB genes in posterior hindbrain, EMBO J., 2003, vol. 22, no. 2, pp. 262–269.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rhinn, M. and Dolle, P., Retinoic acid signalling during development, Development, 2012, vol. 139, pp. 843–858.

    Article  CAS  PubMed  Google Scholar 

  • Rijli, F.M., Gavalas, A., and Chambon, P., Segmentation and specification in the branchial region of the head: the role of the Hox selector genes, Int. J. Dev. Biol., 1998, vol. 42, pp. 393–401.

    CAS  PubMed  Google Scholar 

  • Santini, S., Boore, J.L., and Meyer, A., Evolutionary conservation of regulatory elements in vertebrate Hox gene clusters, Genome Res., 2003, vol. 13, no. 6A, pp. 1111–1122.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schubert, M., Holland, N.D., Laudet, V., and Holland, L.Z., A retinoic acid–Hox hierarchy controls both anterior/ posterior patterning and neuronal specification in the developing central nervous system of the cephalochordate amphioxus, Dev. Biol., 2006, vol. 296, pp. 190–202.

    Article  CAS  PubMed  Google Scholar 

  • Sciarrino, S. and Matranga, V., Effects of retinoic acid and dimethylsulfoxide on the morphogenesis of the sea urchin embryo, Cell Biol. Int. Rep., 1995, vol. 19, pp. 675–680.

    Article  CAS  Google Scholar 

  • Sirbu, I.O., Gresh, L., Barra, J., and Duester, G., Shifting boundaries of retinoic acid activity control hindbrain segmental gene expression, Development, 2005, vol. 132, pp. 2611–2622.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sukiban, J., Bräunig, P., Mey, J., and Bui-Göbbels, K., Retinoic acid as a survival factor in neuronal development of the grasshopper, Locusta migratoria, Cell Tissue Res., 2014, vol. 358, pp. 303–312.

    Article  CAS  PubMed  Google Scholar 

  • Wada, H., Escriva, H., Zhang, S., and Laudet, V., Conserved rare localization in amphioxus Hox clusters and implications for Hox code evolution in the vertebrate neural crest, Dev. Dynam., 2006, vol. 235, pp. 1522–1531.

    Article  CAS  Google Scholar 

  • Young, T., Rowland, J.E., van de Ven, C., Bialecka, M., Novoa, A., Carapuco, M., van Nes, J., de Graaff, W., Duluc, I., Freund, J.N., Beck, F., Mallo, M., and Deschamps, J., Cdx and Hox genes differentially regulate posterior axial growth in mammalian embryos, Dev. Cell, 2009, vol. 17, no. 4, pp. 516–526.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Saint Petersburg University, St. Petersburg, 199034, Russia

    N. I. Bakalenko, A. V. Poznyak, E. L. Novikova & M. A. Kulakova

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  1. N. I. Bakalenko
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  2. A. V. Poznyak
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  3. E. L. Novikova
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  4. M. A. Kulakova
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Correspondence to N. I. Bakalenko.

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Published in Russian in Ontogenez, 2017, Vol. 48, No. 3, pp. 248–256.

The article was translated by the authors.

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Bakalenko, N.I., Poznyak, A.V., Novikova, E.L. et al. Effect of retinoids on Post2 Нох gene expression in nereid polychaetes. Russ J Dev Biol 48, 211–218 (2017). https://doi.org/10.1134/S106236041703002X

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  • DOI: https://doi.org/10.1134/S106236041703002X

Keywords

  • Hox genes
  • RA signaling
  • polychaetes