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Autophagy is required for sea urchin oogenesis and early development

Published online by Cambridge University Press:  01 November 2016

Maria Agnello ,
Roberto Chiarelli ,
Chiara Martino ,
Liana Bosco  and
Maria Carmela Roccheri
Maria Agnello*
Affiliation:
Department of Biological, Chemical, and Pharmaceutical Sciences and Technologies, University of Palermo, Viale delle Scienze Ed. 16, 90128 Palermo, Italy.
Roberto Chiarelli
Affiliation:
Dipartimento di Scienze e Tecnologie Biologiche, Chimiche e Farmaceutiche, Università di Palermo, Viale delle Scienze Ed. 16, Palermo 90128, Italy.
Chiara Martino
Affiliation:
Dipartimento di Scienze e Tecnologie Biologiche, Chimiche e Farmaceutiche, Università di Palermo, Viale delle Scienze Ed. 16, Palermo 90128, Italy.
Liana Bosco
Affiliation:
Dipartimento di Scienze e Tecnologie Biologiche, Chimiche e Farmaceutiche, Università di Palermo, Viale delle Scienze Ed. 16, Palermo 90128, Italy.
Maria Carmela Roccheri
Affiliation:
Dipartimento di Scienze e Tecnologie Biologiche, Chimiche e Farmaceutiche, Università di Palermo, Viale delle Scienze Ed. 16, Palermo 90128, Italy.
*
All correspondence to: Maria Agnello. Department of Biological, Chemical, and Pharmaceutical Sciences and Technologies, University of Palermo, Viale delle Scienze Ed. 16, 90128 Palermo, Italy. Tel: +39 091 238 97 419. Fax: +39 091 65 77 210. E-mail: [email protected]
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Summary

Autophagy is a major intracellular pathway for the degradation and recycling of cytosolic components. Emerging evidence has demonstrated its crucial role during the embryo development of invertebrates and vertebrates. We recently demonstrated a massive activation of autophagy in Paracentrotus lividus embryos under cadmium stress conditions, and the existence of a temporal relationship between induced autophagy and apoptosis. Although there have been numerous studies on the role of autophagy in the development of different organisms, information on the autophagic process during oogenesis or at the start of development in marine invertebrates is very limited. Here we report our recent data on the occurrence of autophagy at these key phases of development. In order to investigate autophagy trends we performed in vivo assays to detect autophagolysomes, as well as in situ analysis with anti-LC3 antibody to detect autophagosomes before the fusion with lysosomes. From data generated through confocal laser scanning microscopy and quantification of autophagic signals we have drawn several unequivocal conclusions. The results showed a copious and rising number of autophagic organelles that had specific localization. Interestingly the increase in autophagy that occurred just after fertilization has been proved to be crucial for correct initiation of the developmental programme: irreversible developmental delays and morphologic anomalies were induced by short autophagic inhibition. This work focused on the sea urchin model system and corroborates evidence on the need for self-digestion during development, enriching the knowledge on autophagy, a biological mechanism belonging to evolutionarily different organisms.

Keywords

LC3Caspase-3EmbryosOocytesParacentrotus lividus
Type
Research Article
Information
Zygote , Volume 24 , Issue 6 , December 2016 , pp. 918 - 926
Copyright
Copyright © Cambridge University Press 2016 

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References

Agnello, M. & Roccheri, M.C. (2010). Apoptosis: focus on sea urchin development. Apoptosis 15, 322–30.Google Scholar
Agnello, M., Filosto, S., Scudiero, R., Rinaldi, A.M. & Roccheri, M.C. (2007). Cadmium induces an apoptotic response in sea urchin embryos. Cell Stress Chaperon. 12, 44–50.Google Scholar
Agnello, M., Bosco, L., Chiarelli, R., Martino, C. & Roccheri, M.C. (2015). The role of autophagy and apoptosis during embryo development. In Cell Death – Autophagy, Apoptosis and Necrosis (ed. Ntuli, T.M.), pp. 83–112. Rijeka: Croatia: INTECH.Google Scholar
Chiarelli, R., Agnello, M. & Roccheri, M.C. (2011). Sea urchin embryos as a model system for studying autophagy induced by cadmium stress. Autophagy 7, 1028–34.Google Scholar
Chiarelli, R., Agnello, M., Bosco, L. & Roccheri, M.C. (2014). Sea urchin embryos exposed to cadmium as an experimental model for studying the relationship between autophagy and apoptosis. Mar. Environ. Res. 93, 47–55.Google Scholar
Chiarelli, R., Martino, C., Agnello, M., Bosco, L. & Roccheri, M.C. (2016). Autophagy as a defense strategy against stress: focus on Paracentrotus lividus sea urchin embryos exposed to cadmium. Cell Stress Chaperon. 21, 19–27.Google Scholar
Di Bartolomeo, S., Nazio, F. & Cecconi, F. (2010). The role of autophagy during development in higher eukaryotes. Traffic 11, 1280–9.Google Scholar
Ettensohn, C.A., Wessel, G.M. & Wray, G.A. (2004). Development of sea urchins, ascidians, and other invertebrate deuterostomes: experimental approaches. In Gaining Access to the Eggs and Embryos (ed. McClay, D.R.), pp. 312–5. San Diego, California, USA: Elsevier Academic Press.Google Scholar
Fissore, R.A., Kurokawa, M., Knott, J., Zhang, M. & Smyth, J. (2002). Mechanisms underlying oocyte activation and postovulatory ageing. Reproduction 124, 745–54.Google Scholar
Giudice, G., Sconzo, G., Bono, A. & Albanese, I. (1972). Studies on sea urchin oocytes. I. Purification and cell fractionation. Exp. Cell Res. 72, 90–4.Google Scholar
Greenwood, J. & Gautier, J. (2005). From oogenesis through gastrulation: developmental regulation of apoptosis. Semin. Cell Dev. Biol. 16, 215–24.CrossRefGoogle ScholarPubMed
Houel-Renault, L., Philippe, L., Piquemal, M. & Ciapa, B. (2013). Autophagy is used as a survival program in unfertilized sea urchin eggs that are destined to die by apoptosis after inactivation of MAPK1/3 (ERK2/1). Autophagy 9, 1527–39.Google Scholar
Kiyomoto, M., Zito, F., Costa, C., Poma, V., Sciarrino, S. & Matranga, V. (2007). Skeletogenesis by transfected secondary mesenchyme cells is dependent on extracellular matrix-ectoderm interactions in Paracentrotus lividus sea urchin embryos. Dev. Growth Differ. 49, 731–41.CrossRefGoogle Scholar
Klionsky, D.J., Abdalla, F.C., Abeliovich, H., Abraham, R.T., Acevedo-Arozena, A., Adeli, K., Agholme, L., Agnello, M., Agostinis, P., Aguirre-Ghiso, J.A. et al. (2012). Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8, 445–544.CrossRefGoogle ScholarPubMed
Klionsky, D.J., Abdelmohsen, K., Abe, A., Abedin, M.J., Abeliovich, H., Acevedo-Arozena, A., Adachi, H., Adams, C.M., Adams, P.D., Adeli, K, et al. (2016). Guidelines for the use and interpretation of assays for monitoring autophagy, 3rd edn. Autophagy 12, 1–222.CrossRefGoogle Scholar
Lera, S. & Pellegrini, D. (2006). Evaluation of the fertilization capability of Paracentrotus lividus sea urchin storaged gametes by the exposure to different aqueous matrices. Environ. Monit. Assess. 119, 1–13.Google Scholar
Levine, B. & Klionsky, D.J. (2004). Development by Self-Digestion. Molecular mechanisms and biological functions of autophagy. Dev. Cell. 6, 463–77.Google Scholar
Morici, G., Agnello, M., Spagnolo, F., Roccheri, M.C., Di Liegro, C.M. & Rinaldi, A.M. (2007). Confocal microscopy study of the distribution, content and activity of mitochondria during Paracentrotus lividus development. J. Microsc. 228, 165–73.Google Scholar
Penaloza, C., Lin, L., Lockshin, R.A. & Zakeri, Z. (2006). Cell death in development: shaping the embryo. Histochem. Cell Biol. 126, 149–58.Google Scholar
Philippe, L., Tosca, L., Zhang, W.L., Piquemal, M. & Ciapa, B. (2014). Different routes lead to apoptosis in unfertilized sea urchin eggs. Apoptosis 19, 436–50.Google Scholar
Robertson, A.J., Croce, J., Carbonneau, S., Voronina, E., Miranda, E., McClay, D.R. & Coffman, J.A. (2006). The genomic underpinnings of apoptosis in Strongylocentrotus purpuratus . Dev. Biol. 300, 321–34.Google Scholar
Roccheri, M.C., Barbata, G., Cardinale, F., Tipa, C., Bosco, L., Oliva, O.A., Cascino, D. & Giudice, G. (1997). Apoptosis in sea urchin embryos. Biochem. Biophys. Res. Commun. 240, 359–66.Google Scholar
Roccheri, M.C., Tipa, C., Bonaventura, R. & Matranga, V. (2002). Physiological and induced apoptosis in sea urchin larvae undergoing metamorphosis. Int. J. Dev. Biol. 46, 801–6.Google ScholarPubMed
Roccheri, M.C., Agnello, M., Bonaventura, R. & Matranga, V. (2004). Cadmium induces the expression of specific stress proteins in sea urchin embryos. Biochem. Biophys. Res. Commun. 321, 80–7.Google Scholar
Song, J.L., Wong, J.L. & Wessel, G.M. (2006). Oogenesis: single cell development and differentiation. Dev. Biol. 300, 385–405.CrossRefGoogle ScholarPubMed
Tettamanti, G., Saló, E., González-Estévez, C., Felix, D.A., Grimaldi, A. & de Eguileor, M. (2008). Autophagy in invertebrates: insights into development, regeneration and body remodeling. Curr. Pharm. Des. 14, 116–25.Google Scholar
Tsukamoto, S., Kuma, A. & Mizushima, N. (2008a). The role of autophagy during the oocyte-to-embryo transition. Autophagy 4, 1076–8.Google Scholar
Tsukamoto, S., Kuma, A., Murakami, M., Kishi, C., Yamamoto, A. & Mizushima, N. (2008b). Autophagy is essential for preimplantation development of mouse embryos. Science 321, 117–20.Google Scholar
Wada, Y., Sun-Wada, G.H., Kawamura, N. & Aoyama, M. (2014). Role of autophagy in embryogenesis. Curr. Opin. Genet. Dev. 27, 60–6.CrossRefGoogle ScholarPubMed
Walker, C.W., Harrington, L.M., Lesser, M.P. & Fagerberg, W.R. (2005). Nutritive phagocyte incubation chambers provide a structural and nutritive microenvironment for germ cells of Strongylocentrotus droebachiensis, the green sea urchin. Biol. Bull. 209, 31–48.CrossRefGoogle ScholarPubMed
Xie, Z. & Klionsky, D.J. (2007). Autophagosome formation: core machinery and adaptations. Nat. Cell Biol. 9, 1102–9.CrossRefGoogle ScholarPubMed
Yamamoto, A., Tagawa, Y., Yoshimori, T., Moriyama, Y., Masaki, R. & Tashiro, Y. (1998). Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell. Struct. Funct. 23, 33–42.Google Scholar
Yang, P. & Zhang, H. (2014). You are what you eat: multifaceted functions of autophagy during C. elegans development. Cell. Res. 24, 80–91.Google Scholar