Skip to main content
SpringerLink
Log in

Autophagy as a defense strategy against stress: focus on Paracentrotus lividus sea urchin embryos exposed to cadmium

  • Mini Review
  • Published:
Cell Stress and Chaperones Aims and scope

Abstract

Autophagy is used by organisms as a defense strategy to face environmental stress. This mechanism has been described as one of the most important intracellular pathways responsible for the degradation and recycling of proteins and organelles. It can act as a cell survival mechanism if the cellular damage is not too extensive or as a cell death mechanism if the damage/stress is irreversible; in the latter case, it can operate as an independent pathway or together with the apoptotic one. In this review, we discuss the autophagic process activated in several aquatic organisms exposed to different types of environmental stressors, focusing on the sea urchin embryo, a suitable system recently included into the guidelines for the use and interpretation of assays to monitor autophagy. After cadmium (Cd) exposure, a heavy metal recognized as an environmental toxicant, the sea urchin embryo is able to adopt different defense mechanisms, in a hierarchical way. Among these, autophagy is one of the main responses activated to preserve the developmental program. Finally, we discuss the interplay between autophagy and apoptosis in the sea urchin embryo, a temporal and functional choice that depends on the intensity of stress conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Agnello M, Roccheri MC (2010) Apoptosis: focus on sea urchin development. Apoptosis 15:322–330

    Article  PubMed  Google Scholar 

  • Agnello M, Filosto S, Scudiero R, Rinaldi AM, Roccheri MC (2006) Cadmium accumulation induces apoptosis in P. lividus embryos. Caryologia 59:403–408

    Google Scholar 

  • Agnello M, Filosto S, Scudiero R, Rinaldi AM, Roccheri MC (2007) Cadmium induces an apoptotic response in sea urchin embryos. Cell Stress Chaperones 12:44–50

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Allen JI, McVeigh A (2004) Towards computational models of cells for environmental toxicology. J Mol Histol 35:697–706

    PubMed  Google Scholar 

  • Bargagli R (2000) Trace metals in Antarctica related to climate change and increasing human impact. Rev Environ Contam Toxicol 166:129–73

    CAS  PubMed  Google Scholar 

  • Byrne M (2012) Global change ecotoxicology: identification of early life history bottlenecks in marine invertebrates, variable species responses and variable experimental approaches. Mar Environ Res 76:3–15

    Article  CAS  PubMed  Google Scholar 

  • Chapman HN, Jacobsen C, Williams SA (1996) Characterisation of dark-field imaging of colloidal gold labels in a scanning transmission X-ray microscope. Ultramicroscopy 62:191–213

    Article  CAS  PubMed  Google Scholar 

  • Cheng J, Chan CM, Veca LM, Poon WL, Chan PK, Qu L, Sun YP, Cheng SH (2009) Acute and long-term effects after single loading of functionalized multi-walled carbon nanotubes into zebrafish (Danio rerio). Toxicol Appl Pharmacol 235:216–25

    Article  CAS  PubMed  Google Scholar 

  • Chiarelli R, Roccheri MC (2012) Heavy metals and metalloids as autophagy inducing agents: focus on cadmium and arsenic. Cells 1:597–616

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chiarelli R, Roccheri MC (2013) Strategie di difesa in risposta a stress in embrioni di riccio di mare. L’embrione di Paracentrotus lividus come modello sperimentale per lo studio della sopravvivenza e della morte cellulare. 1st ed., EAI, Saarbrucken, Germany, 2013, pp 1–125

  • Chiarelli R, Roccheri MC (2014) Marine invertebrates as bioindicators of heavy metal pollution. Open J Metal 4:93–106

    Article  Google Scholar 

  • Chiarelli R, Agnello M, Roccheri MC (2011) Sea urchin embryos as a model system for studying autophagy induced by cadmium stress. Autophagy 7:1028–1034

    Article  CAS  PubMed  Google Scholar 

  • Chiarelli R, Agnello M, Bosco L, Roccheri MC (2014) Sea urchin embryos exposed to cadmium as an experimental model for studying the relationship between autophagy and apoptosis. Marine Environ Researchv 93:47–55

    Article  CAS  Google Scholar 

  • Chora S, Starita-Geribaldi M, Guigonis JM, Samson M, Roméo M, Bebianno MJ (2009) Effect of cadmium in the clam Ruditapes decussatus assessed by proteomic analysis. Aquat Toxicol 94:300–308

    Article  CAS  PubMed  Google Scholar 

  • Cuervo AM (2004) Autophagy: in sickness and in health. Trends Cell Biol 14:70–77

    Article  PubMed  Google Scholar 

  • Di Bartolomeo S, Nazio F, Cecconi F (2010) The role of autophagy during development in higher eukaryotes. Traffic 11:1280–1289

    Article  PubMed  Google Scholar 

  • Dong Z, Wang L, Xu J, Li Y, Zhang Y, Zhang S et al (2009) Promotion of autophagy and inhibition of apoptosis by low concentrations of cadmium in vascular endothelial cells. Toxicol In Vitro 23:105–110

    Article  CAS  PubMed  Google Scholar 

  • Downs CA, Kramarsky-Winter E, Martinez J, Kushmaro A, Woodley CM, Loya Y, Ostrander GK (2009) Symbiophagy as a cellular mechanism for coral bleaching. Autophagy 5:211–216

    Article  CAS  PubMed  Google Scholar 

  • Dunn SR, Schnitzler CE, Weis VM (2007) Apoptosis and autophagy as mechanisms of dinoflagellate symbiont release during cnidarian bleaching: every which way you lose. Proc R Soc B 274:3079–3085

    Article  PubMed Central  PubMed  Google Scholar 

  • Dupont S, Ortega-Martínez O, Thorndyke M (2010) Impact of near-future ocean acidification on echinoderms. Ecotoxicology 19:449–62

    Article  CAS  PubMed  Google Scholar 

  • Evans TG, Watson-Wynn P (2014) Effects of seawater acidification on gene expression: resolving broader-scale trends in sea urchins. Biol Bull 226:237–54

    CAS  PubMed  Google Scholar 

  • Filosto S, Roccheri MC, Bonaventura R, Matranga V (2008) Environmentally relevant cadmium concentrations affect development and induce apoptosis of Paracentrotus lividus larvae cultured in vitro. Cell Biol Toxicol 24:603–610

    Article  CAS  PubMed  Google Scholar 

  • Gao D, Xu Z, Kuang X, Qiao P, Liu S, Zhang L, He P, Jadwiga WS, Wang Y, Min W (2014) Molecular characterization and expression analysis of the autophagic gene Beclin 1 from the purse red common carp (Cyprinus carpio) exposed to cadmium. Comp Biochem Physiol C Toxicol Pharmacol 160:15–22

    Article  CAS  PubMed  Google Scholar 

  • Hamada T, Tanimoto A, Sasaguri Y (1997) Apoptosis induced by cadmium. Apoptosis 2:359–367

    Article  CAS  PubMed  Google Scholar 

  • Hamdoun A, Epel D (2007) Embryo stability and vulnerability in an always changing world. Proc Natl Acad Sci U S A 104:1745–50

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • He X, Aker WG, Hwang HM (2014) An in vivo study on the photo-enhanced toxicities of S-doped TiO2 nanoparticles to zebrafish embryos (Danio rerio) in terms of malformation, mortality, rheotaxis dysfunction, and DNA damage. Nanotoxicology 8:185–95

    Article  CAS  PubMed  Google Scholar 

  • Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K et al (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

    Article  CAS  PubMed  Google Scholar 

  • Iwama G, Thomas PT, Forsyth RB, Vijayan MM (1998) Heat shock protein expression in fish. Rev Fish Biol Fish 8:35–56

    Article  Google Scholar 

  • Klionsky DJ, Emr SD (2000) Autophagy as a regulated pathway of cellular degradation. Science 290:1717–21

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K et al (2012) Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8:445–544

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Koehler A, Marx U, Broeg K, Bahns S, Bressling J (2008) Effects of nanoparticles in Mytilus edulis gills and hepatopancreas—a new threat to marine life? Mar Environ Res 66:12–14

    Article  CAS  PubMed  Google Scholar 

  • McVeigh A, Moore M, Allen JI, Dyke P (2006) Lysosomal responses to nutritional and contaminant stress in mussel hepatopancreatic digestive cells: a modelling study. Mar Environ Res 62:S433–S438

    Article  CAS  PubMed  Google Scholar 

  • Migliaccio O, Castellano I, Romano G, Palumbo A (2014) Stress response to cadmium and manganese in Paracentrotus lividus developing embryos is mediated by nitric oxide. Aquat Toxicol 156:125–134

    Article  CAS  PubMed  Google Scholar 

  • Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y (2004) In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 15:1101–11

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mommsen TP (2004) Salmon spawning migration and muscle protein metabolism: the August Krogh principle at work. Comp Biochem Physiol B Biochem Mol Biol 139:383–400

    Article  PubMed  Google Scholar 

  • Mommsen TP, French CJ, Hochachka PW (1980) Sites and patterns of protein and amino-acid utilization during the spawning migration of salmon. Can J Zool-Rev Can Zool 58:785–99

    Article  Google Scholar 

  • Moore MN (2002) Biocomplexity: the post-genome challenge in ecotoxicology. Aquat Toxicol 59:1–5

    Article  CAS  PubMed  Google Scholar 

  • Moore MN (2004) Diet restriction induced autophagy: a lysosomal protective system against oxidative- and pollutant-stress and cell injury. Mar Environ Res 58:603–607

    Article  PubMed  Google Scholar 

  • Moore MN, Allen JI (2002) A computational model of the digestive gland epithelial cell of marine mussels and its simulated responses to oil-derived aromatic hydrocarbons. Mar Environ Res 54:579–84

    Article  CAS  PubMed  Google Scholar 

  • Moore MN, Allen JI, McVeigh A (2006a) Environmental prognostics: an integrated model supporting lysosomal stress responses as predictive biomarkers of animal health status. Mar Environ Res 61:278–304

    Article  CAS  PubMed  Google Scholar 

  • Moore MN, Allen JI, McVeigh A, Shaw J (2006b) Lysosomal and autophagic reactions as predictive indicators of environmental impact in aquatic animals. Autophagy 2:217–20

    Article  CAS  PubMed  Google Scholar 

  • Moore MN, Allen JI, Somerfield PJ (2006c) Autophagy: role in surviving environmental stress. Mar Environ Res 62:S420–S425

    Article  CAS  PubMed  Google Scholar 

  • Moore MN, Viarengo A, Donkin P, Hawkins AJS (2007) Autophagic and lysosomal reactions to stress in the hepatopancreas of blue mussels. Aquat Toxicol 84:80–91

    Article  CAS  PubMed  Google Scholar 

  • Moore MN, Koehler A, Lowe D, Viarengo A (2008) Lysosomes and autophagy in aquatic animals. In: Daniel J. Klionsky, Editor(s), Methods in enzymology, Academic Press. 451:581‐620

  • Mosser DD, Heikkila JJ, Bols NC (1986) Temperature ranges over which rainbow trout fibroblasts survive and synthesize heat-shock proteins. J Cell Physiol 128:432–440

    Article  CAS  PubMed  Google Scholar 

  • Pagano G, Esposito A, Giordano GG (1982) Fertilization and larval development in sea urchins following exposure of gametes and embryos to cadmium. Arch Environ Contam Toxicol 11:47–55

    Article  CAS  PubMed  Google Scholar 

  • Paxton CW, Davy SK, Weis VM (2013) Stress and death of cnidarian host cells play a role in cnidarian bleaching. J Exp Biol 216:2813–2820

    Article  PubMed  Google Scholar 

  • Pigeot J, Miramand P, Guyot T, Sauriau PG, Fichet D, Le Moine O, Huet V (2006) Cadmium pathways in an exploited intertidal ecosystem with chronic cadmium inputs (Marennes-Oléron, Atlantic coast, France). Mar Ecol Prog Ser 307:101–114

    Article  CAS  Google Scholar 

  • Polakof S, Panserat S, Craig PM, Martyres DJ, Plagnes-Juan E, Savari S, Aris-Brosou S, Moon TW (2011) The metabolic consequences of hepatic AMP-kinase phosphorylation in rainbow trout. PLoS One 6:e20228

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ragusa MA, Costa S, Gianguzza M, Roccheri MC, Gianguzza F (2013) Effects of cadmium exposure on sea urchin development assessed by SSH and RT-qPCR: metallothionein genes and their differential induction. Mol Biol Rep 40:2157–2167

    Article  CAS  PubMed  Google Scholar 

  • Rhee JS, Kim BM, Choi BS, Choi IY, Park H, Ahn IY, Lee JS (2014) Transcriptome information of the Arctic green sea urchin and its use in environmental monitoring. Polar Biol 37:1133–1144

    Article  Google Scholar 

  • Roccheri MC, Matranga V (2010) Cellular, biochemical and molecular effects of cadmium on marine invertebrates: focus on Paracentrotus lividus sea urchin development. In: Parvau RG (ed) Cadmium in the environment. Nova, New York, pp 337–366

    Google Scholar 

  • Roccheri MC, Agnello M, Bonaventura R, Matranga V (2004) Cadmium induces the expression of specific stress proteins in sea urchin embryos. Biochem Biophys Res Commun 321:80–87

    Article  CAS  PubMed  Google Scholar 

  • Russo R, Bonaventura R, Zito F, Schröder HC, Müller I, Müller WE, Matranga V (2003) Stress to cadmium monitored by metallothionein gene induction in Paracentrotus lividus embryos. Cell Stress Chaperones 8:232–241

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Salem M, Kenney PB, Rexroad CE, Yao J (2006) Microarray gene expression analysis in atrophying rainbow trout muscle: a unique non mammalian muscle degradation model. Physiol Genomics 28:33–45

    Article  CAS  PubMed  Google Scholar 

  • Samali A, Cotter TG (1996) Heat shock proteins increase resistance to apoptosis. Exp Cell Res 223:163–170

    Article  CAS  PubMed  Google Scholar 

  • Seiliez I, Gabillard JC, Skiba-Cassy S, Garcia-Serrana D, Gutiérrez J, Kaushik S, Panserat S, Tesseraud S (2008) An in vivo and in vitro assessment of TOR signaling cascade in rainbow trout (Oncorhynchus mykiss). Am J Physiol Regul Integr Comp Physiol 295:329–335

    Article  Google Scholar 

  • Seiliez I, Gutierrez J, Salmeron C, Skiba-Cassy S, Chauvin C, Dias K, Kaushik S, Tesseraud S, Panserat S (2010) An in vivo and in vitro assessment of autophagy-related gene expression in muscle of rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol B Biochem Mol Biol 157:258–66

    Article  PubMed  Google Scholar 

  • Seiliez I, Gabillard J-C, Riflade M, Sadoul B, Dias K, Avérous J, Tesseraud S, Skiba S, Panserat S (2012) Amino acids downregulate the expression of several autophagy-related genes in rainbow trout myoblasts. Autophagy 8:364–75

    Article  CAS  PubMed  Google Scholar 

  • Tasdemir E, Galluzzi L, Maiuri MC, Criollo A, Vitale I, Hangen E et al (2008) Methods for assessing autophagy and autophagic cell death. Methods Mol Biol 445:29–76

    Article  CAS  PubMed  Google Scholar 

  • Templeton DM, Liu Y (2010) Multiple roles of cadmium in cell death and survival. Chem Biol Interact 188:267–75

    Article  CAS  PubMed  Google Scholar 

  • Tu Q, Cameron RA, Davidson EH (2014) Quantitative developmental transcriptomes of the sea urchin Strongylocentrotus purpuratus. Dev Biol 385:160–67

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Waisberg M, Joseph P, Hale B, Beyersmann D (2003) Molecular and cellular mechanisms of cadmium carcinogenesis. Toxicology 192:95–117

    Article  CAS  PubMed  Google Scholar 

  • Walker CW, Lesser MP, Unuma T (2013) Sea urchin gametogenesis-structural, functional and molecular/genomic biology. In: Lawrence CA (ed) Sea urchins: biology and ecology, vol 3, 3rd edn. Academic, San Diego, pp 25–44

    Chapter  Google Scholar 

  • Weis VM (2008) Cellular mechanisms of cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol 19:3059–66

    Article  Google Scholar 

  • Yabu T, Imamura S, Mohammed MS, Touhata K, Minami T, Terayama M, Yamashita M (2011) Differential gene expression of HSC70/HSP70 in yellowtail cells in response to chaperone-mediated autophagy. FEBS J 278:673–85

    Article  CAS  PubMed  Google Scholar 

  • Yabu T, Imamura S, Mizusawa N, Touhata K, Yamashita M (2012) Induction of autophagy by amino acid starvation in fish cells. Mar Biotechnol 14:491–501

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yuan J, Kroemer G (2010) Alternative cell death mechanisms in development and beyond. Genes Dev 24:2592–602

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by “FFR- Fondo Finalizzato alla Ricerca, University of Palermo” to Prof. Maria Carmela Roccheri.

Author information

Authors and Affiliations

  1. Dip.to di Scienze e Tecnologie Biologiche Chimiche e Farmaceutiche (STEBICEF), Università di Palermo, Viale delle Scienze Ed. 16, Palermo, 90128, Italy

    Roberto Chiarelli, Chiara Martino, Maria Agnello, Liana Bosco & Maria Carmela Roccheri

Authors
  1. Roberto Chiarelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chiara Martino
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maria Agnello
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Liana Bosco
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Maria Carmela Roccheri
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maria Carmela Roccheri.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chiarelli, R., Martino, C., Agnello, M. et al. Autophagy as a defense strategy against stress: focus on Paracentrotus lividus sea urchin embryos exposed to cadmium. Cell Stress and Chaperones 21, 19–27 (2016). https://doi.org/10.1007/s12192-015-0639-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12192-015-0639-3

Keywords

Search

Navigation