Skip to main content
Log in

Lysophospholipids in the Mediterranean Sponge Oscarella tuberculata: Seasonal Variability and Putative Biological Role

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Lysophospholipids (LPLs) are recognized as important signaling molecules in metazoan cells. LPLs seem to be widely distributed among marine invertebrates, but their physiological role remains poorly known. Marine sponges produce original phospholipids and LPLs whose isolation and structural elucidation rarely have been reported. Two LPLs were isolated for the first time from the Mediterranean Homoscleromorph sponge Oscarella tuberculata: a bioactive lyso-PAF already identified in some other sponge species; and the new lysophosphatidylethanolamine C20:2 (LPE 1). The expression of LPL metabolites was investigated over time to determine their baseline variations and to relate them to the sponge reproduction pattern in order to better understand their putative role in the sponge life cycle. Expression levels of both compounds appeared to be highly correlated displaying significant seasonal fluctuations with maximal values in summer and minimal in winter. A significant higher LPL content was detected in reproductive sponges and especially in females, with a peak occurring during embryogenesis and larval development. The results suggest that LPLs could play a role of mediators in sponge embryogenesis and morphogenesis.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abdo, D. A., Motti, C. A., Battershill, C. N., and Harvey, E. S. 2007. Temperature and spatiotemporal variability of salicylihalamide A in the sponge Haliclona sp. J. Chem. Ecol. 33:1635–1645.

    Article  PubMed  CAS  Google Scholar 

  • Aiello, A., Fattorusso, E., Magno, S., and Menna, M. 1991. Isolation of 5 New 5-Alpha-Hydroxy-6-Keto-Delta-7 Sterols from the Marine Sponge Oscarella lobularis. Steroids 56:337–340.

    Article  PubMed  CAS  Google Scholar 

  • Alam, N., Bae, B. H., Hong, J., Lee, C.-O., Shin, B. A., IM, K. S., and Jung, J. H. 2001. Additional Bioactive Lyso-PAF Congeners from the Sponge Spirastrella abata. J. Nat. Prod. 64:533–535.

    Article  PubMed  CAS  Google Scholar 

  • Archer, C. B., Page, C. P., Morley, J., and Macdonald, D. M. 1985. Accumulation of inflammatory cells in response to intracutaneous platelet activating factor (Paf-acether) in mang. British J. Dermatol. 112:285–290.

    Article  CAS  Google Scholar 

  • Barnathan, G. 2009. Non-methylene-interrupted fatty acids from marine invertebrates: Occurrence, characterization and biological properties. Biochimie 91:671–678.

    Article  PubMed  CAS  Google Scholar 

  • Becerro, M. A., Uriz, M. J., and Turon, X. 1997. Chemically-mediated interactions in benthic organisms: the chemical ecology of Crambe crambe (Porifera, Poecilosclerida). Hydrobiologia 355:77–89.

    Article  CAS  Google Scholar 

  • Birgbauer, E. and Chun, J. 2006. New developments in the biological functions of lysophospholipids. Cell. Molec. Life Sci. 63:2695–2701.

    Article  PubMed  CAS  Google Scholar 

  • Brachwitz, H. and Vollgraf, C. 1995. Analogs of alkyllysophospholipids: Chemistry, effects on the molecular level and their consequences for normal and malignant cells. Pharmacol. Therapeut. 66:39–82.

    Article  CAS  Google Scholar 

  • Butler, A. J., Vanaltena, I. A., and Dunne, S. J. 1996. Antifouling activity of lyso-platelet-activating factor extracted from Australian sponge Crella incrustans. J. Chem. Ecol. 22:2041–2061.

    Article  CAS  Google Scholar 

  • Cimino, G., Destefano, S., and Minale, L. 1975. Long Alkyl Chains 3-substituted pyrrole-2-aldehyde (−2-carboxylic acid and methyl-ester) from marine sponge Oscarella lobularis. Experientia 31:1387–1389.

    Article  CAS  Google Scholar 

  • D’Arrigo, P. and Servi, S. 2010. Synthesis of Lysophospholipids. Molecules 15:1354–1377.

    Article  PubMed  Google Scholar 

  • Dembitsky, V. M. 1996. Betaine ether-linked glycerolipids: Chemistry and biology. Prog. Lipid Res. 35:1–51.

    Article  PubMed  CAS  Google Scholar 

  • Dembitsky, V. M., Gorina, I. A., Fedorova, I. P., and Solovieva, M. V. 1989. Comparative investigation of plasmalogens, alkylacyl and diacyl glycerophospholipids of the marine sponges (Porifera, Demospongiae). Comp. Biochem. Physiol. B-Biochem. & Molec. Biol. 92:733–736.

    Article  Google Scholar 

  • Dembitsky, V. M., Rezanka, T., and Srebnik, M. 2003. Lipid compounds of freshwater sponges: family Spongillidae class Demospongiae. Chem. Phys. Lipids 123:117–155.

    Article  PubMed  CAS  Google Scholar 

  • Desjardins, R. E., Canfield, C. J., Haynes, J. D., and Chulay, J. D. 1979. Quantitative assessment of anti-malarial activity in vitro by a semiautomated microdilution technique. Antimicrob. Agents Chemotherapy 16:710–718.

    CAS  Google Scholar 

  • Djerassi, C. and Lam, W. K. 1991. Phospholipid studies of marine organisms. 25. Sponge phospholipids Accts. Chem. Res. 24:69–75.

    Article  CAS  Google Scholar 

  • Florenta, I., Mouray, E., Ali, F. D., Drobecq, H., Girault, S., Schrevel, J., Sergheraert, C., and Grellier, P. 2000. Cloning of Plasmodium falciparum protein disulfide isomerase homologue by affinity purification using the antiplasmodial inhibitor 1,4-bis-3-N-(cyclohexyl methyl) amino propylpiperazine. FEBS Letters 484:246–252.

    Article  PubMed  CAS  Google Scholar 

  • Gardell, S. E., Dubin, A. E., and Chun, J. 2006. Emerging medicinal roles for lysophospholipid signaling. Trends in Molec. Med. 12:65–75.

    Article  CAS  Google Scholar 

  • Genin, E., Wielgosz-Collin, G., Njinkoue, J. M., Velosaotsy, N. E., Kornprobst, J. M., Gouygou, J. P., Vacelet, J., and Barnathan, G. 2008. New trends in phospholipid class composition of marine sponges. Comp. Biochem. Physiol. B-Biochem. & Molec. Biol. 150:427–431.

    Article  Google Scholar 

  • Hartmann, T. 2007. From waste products to ecochemicals: Fifty years research of plant secondary metabolism. Phytochemistry 68:2831–2846.

    Article  PubMed  CAS  Google Scholar 

  • Ivanišević, J., Thomas, O., Lejeusne, C., Chevaldonne, P., and Pérez, T. 2011. Metabolic fingerprinting as an indicator of biodiversity: towards understanding inter-specific relationships among Homoscleromorpha sponges. Metabolomics doi:10.1007/s11306-010-0239-2

    Google Scholar 

  • Lee, S., Zhao, Q., Choi, K., Hong, J., Lee, D. S., Lee, C., and Jung, J. H. 2003. A new glycerol ether from a marine sponge Stelletta sp. Nat. Prod. Sci. 9:232–234.

    CAS  Google Scholar 

  • Lopez-Legentil, S., Bontemps-Subielos, N., Turon, X., and Banaigs, B. 2006. Temporal variation in the production of four secondary metabolites in a colonial ascidian. J. Chem. Ecol. 32:2079–2084.

    Article  PubMed  CAS  Google Scholar 

  • Loukaci, A., Muricy, G., Brouard, J.-P., Guyot, M., Vacelet, J., and Boury-Esnault, N. 2004. Chemical divergence between two sibling species of Oscarella (Porifera) from the Mediterranean Sea. Biochem. Systemat. Ecol. 32:893–899.

    Article  CAS  Google Scholar 

  • Mangold, H. K. and Weber, N. 1987. Biosynthesis and biotransformation of ether lipids. Lipids 22:789–799.

    Article  PubMed  CAS  Google Scholar 

  • Mansoor, T., Bae, B., Hong, J., Lee, C.-O., Im, K., and Jung, J. 2005. New fatty acid derivatives from Homaxinella sp., a marine sponge. Lipids 40:981–985.

    Article  PubMed  CAS  Google Scholar 

  • Marti, R., Fontana, A., Uriz, M. J., and Cimino, G. 2003. Quantitative assessment of natural toxicity in sponges: Toxicity bioassay versus compound quantification. J. Chem. Ecol. 29:1307–1318.

    Article  PubMed  CAS  Google Scholar 

  • McClintock, J. B. and Baker, B. J. (Eds). 2001. Marine Chemical Ecology. CRC Press, Boca Raton, Florida.

    Google Scholar 

  • Mills, G. B. and Moolenaar, W. H. 2003. The emerging role of lysophosphatidic acid in cancer. Nature Rev. Cancer 3:582–591.

    Article  CAS  Google Scholar 

  • Moolenaar, W. H. 2000. Development of our current understanding of bioactive lysophospholipids, pp. 1–10, in E.J. Goetzl and K.L. Lynch (eds). Lysophospholipids Eicosanoids Biology Pathophysiology (Annals of the New-York Academy of Sciences, Vol. 905), Blackwell Publishing Ltd., New York.

  • ller, W. E. G., Klemt, M., Thakur, N. L., Schröder, H. C., Aiello, A., D’esposito, M., Menna, M., and Fattorusso, E. 2004. Molecular/chemical ecology in sponges: evidence for an adaptive antibacterial response in Suberites domuncula. Mar. Biol. 144:19–29.

    Article  Google Scholar 

  • Page, M., West, L., Northcote, P., Battershill, C., and Kelly, M. 2005. Spatial and temporal variability of cytotoxic metabolites in populations of the New Zealand sponge Mycale hentscheli. J. Chem. Ecol. 31:1161–1174.

    Article  PubMed  CAS  Google Scholar 

  • Prescott, S. M., Zimmerman, G. A., Stafforini, D. M., and Mcintyre, T. M. 2000. Platelet-activating factor and related lipid mediators. Annu. Rev. Biochem. 69:419–445.

    Article  PubMed  CAS  Google Scholar 

  • Rivera, R. and Chun, J. 2008. Biological effects of lysophospholipids. Rev. Physiol. Biochem. Pharmacol. 160:25–46.

    Article  PubMed  CAS  Google Scholar 

  • Shin, B. A., Kim, Y. R., Lee, I.-S., Sung, C. K., Hong, J., Sim, C. J., Im, K. S., and Jung, J. H. 1999. Lyso-PAF Analogues and Lysophosphatidylcholines from the Marine Sponge Spirastrella abata as Inhibitors of Cholesterol Biosynthesis. J. Nat. Prod. 62:1554–1557.

    Article  PubMed  CAS  Google Scholar 

  • Sipkema, D., Franssen, M. C. R., Osinga, R., Tramper, J., and Wijffels, R. H. 2005. Marine sponges as pharmacy. Marine Biotechnol. 7:142–162.

    Article  CAS  Google Scholar 

  • Snyder, F. 1995. Platelet-activating-factor and its analogs - Metabolic pathways and related intracellular processes. Biochim. Biophys. Acta-Lipids Lipid Metabol. 1254:231–249.

    Article  Google Scholar 

  • Steel, H. C., Cockeran, R., and Anderson, R. 2002. Platelet-activating factor and lyso-PAF possess direct antimicrobial properties in vitro. Apmis 110:158–164.

    Article  PubMed  CAS  Google Scholar 

  • Sugiura, T., Fukuda, T., Miyamoto, T., and Waku, K. 1992. Distribution of alkyl and alkenyl ether-linked phospholipids and platelet-activating-factor-like lipid in various species of invertebrates. Biochim. Biophys. Acta 1126:298–308.

    PubMed  CAS  Google Scholar 

  • Torkhovskaya, T. I., Ipatova, O. M., Zakharova, T. S., Kochetova, M. M., and Khalilov, E. M. 2007. Lysophospholipid receptors in cell signaling. Biochemistry-Moscow 72:125–131.

    Article  PubMed  CAS  Google Scholar 

  • Trager, W. and Jensen, J. B. 1976. Human malaria parasites in continuous culture Science 193:673–675.

    CAS  Google Scholar 

  • Turon, X., Becerro, M. A., and Uriz, M. J. 1996. Seasonal patterns of toxicity in benthic invertebrates: The encrusting sponge Crambe crambe (Poecilosclerida). Oikos 75:33–40.

    Article  Google Scholar 

  • Vadas, P., Gold, M., Perelman, B., Liss, G. M., Lack, G., Blyth, T., Simons, F. E. R., Simons, K. J., Cass, D., and Yeung, J. 2008. Platelet-Activating Factor, PAF Acetylhydrolase, and Severe Anaphylaxis. New England J. Med. 358:28–35.

    Article  CAS  Google Scholar 

  • Vance, J. E. (Editors). 2002. Biochemistry of Lipids, Lipoproteins and Membranes. Elsevier Science, Amsterdam.

    Google Scholar 

  • Zampella, A., Sepe, V., Bellotta, F., Luciano, P., D'auria, M. V., Cresteil, T., Debitus, C., Petek, S., Poupat, C., and Ahond, A. 2009. Homophymines B-E and A1-E1, a family of bioactive cyclodepsipeptides from the sponge Homophymia sp. Organ. Biomolec. Chem. 7:4037–4044.

    Article  CAS  Google Scholar 

  • Zhao, Q., Mansoor, T. A., Hong, J., Lee, C.-O., Im, K. S., Lee, D. S., and Jung, J. H. 2003. New Lysophosphatidylcholines and Monoglycerides from the Marine Sponge Stelletta sp. J. Nat. Prod. 66:725–728.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was funded by ECIMAR project (ANR-06-BDIV-001), and partly by the “Institut de Chimie des Substances Naturelles (ICSN)” and the Pôle Mer PACA. We thank M. Gaysinski and the PFTC of Nice for recording the NMR spectra and J.-M. Guigonis for recording the HRMS spectra. We acknowledge the assistance of Ainara Gonzalez for the study of the sponge life cycle and I. Florent (Muséum National d’Histoire Naturelle de Paris) for the antimalarial bioassay, and the ICSN for the antitumoral assay.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Thierry Pérez.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ivanisevic, J., Pérez, T., Ereskovsky, A.V. et al. Lysophospholipids in the Mediterranean Sponge Oscarella tuberculata: Seasonal Variability and Putative Biological Role. J Chem Ecol 37, 537–545 (2011). https://doi.org/10.1007/s10886-011-9943-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-011-9943-2

Key Words

Navigation