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

  • Julijana Ivanisevic
  • Thierry Pérez
  • Alexander V. Ereskovsky
  • Gilles Barnathan
  • Olivier P. Thomas


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.

Key Words

Lysophospholipids Homoscleromorpha Natural variability Reproductive cycle 



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.


  1. 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.PubMedCrossRefGoogle Scholar
  2. 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.PubMedCrossRefGoogle Scholar
  3. 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.PubMedCrossRefGoogle Scholar
  4. 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.CrossRefGoogle Scholar
  5. Barnathan, G. 2009. Non-methylene-interrupted fatty acids from marine invertebrates: Occurrence, characterization and biological properties. Biochimie 91:671–678.PubMedCrossRefGoogle Scholar
  6. 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.CrossRefGoogle Scholar
  7. Birgbauer, E. and Chun, J. 2006. New developments in the biological functions of lysophospholipids. Cell. Molec. Life Sci. 63:2695–2701.PubMedCrossRefGoogle Scholar
  8. 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.CrossRefGoogle Scholar
  9. 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.CrossRefGoogle Scholar
  10. 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.CrossRefGoogle Scholar
  11. D’Arrigo, P. and Servi, S. 2010. Synthesis of Lysophospholipids. Molecules 15:1354–1377.PubMedCrossRefGoogle Scholar
  12. Dembitsky, V. M. 1996. Betaine ether-linked glycerolipids: Chemistry and biology. Prog. Lipid Res. 35:1–51.PubMedCrossRefGoogle Scholar
  13. 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.CrossRefGoogle Scholar
  14. Dembitsky, V. M., Rezanka, T., and Srebnik, M. 2003. Lipid compounds of freshwater sponges: family Spongillidae class Demospongiae. Chem. Phys. Lipids 123:117–155.PubMedCrossRefGoogle Scholar
  15. 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.Google Scholar
  16. Djerassi, C. and Lam, W. K. 1991. Phospholipid studies of marine organisms. 25. Sponge phospholipids Accts. Chem. Res. 24:69–75.CrossRefGoogle Scholar
  17. 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.PubMedCrossRefGoogle Scholar
  18. Gardell, S. E., Dubin, A. E., and Chun, J. 2006. Emerging medicinal roles for lysophospholipid signaling. Trends in Molec. Med. 12:65–75.CrossRefGoogle Scholar
  19. 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.CrossRefGoogle Scholar
  20. Hartmann, T. 2007. From waste products to ecochemicals: Fifty years research of plant secondary metabolism. Phytochemistry 68:2831–2846.PubMedCrossRefGoogle Scholar
  21. 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
  22. 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.Google Scholar
  23. 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.PubMedCrossRefGoogle Scholar
  24. 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.CrossRefGoogle Scholar
  25. Mangold, H. K. and Weber, N. 1987. Biosynthesis and biotransformation of ether lipids. Lipids 22:789–799.PubMedCrossRefGoogle Scholar
  26. 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.PubMedCrossRefGoogle Scholar
  27. 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.PubMedCrossRefGoogle Scholar
  28. McClintock, J. B. and Baker, B. J. (Eds). 2001. Marine Chemical Ecology. CRC Press, Boca Raton, Florida.Google Scholar
  29. Mills, G. B. and Moolenaar, W. H. 2003. The emerging role of lysophosphatidic acid in cancer. Nature Rev. Cancer 3:582–591.CrossRefGoogle Scholar
  30. 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.Google Scholar
  31. 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.CrossRefGoogle Scholar
  32. 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.PubMedCrossRefGoogle Scholar
  33. 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.PubMedCrossRefGoogle Scholar
  34. Rivera, R. and Chun, J. 2008. Biological effects of lysophospholipids. Rev. Physiol. Biochem. Pharmacol. 160:25–46.PubMedCrossRefGoogle Scholar
  35. 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.PubMedCrossRefGoogle Scholar
  36. Sipkema, D., Franssen, M. C. R., Osinga, R., Tramper, J., and Wijffels, R. H. 2005. Marine sponges as pharmacy. Marine Biotechnol. 7:142–162.CrossRefGoogle Scholar
  37. Snyder, F. 1995. Platelet-activating-factor and its analogs - Metabolic pathways and related intracellular processes. Biochim. Biophys. Acta-Lipids Lipid Metabol. 1254:231–249.CrossRefGoogle Scholar
  38. 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.PubMedCrossRefGoogle Scholar
  39. 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.PubMedGoogle Scholar
  40. 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.PubMedCrossRefGoogle Scholar
  41. Trager, W. and Jensen, J. B. 1976. Human malaria parasites in continuous culture Science 193:673–675.Google Scholar
  42. 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.CrossRefGoogle Scholar
  43. 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.CrossRefGoogle Scholar
  44. Vance, J. E. (Editors). 2002. Biochemistry of Lipids, Lipoproteins and Membranes. Elsevier Science, Amsterdam.Google Scholar
  45. 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.CrossRefGoogle Scholar
  46. 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.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Julijana Ivanisevic
    • 1
    • 2
  • Thierry Pérez
    • 1
  • Alexander V. Ereskovsky
    • 1
  • Gilles Barnathan
    • 3
  • Olivier P. Thomas
    • 2
  1. 1.Centre d’Océanologie de Marseille, Diversité, Evolution et Ecologie Fonctionnelle MarineUniversité de la MéditérranéeMarseilleFrance
  2. 2.Laboratoire de Chimie des Molécules Bioactives et des ArômesUniversité de Nice-Sophia AntipolisNiceFrance
  3. 3.Pôle Mer et Littoral—UPRES-EA 2160, Groupe Substances marines à activité biologiqueLaboratoire de Chimie marine—ISOMerNantesFrance

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