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Cellular and Molecular Neurobiology logoLink to Cellular and Molecular Neurobiology
. 2005 Nov;25(7):1107–1122. doi: 10.1007/s10571-005-8221-7

Expression and Induction of Secretory Phospholipase A Group IB in Brain

Miriam Kolko 1,2, Nanna R Christoffersen 1, Hélène Varoqui 1, Nicolas G Bazan1 1,3,
PMCID: PMC11529634  PMID: 16392040

Abstract

Secretory phospholipases A2 (sPLA2) form a diverse family of enzymes involved in physiologicand pathologic processes. Common among all sPLA2 is the ability to cleave acyl groups of phospholipids at 2C of the glycerol backbone, thereby releasingfatty acid and a lysophospholipid. Several sPLA2 have been cloned and characterized in various tissues.Furthermore, receptors have been identified. In the nervous system sPLA2 groups IIA, IIE, IIF, V, and XII have been identified, and binding sites for sPLA2 group IB (sPLA2-IB) have been found. Here, we report sPLA2-IB in rat and human brain as well as in neurons in primary culture. The distribution of sPLA2-IB seems to be mainly neuronal, with the highest abundance occurring in the cerebral cortex and hippocampus. We also find that genes encoding sPLA2-IB are induced by kainic acid and by electroshock-induced convulsions.Based on the present results we suggest that sPLA2-IB may be a neuronal intercellular signalling modulator.

Key Words: secretory phospholipase A2 group IB, neuronal expression, seizure, epilepsy, gene induction

Abbreviations:

AA

arachidonic acid

Ca2+

calcium

ORF

open reading frame

RT-PCR

reverse transcription-polymerase chain reaction

sPLA2

secreted phospholipase A2

References

  1. Balboa, M. A., Varela-Nieto, I., Lucas, K. K., and Dennis, E. A. (2002). Expression and function of phospholipase A2 in brain. FEBS Lett.531:12–17. [DOI] [PubMed] [Google Scholar]
  2. Baran, H., Vass, K., Lassmann, H., and Hornykiewicz, O. (1994). The cyclooxygenase and lipoxygenase inhibitor BW755C protects rats against kainic acid-induced seizures and neurotoxicity. Brain Res.646:201–206. [DOI] [PubMed] [Google Scholar]
  3. Bazan, N. G. (2003). Synaptic lipid signalling: significance of polyunsaturated fatty acids and platelet-activating factor. J. Lipid Res.44:2221–2233. [DOI] [PubMed] [Google Scholar]
  4. Chen, J., Engle, S. J., Seilhamer, J. J., and Tischfield, J. A. (1994). Cloning, expression and partial characterization of a novel rat phospholipase A2. Biochim. Biophys. Acta.1215:115–120. [DOI] [PubMed] [Google Scholar]
  5. Chen, M., Yang, Z., Naji, A., and Wolf, B. A. (1996). Identification of calcium-dependent phospholipase A2 isoforms in human and rat pancreatic islets and insulin secreting beta-cell lines. Endocrinology137:2901–2909. [DOI] [PubMed] [Google Scholar]
  6. Copic, A., Vucemilo, N., Gubensek, F., and Krizaj, I. (1999). Identification and purification of a novel receptor for secretory phospholipase A(2) in porcine cerebral cortex. J. Biol. Chem.274:26315–26320. [DOI] [PubMed] [Google Scholar]
  7. Cupillard, L., Mulherkar, R., Gomez, N., Kadam, S., Valentin, E., Lazdunski, M., and Lambeau, G. (1999). Both group IB and group IIA secreted phospholipases A2 are natural ligands of the mouse 180-kDa M-type receptor. J. Biol. Chem.274:7043–7051. [DOI] [PubMed] [Google Scholar]
  8. DeCoster, M. A., and Yourick, D. L. (1994). Development of glutamate-stimulated phosphatidylinositol metabolism in primary neuronal and astrocyte cultures. Int. J. Dev. Neurosci.12:227–233. [DOI] [PubMed] [Google Scholar]
  9. Hanasaki, K., and Arita, H. (1992). Characterization of a high affinity binding site for pancreatic-type phospholipase A2 in the rat. Its cellular and tissue distribution. J. Biol. Chem.267:6414–6420. [PubMed] [Google Scholar]
  10. Hanasaki, K., and Arita, H. (1999). Biological and pathological functions of phospholipase A(2) receptor. Arch. Biochem. Biophys.372:215–223. [DOI] [PubMed] [Google Scholar]
  11. Hanasaki, K., and Arita, H. (2002). Phospholipase A2 receptor: A regulator of biological functions of secretory phospholipase A2. Prostaglandins Other Lipid Mediat.68–69:71–82. [DOI] [PubMed] [Google Scholar]
  12. Horrocks, L. A., and Farooqui, A. A. (1994). NMDA receptor-stimulated release of arachidonic acid: Mechanisms for the Bazan effect. In: Municio, A. M., and Miras-Portugal, M. T. (eds.), Cell Signal Transduction, Second Messengers, and Protein Phosphorylation in Health and Disease. Plenum Press, New York, NY, pp. 113–128. [Google Scholar]
  13. Kolko, M., DeCoster, M. A., Rodriguez de Turco, E. B., and Bazan, N. G. (1996). Synergy by secretory phospholipase A2 and glutamate on inducing cell death and sustained arachidonic acid metabolic changes in primary cortical neuronal cultures. J. Biol. Chem.271:32722–32728. [DOI] [PubMed] [Google Scholar]
  14. Kolko, M., Nielsen, M., Bazan, N. G., and Diemer, N. H. (2002). Secretory phospholipase A(2) induces delayed neuronal COX-2 expression compared with glutamate. J. Neurosci. Res.69:169–177. [DOI] [PubMed] [Google Scholar]
  15. Kolko, M., Rodriguez de Turco, E. B., Diemer, N. H., and Bazan, N. G. (2003). Neuronal damage by secretory phospholipase A2: modulation by cytosolic phospholipase A2, platelet-activating factor, and cyclooxygenase-2 in neuronal cells in culture. Neurosci. Lett.338:164–168. [DOI] [PubMed] [Google Scholar]
  16. Kolko, M., Christoffersen, N. R., Barreiro, S. G., and Bazan, N. G. (2004). Expression and location of mRNAs encoding multiple forms of secretory phospholipase A2 in the rat retina. J. Neurosci. Res.77:517–524. [DOI] [PubMed] [Google Scholar]
  17. Kudo, I., and Murakami, M. (2002). Phospholipase A2 enzymes. Prostaglandins Other Lipid Mediat.68–69:3–58. [DOI] [PubMed] [Google Scholar]
  18. Marcheselli, V. L., and Bazan, N. G. (1996). Sustained induction of prostaglandin endoperoxide synthase-2 by seizures in hippocampus. Inhibition by a platelet-activating factor antagonist. J. Biol. Chem.271:24794–24799. [DOI] [PubMed] [Google Scholar]
  19. Marcheselli, V. L., Hong, S., Lukiw, W. J., Tian, X., Gronert, K., Musto, A., Hardy, M., Gimenez, J. M., Chiang, N., Serhan, C. N., and Bazan, N. G. (2003). Novel docosanoids inhibit brain ischemia-reperfusion-mediated leukocyte infiltration and pro-inflammatory gene expression. J. Biol. Chem.278:43908–43817. [DOI] [PubMed] [Google Scholar]
  20. Molloy, G. Y., Rattray, M., and Williams, R. J. (1998). Genes encoding multiple forms of phospholipase A2 are expressed in rat brain. Neurosci. Lett.258:139–142. [DOI] [PubMed] [Google Scholar]
  21. Ohara, O., Tamaki, M., Nakamura, E., Tsuruta, Y., Fujii, Y., Shin, M., Teraoka, H., and Okamoto, M. (1986). Dog and rat pancreatic phospholipases A2: complete amino acid sequences deduced from complementary DNAs. J. Biochem. (Tokyo)99:733–739. [DOI] [PubMed] [Google Scholar]
  22. Six, D. A., and Dennis, E. (2000). The expanding superfamily of phospholipase A(2) enzymes: classification and characterization. Biochim. Biophys. Acta.1488:1–19. [DOI] [PubMed] [Google Scholar]
  23. Sribar, J., Copic, A., Paris, A., Sherman, N. E., Gubensek, F., Fox, J. W., and Krizaj, I. (2001). A high affinity acceptor for phospholipase A2 with neurotoxic activity is a calmodulin. J. Biol. Chem.276:12493–12496. [DOI] [PubMed] [Google Scholar]
  24. Sun, G. Y., Xu, J., Jensen, M. D., and Simonyi, A. (2004). Phospholipase A2 in the central nervous system: implications for neurodegenerative diseases. J. Lipid Res.45:205–213. [DOI] [PubMed] [Google Scholar]
  25. Valentin, E., and Lambeau, G. (2000a). What can venom phospholipases A(2) tell us about the functional diversity of mammalian secreted phospholipases A(2)? Biochimie.82:815–831. [DOI] [PubMed] [Google Scholar]
  26. Valentin, E., and Lambeau, G. (2000b). Increasing molecular diversity of secreted phospholipases A(2) and their receptors and binding proteins. Biochim. Biophys. Acta1488:59–70. [DOI] [PubMed] [Google Scholar]
  27. Valentin, E., Ghomashchi, F., Gelb, M. H., Lazdunski, M., and Lambeau, G. (1999). On the diversity of secreted phospholipases A(2). Cloning, tissue distribution, and functional expression of two novel mouse group II enzymes. J. Biol. Chem.274:31195–311202. [DOI] [PubMed] [Google Scholar]
  28. Yagami, T., Ueda, K., Asakura, K., Hata, S., Kuroda, T., Sakaeda, T., Kishino, J., Sakaguchi, G., Itoh, N., and Hori, Y. (2002a). Group IB secretory phospholipase A(2)induces cell death in the cultured cortical neurons: a possible involvement of its binding sites. Brain Res.949:197–201. [DOI] [PubMed] [Google Scholar]
  29. Yagami, T., Ueda, K., Asakura, K., Hayasaki-Kajiwara, Y., Nakazato, H., Sakaeda, T., Hata, S., Kuroda, T., Takasu, N. and Hori, Y. (2002b). Group IB secretory phospholipase A2 induces neuronal cell death via apoptosis. J. Neurochem.81:449–461. [DOI] [PubMed] [Google Scholar]
  30. Yagami, T., Ueda, K., Asakura, K., Sakaeda, T., Hata, S., Kuroda, T., Sakaguchi, G., Itoh, N., Hashimoto, Y., and Hori, Y. (2003). Porcine pancreatic group IB secretory phospholipase A2 potentiates Ca2+ influx through L-type voltage-sensitive Ca2+ channels. Brain Res.960:71–80. [DOI] [PubMed] [Google Scholar]

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