Skip to main content
SpringerLink
Log in

The initial surface composition and topography modulate sphingomyelinase-driven sphingomyelin to ceramide conversion in lipid monolayers

  • Original Paper
  • Published:
Cell Biochemistry and Biophysics Aims and scope Submit manuscript

Abstract

Changes of the initial composition and topography of mixed monolayers of Sphingomyelin and Ceramide modulate the degradation of Sphingomyelin by Bacillus cereus Sphingomyelinase. The presence of initial lateral phase boundary due to coexisting condensed and expanded phase domains favors the precatalytic steps of the reaction. The amount and quality of the domain lateral interface, defined by the type of boundary undulation, appears as a modulatory supramolecular code which regulates the catalytic efficiency of the enzyme. The long range domain lattice structuring is determined by the Sphingomyelinase activity.

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
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

SMase:

Sphingomyelinase

Cer:

Ceramide

SM:

Sphingomyelin

Pm:

Palmitic Acid

dlPC:

Dilauroylphosphatidylcholine

DiIC12:

1,1’didodecyl-3,3,3′,3′–tetramethylindocarbocyanine

LE:

liquid expanded phase

LC:

liquid condensed phase

References

  1. Goni, F. M., & Alonso, A. (2002). Sphingomyelinases: enzymology and membrane activity. FEBS Letters, 531, 38–46.

    Article  PubMed  CAS  Google Scholar 

  2. Fujii, S., Itoh, H., Yoshida, A., Higashi, S., Ikezawa, H., & Ikeda, K. (2005). Activation of sphingomyelinase from Bacillus cereus by Zn2+ hitherto accepted as a strong inhibitor. Archives of Biochemistry and Biophysics, 436, 227–36.

    Article  PubMed  CAS  Google Scholar 

  3. Tomita, M., Taguchi, R., & Ikezawa H. (1991). Sphingomyelinase of Bacillus cereus as a bacterial hemolysin. Journal of Toxicology: Toxin Reviews, 10, 169–207.

    CAS  Google Scholar 

  4. Kronke, M. (1999). Biophysics of ceramide signaling: interaction with proteins and phase transition of membranes. Chemistry and Physics of Lipids, 101, 109–21.

    Article  PubMed  CAS  Google Scholar 

  5. Hannun, Y. A., & Luberto, C. (2000). Ceramide in the eukaryotic stress response. Trends in Cell Biology, 10, 73–80.

    Article  PubMed  CAS  Google Scholar 

  6. Maggio, B., Carrer, D. C., Fanani, M. L., Oliveira, R. G., & Rosetti, C. M. (2004). Interfacial behavior of glycosphingolipids and related sphingolipids Curr. Opinions in Colloid Interface Science, 8, 448–458.

    Article  CAS  Google Scholar 

  7. Goni, F. M., & Alonso, A. (2006). Biophysics of sphingolipids I. Membrane properties of sphingosine, ceramides and other simple sphingolipids. Biochimica Et Biophysica Acta, 1758, 1902–21.

    Article  PubMed  CAS  Google Scholar 

  8. Fanani, M. L., Hartel, S., Oliveira, R. G., & Maggio, B. (2002). Bidirectional control of sphingomyelinase activity and surface topography in lipid monolayers. Biophysical Journal, 83, 3416–24.

    PubMed  CAS  Google Scholar 

  9. Morita, S. Y., Nakano, M., Sakurai, A., Deharu, Y., Vertut-Doi, A., & Handa, T. (2005). Formation of ceramide-enriched domains in lipid particles enhances the binding of apolipoprotein. E FEBS Letters, 579, 1759–64.

    Article  PubMed  CAS  Google Scholar 

  10. Kinnunen, P. K., Koiv, A., Lehtonen, J. Y. A., Rytomaa, M., & Mustonen, P. (1994). Lipid dynamic and peripheral interactions of proteins with membranes surfaces. Chemistry and Physics of Lipids, 73, 181–207.

    Article  PubMed  CAS  Google Scholar 

  11. Boguslavsky, V., Rebecchi, M., Morris, A. J., Jhon, D. Y., Rhee, S. G., & McLaughlin, S. (1994). Effect of monolayer surface pressure on the activities of phosphoinositide-specific phospholipase C-beta 1, -gamma 1, and -delta 1. Biochemistry, 33, 3032–7.

    Article  PubMed  CAS  Google Scholar 

  12. Maggio, B. (1996). Control by ganglioside GD1a of phospholipase A2 activity through modulation of the lamellar-hexagonal (HII) phase transition. Molecular Membrane Biology, 13, 109–12.

    Article  PubMed  CAS  Google Scholar 

  13. Maggio, B. (1999). Modulation of phospholipase A2 by electrostatic fields and dipole potential of glycosphingolipids in monolayers. Journal of Lipid Research, 40, 930–9.

    PubMed  CAS  Google Scholar 

  14. Ahyayauch, H., Villar, A. V., Alonso, A., & Goni, F. M. (2005). Modulation of PI-specific phospholipase C by membrane curvature and molecular order. Biochemistry, 44, 11592–600.

    Article  PubMed  CAS  Google Scholar 

  15. Ruiz-Arguello, M. B., Veiga, M. P., Arrondo, J. L., Goni, F. M., & Alonso, A. (2002). Sphingomyelinase cleavage of sphingomyelin in pure and mixed lipid membranes. Influence of the physical state of the sphingolipid. Chemistry and Physics of Lipids, 114, 11–20.

    Article  PubMed  CAS  Google Scholar 

  16. Volwerk, J. J., Filthuth, E., Griffith, O. H., & Jain, M. K. (1994). Phosphatidylinositol-specific phospholipase C from Bacillus cereus at the lipid-water interface: interfacial binding, catalysis, and activation. Biochemistry, 33, 3464–74.

    Article  PubMed  CAS  Google Scholar 

  17. Fanani, M. L., & Maggio, B. (1997). Mutual modulation of sphingomyelinase and phospholipase A2 activities against mixed lipid monolayers by their lipid intermediates and glycosphingolipids. Molecular Membrane Biology, 14, 25–9.

    PubMed  CAS  Google Scholar 

  18. Fanani, M. L., & Maggio, B. (1998). Surface pressure-dependent cross-modulation of sphingomyelinase and phospholipase A2 in monolayers. Lipids, 33, 1079–87.

    Article  PubMed  CAS  Google Scholar 

  19. Jungner, M., Ohvo, H., & Slotte, J. P. (1997). Interfacial regulation of bacterial sphingomyelinase activity. Biochimica Et Biophysica Acta, 1344, 230–240.

    PubMed  CAS  Google Scholar 

  20. Fanani, M. L., & Maggio, B. (2000). Kinetic steps for the hydrolysis of sphingomyelin by bacillus cereus sphingomyelinase in lipid monolayers. Journal of Lipid Research, 41, 1832–40.

    PubMed  CAS  Google Scholar 

  21. Bianco, I. D., Fidelio, G. D., & Maggio, B. (1989). Modulation of phospholipase A2 activity by neutral and anionic glycosphingolipids in monolayers. Biochemical Journal, 258, 95–9.

    PubMed  CAS  Google Scholar 

  22. Bianco, I. D., Fidelio, G. D., & Maggio, B. (1990). Effect of sulfatide and gangliosides on phospholipase C and phospholipase A2 activity. A monolayer study. Biochimica Et Biophysica Acta, 1026, 179–85.

    Article  PubMed  CAS  Google Scholar 

  23. Ransac, S., Moreau, H., Riviere, C., & Verger, R. (1991). Monolayer techniques for studying phospholipase kinetics. Methods in Enzymology, 197, 49–65.

    Article  PubMed  CAS  Google Scholar 

  24. Grainger, D. W., Reichert, A., Ringsdorf, H., & Salesse, C. (1990). Hydrolytic action of phospholipase A2 in monolayers in the phase transition region: direct observation of enzyme domain formation using fluorescence microscopy. Biochimica Et Biophysica Acta, 1023, 365–79.

    Article  PubMed  CAS  Google Scholar 

  25. Muderhwa, J. M., & Brockman, H. L. (1992). Lateral lipid distribution is a major regulator of lipase activity. Implications for lipid-mediated signal transduction. Journal of Biological Chemistry, 267, 24184–92.

    PubMed  CAS  Google Scholar 

  26. Huang, H. W., Goldberg, E. M., & Zidovetzki, R. (1996). Ceramide induces structural defects into phosphatidylcholine bilayers and activates phospholipase A2. Biochemical and Biophysical Research Community, 220, 834–8.

    Article  CAS  Google Scholar 

  27. Grandbois, M., Clausen-Schaumann, H., & Gaub, H. (1998). Atomic force microscope imaging of phospholipid bilayer degradation by phospholipase A2. Biophysical Journal, 74, 2398–404.

    Article  PubMed  CAS  Google Scholar 

  28. Hartel, S., Fanani, M. L., & Maggio, B. (2005). Shape transitions and lattice structuring of ceramide-enriched domains generated by sphingomyelinase in lipid monolayers. Biophysical Journal, 88, 287–304.

    Article  PubMed  CAS  Google Scholar 

  29. Clarke, C. J., & Hannun Y. A. (2006). Neutral sphingomyelinases and nSMase2: Bridging the gaps. Biochimica Et Biophysica Acta, 1758, 1893–901.

    Article  PubMed  CAS  Google Scholar 

  30. Carrer, D. C., & Maggio, B. (2001). Transduction to self-assembly of molecular geometry and local interactions in mixtures of ceramides and ganglioside GM1. Biochimica Et Biophysica Acta, 1514, 87–99.

    Article  PubMed  CAS  Google Scholar 

  31. Bianco, I. D., & Maggio, B. (1989). Interactions of Neutral and Anionic Glycosphingolipids with Dilauroylphosphatidylcholine and Dilauroylphosphatidic Acid in Mixed Monolayers. Colloids and Surfaces, 40, 249–260.

    Article  CAS  Google Scholar 

  32. Spink, C. H., Yeager, M. D., & Feigenson, G. W. (1990). Partitioning behavior of indocarbocyanine probes between coexisting gel and fluid phases in model membranes. Biochimica Et Biophysica Acta, 1023, 25–33.

    Article  PubMed  CAS  Google Scholar 

  33. Kass, M., Witkin, A., & Terzopoulos, D. (1988). Snakes: active contour models. International Journal of Computer Vision, 1, 321–331.

    Article  Google Scholar 

  34. Xu, C., & Prince, J. L. (1998). Generalized Gradient Vector Flow External Forces for Active Contours Signal Processing.

  35. Maggio, B., & Lucy, J. A. (1975). Studies on mixed monolayers of phospholipids and fusogenic lipids. Biochemical Journal, 149, 597–608.

    PubMed  CAS  Google Scholar 

  36. Fanani, ML. (2001) Supramolecular Modulation of Sphingomyelinase activity in biointerfaces. Ph D. Thesis., Facultad de Ciencias Químicas, Univ. Nacional de Córdoba, Argentina.

  37. Basanez, G., Nieva, J. L., Goni, F. M., & Alonso, A. (1996). Origin of the lag period in the phospholipase C cleavage of phospholipids in membranes. Concomitant vesicle aggregation and enzyme activation. Biochemistry, 35, 15183–7.

    Article  PubMed  CAS  Google Scholar 

  38. Apitz-Castro, R., Jain, M. K., & De Haas, G. H. (1982). Origin of the latency phase during the action of phospholipase A2 on unmodified phosphatidylcholine vesicles. Biochimica Et Biophysica Acta, 688, 349–56.

    Article  PubMed  CAS  Google Scholar 

  39. Burack, W. R., Yuan, Q., & Biltonen, R. L. (1993). Role of lateral phase separation in the modulation of phospholipase A2 activity. Biochemistry, 32, 583–9.

    Article  PubMed  CAS  Google Scholar 

  40. Burack, W. R., Dibble, R. G., & Biltonen, R. L. (1997). The relationship between compositional phase separation and vesicle morphology: Implications for the regulation of phospholipase A2 by membrane structure. Chemistry and Physics of Lipids, 90, 87–95.

    Article  PubMed  CAS  Google Scholar 

  41. Ransac, S., Deveer, A. M. T. J., & Riviere, C., et al. (1992). Competitive inhibition of lipolytic enzymes. V. A monolayer study using enantiomeric acylamino analogues of phospholipids as potent competitive inhibitors of porcine pancreatic phospholipase A2. Biochimica Et Biophysicica Acta, 1123, 92–100, (Abstract).

    CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by: SECyT-UNC, CONICET and FONCyT (Argentina); FONDECYT, Empresas CMPC, the Millenium Science Initiative, Fundación Andes and the Tinker Foundation (Chile). L.D. is Doctoral Fellow of FONCYT, B.M. and M.L.F. are Research Investigators of CONICET, S.H. is PI of FONDECYT 1060890 and Jorge Jara was supported by FONDECYT 1030627.

Author information

Authors and Affiliations

  1. Departamento de Química Biológica – Centro de Investigaciones en Química Biológica de Córdoba (CIQUIBIC), Facultad de Ciencias Químicas – CONICET, Universidad Nacional de Córdoba, Haya de la Torre y Medina Allende, Ciudad Universitaria, X5000HUA, Córdoba, República Argentina

    Luisina De Tullio, Bruno Maggio & Maria Laura Fanani

  2. Anatomy and Development Biology Program, ICBM Faculty of Medicine, Universidad de Chile, Avda Independencia 1027, Comuna de Independencia, Santiago, Chile

    Steffen Hartel

  3. Centro de Estudios Científicos CECS, Universidad Austral de Chile, Independencia 641, Valdivia, Chile

    Jorge Jara

Authors
  1. Luisina De Tullio
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bruno Maggio
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Steffen Hartel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jorge Jara
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Maria Laura Fanani
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maria Laura Fanani.

Rights and permissions

Reprints and permissions

About this article

Cite this article

De Tullio, L., Maggio, B., Hartel, S. et al. The initial surface composition and topography modulate sphingomyelinase-driven sphingomyelin to ceramide conversion in lipid monolayers. Cell Biochem Biophys 47, 169–177 (2007). https://doi.org/10.1007/s12013-007-0001-1

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12013-007-0001-1

Keywords

Search

Navigation