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Affinity of PIP-aquaporins to sterol-enriched domains in plasma membrane of the cells of etiolated pea seedlings

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Biochemistry (Moscow) Supplement Series A: Membrane and Cell Biology Aims and scope

Abstract

The hypothesis that sterol-enriched domains represent sites of preferred localization of PIP-aquaporins was tested in experiments on plasma membranes isolated from cells of etiolated pea (Pisum sativum L.) seedlings. Plasma membranes were isolated from microsomes by the partition in the aqueous two-phase polymer system and separated into vesicle fractions of different buoyant density by flotation in discontinuous OptiPrep gradient. Two types of plasma membrane preparations were used: one was treated with cold 1% Triton X-100 and the other was not. In untreated preparations, three populations of plasma membrane vesicles were obtained, while in the case of treated preparations, fractions of detergent-resistant membranes (DRM) and solubilized membrane proteins were obtained. In all membrane fractions collected after OptiPrep flotation, the amounts of proteins, sterols, and PIP-aquaporins were determined. The highest sterol content was detected in the membrane fraction with buoyant density 1.098 g/cm3 and in the DRM fraction (1.146 g/cm3). These fractions contained much more PIP-aquaporins than the other ones. Phase state of the lipid bilayer was determined by measuring generalized polarization excitation of fluorescence (GPEX) of laurdan incorporated into the membranes of different fractions. It was revealed that the lipid bilayer of the membranes with density of 1.098 g/cm3 had a higher extent of ordering than that of the fractions with density of ∼1.146 g/cm3. The results indicated that uppermost local concentrations of PIP-aquaporins were associated with tightly packed sterol-enriched domains. Moreover, upon solubilization of plasma membrane with Triton X-100, PIP-aquaporins mainly resided in DRM, thus exhibiting a high affinity to sterols.

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References

  1. Verkman A.S. 1992. Water channels in cell membranes. Annu. Rev. Physiol. 54, 97–108.

    Article  PubMed  CAS  Google Scholar 

  2. Agre P., Sasaki S., Chrispeels M.J. 1993. Aquaporins: A family of water channel proteins. Am. J. Physiol. 265, F641–F677.

    Google Scholar 

  3. Maurel C. 1997. Aquaporins and water permeability of plant membranes. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 399–429.

    Article  PubMed  CAS  Google Scholar 

  4. Tyerman S.D., Bohnert H.J., Maurel C., Steule E., Smith J.A.C. 1999. Plant aquaporins: Their molecular biology, biophysics and significance for plant water relations. J. Exp. Bot. 50, 1055–1071.

    Article  CAS  Google Scholar 

  5. Verkman A.S., Mitra A.K. 2000. Structure and function of aquaporin water channels. Am. J. Physiol. Renal. Physiol. 278, F13–F28.

    PubMed  CAS  Google Scholar 

  6. Zeidel M.L., Ambudkar S.V., Smith B. L., Agre P. 1992. Reconstitution of functional water channels in liposomes containing purified red cell CHIP28 protein. Biochemistry. 25, 7436–7440.

    Article  Google Scholar 

  7. Preston G.M., Agre P. 1991. Isolation of the cDNA for erythrocyte integral membrane protein of 28 kilodaltons: Member of an ancient channel family. Proc. Natl. Acad. Sci. USA. 88, 11110–11114.

    Article  PubMed  CAS  Google Scholar 

  8. Zardoya R., Villalba S. 2001. A phylogenetic framework for the aquaporin family in eukaryotes. J. Mol. Evol. 52, 391–404.

    PubMed  CAS  Google Scholar 

  9. Hachez C., Zelazny E., Chaumont F. 2006. Modulating the expression of aquaporin genes in planta: A key to understand their physiological functions? Biochim. Biophys. Acta. 1758, 1142–1156.

    Article  PubMed  CAS  Google Scholar 

  10. Maurel C., Verdoucq L., Luu D.-T., Santoni V. 2008. Plant aquaporins: Membrane channels with multiple integrated functions. Annu. Rev. Plant Biol. 59, 595–624.

    Article  PubMed  CAS  Google Scholar 

  11. Lande M.B., Donovan J.M., Zeidel M.L. 1995. The relationship between membrane fluidity and permeabilities to water, solutes, ammonia, and protons. J. Gen. Physiol. 106, 67–84.

    Article  PubMed  CAS  Google Scholar 

  12. Olbrich K., Rawicz W., Needman D., Evans E. 2000. Water permeability and mechanical strength of polyunsaturated lipid bilayers. Biophys. J. 79, 321–327.

    Article  PubMed  CAS  Google Scholar 

  13. Mathai J.C., Tristram-Nagle S., Nagle J.F., Zeidel M.L. 2008. Structural determinants of water permeability through the lipid membrane. J. Gen. Physiol. 31, 69–76.

    Google Scholar 

  14. Simons K., Ikonen E. 1997. Functional rafts in cell membranes. Nature. 387, 569–572.

    Article  PubMed  CAS  Google Scholar 

  15. Brown D.A., London E. 2000. Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J. Biol. Chem. 275, 17221–17224.

    Article  PubMed  CAS  Google Scholar 

  16. Pike L.J. 2003. Lipid rafts: Bringing order to chaos. J. Lipid Res. 44, 655–667.

    Article  PubMed  CAS  Google Scholar 

  17. Lingwood D., Simons K. 2010. Lipid rafts as a membrane organizing principle. Science. 327, 46–50.

    Article  PubMed  CAS  Google Scholar 

  18. Simons K., Vaz W.L.C. 2004. Model systems, lipid rafts, and cell membranes. Annu. Rev. Biophys. Biomol. Struct. 33, 269–295.

    Article  PubMed  CAS  Google Scholar 

  19. Brown D.A. 2006. Lipid rafts, detergent-resistant membranes, and raft targeting signals. Physiology. 21, 430–439.

    Article  PubMed  CAS  Google Scholar 

  20. Zappel N.F., Panstruga R. 2008. Heterogeneity and lateral compartmentalization of plant plasma membranes. Curr. Opin. Plant Biol. 11, 632–640.

    Article  PubMed  CAS  Google Scholar 

  21. Kusumi A., Suzuki K. 2005. Toward understanding the dynamics of membrane-raft-based molecular interactions. Biochim. Biophys. Acta. 1746, 234–251.

    Article  PubMed  CAS  Google Scholar 

  22. Lichtenberg D., Gonñi F.M. Heerklotz H. 2005. Detergent-resistant membranes should not be identified with membrane rafts. Trends Biochem. Sci. 30, 430–436.

    Article  PubMed  CAS  Google Scholar 

  23. Lingwood D., Simons K. 2007. Detergent resistance as a tool in membrane research. Nat. Prot. 2, 2159–2165.

    Article  CAS  Google Scholar 

  24. Mongrand S., Morel J., Laroche J., Claverol S., Carde J.-P., Hartmann M.-A., Bonneu M., Simon-Plas F., Lessire R., Bessoule J.-J. 2004. Lipid rafts in higher plant cells. J. Biol. Chem. 279, 36277–36286.

    Article  PubMed  CAS  Google Scholar 

  25. Borner G.H.H., Sherrier D.J., Weimar T., Michaelson L.V., Hawkins N.D., MacAskill A., Napier J.A., Beale M.H., Lilley K.S., Dupree P. 2005. Analysis of detergent-resistant membranes in Arabidopsis. Evidence for plasma membrane lipid rafts. Plant Physiol. 137, 104–116.

    Article  PubMed  CAS  Google Scholar 

  26. Morel J., Claverol S., Mongrand S., Furt F., Fromentin J., Bessoule J.-J., Blein J.-P., Simon-Plas F. 2006. Proteomics of plant detergent-resistant membranes. Mol. Cell. Proteomics. 5, 1396–1411.

    Article  PubMed  CAS  Google Scholar 

  27. Marmagne A., Ferro M., Meinnel T., Bruley C., Kuhn L., Garin J., Barbier-Brygoo H., Ephritikhine G. 2007. A high content in lipid-modified peripheral proteins and integral receptor kinases features in the Arabidopsis plasma membrane proteome. Mol. Cell. Proteomics. 6, 1980–1996.

    Article  PubMed  CAS  Google Scholar 

  28. Larsson C., Sommarin M., Widell S. 1994. Isolation of highly purified plasma membranes and the separation of inside-out and right-side-out vesicles. Methods Enzymol. 228, 451–469.

    Article  CAS  Google Scholar 

  29. Ampilogova Ya.N., Zhestkova I.M., Trofimova M.S. 2006. Redox modulation of osmotic water permeability in plasma membranes isolated from roots and shoots of pea seedlings. Fiziologia rastenii (Rus.) 53, 622–628.

    CAS  Google Scholar 

  30. Briskin D.P., Leonard R.T., Hodges T.K. 1987. Isolation of the plasma membrane: Membrane markers and general principles. Methods Enzymol. 148, 542–558.

    Article  CAS  Google Scholar 

  31. Laemmli U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227, 680–685.

    Article  PubMed  CAS  Google Scholar 

  32. Parasassi T., Gratton E. 1995. Membrane lipid domains and dynamics as detected by laurdan fluorescence. J. Fluoresc. 5, 59–68.

    Article  CAS  Google Scholar 

  33. Peskan T., Westermann M., Oelmüller R. 2000. Identification of low density Triton X-100-insoluble plasma membrane microdomains in higher plants. Eur. J. Biochem. 267, 6989–6995.

    Article  PubMed  CAS  Google Scholar 

  34. Poole R.J., Briskin D.P., Kratky Z., Johnstone R.M. 1984. Density gradient localization of plasma membrane and tonoplast from storage tissue of growing and dormant red beet. Plant Physiol. 74, 549–556.

    Article  PubMed  CAS  Google Scholar 

  35. Beck J.G., Mathieu D., Loudet C., Buchoux S., Dufourc E.J. 2007. Plant sterols in “rafts”: A better way to regulate membrane thermal shocks. FASEB J. 21, 1714–1723.

    Article  PubMed  CAS  Google Scholar 

  36. Roche Y., Gerbeau-Pissot P., Buhot B., Thomas D., Bonneau L., Gresti J., Mongrand S., Perrier-Cornet J.-M., Simon-Plas F. 2008. Depletion of phytosterols from the plant plasma membrane provides evidence for disruption of lipid rafts. FASEB J. 22, 3980–3991.

    Article  PubMed  CAS  Google Scholar 

  37. Minami A., Fujiwara M., Furuto A., Fukao Y., Yamashita T., Kamo M., Kawamura Y., Uemura M. 2009. Alterations in detergent-resistant plasma membrane microdomains in Arabidopsis thaliana during cold acclimation. Plant Cell. Physiol. 50, 341–359.

    Article  PubMed  CAS  Google Scholar 

  38. Uemura M., Joseph R.A., Steponkus P.L. 1995. Cold acclimation of Arabidopsis thaliana: Effect on plasma membrane lipid composition and freeze-induced lesions. Plant Physiol. 109, 15–30.

    PubMed  CAS  Google Scholar 

  39. Uemura M., Tominaga Y., Nakagawara C., Shigematsu S., Minami A., Kawamura Y. 2006. Responses of the plasma membrane to low temperatures. Physiol. Plantarum. 126, 81–89.

    Article  CAS  Google Scholar 

  40. Wang X., Li W., Li M., Welti R. 2006. Profiling lipid changes in plant response to low temperatures. Physiol. Plantarum. 126, 90–96.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya ul., 35, Moscow, 127276, Russia

    B. V. Belugin, I. M. Zhestkova & M. S. Trofimova

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  1. B. V. Belugin
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  2. I. M. Zhestkova
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  3. M. S. Trofimova
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Correspondence to M. S. Trofimova.

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Original Russian Text © B.V. Belugin, I.M. Zhestkova, M.S. Trofimova, 2010, published in Biologicheskie Membrany, 2010, Vol. 27, No. 5, pp. 394–403.

The article was translated by the authors.

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Belugin, B.V., Zhestkova, I.M. & Trofimova, M.S. Affinity of PIP-aquaporins to sterol-enriched domains in plasma membrane of the cells of etiolated pea seedlings. Biochem. Moscow Suppl. Ser. A 5, 56–63 (2011). https://doi.org/10.1134/S1990747810051010

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  • DOI: https://doi.org/10.1134/S1990747810051010

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