Cell membranes composition is defined in ER and their restitution proceed by en bloc fusion of ER generated transport vesicles

Amalia Slomiany, Bronislaw L. Slomiany

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DOI: 10.4236/health.2010.212214                

Abstract

The synthesis of endoplasmic reticulum (ER)-derived transport vesicles is dictated by the contents and derivation of the cellular cytosol. The ER transport vesicles synthesized in the presence of gastric epithelial cells cytosol are destined for en bloc fusion with apical epithelial membrane, whereas those generated in hepa-tocytes-derived cytosol are destined for en bloc fusion with basolateral membrane. Moreover, during assembly of the dominant fraction of the apical or basolateral transport vesicles, a sub-stantial fraction of the vesicles is produced that fuses with endosomes, and the vesicles with still unknown destination that remain in cytosol. The process of ER vesicles synthesis is blocked by RNase treatment, whereas Golgi vesicles as-sembly is not affected. The experiments indicate that transport vesicles’ membrane composition and fidelity of its construction is defined in ER. The process involves synchronous membrane lipid synthesis, cotranslational intercalation of integral membrane proteins and containment of the vesicular cargo.

Keywords

Membrane Biogenesis; Repair Fidelity; Vesicular Transport; En Bloc Fusion

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	Sudhof, T.C. and Rothman, J.E. (2009) Membrane fusion: Grappling with SNARE and SM proteins. Science, 323, 474-477.
[2]	Glick, B.S. and Nakano, A. (2009) Membrane traffic within the Golgi apparatus. Annual Review of Cell Development Biology, 25, 113-132.
[3]	Lemmon, M.A. (2008) Membrane recognition by phospholipid binding proteins. National Review of the Molecular Cell Biology, 9, 99-111.
[4]	Weisz, O.A. and Rodriguez-Boulan, E. (2009) Apical trafficking in epithelial cells: signals, clusters and motors. Journal of Cell Science, 122, 4253-4266.
[5]	Deborde, S., Perret, E., Gravotta, D., Deora, A., Salvarezza, S., Schreiner, R. and Rodriguez-Boulan, E. (2008) Clathrin is a key regulator of basolateral polarity. Nature, 452,719-723.
[6]	Folsch, H., Matilla, P.E. and O. A. Weisz, O.A. (2009) Taking the scenic route: biosynthetic traffic to the plasma membrane in polarized epithelial cells. Traffic, 8, 972-981.
[7]	Mellman, I. and Nelson, W.J. (2008) Coordinated protein sorting, targeting and distribution in polarized cells. National Review of the Molecular Cell Biology, 9, 833-845.
[8]	Walter, A.M., Wiederhold, K., Bruns, D., Fasshauer, D. and Sorensen, J.B. (2010) Synaptobrevin N-terminally bound to syntaxin-SNAP-25 defines the primed vesicle state in regulated exocytosis. Journal of Cell Biology, 188, 401-413.
[9]	Chapmen, E.R. (2008) How does synaptotagmin trigger neurotransmitter release?. Annual Review of Biochemistry, 77, 615-641.
[10]	Idone, V.,Tam, C.and Andrews, N.W. (2008)Two-way traffic on the road to plasma membrane repair”, Trends in Cellular Biology, 18, 552-559.
[11]	van Meer, G., Voelker, D.R. and Feigenson, G.W. (2008) Membrane lipids; where they are and how they behave. National Review of Cell Molecular Biology, 9, 112-124.
[12]	Lingwood, D. and Simon,K. (2010) Lipid rafts as a membrane organizing principle. Science, 327, 46-50.
[13]	Nohturfft, A. and Zhang, S.C. (2009) Coordination of lipid metabolism in membrane biogenesis. Annual Review of Cell Development Biology, 25, 539-566.
[14]	Baron, W. and Hoekstra, D. (2010) On biogenesis of myelin membranes: Sorting, trafficking and cell polarity. FEBS Letters, 584,1760-1770.
[15]	Slomiany, A., Nowak, P., Piotrowski, E. and Slomiany, B.L. (1998) Effect of ethanol on intracellular vesicular transport from Golgi to apical cell membrane: Role of phosphatidylinositol 3-kinase and phospholipase A2 in Golgi vesicles association and fusion with the apical membrane”, Alcoholism: Clinical and Experimental Research, 22,167-175.
[16]	Slomiany, A. and Slomiany, B.L. (2003) Lipidomic processes in homeostatic and LPS- modified cell renewal cycle. Role of phosphatidylinositol 3-kinase pathway in biomembrane synthesis and restitution of apical epithelial membrane. Journal of Physiology and Pharmacology, 54, 533-551.
[17]	Slomiany, A., Sano, S., Grabska, M., Yamaki, K. and Slomiany, B.L. (2004) Gastric mucosal cell homeostatic physiome. Critical role of ER-initiated membrane restitution in the fidelity of cell function renewal. Journal of Physiology and Pharmacology, 55, 837-860.
[18]	Slomiany, A., Grzelinska, E., Yamaki, K., Palecz, D. and Slomiany, B.L. (1992) Biogenesis of endoplasmic reticulum transport vesicles transferring gastric apomucin from ER to Golgi”, Experimental Cell Research, 201, 1669-1682.
[19]	Slomiany, A., Grzelinska, E., Grabska, M., Yamaki, K., Tamura, S. and Slomiany, B.L. (1992) Intracellular processes associated with glycoprotein transport and processing. Archives of Biochemistry and Biophysics, 298, 167-175.
[20]	A. Slomiany, A., Grabska, M., Piotrowski, E., Morita, M. and Slomiany, B.L. (1994) Intracellular processes associated with vesicular transport from endoplasmic reticulum to Golgi and exocytosis; Ethanol-induced changes in membrane biogenesis. Archives of Biochemistry and Biophysics, 310, 247-255.
[21]	A. Slomiany, A., Grabska, M. and Slomiany, B.L. (2001) Essential components of antimicrobial epithelial barrier: Specific interaction of mucin with an integral apical membrane protein of gastric mucosa. Molecular Medicine, 7, 1-10.
[22]	Slomiany, A.,Tamura, S., Grzelinska, E., Piotrowski, J. and Slomiany, B.L.(1992) Characterization of the ‘link’ component of submandibular mucus glycoprotein. International Journal of Biochemistry, 24,1003-1015.
[23]	Brown, D.A. (2006) Lipid rafts, detergent-resistant membranes and raft targeting signals. Physiology, 21, 430-439.
[24]	Slomiany, A., Grabska, M. and Slomiany, B.L. (2006) Homeostatic restitution of cell membranes. Nuclear membrane lipid biogenesis and transport of protein from cytosol to intranuclear spaces. International Journal of Biological Sciences, 2, 216-226.
[25]	Fagone P. and Jackowski, S. (2009) Membrane phospholipid synthesis and endoplasmic reticulum function. Journal of Lipid Research, 50, S311-S316.
[26]	Mayinger, P. (2008) Regulation of Golgi function via phosphoinositide lipids. Seminars in Cell and Developmental Biology, 20, 793-809.
[27]	Prydz, K., Dick, G. and Tveit, H. (2008) How many ways through the Golgi maize?. Traffic, 9, 299-304.
[28]	Kawano, M., Kumagai, K., Nishijima, M. and Handa, K. (2006) Efficient trafficking of ceramide from endoplasmic reticulum to the Golgi apparatus requires VAMP-associated protein-interacting FFAT motif of CERT. Journal of Biological Chemistry, 281, 30279-30288.
[29]	van Meer, G., Halter, D., Sprong,H., Somerharju, P. and Egmond, M.R. (2006)ABC lipid transporters: extruders, flippases, or flopless activators?. FEBS Letters, 580,1171-1177.
[30]	Huizing, M., Helip-Wooley, A., Westbroek, W., Gunay-Aygun, M. and Gahl, W.A. (2008) Disorders of lysosome-related organelle biogenesis: clinical and molecular genetics. Annual Review of Genomics and Human Genetics, 9, 359-386.
[31]	Bryant, D.M. and Mostov, K.E. (2008) From cells to organs building polarized tissue. National Review of Molecular Cell Biology, 9, 887-901.
[32]	Ladinsky, M.S., Mastronarde, D.N. and McIntosh, J.R. (1999)Golgi structure in three dimensions: functional insights from the normal kidney cell. Journal of Cell Biology,144, pp. 1135-1149.
[33]	Gill, D.J., Chia, J., Senewiratne, J. and Bard, F. (2010) Regulation of O-glycosylation through Golgi-to-ER relocation of initiation enzymes. Journal of Cell Biology, 189, 843-858.
[34]	Tsai, N.P., Lin, Y.L. and Wei, L.N. (2010) Dual action of epidermal growth factor: extracellular signal-stimulated nuclear-cytoplasmic export and coordinated translation of selected messenger RNA. Journal of Cell Biology, 188, 325-338.
[35]	Wymann, M.P. and Schneiter, R. (2008) Lipid signaling in disease. Nature Reviews. Molecular Cell Biology, 9,162-176.
[36]	Heringdorf, D.M. and Jacobs, K.H. (2007) Lysophospholipid receptors: Signalling, pharmacology and regulation of by lysophospholipid metabolism. Biochemica et Biophysica Acta, 1768, 923-940.
[37]	Tam, C., Idone, V., Davlin, C., Fernandes, M.C., Flannary, A., He, X., Schuchman, E., Tabas, E. and Andrews, N.W. (2010) Exocytosis of acid sphingomyelinase by wounded cells promotes endocytosis and plasma membrane repair. Journal of Cell Biology, 189,1027-1038.