ABC> Vol.4 No.5, August 2014

Concluding Step in Cell Restitution Cycle: ER Transport Vesicles with Sphingolipids in the Outer Leaflet of the Membrane Restore Lysosomes

DownloadDownload as PDF (Size:1133KB)  HTML   XML  PP. 301-321  

ABSTRACT

Restitution of the cell organelles and the membrane implicates serine palmitoyltransferase (SPT) in signal-specific and selective assembly of the transport vesicles. Here, we reveal that SPT, embedded in the outer leaflet (OL) of endoplasmic reticulum (ER), is engaged in the synthesis of ER transport vesicles that recondition cell organelles, and the inner leaflet (IL) SPT in the restitution of the cell membrane. The OL SPT impacts assembly of sphingomyelinase (SMase)—susceptible ER vesicles but not the SMase-resistant and sphingolipid (SPhL) core—carrying vesicles that refurbish the cell membrane. The investigation of the SPT-initiated differences in the placement of SPhL in vesicular membranes by utilizing ER depleted of OL SPT, allows us to conclude that the restitution of endosomal and lysosomal membranes is achieved with the involvement of OL SPT, whereas the IL SPT is involved in formation of the lipid core for glycosphingolipids (GSL) and sphingomyelin (SM) of the apical and basolateral cell membrane. These findings along with our previously published report (Slomiany and Slomiany, Advances in Biological Chemistry, 2013, 3, 275-287), provide a clear distinction between the processes that renovate cell membrane and its organelles from that of the endocytotic cell debridement, and show that vesicles are navigated to the specific organelles and the cell membrane by the biomembrane constituents programmed in ER.

Cite this paper

Slomiany, A. and Slomiany, B. (2014) Concluding Step in Cell Restitution Cycle: ER Transport Vesicles with Sphingolipids in the Outer Leaflet of the Membrane Restore Lysosomes. Advances in Biological Chemistry, 4, 301-321. doi: 10.4236/abc.2014.45036.

References

[1] Kapp, L.D. and Lorsch, J.R. (2004) The Molecular Mechanics of Eukaryotic Translation. Annual Reviews of Biochemistry, 73, 657-704.
http://dx.doi.org/10.1146/annurev.biochem.73.030403.080419
[2] Koga, H., Kaushik, S. and Cuervo, A.M. (2011) Protein Homeostasis and Aging: The Importance of Exquisite Quality Control. Ageing Research Review, 10, 205-215.
http://dx.doi.org/10.1016/j.arr.2010.02.001
[3] Walter, P. and Ron, D. (2011) The Unfolded Protein Response: From Stress Pathway to Homeostatic Regulation. Science, 334, 1081-1086.
http://dx.doi.org/10.1126/science.1209038
[4] Vincenz, L. and Hartl, U. (2014) Sugarcoating ER Stress. Cell, 156, 1125-1127.
http://dx.doi.org/10.1016/j.cell.2014.02.035
[5] Jung, H., Gkogkas, C.G., Sonenberg, N. and Holt, C.H. (2014) Remote Control of Gene Function by Local Translation. Cell, 157, 26-40.
http://dx.doi.org/10.1016/j.cell.2014.03.005
[6] Lusk, C.P., Blobel, G. and King, M.C. (2007) Highway to the Inner Nuclear Membrane: Rules for the Road. National Review of the Molecular Biology, 8, 414-420.
http://dx.doi.org/10.1038/nrm2165
[7] Siniossoglou, S. (2009) Lipins, Lipids and Nuclear Envelope Structure. Traffic, 10, 1181-1187.
http://dx.doi.org/10.1111/j.1600-0854.2009.00923.x
[8] Adams, R.L. and Wente, S.R. (2013) Uncovering Nuclear Pore Complexity with Innovation. Cell, 152, 1218-1221.
http://dx.doi.org/10.1016/j.cell.2013.02.042
[9] Rothman, J.E. (1994) Mechanisms of Intracellular Protein Transport. Nature, 372, 55-63.
http://dx.doi.org/10.1038/372055a0
[10] Bilder, D., Schober, M. and Perrimon, N. (2003) Integrated Activity of PDZ Complexes Regulates Epithelial Polarity. Nature Cell Biology, 5, 53-58.
http://dx.doi.org/10.1038/ncb897
[11] Sharma, N., Low, S.H., Misra, S., Pallavi, B. and Weimbs, T. (2006) Apical Targeting of Synthaxin 3 Is Essential for Epithelial Cell Polarity. Journal of Cell Biology, 173, 937-948.
http://dx.doi.org/10.1083/jcb.200603132
[12] 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. The Journal of Biological Chemistry, 281, 30279-30288.
http://dx.doi.org/10.1074/jbc.M605032200
[13] 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.
http://dx.doi.org/10.1016/j.febslet.2005.12.019
[14] Fölch, H. (2008) Regulation of Membrane Traf-ficking in Polarized Epithelial Cells. Current Opinions in Cell Biology, 20, 208-213.
http://dx.doi.org/10.1016/j.ceb.2008.01.003
[15] Pfeffer, S.R. (2007) Unsolved Mysteries of Membrane Traffic. Annual Review of Biochemistry, 76, 629-645.
http://dx.doi.org/10.1146/annurev.biochem.76.061705.130002
[16] Gohil, V.M. and Greenberg, M.L. (2009) Mitochondrial Membrane Biogenesis: Phospholipids and Proteins Go Hand in Hand. Journal of Cell Biology, 184, 469-472.
[17] Südhof, T.C. and Rothman, J.E. (2009) Membrane Fusion: Grappling with SNARE and SM Proteins. Science, 323, 474-477.
http://dx.doi.org/10.1126/science.1161748
[18] Beck, R., Prinz, S., Distellköter-Bechart, P., Röhling, S., Adolf, F., Hoehner, K., et al. (2011) Coatomer and Dimeric ADP Ribosylation Factor 1 Promote Distinct Steps in Membrane Scission. Journal of Cell Biology, 194, 765-777.
[19] Brodsky, J.L. (2012) Cleaning Up: ER-Associated Degradation to the Rescue. Cell, 151, 1163-1167.
http://dx.doi.org/10.1016/j.cell.2012.11.012
[20] Keiser, M., Alfalah, M., Propsting, M.J., Castelletti, D. and Naim, H.Y. (2006) Altered Folding, Turnover, and Polarized Sorting Act in Concert to Define a Novel Pathomechanism of Congenital Sucrose-Isomaltase Deficiency. Journal of Biological Chemistry, 281, 14393-14399.
http://dx.doi.org/10.1074/jbc.M513631200
[21] Smith, M.H., Ploegh, H.L. and Weissman, J.S. (2011) Road to Ruin: Targeting Proteins for Degradation in the Endoplasmic Reticulum. Science, 334, 1086-1090.
http://dx.doi.org/10.1126/science.1209235
[22] Marion, G., Madeo, F. and Kroemer, G. (2011) Autophagy for Tissue Homeostasis and Neuroprotection. Current Opinions in Cell Biology, 23, 198-206.
http://dx.doi.org/10.1016/j.ceb.2010.10.001
[23] Lukacs, G.L. and Verkman, A.S. (2012) CFTR: Folding, Mis-folding and Correcting the ΔF508 Conformational Defect. Trends in Molecular Medicine, 18, 81-91.
http://dx.doi.org/10.1016/j.molmed.2011.10.003
[24] Ron, E., Shenkman, M., Groisman, B., Izenshtein, Y B., Leitman, J. and Lederkremer, G.Z. (2011) Bypyss of Glycan-Dependent Glycoprotein Delivery to ERAD by Up-Regulated EDEM1. Molecular Biology of the Cell, 22, 3945-3954.
http://dx.doi.org/10.1091/mbc.E10-12-0944
[25] Rodriguez-Boulan, E. and Müsch, A. (2005) Protein Sorting in Golgi Complex: Shifting Paradigms. Biochimica et Biophysica Acta (BBA), Molecular Cell Research, 1744, 455-464.
http://dx.doi.org/10.1016/j.bbamcr.2005.04.007
[26] De Matteis, M.A. and Luini, A. (2008) Exiting the Golgi Complex. Nature Reviews of Molecular Cell Biology, 9, 273-284.
http://dx.doi.org/10.1038/nrm2378
[27] Mertins, P., Qiao, J.W., Patel, J., Udeshi, N.D., Clauser, K.R., Mani, D.R., Burgess, M.W., Gillette M.A., Jaffe, J.D. and Carr, S.A. (2013) Integrated Proteomic Analysis of Post-Translational Modifications by Serial Enrichment. Nature Methods, 10, 634-637.
http://dx.doi.org/10.1038/nmeth.2518
[28] Swaney, D.L., Beltrao, P., Starita, L., Guo, A., Rush, J., Fields, S., Krogan, N.J. and Villén, J. (2013) Global Analysis of Phosphorylation and Ubiquitylation Cross-Talk in Protein Degradation. Nature Methods, 10, 676-682.
http://dx.doi.org/10.1038/nmeth.2519
[29] Toulmay, A. and Prinz, W.A. (2011) Lipid Transfer and Signaling at Organelle Contact Sites: The Tip of the Iceberg. Current Opinions in Cell Biology, 23, 458-463.
[30] Mellman, I. and Nelson, W.J. (2008) Coordinated Protein Sorting, Targeting and Distribution in Polarized Cells. Nature Reviews Molecular Cell Biology, 9, 833-855.
http://dx.doi.org/10.1038/nrm2525
[31] Lee, M.C., Miller, E.A., Goldberg, J., Orci, L. and Schekman, R. (2004) Bi-Directional Protein Transport between the ER and Golgi. Annual Reviews of Cell Development and Biology, 20, 87-123.
http://dx.doi.org/10.1146/annurev.cellbio.20.010403.105307
[32] Glick, B.S. and Nakano, A. (2009) Membrane Traffic within the Golgi Apparatus. Annual Review of Cell Development Biology, 25, 113-132.
http://dx.doi.org/10.1146/annurev.cellbio.24.110707.175421
[33] Houtkooper, R.H. and Vaz, F.M. (2008) Cardiolipin, the Heart of Mitochondrial Metabolism. Cellular and Molecular Life Sciences, 65, 2493-2206.
http://dx.doi.org/10.1007/s00018-008-8030-5
[34] Lemmon, M.A. (2008) Membrane Recognition by Phospholipids Binding Proteins. Nature Reviews of Molecular Cell Biology, 9, 99-111.
http://dx.doi.org/10.1038/nrm2328
[35] Whitelegge, J. (2011) Up Close with Membrane Lipid-Protein Complexes. Science, 334, 320-321.
http://dx.doi.org/10.1126/science.1214084
[36] Osman, C., Voelker, D.R. and Langer, T. (2011) Making Heads or Tails of Phospholipids in Mitochondria. Journal of Cell Biology, 192, 7-16.
[37] Rusinova, R., Hobart, E.A, Koeppe II, R.E. and Andersen, O.S. (2013) Phosphoinositides Alter Lipid Bilayer Properties. Journal of General Physiology, 141, 673-690.
http://dx.doi.org/10.1085/jgp.201310960
[38] Park, S.H., Das, B.B., Casagrande, F., Tian, Y., Nothnagel, H.J., Chu, M., Kiefer, H., Maier, K., De Angelis, A.A., Marassi, F.M. and Opella, S.J. (2012) Structure of the Chemokine Receptor CXCR1 in Phospholipid Bilayers. Nature, 491, 779-783.
[39] Slomiany, A., Grzelinska, E., Kasinathan, C., Yamaki, K., Palecz, D., Slomiany, B.A., et al. (1992) Biogenesis of Endoplasmic Reticulum Transport Vesicles Transferring Gastric Apomucin from ER to Golgi. Experimental Cell Research, 201, 1669-1682.
http://dx.doi.org/10.1016/0014-4827(92)90280-L
[40] Slomiany, A. and Slomiany, B.L. (2011) Transformations of Phosphatidylinositol Phosphates in the Outer and Inner Nuclear Membrane Are Linked to Synthesis and Restitution of Cellular Membranes. Health, 3, 187-199.
http://dx.doi.org/10.4236/health.2011.34035
[41] 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.
http://dx.doi.org/10.7150/ijbs.2.216
[42] Slomiany, A. and Slomiany, B.L. (2013) Homeostatic Cell Cycle and the Origin of Autophagosomal Vesicles. Advances in Biological Chemistry, 3, 275-287.
http://dx.doi.org/10.4236/abc.2013.33031
[43] Slomiany, A. and Slomiany, B.L. (2012) Phosphatidylglycerol-Containing ER-Transport Vesicles Built and Restore Outer Mitochondrial Membrane and Deliver Nuclear DNA Translation Products to Generate Cardiolipin in the Inner Mitochondrial Membrane. Advances in Biological Chemistry, 2, 132-145.
http://dx.doi.org/10.4236/abc.2012.22016
[44] Sano, S., Slomiany, B.L. and Slomiany, A. (1995) Isolation and Characterization of the First Enzyme in the Pathway of Sphingolipids Synthesis. FASEB Journal, 9, A2719.
[45] Slomiany, A., Grzelinska, E., Grabska, M. and Slomiany, B.L. (1992) Intracelular Processes Associated with Glycoprotein Transport and Processing. Archives of Biochemistry and Biophysics, 298, 167-175.
http://dx.doi.org/10.1016/0003-9861(92)90108-9
[46] Slomiany, A., Grzelinska, E., Yamaki, K. and Slomiany, B.L. (1992) Function of Intracellular Phospholipase A2 in Vectorial Transport of Apoproteins from ER to Golgi. International Journal of Biochemistry, 24, 1397-1406.
http://dx.doi.org/10.1016/0020-711X(92)90065-9
[47] Slomiany, A., Grabska, M., Piotrowski, E. and Slomiany, B.L. (1994) Intracellular Processes Associated with Vesicular Transport from Endoplasmic Reticulum to Golgi and Exocytosis. Archives of Biochemistry and Biophysics, 310, 247-255.
http://dx.doi.org/10.1006/abbi.1994.1164
[48] 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 Physiology and Pharmacology, 54, 533-551.
[49] 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.
[50] Slomiany, A. and Slomiany, B.L. (2010) Cell Membranes Composition Is Defined in ER and Their Restitution Proceeds by en Bloc Fusion of ER Generated Transport Vesicles. Health, 2, 1444-1454.
http://dx.doi.org/10.4236/health.2010.212214
[51] Obrig, T.G., Culp, W.J., McKeehan, W.L. and Hardesty, B. (1971) The Mechanism by Which Cycloheximide and Related Glutarimide Antibiotics Inhibit Peptide Synthesis on Reticulocyte Ribosomes. Journal of Biological Chemistry, 246, 174-181.
[52] Croze, E.M. and Morré, D.J. (1984) Isolation of Plasma Membrane, Golgi Apparatus, and Endoplasmic Reticulum from Single Homogenates of Mouse Liver. Journal of Cellular Physiology, 119, 46-57.
http://dx.doi.org/10.1002/jcp.1041190109
[53] Slomiany, A., Nowak, P., Piotrowski, E. and Slomiany, B.L. (1998) Effect of Ethanol on Intracellular Vesicular Transport from Golgi to the Apical Membrane. Role of Phosphatidylinositol 3-Kinase and Phospholipase A2 in Golgi Transport Vesicles Association and Fusion with the Apical Membrane. Alcohol, Clinical and Experimental Research, 22, 167-175.
[54] Parsons, D.F., Willims, G.R. and Chance, B. (1966) Characteristics of Isolated and Purified Preparations of the Outer and Inner Membranes of Mitochondria. Annals of the New York Academy of Sciences, 137, 643-666.
http://dx.doi.org/10.1111/j.1749-6632.1966.tb50188.x
[55] Tjelle, T.E., Brech, A., Juvet, L.K., Griffiths, G. and Berg, T. (1996) Isolation and Characterization of Early Endosomes, Late Endosomes, Late Endosomes and Terminal Lysosomes: Their Role in Protein Degradation. Journal of Cell Sciences, 109, 2905-2914.
[56] Rome, L.H. and Crain, L.R. (1981) Degradation of Mucopolysacharide in Intact Isolated Lysosomes. Journal of Biological Chemistry, 256, 10763-10768.
[57] Schneider-Poetsch, T., Ju, J., Eyler, D.E., Dang, Y., Bhat, S., Merrick, W.C., Green, R., Shen, B. and Liu, J.O. (2010) Inhibition of Eukaryotic Translation Elongation by Cycloheximide and Lactimidomycin. Nature Chemistry and Biology, 6, 209-217.
http://dx.doi.org/10.1038/nchembio.304
[58] Kawashima, A., Sato, A., Kawashima, M., Nitta, K., Yamura, W., Sugino, N., Nihei, H. and Natori, Y. (1998) A Simple Procedure for the Isolation of Rat Kidney Lysosomes. Kidney International, 54, 275-278.
http://dx.doi.org/10.1046/j.1523-1755.1998.00958.x
[59] Liu, P. and Anderson, R.G.W. (1995) Compartmentalized Production of Ceramide at the Cell Surface. Journal of Biological Chemistry, 270, 27179-27185.
http://dx.doi.org/10.1074/jbc.270.45.27179
[60] Slomiany, A., Grabska, M., Slomiany, B.A., Grzelinska, E., Morita, M. and Slomiany, B.L. (1993) Intracellular Transport, Organelle Biogenesis and Establishment of Golgi Identity: Impact of Brefeldin A on the Activity of Lipid Synthesizing Enzymes. International Journal of Biochemistry, 25, 891-901.
http://dx.doi.org/10.1016/0020-711X(93)90245-A
[61] Nunnari, J. and Walter, P. (1996) Regulation of Organelle Biogenesis. Cell, 84, 389-394.
http://dx.doi.org/10.1016/S0092-8674(00)81283-0
[62] Burke, B. and Ellenberg, J. (2002) Remodeling the Walls of the Nucleus. Nature Reviews Molecular Cell Biology, 3, 487-497.
http://dx.doi.org/10.1038/nrm860
[63] Akhtar, A. and Gasser, S.M. (2007) The Nuclear Envelope and Transcriptional Control. National Review Genetics, 8, 507-517. http://dx.doi.org/10.1038/nrg2122
[64] Saftig, P. and Klumperman, J. (2009) Lysosome Biogenesis and Lysosomal Membrane Proteins: Trafficking Meets Function. Nature Reviews Molecular Cell Biology, 10, 623-635.
http://dx.doi.org/10.1038/nrm2745
[65] Slomiany, A. and Slomiany, B.L. (2011) Transformations of Phosphatidylinositol Phosphates in the Outer and Inner Nuclear Membrane Are Linked to Synthesis and Restitution of Cellular Membranes. Health, 4, 187-199.
[66] Lloyd, A.C. (2013) The Regulation of Cell Size. Cell, 154, 1194-1205.
http://dx.doi.org/10.1016/j.cell.2013.08.053
[67] Atilla-Gokcumen, G.E., Muro, E., Relat-Goberna, J., Sasse, S., Bedigian, A., Coughlin, M., Garcia-Manyes S. and Eggert, U.S. (2014) Dividing Cells Regulate Their Lipid Composition and Localization. Cell, 156, 428-439.
http://dx.doi.org/10.1016/j.cell.2013.12.015
[68] Mari, M., Tooze, S.E. and Reggiori, F. (2011) The Puzzling Origin of the Autophagosomal Membrane. F1000 Biology Reports, 3, 25-34.
[69] Maiuri, M.C., Zalckvar, E., Kimchi, A. and Kroemer, G. (2007) Self-Eating and Self-Killing: Cross Talk between Autophagy and Apoptosis. Nature Reviews Molecular Cell Biology, 8, 741-752.
http://dx.doi.org/10.1038/nrm2239
[70] Karunakaren, V. and Wickner, W. (2013) Fusion Proteins and Select Lipids Cooperate as Membrane Receptors for the soluble N-Methylmaleimide-Sensitive Factor Attachment Protein Receptor (SNARE) Vam7p. The Journal of Biological Chemistry, 288, 28557-28566.
http://dx.doi.org/10.1074/jbc.M113.484410
[71] Hetz, C. (2012) The Unfolded Protein Response: Controlling Cell Fate Decision under ER Stress and Beyond. National Reviews Molecular Cell Biology, 13, 89-102.
[72] 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.
http://dx.doi.org/10.1016/j.tcb.2008.09.001
[73] Neupert, H. and Herrmann, J.M. (2007) Translocation of Proteins into Mitochondria. Annual Review of Biochemistry, 76, 723-749.
http://dx.doi.org/10.1146/annurev.biochem.76.052705.163409
[74] Kobayashi, T., Beuchat, M.H., Chevallier, J., Makino, A., Mayran, N., Escola, J.M., Lebrand, C., Cosson, P., Kobayashi, T. and Gruenberg, J. (2002) Separation and Characterization of Late Endosomal Membrane Domains. Journal of Biological Chemistry, 277, 32157-32164.
http://dx.doi.org/10.1074/jbc.M202838200
[75] Hammond, G.R.V., Machner, M.P. and Balla, T. (2014) A Novel Probe for Phosphatidylinositol 4-Phosphate Reveals Multiple Pools beyond the Golgi. Journal of Cell Biology, 205, 113-126.
http://dx.doi.org/10.1083/jcb.201312072
[76] Yoshimori, T. and Noda, T. (2008) Toward Unraveling Membrane Biogenesis in Mammalian Autophagy. Current Opinions in Cell Biology, 20, 401-407.
http://dx.doi.org/10.1016/j.ceb.2008.03.010
[77] Hayashi-Nishino, M., Fujita, M., Noda, T., Yamaguchi, A., Yoshimori, T. and Yamamoto, A. (2009) A Subdomain of the Endoplasmic Reticulum Forms a Cradle for Autophagosome Formation. National Cell Biology, 5, 1180-1185.
[78] Tooze, S.E. and Yoshimuri, T. (2010) The Origin of the Autophagosomal Membrane. National Cell Biology, 12, 831-835.
http://dx.doi.org/10.1038/ncb0910-831
[79] Hailey, D.W., Rambold, A.S., Satpute-Krishnan, P., Mitra, K., Sougrat, R., Kim, P.K. and Lippincott-Schwartz, J. (2010) Mitochondra Supply Membranes for Autophagosomal Biogenesis during Starvation. Cell, 141, 656-667.
http://dx.doi.org/10.1016/j.cell.2010.04.009
[80] van der Vaart, A. and Reggiori, F. (2010) The Golgi Complex as a Source for Yeast Autophagosomal Membranes. Autophagy, 6, 800-801.
http://dx.doi.org/10.4161/auto.6.6.12575
[81] Ravikumar, B., Moreau, K., Jahreiss, L., Puri, C. and Rubinsztein, D.C. (2010) Plasma Membrane Contributes to the Formation of Pre-Autophagosomal Structures. National Cell Biology, 12, 747-757.
http://dx.doi.org/10.1038/ncb2078
[82] Hurley, J.H. and Schulman, B.A. (2014) Atomistic Autophagy: The Structures of Cellular Self-Digestion. Cell, 157, 300-311.
http://dx.doi.org/10.1016/j.cell.2014.01.070

  
comments powered by Disqus

Copyright © 2014 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.