Purification of Plasma Membrane Proteins for Mass Spectrometry-based Proteomic Analysis
Abstract
As a barrier between intracellular and extracellular environment, plasma membrane (PM) proteins play crucial roles in cell communication, cell recognition, signaling and molecular transport. Thus, detection of changes in PM proteome could lead to identification of novel biomarkers for disease diagnostics and development of novel drug targets for therapeutics. Current development of mass spectrometry technologies has made it possible to study a snapshot of all proteins presented in the system; however, there are some limitations for the PM proteomic study. Main challenges result from their low abundance and their hydrophobic property. This review focuses on principles and applications of commonly used and advanced approaches for enrichment of the PM proteins, in order to increase their purity and deplete contaminating proteins from other organelles. Since each method has its own advantages and limitations, careful consideration for sample preparation techniques could help enhancing PM proteins identification and quantification to elucidate their roles in disease-associated cellular responses. Keywords : plasma membrane, proteomics, mass spectrometry, nanoparticle pellicle, biotinylationReferences
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Arjunan, S., Reinartz, M., Emde, B., Zanger, K., & Schrader, J. (2009). Limitations of the colloidal silica method in mapping the endothelial plasma membrane proteome of the mouse heart. Cell Biochemistry and Biophysics, 53(3), 135-143.
Bendz, M., Skwark, M., Nilsson, D., Granholm, V., Cristobal, S., Käll L., & Elofsson, A. (2013). Membrane protein shaving with thermolysin can be used to evaluate topology predictors. Proteomics, 13(9), 1467-1480
Boheler, K.R., Bhattacharya, S., Kropp, E.M., Chuppa, S., Riordon, D.R., Bausch-Fluck, D., Burridge, P.W., Wu, J.C., Wersto, R.P., Chan, G.C., Rao, S., Wollscheid, B. & Gundry, R.L. (2014). A human pluripotent stem cell surface N-glycoproteome resource reveals markers, extracellular epitopes, and drug targets. Stem Cell Reports, 3(1), 185-203.
Cao, R., He, Q., Zhou, J., He, Q., Liu, Z., Wang, X., Chen, P., Xie, J., & Liang, S. (2008). High-throughput analysis of rat liver plasma membrane proteome by a nonelectrophoretic in-gel tryptic digestion coupled with mass spectrometry identification. Journal of Proteome Research, 7(2), 535-545.
Cathro, P., McCarthy, P., Hoffmann, P., & Zilm, P. (2016). Isolation and identification of Enterococcus faecalis membrane proteins using membrane shaving, 1D SDS/PAGE, and mass spectrometry. FEBS Open Bio, 6(6), 586-593.
Chaney, L.K., & Jacobson, B.S. (1983). Coating cells with colloidal silica for high yield isolation of plasma membrane sheets and identification of transmembrane proteins. Journal of Biological Chemistry, 258(16), 10062-10072.
Chen, R., Jiang, X., Sun, D., Han, G., Wang, F., Ye, M., Wang, L., & Zou, H. (2009). Glycoproteomics analysis of human liver tissue by combination of multiple enzyme digestion and hydrazide chemistry. Journal of Proteome Research, 8(2), 651-661.
Choksawangkarn, W., Kim, S.K., Cannon, J.R., Edwards, N.J., Lee, S.B., & Fenselau, C. (2013). Enrichment of plasma membrane proteins using nanoparticle pellicles: comparison between silica and higher density nanoparticles. Journal of Proteome Research, 12(3), 1134-1141.
Choksawangkarn, W., Graham, L.M., Burke, M., Lee, S. B., Ostrand-Rosenberg, S., Fenselau, C., & Edwards, N. (2016). Peptide-based systems analysis of inflammation induced myeloid-derived suppressor cells reveals diverse signaling pathways. Proteomics, 16(13), 1881-1888.
Cordwell, S.J., & Thingholm, T.E. (2010). Technologies for plasma membrane proteomics. Proteomics, 10(4), 611-627.
Durr, E., Yu, J., Krasinska, K.M., Carver, L.A., Yates, J.R., Testa, J.E., Oh, P., & Schnitzer, J.E. (2004). Direct proteomic mapping of the lung microvascular endothelial cell surface in vivo and in cell culture. Nature Biotechnology, 22(8), 985-992.
Eichacker, L.A., Granvogl, B., Mirus, O., Muller, B.C., Miess, C., & Schleiff, E. (2004). Hiding behind hydrophobicity. Transmembrane segments in mass spectrometry. Journal of Biological Chemistry, 279(49), 50915-50922.
Elia, G. (2008). Biotinylation reagents for the study of cell surface proteins. Proteomics, 8(19), 4012-4024.
Gasser, K.W., DiDomenico, J., & Hopfer, U. (1988). Separation of cell organelles in density gradients based on their permeability characteristics. Analytical Biochemistry, 171(1), 41-46.
Graham, J. M., & Rickwood, D. (2001). Biological Centrifugation. Oxford: BIOS Scientific Publishers Ltd.
Gundry, R. L., Raginski, K., Tarasova, Y., Tchernyshyov, I., Bausch-Fluck, D., Elliott, S. T., Boheler, K.R., Van Eyk, J.E., & Wollscheid, B. (2009). The mouse C2C12 myoblast cell surface N-linked glycoproteome: identification, glycosite occupancy, and membrane orientation. Molecular and Cellular Proteomics, 8(11), 2555-2569.
Hormann, K., Stukalov, A., Muller, A.C., Heinz, L.X., Superti-Furga, G., Colinge, J., & Bennett, K.L. (2016). A Surface biotinylation strategy for reproducible plasma membrane protein purification and tracking of genetic and drug-induced alterations. Journal of Proteome Research, 15(2), 647-658.
Josic, D., & Clifton, J.G. (2007). Mammalian plasma membrane proteomics. Proteomics, 7(16), 3010-3029.
Josic, D., Clifton, J.G., Kovac, S., & Hixson, D.C. (2008). Membrane proteins as diagnostic biomarkers and targets for new therapies. Current Opinion in Molecular Therapeutics, 10(2), 116-123.
Kearney, P., & Thibault, P. (2003). Bioinformatics meets proteomics--bridging the gap between mass spectrometry data analysis and cell biology. Journal of Bioinformatics and Computational Biology, 1(1), 183-200.
Kim, S.K., Choksawangkarn, W., Rose, R., Fenselau, C., & Lee, S.B. (2014). Nanowire pellicles for eukaryotic cells: nanowire coating and interaction with cells. Nanomedicine (Lond), 9(8), 1171-1180.
Kim, S.K., Rose, R., Choksawangkarn, W., Graham, L., Hu, J., Fenselau, C., & Lee, S.B. (2013). Comparison of nanowire pellicles for plasma membrane enrichment: coating nanowires on cell. Journal of Nanoparticle Research, 15(12), 2133.
Leth-Larsen, R., Lund, R.R., & Ditzel, H.J. (2010). Plasma membrane proteomics and its application in clinical cancer biomarker discovery. Molecular and Cellular Proteomics, 9(7), 1369-1382.
Li, X., Jia, X., Xie, C., Lin, Y., Cao, R., He, Q., Chen, P., Wang, X., & Liang, S. (2009). Development of cationic colloidal silica-coated magnetic nanospheres for highly selective and rapid enrichment of plasma membrane fractions for proteomics analysis. Biotechnolology and Applied Biochemistry, 54(4), 213-220.
Li, X., Jin, Q., Cao, J., Xie, C., Cao, R., Liu, Z., Xiong, J., Li, J., Yang, X., Chen, P., & Liang, S. (2009). Evaluation of two cell surface modification methods for proteomic analysis of plasma membrane from isolated mouse hepatocytes. Biochimica et Biophysica Acta, 1794(1), 32-41.
Livnah, O., Bayer, E. A., Wilchek, M., & Sussman, J. L. (1993). Three-dimensional structures of avidin and the avidin-biotin complex. Proceedings of the National Academy of Science of the United States of America, 90(11), 5076-5080.
Long, J., Basu Roy, R., Zhang, Y.J. , Antrobus, R., Du, Y., Smith, D.L., Weekes, M.P., & Javid, B. (2016). Plasma membrane profiling reveals upregulation of ABCA1 by macrophages leading to restriction of Mycobacterial growth. Frontiers in Microbiology, 7, 1086.
Matheson, N.J., Sumner, J., Wals, K., Rapiteanu, R., Weekes, M.P., Vigan, R., Weinelt, J., Schindler, M., Antrobus, R., Costa, A.S.H., Frezza, C., Clish, C.B., Neil, S.J.D., & Lehner, P.J. (2015). Cell surface proteomic map of HIV infection reveals antagonism of amino acid metabolism by Vpu and Nef. Cell Host & Microbe, 18(4), 409-423.
Mathias, R.A., Chen, Y.S., Goode, R.J., Kapp, E.A., Mathivanan, S., Moritz, R.L., Zhu, H.J., & Simpson, R.J. (2011). Tandem application of cationic colloidal silica and Triton X-114 for plasma membrane protein isolation and purification: towards developing an MDCK protein database. Proteomics, 11(7), 1238-1253.
Nielsen, P.A., Olsen, J.V., Podtelejnikov, A.V., Andersen, J.R., Mann, M., & Wisniewski, J.R. (2005). Proteomic mapping of brain plasma membrane proteins. Molecular and Cellular Proteomics, 4(4), 402-408.
Ohtsubo, K., & Marth, J.D. (2006). Glycosylation in cellular mechanisms of health and disease. Cell, 126(5), 855-867.
Overington, J.P., Al-Lazikani, B., & Hopkins, A.L. (2006). Opinion - How many drug targets are there? Nature Reviews Drug Discovery, 5(12), 993-996.
Prior, M.J., Larance, M., Lawrence, R.T., Soul, J., Humphrey, S., Burchfield, J., Kistler, C., Davey, J.R., La-Borde, P.J., Buckley, M., Kanazawa, H., Parton, R.G., Guilhaus, M., & James, D.E. (2011). Quantitative proteomic analysis of the adipocyte plasma membrane. Journal of Proteome Research, 10(11), 4970-4982.
Rahbar, A.M., & Fenselau, C. (2004). Integration of Jacobson's pellicle method into proteomic strategies for plasma membrane proteins. Journal of Proteome Research, 3(6), 1267-1277.
Reeke, G.N., Jr., Becker, J.W., Cunningham, B.A., Wang, J.L., Yahara, I., & Edelman, G.M. (1975). Structure and function of concanavalin A. Advances in Experimental Medicine and Biology, 55, 13-33.
Robinson, J.M., Ackerman, W.E., Tewari, A.K., Kniss, D.A., & Vandre, D.D. (2009). Isolation of highly enriched apical plasma membranes of the placental syncytiotrophoblast. Analalytical Biochemistry, 387(1), 87-94.
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Rybak, J.N., Ettorre, A., Kaissling, B., Giavazzi, R., Neri, D., & Elia, G. (2005). In vivo protein biotinylation for identification of organ-specific antigens accessible from the vasculature. Nature Methods, 2(4), 291-298.
Simpson, R. J. (2010). Disruption of cultured cells by nitrogen cavitation. Cold Spring Harbor Protocol, 2010(11), pdb prot5513.
Solis, N., Cain, J.A., & Cordwell, S.J. (2016). Comparative analysis of Staphylococcus epidermidis strains utilizing quantitative and cell surface shaving proteomics. Journal of Proteomics, 130, 190-199.
Solis, N., Larsen, M.R., & Cordwell, S.J. (2010). Improved accuracy of cell surface shaving proteomics in Staphylococcus aureus using a false-positive control. Proteomics, 10(10), 2037-2049.
Song, W., Mentink, R.A., Henquet, M.G., Cordewener, J.H., van Dijk, A.D., Bosch, D., America, A.H., & van der Krol, A.R. (2013). N-glycan occupancy of Arabidopsis N-glycoproteins. Journal of Proteomics, 93, 343-355.
Speers, A.E., Blackler, A.R., & Wu, C.C. (2007). Shotgun analysis of integral membrane proteins facilitated by elevated temperature. Analytical Chemistry, 79(12), 4613-4620.
Speers, A.E., & Wu, C.C. (2007). Proteomics of integral membrane proteins--theory and application. Chemical Reviews, 107(8), 3687-3714.
Stolz, D.B., & Jacobson, B.S. (1992). Examination of transcellular membrane protein polarity of bovine aortic endothelial cells in vitro using the cationic colloidal silica microbead membrane-isolation procedure. Journal of Cell Science, 103(Pt 1), 39-51.
Tan, S., Tan, H.T., & Chung, M.C. (2008). Membrane proteins and membrane proteomics. Proteomics, 8(19), 3924-3932.
Trotter, J., & Hamilton, J. A. (1966). The absolute configuration of biotin. Biochemistry, 5(2), 713-714.
Weekes, M.P., Antrobus, R., Lill, J.R., Duncan, L.M., Hor, S., & Lehner, P.J. (2010). Comparative analysis of techniques to purify plasma membrane proteins. Journal of Biomolecular Techniques, 21(3), 108-115.
Weekes, M.P., Tomasec, P., Huttlin, E.L., Fielding, C.A., Nusinow, D., Stanton, R.J., Wang, E.C., Aicheler, R., Murrell, I., Wilkinson, G.W., Lehner, P.J., & Gygi, S.P. (2014). Quantitative temporal viromics: an approach to investigate host-pathogen interaction. Cell, 157(6), 1460-1472.
Wollscheid, B., Bausch-Fluck, D., Henderson, C., O'Brien, R., Bibel, M., Schiess, R., Aebersold, R., & Watts, J.D. (2009). Mass-spectrometric identification and relative quantification of N-linked cell surface glycoproteins. Nature Biotechnology, 27(4), 378-386.
Wu, C.C., MacCoss, M.J., Howell, K.E., & Yates, J.R., 3rd. (2003). A method for the comprehensive proteomic analysis of membrane proteins. Nature Biotechnology, 21(5), 532-538.
Wu, C.C., & Yates, J.R., 3rd. (2003). The application of mass spectrometry to membrane proteomics. Nature Biotechnology, 21(3), 262-267.
Zeng, Y., Ramya, T.N., Dirksen, A., Dawson, P.E., & Paulson, J.C. (2009). High-efficiency labeling of sialylated glycoproteins on living cells. Nature Methods, 6(3), 207-209.
Zhang, H., Li, X.J., Martin, D.B., & Aebersold, R. (2003). Identification and quantification of N-linked glycoproteins using hydrazide chemistry, stable isotope labeling and mass spectrometry. Nature Biotechnology, 21(6), 660-666.
Zhang, L., Xie, J., Wang, X., Liu, X., Tang, X., Cao, R., Hu, W., Nie, S., Fan, C., & Liang, S. (2005). Proteomic analysis of mouse liver plasma membrane: use of differential extraction to enrich hydrophobic membrane proteins. Proteomics, 5(17), 4510-4524.
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Arjunan, S., Reinartz, M., Emde, B., Zanger, K., & Schrader, J. (2009). Limitations of the colloidal silica method in mapping the endothelial plasma membrane proteome of the mouse heart. Cell Biochemistry and Biophysics, 53(3), 135-143.
Bendz, M., Skwark, M., Nilsson, D., Granholm, V., Cristobal, S., Käll L., & Elofsson, A. (2013). Membrane protein shaving with thermolysin can be used to evaluate topology predictors. Proteomics, 13(9), 1467-1480
Boheler, K.R., Bhattacharya, S., Kropp, E.M., Chuppa, S., Riordon, D.R., Bausch-Fluck, D., Burridge, P.W., Wu, J.C., Wersto, R.P., Chan, G.C., Rao, S., Wollscheid, B. & Gundry, R.L. (2014). A human pluripotent stem cell surface N-glycoproteome resource reveals markers, extracellular epitopes, and drug targets. Stem Cell Reports, 3(1), 185-203.
Cao, R., He, Q., Zhou, J., He, Q., Liu, Z., Wang, X., Chen, P., Xie, J., & Liang, S. (2008). High-throughput analysis of rat liver plasma membrane proteome by a nonelectrophoretic in-gel tryptic digestion coupled with mass spectrometry identification. Journal of Proteome Research, 7(2), 535-545.
Cathro, P., McCarthy, P., Hoffmann, P., & Zilm, P. (2016). Isolation and identification of Enterococcus faecalis membrane proteins using membrane shaving, 1D SDS/PAGE, and mass spectrometry. FEBS Open Bio, 6(6), 586-593.
Chaney, L.K., & Jacobson, B.S. (1983). Coating cells with colloidal silica for high yield isolation of plasma membrane sheets and identification of transmembrane proteins. Journal of Biological Chemistry, 258(16), 10062-10072.
Chen, R., Jiang, X., Sun, D., Han, G., Wang, F., Ye, M., Wang, L., & Zou, H. (2009). Glycoproteomics analysis of human liver tissue by combination of multiple enzyme digestion and hydrazide chemistry. Journal of Proteome Research, 8(2), 651-661.
Choksawangkarn, W., Kim, S.K., Cannon, J.R., Edwards, N.J., Lee, S.B., & Fenselau, C. (2013). Enrichment of plasma membrane proteins using nanoparticle pellicles: comparison between silica and higher density nanoparticles. Journal of Proteome Research, 12(3), 1134-1141.
Choksawangkarn, W., Graham, L.M., Burke, M., Lee, S. B., Ostrand-Rosenberg, S., Fenselau, C., & Edwards, N. (2016). Peptide-based systems analysis of inflammation induced myeloid-derived suppressor cells reveals diverse signaling pathways. Proteomics, 16(13), 1881-1888.
Cordwell, S.J., & Thingholm, T.E. (2010). Technologies for plasma membrane proteomics. Proteomics, 10(4), 611-627.
Durr, E., Yu, J., Krasinska, K.M., Carver, L.A., Yates, J.R., Testa, J.E., Oh, P., & Schnitzer, J.E. (2004). Direct proteomic mapping of the lung microvascular endothelial cell surface in vivo and in cell culture. Nature Biotechnology, 22(8), 985-992.
Eichacker, L.A., Granvogl, B., Mirus, O., Muller, B.C., Miess, C., & Schleiff, E. (2004). Hiding behind hydrophobicity. Transmembrane segments in mass spectrometry. Journal of Biological Chemistry, 279(49), 50915-50922.
Elia, G. (2008). Biotinylation reagents for the study of cell surface proteins. Proteomics, 8(19), 4012-4024.
Gasser, K.W., DiDomenico, J., & Hopfer, U. (1988). Separation of cell organelles in density gradients based on their permeability characteristics. Analytical Biochemistry, 171(1), 41-46.
Graham, J. M., & Rickwood, D. (2001). Biological Centrifugation. Oxford: BIOS Scientific Publishers Ltd.
Gundry, R. L., Raginski, K., Tarasova, Y., Tchernyshyov, I., Bausch-Fluck, D., Elliott, S. T., Boheler, K.R., Van Eyk, J.E., & Wollscheid, B. (2009). The mouse C2C12 myoblast cell surface N-linked glycoproteome: identification, glycosite occupancy, and membrane orientation. Molecular and Cellular Proteomics, 8(11), 2555-2569.
Hormann, K., Stukalov, A., Muller, A.C., Heinz, L.X., Superti-Furga, G., Colinge, J., & Bennett, K.L. (2016). A Surface biotinylation strategy for reproducible plasma membrane protein purification and tracking of genetic and drug-induced alterations. Journal of Proteome Research, 15(2), 647-658.
Josic, D., & Clifton, J.G. (2007). Mammalian plasma membrane proteomics. Proteomics, 7(16), 3010-3029.
Josic, D., Clifton, J.G., Kovac, S., & Hixson, D.C. (2008). Membrane proteins as diagnostic biomarkers and targets for new therapies. Current Opinion in Molecular Therapeutics, 10(2), 116-123.
Kearney, P., & Thibault, P. (2003). Bioinformatics meets proteomics--bridging the gap between mass spectrometry data analysis and cell biology. Journal of Bioinformatics and Computational Biology, 1(1), 183-200.
Kim, S.K., Choksawangkarn, W., Rose, R., Fenselau, C., & Lee, S.B. (2014). Nanowire pellicles for eukaryotic cells: nanowire coating and interaction with cells. Nanomedicine (Lond), 9(8), 1171-1180.
Kim, S.K., Rose, R., Choksawangkarn, W., Graham, L., Hu, J., Fenselau, C., & Lee, S.B. (2013). Comparison of nanowire pellicles for plasma membrane enrichment: coating nanowires on cell. Journal of Nanoparticle Research, 15(12), 2133.
Leth-Larsen, R., Lund, R.R., & Ditzel, H.J. (2010). Plasma membrane proteomics and its application in clinical cancer biomarker discovery. Molecular and Cellular Proteomics, 9(7), 1369-1382.
Li, X., Jia, X., Xie, C., Lin, Y., Cao, R., He, Q., Chen, P., Wang, X., & Liang, S. (2009). Development of cationic colloidal silica-coated magnetic nanospheres for highly selective and rapid enrichment of plasma membrane fractions for proteomics analysis. Biotechnolology and Applied Biochemistry, 54(4), 213-220.
Li, X., Jin, Q., Cao, J., Xie, C., Cao, R., Liu, Z., Xiong, J., Li, J., Yang, X., Chen, P., & Liang, S. (2009). Evaluation of two cell surface modification methods for proteomic analysis of plasma membrane from isolated mouse hepatocytes. Biochimica et Biophysica Acta, 1794(1), 32-41.
Livnah, O., Bayer, E. A., Wilchek, M., & Sussman, J. L. (1993). Three-dimensional structures of avidin and the avidin-biotin complex. Proceedings of the National Academy of Science of the United States of America, 90(11), 5076-5080.
Long, J., Basu Roy, R., Zhang, Y.J. , Antrobus, R., Du, Y., Smith, D.L., Weekes, M.P., & Javid, B. (2016). Plasma membrane profiling reveals upregulation of ABCA1 by macrophages leading to restriction of Mycobacterial growth. Frontiers in Microbiology, 7, 1086.
Matheson, N.J., Sumner, J., Wals, K., Rapiteanu, R., Weekes, M.P., Vigan, R., Weinelt, J., Schindler, M., Antrobus, R., Costa, A.S.H., Frezza, C., Clish, C.B., Neil, S.J.D., & Lehner, P.J. (2015). Cell surface proteomic map of HIV infection reveals antagonism of amino acid metabolism by Vpu and Nef. Cell Host & Microbe, 18(4), 409-423.
Mathias, R.A., Chen, Y.S., Goode, R.J., Kapp, E.A., Mathivanan, S., Moritz, R.L., Zhu, H.J., & Simpson, R.J. (2011). Tandem application of cationic colloidal silica and Triton X-114 for plasma membrane protein isolation and purification: towards developing an MDCK protein database. Proteomics, 11(7), 1238-1253.
Nielsen, P.A., Olsen, J.V., Podtelejnikov, A.V., Andersen, J.R., Mann, M., & Wisniewski, J.R. (2005). Proteomic mapping of brain plasma membrane proteins. Molecular and Cellular Proteomics, 4(4), 402-408.
Ohtsubo, K., & Marth, J.D. (2006). Glycosylation in cellular mechanisms of health and disease. Cell, 126(5), 855-867.
Overington, J.P., Al-Lazikani, B., & Hopkins, A.L. (2006). Opinion - How many drug targets are there? Nature Reviews Drug Discovery, 5(12), 993-996.
Prior, M.J., Larance, M., Lawrence, R.T., Soul, J., Humphrey, S., Burchfield, J., Kistler, C., Davey, J.R., La-Borde, P.J., Buckley, M., Kanazawa, H., Parton, R.G., Guilhaus, M., & James, D.E. (2011). Quantitative proteomic analysis of the adipocyte plasma membrane. Journal of Proteome Research, 10(11), 4970-4982.
Rahbar, A.M., & Fenselau, C. (2004). Integration of Jacobson's pellicle method into proteomic strategies for plasma membrane proteins. Journal of Proteome Research, 3(6), 1267-1277.
Reeke, G.N., Jr., Becker, J.W., Cunningham, B.A., Wang, J.L., Yahara, I., & Edelman, G.M. (1975). Structure and function of concanavalin A. Advances in Experimental Medicine and Biology, 55, 13-33.
Robinson, J.M., Ackerman, W.E., Tewari, A.K., Kniss, D.A., & Vandre, D.D. (2009). Isolation of highly enriched apical plasma membranes of the placental syncytiotrophoblast. Analalytical Biochemistry, 387(1), 87-94.
Rodriguez-Ortega, M.J., Norais, N., Bensi, G., Liberatori, S., Capo, S., Mora, M., Scarselli, M., Doro, F., Ferrari, G., Garaguso, I., Maggi, T., Neumann, A., Covre, A., Telford, J.L., & Grandi, G. (2006). Characterization and identification of vaccine candidate proteins through analysis of the group A Streptococcus surface proteome. Nature Biotechnology, 24(2), 191-197.
Rybak, J.N., Ettorre, A., Kaissling, B., Giavazzi, R., Neri, D., & Elia, G. (2005). In vivo protein biotinylation for identification of organ-specific antigens accessible from the vasculature. Nature Methods, 2(4), 291-298.
Simpson, R. J. (2010). Disruption of cultured cells by nitrogen cavitation. Cold Spring Harbor Protocol, 2010(11), pdb prot5513.
Solis, N., Cain, J.A., & Cordwell, S.J. (2016). Comparative analysis of Staphylococcus epidermidis strains utilizing quantitative and cell surface shaving proteomics. Journal of Proteomics, 130, 190-199.
Solis, N., Larsen, M.R., & Cordwell, S.J. (2010). Improved accuracy of cell surface shaving proteomics in Staphylococcus aureus using a false-positive control. Proteomics, 10(10), 2037-2049.
Song, W., Mentink, R.A., Henquet, M.G., Cordewener, J.H., van Dijk, A.D., Bosch, D., America, A.H., & van der Krol, A.R. (2013). N-glycan occupancy of Arabidopsis N-glycoproteins. Journal of Proteomics, 93, 343-355.
Speers, A.E., Blackler, A.R., & Wu, C.C. (2007). Shotgun analysis of integral membrane proteins facilitated by elevated temperature. Analytical Chemistry, 79(12), 4613-4620.
Speers, A.E., & Wu, C.C. (2007). Proteomics of integral membrane proteins--theory and application. Chemical Reviews, 107(8), 3687-3714.
Stolz, D.B., & Jacobson, B.S. (1992). Examination of transcellular membrane protein polarity of bovine aortic endothelial cells in vitro using the cationic colloidal silica microbead membrane-isolation procedure. Journal of Cell Science, 103(Pt 1), 39-51.
Tan, S., Tan, H.T., & Chung, M.C. (2008). Membrane proteins and membrane proteomics. Proteomics, 8(19), 3924-3932.
Trotter, J., & Hamilton, J. A. (1966). The absolute configuration of biotin. Biochemistry, 5(2), 713-714.
Weekes, M.P., Antrobus, R., Lill, J.R., Duncan, L.M., Hor, S., & Lehner, P.J. (2010). Comparative analysis of techniques to purify plasma membrane proteins. Journal of Biomolecular Techniques, 21(3), 108-115.
Weekes, M.P., Tomasec, P., Huttlin, E.L., Fielding, C.A., Nusinow, D., Stanton, R.J., Wang, E.C., Aicheler, R., Murrell, I., Wilkinson, G.W., Lehner, P.J., & Gygi, S.P. (2014). Quantitative temporal viromics: an approach to investigate host-pathogen interaction. Cell, 157(6), 1460-1472.
Wollscheid, B., Bausch-Fluck, D., Henderson, C., O'Brien, R., Bibel, M., Schiess, R., Aebersold, R., & Watts, J.D. (2009). Mass-spectrometric identification and relative quantification of N-linked cell surface glycoproteins. Nature Biotechnology, 27(4), 378-386.
Wu, C.C., MacCoss, M.J., Howell, K.E., & Yates, J.R., 3rd. (2003). A method for the comprehensive proteomic analysis of membrane proteins. Nature Biotechnology, 21(5), 532-538.
Wu, C.C., & Yates, J.R., 3rd. (2003). The application of mass spectrometry to membrane proteomics. Nature Biotechnology, 21(3), 262-267.
Zeng, Y., Ramya, T.N., Dirksen, A., Dawson, P.E., & Paulson, J.C. (2009). High-efficiency labeling of sialylated glycoproteins on living cells. Nature Methods, 6(3), 207-209.
Zhang, H., Li, X.J., Martin, D.B., & Aebersold, R. (2003). Identification and quantification of N-linked glycoproteins using hydrazide chemistry, stable isotope labeling and mass spectrometry. Nature Biotechnology, 21(6), 660-666.
Zhang, L., Xie, J., Wang, X., Liu, X., Tang, X., Cao, R., Hu, W., Nie, S., Fan, C., & Liang, S. (2005). Proteomic analysis of mouse liver plasma membrane: use of differential extraction to enrich hydrophobic membrane proteins. Proteomics, 5(17), 4510-4524.
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2017-09-07
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