On-Membrane Digestion Technology for Muscle Proteomics
DOI:
https://doi.org/10.6000/1929-6037.2013.02.01.1Keywords:
Dystrophin, on-membrane digestion, mass spectrometry, muscle proteomics, ryanodine receptor.Abstract
High-resolution two-dimensional gel electrophoresis and in-gel digestion are routinely used for large-scale protein separation and peptide generation in mass spectrometry-based proteomics, respectively. However, the combination of isoelectric focusing in the first dimension and polyacrylamide slab gel electrophoresis in the second dimension is not suitable for the proper separation of integral proteins and high-molecular-mass proteins. In addition, in-gel trypsination may not result in a high degree of efficient digestion levels for the production of large numbers of peptides in the case of certain protein species. The application of gradient one-dimensional gel electrophoresis and on-membrane digestion can overcome these technical problems and be extremely helpful for the comprehensive identification of proteins that are underrepresented in routine two-dimensional gel electrophoretic approaches. This review critically examines the general application of on-membrane digestion techniques in proteomics and its recent application for the identification of very large integral membrane proteins from skeletal muscle by mass spectrometry. This includes the discussion of proteomic studies that have focused on the proteomic characterization of the membrane cytoskeletal protein dystrophin from sarcolemma vesicles and the ryanodine receptor calcium release channel of the sarcoplasmic reticulum from skeletal muscle.
References
Hayes PC, Wolf CR, Hayes JD. Blotting techniques for the study of DNA, RNA, and proteins. BMJ 1989; 299: 965-8. http://dx.doi.org/10.1136/bmj.299.6705.965 DOI: https://doi.org/10.1136/bmj.299.6705.965
Southern EM. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 1975; 98: 503-17. http://dx.doi.org/10.1016/S0022-2836(75)80083-0 DOI: https://doi.org/10.1016/S0022-2836(75)80083-0
Alwine JC, Kemp DJ, Stark GR. Method for detection of specific RNAs in agarose gels by transfer to diazobenzyloxymethyl-paper and hybridization with DNA probes. Proc Natl Acad Sci USA 1977; 74: 5350-4. http://dx.doi.org/10.1073/pnas.74.12.5350 DOI: https://doi.org/10.1073/pnas.74.12.5350
Burnette WN. "Western blotting": electrophoretic transfer of proteins from sodium dodecyl sulfate-polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal Biochem 1981; 112: 195-203. http://dx.doi.org/10.1016/0003-2697(81)90281-5 DOI: https://doi.org/10.1016/0003-2697(81)90281-5
Kroczek RA. Southern and northern analysis. J Chromatogr 1993; 618: 133-45. DOI: https://doi.org/10.1016/0378-4347(93)80031-X
Kurien BT, Scofield RH. Protein blotting: a review. J Immunol Methods 2003; 274: 1-15. http://dx.doi.org/10.1016/S0022-1759(02)00523-9 DOI: https://doi.org/10.1016/S0022-1759(02)00523-9
Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 1979; 76: 4350-4. http://dx.doi.org/10.1073/pnas.76.9.4350 DOI: https://doi.org/10.1073/pnas.76.9.4350
Ursitti JA, Mozdzanowski J, Speicher DW. Electroblotting from polyacrylamide gels. Curr Protoc Protein Sci 2001; Chapter 10: Unit 10.7.
Kurien BT, Scofield RH. Western blotting. Methods 2006; 38: 283-93. http://dx.doi.org/10.1016/j.ymeth.2005.11.007 DOI: https://doi.org/10.1016/j.ymeth.2005.11.007
Kurien BT, Scofield RH. A brief review of other notable protein blotting methods. Methods Mol Biol 2009; 536: 367-84. http://dx.doi.org/10.1007/978-1-59745-542-8_38 DOI: https://doi.org/10.1007/978-1-59745-542-8_38
MacPhee DJ. Methodological considerations for improving Western blot analysis. J Pharmacol Toxicol Methods 2010; 61: 171-7. http://dx.doi.org/10.1016/j.vascn.2009.12.001 DOI: https://doi.org/10.1016/j.vascn.2009.12.001
Handen JS, Rosenberg HF. An improved method for Southwestern blotting. Front Biosci 1997; 2: c9-c11. DOI: https://doi.org/10.2741/A166
Siu FK, Lee LT, Chow BK. Southwestern blotting in investigating transcriptional regulation. Nat Protoc 2008; 3: 51-8. http://dx.doi.org/10.1038/nprot.2007.492 DOI: https://doi.org/10.1038/nprot.2007.492
Labbe S, Harrisson JF, Seguin C. Identification of sequence-specific DNA-binding proteins by southwestern blotting. Methods Mol Biol 2009; 543: 151-61. http://dx.doi.org/10.1007/978-1-60327-015-1_12 DOI: https://doi.org/10.1007/978-1-60327-015-1_12
Edmondson DG, Roth SY. Identification of protein interactions by far Western analysis. Curr Protoc Mol Biol 2001; Chapter 20: Unit 20.6.
Chan CS, Winstone TM, Turner RJ. Investigating protein-protein interactions by far-Westerns. Adv Biochem Eng Biotechnol 2008; 110: 195-14. http://dx.doi.org/10.1007/10_2007_090 DOI: https://doi.org/10.1007/10_2007_090
Machida K, Mayer BJ. Detection of protein-protein interactions by far-western blotting. Methods Mol Biol 2009; 536: 313-29. http://dx.doi.org/10.1007/978-1-59745-542-8_34 DOI: https://doi.org/10.1007/978-1-59745-542-8_34
Glover L, Froemming G, Ohlendieck K. Calsequestrin blot overlay of two-dimensional electrophoretically separated microsomal proteins from skeletal muscle. Anal Biochem 2001; 299: 268-71. http://dx.doi.org/10.1006/abio.2001.5424 DOI: https://doi.org/10.1006/abio.2001.5424
Glover L, Quinn S, Ryan M, Pette D, Ohlendieck K. Supramolecular calsequestrin complex. Eur J Biochem 2002; 269: 4607-16. http://dx.doi.org/10.1046/j.1432-1033.2002.03160.x DOI: https://doi.org/10.1046/j.1432-1033.2002.03160.x
Strom A, Diecke S, Hunsmann G, Stuke AW. Identification of prion protein binding proteins by combined use of far-Western immunoblotting, two dimensional gel electrophoresis and mass spectrometry. Proteomics 2006; 6: 26-34. http://dx.doi.org/10.1002/pmic.200500066 DOI: https://doi.org/10.1002/pmic.200500066
Ino Y, Hirano H. Mass spectrometric characterization of proteins transferred from polyacrylamide gels to membrane filters. FEBS J 2011; 278: 3807-14. http://dx.doi.org/10.1111/j.1742-4658.2011.08303.x DOI: https://doi.org/10.1111/j.1742-4658.2011.08303.x
Simspon RJ. On-membrane proteolytic digestion of electroblotted proteins. Cold Spring Harb Protoc 2011; 2011: 995-7. DOI: https://doi.org/10.1101/pdb.prot4589
Han X, Aslanian A, Yates JR 3rd. Mass spectrometry for proteomics. Curr Opin Chem Biol 2008; 12: 483-90. http://dx.doi.org/10.1016/j.cbpa.2008.07.024 DOI: https://doi.org/10.1016/j.cbpa.2008.07.024
Chait BT. Mass spectrometry in the postgenomic era. Annu Rev Biochem 2011; 80: 239-46. http://dx.doi.org/10.1146/annurev-biochem-110810-095744 DOI: https://doi.org/10.1146/annurev-biochem-110810-095744
Angel TE, Aryal UK, Hengel SM, Baker ES, Kelly RT, Robinson EW, et al. Mass spectrometry-based proteomics: existing capabilities and future directions. Chem Soc Rev 2012; 41: 3912-28. http://dx.doi.org/10.1039/c2cs15331a DOI: https://doi.org/10.1039/c2cs15331a
Walther TC, Mann M. Mass spectrometry-based proteomics in cell biology. J Cell Biol 2010; 190: 491-500. http://dx.doi.org/10.1083/jcb.201004052 DOI: https://doi.org/10.1083/jcb.201004052
Schirle M, Bantscheff M, Kuster B. Mass spectrometry-based proteomics in preclinical drug discovery. Chem Biol 2012; 19: 72-84. http://dx.doi.org/10.1016/j.chembiol.2012.01.002 DOI: https://doi.org/10.1016/j.chembiol.2012.01.002
Sabido E, Selevsek N, Aebersold R. Mass spectrometry-based proteomics for systems biology. Curr Opin Biotechnol 2012; 23: 591-7. http://dx.doi.org/10.1016/j.copbio.2011.11.014 DOI: https://doi.org/10.1016/j.copbio.2011.11.014
Xie F, Liu T, Qian WJ, Petyuk VA, Smith RD. Liquid chromatography-mass spectrometry-based quantitative proteomics. J Biol Chem 2011; 286: 25443-9. http://dx.doi.org/10.1074/jbc.R110.199703 DOI: https://doi.org/10.1074/jbc.R110.199703
Gauci VJ, Wright EP, Coorssen JR. Quantitative proteomics: assessing the spectrum of in-gel protein detection methods. J Chem Biol 2011; 4: 3-29. http://dx.doi.org/10.1007/s12154-010-0043-5 DOI: https://doi.org/10.1007/s12154-010-0043-5
Yates JR 3rd, Gilchrist A, Howell KE, Bergeron JJ. Proteomics of organelles and large cellular structures. Nat Rev Mol Cell Biol 2005; 6: 702-14. http://dx.doi.org/10.1038/nrm1711 DOI: https://doi.org/10.1038/nrm1711
Gauthier DJ, Lazure C. Complementary methods to assist subcellular fractionation in organellar proteomics. Expert Rev Proteomics 2008; 5: 603-17. http://dx.doi.org/10.1586/14789450.5.4.603 DOI: https://doi.org/10.1586/14789450.5.4.603
Lee YH, Tan HT, Chung MC. Subcellular fractionation methods and strategies for proteomics. Proteomics 2010; 10: 3935-56. http://dx.doi.org/10.1002/pmic.201000289 DOI: https://doi.org/10.1002/pmic.201000289
Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 2006; 1: 2856-60. http://dx.doi.org/10.1038/nprot.2006.468 DOI: https://doi.org/10.1038/nprot.2006.468
Granvogl B, Plöscher M, Eichacker LA. Sample preparation by in-gel digestion for mass spectrometry-based proteomics. Anal Bioanal Chem 2007; 389: 991-1002. http://dx.doi.org/10.1007/s00216-007-1451-4 DOI: https://doi.org/10.1007/s00216-007-1451-4
Righetti PG, Candiano G. Recent advances in electrophoretic techniques for the characterization of protein biomolecules: a poker of aces. J Chromatogr A 2011; 1218: 8727-37. http://dx.doi.org/10.1016/j.chroma.2011.04.011 DOI: https://doi.org/10.1016/j.chroma.2011.04.011
Wittig I, Schagger H. Native electrophoretic techniques to identify protein-protein interactions. Proteomics 2009; 9: 5214-23. http://dx.doi.org/10.1002/pmic.200900151 DOI: https://doi.org/10.1002/pmic.200900151
Righetti PG, Castagna A, Herbert B, Reymond F, Rossier JS. Prefractionation techniques in proteome analysis. Proteomics 2003; 3: 1397-407. http://dx.doi.org/10.1002/pmic.200300472 DOI: https://doi.org/10.1002/pmic.200300472
Mulvey C, Ohlendieck K. Use of continuous-elution gel electrophoresis as a preparative tool for blot overlay analysis. Anal Biochem 2003; 319: 122-30. http://dx.doi.org/10.1016/S0003-2697(03)00321-X DOI: https://doi.org/10.1016/S0003-2697(03)00321-X
Righetti PG, Castagna A, Antonioli P, Boschetti E. Prefractionation techniques in proteome analysis: the mining tools of the third millennium. Electrophoresis 2005; 26: 297-19. http://dx.doi.org/10.1002/elps.200406189 DOI: https://doi.org/10.1002/elps.200406189
Ros A, Faupel M, Mees H, Oostrum J, Ferrigno R, Reymond F, et al. Protein purification by Off-Gel electrophoresis. Proteomics 2002; 2: 151-6. http://dx.doi.org/10.1002/1615-9861(200202)2:2<151::AID-PROT151>3.0.CO;2-9 DOI: https://doi.org/10.1002/1615-9861(200202)2:2<151::AID-PROT151>3.0.CO;2-9
Horth P, Miller CA, Preckel T, Wenz C. Efficient fractionation and improved protein identification by peptide OFFGEL electrophoresis. Mol Cell Proteomics 2006; 5: 1968-74. http://dx.doi.org/10.1074/mcp.T600037-MCP200 DOI: https://doi.org/10.1074/mcp.T600037-MCP200
Keidel EM, Dosch D, Brunner A, Kellermann J, Lottspeich F. Evaluation of protein loading techniques and improved separation in OFFGEL isoelectric focusing. Electrophoresis 2011; 32: 1659-66. DOI: https://doi.org/10.1002/elps.201000544
Gannon J, Ohlendieck K. Subproteomic analysis of basic proteins in aged skeletal muscle following offgel pre-fractionation. Mol Med Report 2012; 5: 993-1000. DOI: https://doi.org/10.3892/mmr.2012.759
Garfin DE. Two-dimensional gel electrophoresis: an overview. Trends Anal Chem 2003; 22: 263-72. http://dx.doi.org/10.1016/S0165-9936(03)00506-5 DOI: https://doi.org/10.1016/S0165-9936(03)00506-5
Gorg A, Weiss W, Dunn MJ. Current two-dimensional electrophoresis technology for proteomics. Proteomics 2004; 4: 3665-85. http://dx.doi.org/10.1002/pmic.200401031 DOI: https://doi.org/10.1002/pmic.200401031
Wittmann-Liebold B, Graack HR, Pohl T. Two-dimensional gel electrophoresis as tool for proteomics studies in combination with protein identification by mass spectrometry. Proteomics 2006; 6: 4688-703. http://dx.doi.org/10.1002/pmic.200500874 DOI: https://doi.org/10.1002/pmic.200500874
Rabilloud T, Chevallet M, Luche S, Lelong C. Two-dimensional gel electrophoresis in proteomics: Past, present and future. J Proteomics 2010; 73: 2064-77. http://dx.doi.org/10.1016/j.jprot.2010.05.016 DOI: https://doi.org/10.1016/j.jprot.2010.05.016
Rabilloud T, Lelong C. Two-dimensional gel electrophoresis in proteomics: a tutorial. J Proteomics 2011; 74: 1829-41. http://dx.doi.org/10.1016/j.jprot.2011.05.040 DOI: https://doi.org/10.1016/j.jprot.2011.05.040
Wittig I, Schagger H. Features and applications of blue-native and clear-native electrophoresis. Proteomics 2008; 8: 3974-90. http://dx.doi.org/10.1002/pmic.200800017 DOI: https://doi.org/10.1002/pmic.200800017
Froemming GR, Murray BE, Ohlendieck K. Self-aggregation of triadin in the sarcoplasmic reticulum of rabbit skeletal muscle. Biochim Biophys Acta 1999; 1418: 197-205. http://dx.doi.org/10.1016/S0005-2736(99)00024-3 DOI: https://doi.org/10.1016/S0005-2736(99)00024-3
Wu J, Lenchik NJ, Pabst MJ, Solomon SS, Shull J, Gerling IC. Functional characterization of two-dimensional gel-separated proteins using sequential staining. Electrophoresis 2005; 26: 225-37. http://dx.doi.org/10.1002/elps.200406176 DOI: https://doi.org/10.1002/elps.200406176
Weiss W, Gorg A. High-resolution two-dimensional electrophoresis. Methods Mol Biol 2009; 564: 13-32. http://dx.doi.org/10.1007/978-1-60761-157-8_2 DOI: https://doi.org/10.1007/978-1-60761-157-8_2
Steinberg TH. Protein gel staining methods: an introduction and overview. Methods Enzymol 2009; 463: 541-63. http://dx.doi.org/10.1016/S0076-6879(09)63031-7 DOI: https://doi.org/10.1016/S0076-6879(09)63031-7
Weiss W, Weiland F, Gorg A. Protein detection and quantitation technologies for gel-based proteome analysis. Methods Mol Biol 2009; 564: 59-82. http://dx.doi.org/10.1007/978-1-60761-157-8_4 DOI: https://doi.org/10.1007/978-1-60761-157-8_4
Brewis IA, Brennan P. Proteomics technologies for the global identification and quantification of proteins. Adv Protein Chem Struct Biol 2010; 80: 1-44. http://dx.doi.org/10.1016/B978-0-12-381264-3.00001-1 DOI: https://doi.org/10.1016/B978-0-12-381264-3.00001-1
Rabilloud T. Silver staining of 2D electrophoresis gels. Methods Mol Biol 2012; 893: 61-73. http://dx.doi.org/10.1007/978-1-61779-885-6_5 DOI: https://doi.org/10.1007/978-1-61779-885-6_5
Lopez MF, Berggren K, Chernokalskaya E, Lazarev A, Robinson M, Patton WF. A comparison of silver stain and SYPRO Ruby Protein Gel Stain with respect to protein detection in two-dimensional gels and identification by peptide mass profiling. Electrophoresis 2000; 21: 3673-83. http://dx.doi.org/10.1002/1522-2683(200011)21:17<3673::AID-ELPS3673>3.0.CO;2-M DOI: https://doi.org/10.1002/1522-2683(200011)21:17<3673::AID-ELPS3673>3.0.CO;2-M
Patton WF. A thousand points of light: the application of fluorescence detection technologies to two-dimensional gel electrophoresis and proteomics. Electrophoresis 2000; 21: 1123-44. http://dx.doi.org/10.1002/(SICI)1522-2683(20000401)21:6<1123::AID-ELPS1123>3.0.CO;2-E DOI: https://doi.org/10.1002/(SICI)1522-2683(20000401)21:6<1123::AID-ELPS1123>3.0.CO;2-E
Westermeier R, Marouga R. Protein detection methods in proteomics research. Biosci Rep 2005; 25: 19-32. http://dx.doi.org/10.1007/s10540-005-2845-1 DOI: https://doi.org/10.1007/s10540-005-2845-1
Aude-Garcia C, Collin-Faure V, Luche S, Rabilloud T. Improvements and simplifications in in-gel fluorescent detection of proteins using ruthenium II tris-(bathophenanthroline disulfonate): the poor man's fluorescent detection method. Proteomics 2011; 11: 324-8. http://dx.doi.org/10.1002/pmic.201000370 DOI: https://doi.org/10.1002/pmic.201000370
Minden JS, Dowd SR, Meyer HE, Stühler K. Difference gel electrophoresis. Electrophoresis 2009; 30(Suppl 1): S156-61. http://dx.doi.org/10.1002/elps.200900098 DOI: https://doi.org/10.1002/elps.200900098
Marouga R, David S, Hawkins E. The development of the DIGE system: 2D fluorescence difference gel analysis technology. Anal Bioanal Chem 2005; 382: 669-78. http://dx.doi.org/10.1007/s00216-005-3126-3 DOI: https://doi.org/10.1007/s00216-005-3126-3
Timms JF, Cramer R. Difference gel electrophoresis. Proteomics 2008; 8: 4886-97. http://dx.doi.org/10.1002/pmic.200800298 DOI: https://doi.org/10.1002/pmic.200800298
Dautel F, Kalkhof S, Trump S, Lehmann I, Beyer A, von Bergen M. Large-scale 2-D DIGE studies - guidelines to overcome pitfalls and challenges along the experimental procedure. J Integr OMICS 2011; 1: 170-9. DOI: https://doi.org/10.5584/jiomics.v1i1.50
Alban A, David SO, Bjorkesten L, Andersson C, Sloge E, Lewis S, et al. A novel experimental design for comparative two-dimensional gel analysis: two-dimensional difference gel electrophoresis incorporating a pooled internal standard. Proteomics 2003; 3: 36-44. http://dx.doi.org/10.1002/pmic.200390006 DOI: https://doi.org/10.1002/pmic.200390006
Doran P, Martin G, Dowling P, Jockusch H, Ohlendieck K. Proteome analysis of the dystrophin-deficient MDX diaphragm reveals a drastic increase in the heat shock protein cvHSP. Proteomics 2006; 6(16): 4610-21. http://dx.doi.org/10.1002/pmic.200600082 DOI: https://doi.org/10.1002/pmic.200600082
Doran P, O'Connell K, Gannon J, Kavanagh M, Ohlendieck K. Opposite pathobiochemical fate of pyruvate kinase and adenylate kinase in aged rat skeletal muscle as revealed by proteomic DIGE analysis. Proteomics 2008; 8: 364-77. http://dx.doi.org/10.1002/pmic.200700475 DOI: https://doi.org/10.1002/pmic.200700475
Lewis C, Doran P, Ohlendieck K. Proteomic analysis of dystrophic muscle. Methods Mol Biol 2012; 798: 357-69. http://dx.doi.org/10.1007/978-1-61779-343-1_20 DOI: https://doi.org/10.1007/978-1-61779-343-1_20
Beranova-Giorgianni S. Proteome analysis by two-dimensional gel electrophoresis and mass spectrometry:
strengths and limitations. Trends Anal Chem 2003; 22: 273281. http://dx.doi.org/10.1016/S0165-9936(03)00508-9 DOI: https://doi.org/10.1016/S0165-9936(03)00508-9
Tan S, Tan HT, Chung MC. Membrane proteins and membrane proteomics. Proteomics 2008; 8: 3924-32. http://dx.doi.org/10.1002/pmic.200800597 DOI: https://doi.org/10.1002/pmic.200800597
Helbig AO, Heck AJ, Slijper M. Exploring the membrane proteome-challenges and analytical strategies. J Proteomics 2010; 73: 868-78. http://dx.doi.org/10.1016/j.jprot.2010.01.005 DOI: https://doi.org/10.1016/j.jprot.2010.01.005
Groen AJ, Lilley KS. Proteomics of total membranes and subcellular membranes. Expert Rev Proteomics 2010; 7: 867-78. http://dx.doi.org/10.1586/epr.10.85 DOI: https://doi.org/10.1586/epr.10.85
Mozdzanowski J, Speicher DW. Microsequence analysis of electroblotted proteins. I. Comparison of electroblotting recoveries using different types of PVDF membranes. Anal Biochem 1992; 207: 11-8. http://dx.doi.org/10.1016/0003-2697(92)90492-P DOI: https://doi.org/10.1016/0003-2697(92)90492-P
Reim DF, Speicher DW. Microsequence analysis of electroblotted proteins. II. Comparison of sequence performance on different types of PVDF membranes. Anal Biochem 1992; 207: 19-23. http://dx.doi.org/10.1016/0003-2697(92)90493-Q DOI: https://doi.org/10.1016/0003-2697(92)90493-Q
Komatsu S. Western blotting/Edman sequencing using PVDF membrane. Methods Mol Biol 2009; 536: 163-71. http://dx.doi.org/10.1007/978-1-59745-542-8_18 DOI: https://doi.org/10.1007/978-1-59745-542-8_18
Baker CS, Dunn MJ. Preparation of proteins from gels for protein microsequencing. Methods Mol Biol 1994; 32: 177-84. DOI: https://doi.org/10.1385/0-89603-268-X:177
Sirawaraporn W. Preparation of blotted membrane for protein microsequencing. Methods Mol Biol 1993; 21: 431-40. DOI: https://doi.org/10.1385/0-89603-239-6:431
Kurien BT, Scofield RH. Extraction of proteins from gels: a brief review. Methods Mol Biol 2012; 869: 403-5. http://dx.doi.org/10.1007/978-1-61779-821-4_33 DOI: https://doi.org/10.1007/978-1-61779-821-4_33
Aebersold RH, Leavitt J, Saavedra RA, Hood LE, Kent SB. Internal amino acid sequence analysis of proteins separated by one- or two-dimensional gel electrophoresis after in situ protease digestion on nitrocellulose. Proc Natl Acad Sci USA 1987; 84: 6970-4. http://dx.doi.org/10.1073/pnas.84.20.6970 DOI: https://doi.org/10.1073/pnas.84.20.6970
Matsudaira P. Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes. J Biol Chem 1987; 262: 10035-8. DOI: https://doi.org/10.1016/S0021-9258(18)61070-1
Hirano H, Komatsu S, Kajiwara H, Takagi Y, Tsunasawa S. Microsequence analysis of the N-terminally blocked proteins immobilized on polyvinylidene difluoride membrane by western blotting. Electrophoresis 1993; 14: 839-46. http://dx.doi.org/10.1002/elps.11501401134 DOI: https://doi.org/10.1002/elps.11501401134
Speicher KD, Kolbas O, Harper S, Speicher DW. Systematic analysis of peptide recoveries from in-gel digestions for protein identifications in proteome studies. J Biomol Tech 2000; 11: 74-86.
Finehout EJ, Lee KH. Comparison of automated in-gel digest methods for femtomole level samples. Electrophoresis 2003; 24: 3508-16. http://dx.doi.org/10.1002/elps.200305615 DOI: https://doi.org/10.1002/elps.200305615
Courchesne PL, Luethy R, Patterson SD. Comparison of in-gel and on-membrane digestion methods at low to sub-pmol level for subsequent peptide and fragment-ion mass analysis using matrix-assisted laser-desorption/ionization mass spectrometry. Electrophoresis 1997; 18: 369-81. http://dx.doi.org/10.1002/elps.1150180311 DOI: https://doi.org/10.1002/elps.1150180311
Schleuder D, Hillenkamp F, Strupat K. IR-MALDI-mass analysis of electroblotted proteins directly from the membrane: comparison of different membranes, application to on-membrane digestion, and protein identification by database searching. Anal Chem 1999; 71: 3238-47. http://dx.doi.org/10.1021/ac9810720 DOI: https://doi.org/10.1021/ac9810720
Methogo RM, Dufresne-Martin G, Leclerc P, Leduc R, Klarskov K. Mass spectrometric peptide fingerprinting of proteins after Western blotting on polyvinylidene fluoride and enhanced chemiluminescence detection. J Proteome Res 2005; 4: 2216-24. http://dx.doi.org/10.1021/pr050014+ DOI: https://doi.org/10.1021/pr050014+
Nakanishi T, Ohtsu I, Furuta M, Ando E, Nishimura O. Direct MS/MS analysis of proteins blotted on membranes by a matrix-assisted laser desorption/ionization-quadrupole ion trap-time-of-flight tandem mass spectrometer. J Proteome Res 2005; 4: 743-7. http://dx.doi.org/10.1021/pr0497834 DOI: https://doi.org/10.1021/pr0497834
Ohtsu I, Nakanisi T, Furuta M, Ando E, Nishimura O. Direct matrix-assisted laser desorption/ionization time-of-flight mass spectrometric identification of proteins on membrane detected by Western blotting and lectin blotting. J Proteome Res 2005; 4: 1391-6. http://dx.doi.org/10.1021/pr050073n DOI: https://doi.org/10.1021/pr050073n
Luque-Garcia JL, Zhou G, Sun TT, Neubert TA. Use of nitrocellulose membranes for protein characterization by matrix-assisted laser desorption/ionization mass spectrometry. Anal Chem 2006; 78: 5102-8. http://dx.doi.org/10.1021/ac060344t DOI: https://doi.org/10.1021/ac060344t
Lin Y, Li Y, Liu Y, Han W, He Q, Li J, et al. Improvement of gel-separated protein identification by DMF-assisted digestion and peptide recovery after electroblotting. Electrophoresis 2009; 30: 3626-35. http://dx.doi.org/10.1002/elps.200900070 DOI: https://doi.org/10.1002/elps.200900070
Luque-Garcia JL, Neubert TA. On-membrane tryptic digestion of proteins for mass spectrometry analysis. Methods Mol Biol 2009; 536: 331-41. http://dx.doi.org/10.1007/978-1-59745-542-8_35 DOI: https://doi.org/10.1007/978-1-59745-542-8_35
Strader MB, Tabb DL, Hervey WJ, Pan C, Hurst GB. Efficient and specific trypsin digestion of microgram to nanogram quantities of proteins in organic-aqueous solvent systems. Anal Chem 2006; 78: 125-34. http://dx.doi.org/10.1021/ac051348l DOI: https://doi.org/10.1021/ac051348l
Wall MJ, Crowell AM, Simms GA, Carey GH, Liu F, Doucette AA. Implications of partial tryptic digestion in organic-aqueous solvent systems for bottom-up proteome analysis. Anal Chim Acta 2011; 703:194-203. http://dx.doi.org/10.1016/j.aca.2011.07.025 DOI: https://doi.org/10.1016/j.aca.2011.07.025
Glatter T, Ludwig C, Ahrné E, Aebersold R, Heck AJ, Schmidt A. Large-scale quantitative assessment of different in-solution protein digestion protocols reveals superior cleavage efficiency of tandem Lys-C/trypsin proteolysis over trypsin digestion. J Proteome Res 2012; 11: 5145-56. http://dx.doi.org/10.1021/pr300273g DOI: https://doi.org/10.1021/pr300273g
Luque-Garcia JL, Zhou G, Spellman DS, Sun TT, Neubert TA. Analysis of electroblotted proteins by mass spectrometry: protein identification after Western blotting. Mol Cell Proteomics 2008; 7: 308-14. http://dx.doi.org/10.1074/mcp.M700415-MCP200 DOI: https://doi.org/10.1074/mcp.M700415-MCP200
Lewis C, Ohlendieck K. Mass spectrometric identification of dystrophin isoform Dp427 by on-membrane digestion of sarcolemma from skeletal muscle. Anal Biochem 2010; 404: 197-203. http://dx.doi.org/10.1016/j.ab.2010.05.017 DOI: https://doi.org/10.1016/j.ab.2010.05.017
Staunton L, Ohlendieck K. Mass spectrometric characterization of the sarcoplasmic reticulum from rabbit skeletal muscle by on-membrane digestion. Protein Pept Lett 2012; 19: 252-63. http://dx.doi.org/10.2174/092986612799363208 DOI: https://doi.org/10.2174/092986612799363208
Steinberg TH, Pretty On Top K, Berggren KN, Kemper C, Jones L, Diwu Z, et al. Rapid and simple single nanogram detection of glycoproteins in polyacrylamide gels and on electroblots. Proteomics 2001; 1: 841-55. http://dx.doi.org/10.1002/1615-9861(200107)1:7<841::AID-PROT841>3.0.CO;2-E DOI: https://doi.org/10.1002/1615-9861(200107)1:7<841::AID-PROT841>3.0.CO;2-E
Hart C, Schulenberg B, Steinberg TH, Leung WY, Patton WF. Detection of glycoproteins in polyacrylamide gels and on electroblots using Pro-Q Emerald 488 dye, a fluorescent periodate Schiff-base stain. Electrophoresis 2003; 24: 588-98. http://dx.doi.org/10.1002/elps.200390069 DOI: https://doi.org/10.1002/elps.200390069
Kimura S, Kameyama A, Nakaya S, Ito H, Narimatsu H. Direct on-membrane glycoproteomic approach using MALDI-TOF mass spectrometry coupled with microdispensing of multiple enzymes. J Proteome Res 2007; 6: 2488-94. http://dx.doi.org/10.1021/pr070067m DOI: https://doi.org/10.1021/pr070067m
Goodman T, Schulenberg B, Steinberg TH, Patton WF. Detection of phosphoproteins on electroblot membranes using a small-molecule organic fluorophore. Electrophoresis 2004; 25: 2533-8. http://dx.doi.org/10.1002/elps.200406008 DOI: https://doi.org/10.1002/elps.200406008
Nakanishi T, Ando E, Furuta M, Tsunasawa S, Nishimura O. Direct on-membrane peptide mass fingerprinting with MALDI-MS of tyrosine-phosphorylated proteins detected by immunostaining. J Chromatogr B Analyt Technol Biomed Life Sci 2007; 847: 24-9. http://dx.doi.org/10.1016/j.jchromb.2006.08.024 DOI: https://doi.org/10.1016/j.jchromb.2006.08.024
Bockus LB, Scofield RH. Phosphoprotein detection on protein electroblot using a phosphate-specific fluorophore. Methods Mol Biol 2009; 536: 385-93. http://dx.doi.org/10.1007/978-1-59745-542-8_39 DOI: https://doi.org/10.1007/978-1-59745-542-8_39
Jiang D, Jia Y, Zhou Y, Jarrett HW. Two-dimensional southwestern blotting and characterization of transcription factors on-blot. J Proteome Res 2009; 8: 3693-701. http://dx.doi.org/10.1021/pr900214p DOI: https://doi.org/10.1021/pr900214p
Jiang D, Jia Y, Jarrett HW. Transcription factor proteomics: identification by a novel gel mobility shift-three-dimensional electrophoresis method coupled with southwestern blot and high-performance liquid chromatography-electrospray-mass spectrometry analysis. J Chromatogr A 2011; 1218: 7003-15. http://dx.doi.org/10.1016/j.chroma.2011.08.023 DOI: https://doi.org/10.1016/j.chroma.2011.08.023
Jarrett HW. Proteomic methodologies to study transcription factor function. Methods Mol Biol 2012; 786: 315-34. http://dx.doi.org/10.1007/978-1-61779-292-2_19 DOI: https://doi.org/10.1007/978-1-61779-292-2_19
Paulo JA, Kadiyala V, Banks PA, Steen H, Conwell DL. Mass spectrometry-based proteomics for translational research: a technical overview. Yale J Biol Med 2012; 85: 59-73.
Terry DE, Umstot E, Desiderio DM. Optimized sample-processing time and peptide recovery for the mass spectrometric analysis of protein digests. J Am Soc Mass Spectrom 2004; 15: 784-94. http://dx.doi.org/10.1016/j.jasms.2004.02.005 DOI: https://doi.org/10.1016/j.jasms.2004.02.005
Domon B, Aebersold R. Mass spectrometry and protein analysis. Science 2006; 312: 212-7. http://dx.doi.org/10.1126/science.1124619 DOI: https://doi.org/10.1126/science.1124619
Zhang G, Annan RS, Carr SA, Neubert TA. Overview of peptide and protein analysis by mass spectrometry. Curr Protoc Protein Sci 2010; Chapter 16: Unit16.1. DOI: https://doi.org/10.1002/0471140864.ps1601s62
Yates JR, Ruse CI, Nakorchevsky A. Proteomics by mass spectrometry: approaches, advances, and applications. Annu Rev Biomed Eng 2009; 11: 49-79. http://dx.doi.org/10.1146/annurev-bioeng-061008-124934 DOI: https://doi.org/10.1146/annurev-bioeng-061008-124934
Gundry RL, White MY, Murray CI, Kane LA, Fu Q, Stanley BA, et al. Preparation of proteins and peptides for mass spectrometry analysis in a bottom-up proteomics workflow. Curr Protoc Mol Biol 2009; Chapter 10: Unit10.25.
Dave KA, Headlam MJ, Wallis TP, Gorman JJ. Preparation and analysis of proteins and peptides using MALDI TOF/TOF mass spectrometry. Curr Protoc Protein Sci 2011; Chapter 16: Unit 16.13. DOI: https://doi.org/10.1002/0471140864.ps1613s63
Ohlendieck K. Proteomics of skeletal muscle differentiation, neuromuscular disorders and fiber aging. Expert Rev Proteomics 2010; 7: 283-96. http://dx.doi.org/10.1586/epr.10.2 DOI: https://doi.org/10.1586/epr.10.2
Gelfi C, Vasso M, Cerretelli P. Diversity of human skeletal muscle in health and disease: contribution of proteomics. J Proteomics 2011; 74: 774-95. http://dx.doi.org/10.1016/j.jprot.2011.02.028 DOI: https://doi.org/10.1016/j.jprot.2011.02.028
Ohlendieck K. Skeletal muscle proteomics: current approaches, technical challenges and emerging techniques. Skelet Muscle 2011; 1(1): 6. http://dx.doi.org/10.1186/2044-5040-1-6 DOI: https://doi.org/10.1186/2044-5040-1-6
Ohlendieck K. Towards an understanding of the dystrophin-glycoprotein complex: linkage between the extracellular matrix and the membrane cytoskeleton in muscle fibers. Eur J Cell Biol 1996; 69: 1-10.
Capes EM, Loaiza R, Valdivia HH. Ryanodine receptors. Skelet Muscle 2011; 1(1): 18. http://dx.doi.org/10.1186/2044-5040-1-18 DOI: https://doi.org/10.1186/2044-5040-1-18
Broderick MJ, Winder SJ. Spectrin, alpha-actinin, and dystrophin. Adv Protein Chem 2005; 70: 203-46. http://dx.doi.org/10.1016/S0065-3233(05)70007-3 DOI: https://doi.org/10.1016/S0065-3233(05)70007-3
Dalkilic I, Kunkel LM. Muscular dystrophies: genes to pathogenesis. Curr Opin Genet Dev 2003; 13: 231-8. http://dx.doi.org/10.1016/S0959-437X(03)00048-0 DOI: https://doi.org/10.1016/S0959-437X(03)00048-0
Ohlendieck K, Ervasti JM, Snook JB, Campbell KP. Dystrophin-glycoprotein complex is highly enriched in isolated skeletal muscle sarcolemma. J Cell Biol 1991; 112: 135-48. http://dx.doi.org/10.1083/jcb.112.1.135 DOI: https://doi.org/10.1083/jcb.112.1.135
Ohlendieck K, Campbell KP. Dystrophin constitutes 5% of membrane cytoskeleton in skeletal muscle. FEBS Lett 1991; 283: 230-4. http://dx.doi.org/10.1016/0014-5793(91)80595-T DOI: https://doi.org/10.1016/0014-5793(91)80595-T
Ohlendieck K, Campbell KP. Dystrophin-associated proteins are greatly reduced in skeletal muscle from mdx mice. J Cell Biol 1991; 115: 1685-94. http://dx.doi.org/10.1083/jcb.115.6.1685 DOI: https://doi.org/10.1083/jcb.115.6.1685
Ohlendieck K, Matsumura K, Ionasescu VV, Towbin JA, Bosch EP, Weinstein SL, et al. Duchenne muscular dystrophy: deficiency of dystrophin-associated proteins in the sarcolemma. Neurology 1993; 43(4): 795-800. http://dx.doi.org/10.1212/WNL.43.4.795 DOI: https://doi.org/10.1212/WNL.43.4.795
Culligan KG, Mackey AJ, Finn DM, Maguire PB, Ohlendieck K. Role of dystrophin isoforms and associated proteins in muscular dystrophy (review). Int J Mol Med 1998; 2: 639-48. DOI: https://doi.org/10.3892/ijmm.2.6.639
Lewis C, Carberry S, Ohlendieck K. Proteomic profiling of x-linked muscular dystrophy. J Muscle Res Cell Motil 2009; 30: 267-9. http://dx.doi.org/10.1007/s10974-009-9197-6 DOI: https://doi.org/10.1007/s10974-009-9197-6
Ge Y, Molloy MP, Chamberlain JS, Andrews PC. Proteomic analysis of mdx skeletal muscle: Great reduction of adenylate kinase 1 expression and enzymatic activity. Proteomics 2003; 3: 1895-903. http://dx.doi.org/10.1002/pmic.200300561 DOI: https://doi.org/10.1002/pmic.200300561
Doran P, Wilton SD, Fletcher S, Ohlendieck K. Proteomic profiling of antisense-induced exon skipping reveals reversal of pathobiochemical abnormalities in dystrophic mdx diaphragm. Proteomics 2009; 9: 671-85. http://dx.doi.org/10.1002/pmic.200800441 DOI: https://doi.org/10.1002/pmic.200800441
Lewis C, Ohlendieck K. Proteomic profiling of naturally protected extraocular muscles from the dystrophin-deficient mdx mouse. Biochem Biophys Res Commun 2010; 396: 1024-9. http://dx.doi.org/10.1016/j.bbrc.2010.05.052 DOI: https://doi.org/10.1016/j.bbrc.2010.05.052
Ohlendieck K. Characterisation of the dystrophin-related protein utrophin in highly purified skeletal muscle sarcolemma vesicles. Biochim Biophys Acta 1996; 1283: 215-22. http://dx.doi.org/10.1016/0005-2736(96)00102-2 DOI: https://doi.org/10.1016/0005-2736(96)00102-2
Yoon JH, Johnson E, Xu R, Martin LT, Martin PT, Montanaro F. Comparative Proteomic Profiling of Dystroglycan-Associated Proteins in Wild Type, mdx, and Galgt2 Transgenic Mouse Skeletal Muscle. J Proteome Res 2012; 11: 4413-24. http://dx.doi.org/10.1021/pr300328r DOI: https://doi.org/10.1021/pr300328r
Murray BE, Froemming GR, Maguire PB, Ohlendieck K. Excitation-contraction-relaxation cycle: role of Ca2+-regulatory membrane proteins in normal, stimulated and pathological skeletal muscle (review). Int J Mol Med 1998; 1: 677-87. DOI: https://doi.org/10.3892/ijmm.1.4.677
Rossi D, Barone V, Giacomello E, Cusimano V, Sorrentino V. The sarcoplasmic reticulum: an organized patchwork of specialized domains. Traffic 2008; 9: 1044-9. http://dx.doi.org/10.1111/j.1600-0854.2008.00717.x DOI: https://doi.org/10.1111/j.1600-0854.2008.00717.x
Leong P, MacLennan DH. Complex interactions between skeletal muscle ryanodine receptor and dihydropyridine receptor proteins. Biochem Cell Biol 1998; 76: 681-94. http://dx.doi.org/10.1139/o98-079 DOI: https://doi.org/10.1139/o98-079
Murray BE, Ohlendieck K. Cross-linking analysis of the ryanodine receptor and alpha1-dihydropyridine receptor in rabbit skeletal muscle triads. Biochem J 1997; 324: 689-96. DOI: https://doi.org/10.1042/bj3240689
Xu KY, Becker LC. Ultrastructural localization of glycolytic enzymes on sarcoplasmic reticulum vesticles. J Histochem Cytochem 1998; 46: 419-27. http://dx.doi.org/10.1177/002215549804600401 DOI: https://doi.org/10.1177/002215549804600401
Ohlendieck K. Proteomics of skeletal muscle glycolysis. Biochim Biophys Acta 2010; 1804: 2089-101. DOI: https://doi.org/10.1016/j.bbapap.2010.08.001
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