Application of fluorescence two-dimensional difference in-gel electrophoresis as a proteomic biomarker discovery tool in muscular dystrophy research

Biology

Volumn 2, Issue 4, 2013, Pages 1438-1464

  Carberry, Steven ^a   Zweyer, Margit ^b   Swandulla, Dieter ^b   Ohlendieck, Kay ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^b UNIVERSITY OF BONN   (Germany)

Author keywords

CvHsp; Diaphragm; DIGE; Duchenne muscular dystrophy; Dystrophinopathy; Gel electrophoresis; HspB7; Mdx; Mouse model; Parvalbumin

Indexed keywords

EID: 84897566332     PISSN: None     EISSN: 20797737     Source Type: Journal    
DOI: 10.3390/biology2041438     Document Type: Article

References (85)

1. Isfort, R.J. Proteomic analysis of striated muscle. J. Chromatogr. B 2002, 771, 155-165.
2. Ohlendieck, K. Proteomics of skeletal muscle differentiation, neuromuscular disorders and fiber aging. Expert Rev. Proteomics 2010, 7, 283-296.
3. Gelfi, C.; Vasso, M.; Cerretelli, P. Diversity of human skeletal muscle in health and disease: Contribution of proteomics. J. Proteomics 2011, 74, 774-795.
4. Ohlendieck, K. Proteomic identification of biomarkers of skeletal muscle disorders. Biomark. Med. 2013, 7, 169-186.
5. Chevalier, F. Highlights on the capacities of "Gel-based" proteomics. Proteome Sci. 2010, 8, 23.
6. Rabilloud, T.; Chevallet, M.; Luche, S.; Lelong, C. Two-dimensional gel electrophoresis in proteomics: Past, present and future. J. Proteomics 2010, 73, 2064-2077.
7. Westermeier, R.; Görg, A. Two-dimensional electrophoresis in proteomics. Methods Biochem. Anal. 2011, 54, 411-439.
8. Ohlendieck, K. Skeletal muscle proteomics: Current approaches, technical challenges and emerging techniques. Skelet. Muscle 2011, 1, 6.
9. Parker, K.C.; Walsh, R.J.; Salajegheh, M.; Amato, A.A.; Krastins, B.; Sarracino, D.A.; Greenberg, S.A. Characterization of human skeletal muscle biopsy samples using shotgun proteomics. J. Proteome Res. 2009, 8, 3265-3277.
10. Holland, A.; Ohlendieck, K. Proteomic profiling of the contractile apparatus from skeletal muscle. Expert Rev. Proteomics 2013, 10, 239-257.
11. Maughan, D.W.; Henkin, J.A.; Vigoreaux, J.O. Concentrations of glycolytic enzymes and other cytosolic proteins in the diffusible fraction of a vertebrate muscle proteome. Mol. Cell. Proteomics 2005, 4, 1541-1549.
12. Højlund, K.; Yi, Z.; Hwang, H.; Bowen, B.; Lefort, N.; Flynn, C.R.; Langlais, P.; Weintraub, S.T.; Mandarino, L.J. Characterization of the human skeletal muscle proteome by one-dimensional gel electrophoresis and HPLC-ESI-MS/MS. Mol. Cell. Proteomics 2008, 7, 257-267.
13. Nishimura, R.N.; Sharp, F.R. Heat shock proteins and neuromuscular disease. Muscle Nerve 2005, 32, 693-709.
14. Choi, Y.S. Reaching for the deep proteome: Recent nano liquid chromatography coupled with tandem mass spectrometry-based studies on the deep proteome. Arch. Pharm. Res. 2012, 35, 1861-1870.
15. Hamano, K.; Takeya, T.; Iwasaki, N.; Okoshi, N.; Fukubayashi, T.; Kirinoki, M.; Yao, Y.; Hirabayashi, T.; Takita, H. Analysis of dystrophin in muscular diseases by two-dimensional gel electrophoresis using agarose gels in the first dimension. Acta Neurol. Belg. 1996, 96, 102-107.
16. Oh-Ishi, M.; Maeda, T. Disease proteomics of high-molecular-mass proteins by two-dimensional gel electrophoresis with agarose gels in the first dimension (Agarose 2-DE). J. Chromatogr. B 2007, 849, 211-222.
17. Reisinger, V.; Eichacker, L.A. Isolation of membrane protein complexes by blue native electrophoresis. Methods Mol. Biol. 2008, 424, 423-431.
18. Wittig, I.; Schägger, H. Native electrophoretic techniques to identify protein-protein interactions. Proteomics 2009, 9, 5214-5223.
19. Froemming, G.R.; Murray, B.E.; Ohlendieck, K. Self-aggregation of triadin in the sarcoplasmic reticulum of rabbit skeletal muscle. Biochim. Biophys. Acta 1999, 1418, 197-205.
20. Brennan, J.P.; Wait, R.; Begum, S.; Bell, J.R.; Dunn, M.J.; Eaton, P. Detection and mapping of widespread intermolecular protein disulfide formation during cardiac oxidative stress using proteomics with diagonal electrophoresis. J. Biol. Chem. 2004, 279, 41352-41360.
21. Fraterman, S.; Zeiger, U.; Khurana, T.S.; Rubinstein, N.A.; Wilm, M. Combination of peptide OFFGEL fractionation and label-free quantitation facilitated proteomics profiling of extraocular muscle. Proteomics 2007, 7, 3404-3416.
22. Gannon, J.; Ohlendieck, K. Subproteomic analysis of basic proteins in aged skeletal muscle following offgel pre-fractionation. Mol. Med. Rep. 2012, 5, 993-1000.
23. Staunton, L.; Ohlendieck, K. Mass spectrometric characterization of the sarcoplasmic reticulum from rabbit skeletal muscle by on-membrane digestion. Protein Pept. Lett. 2012, 19, 252-263.
24. Ohlendieck, K. On-membrane digestion technology for muscle proteomics. J. Membr. Sep. Technol. 2013, 2, 1-12.
25. Guevel, L.; Lavoie, J.R.; Perez-Iratxeta, C.; Rouger, K.; Dubreil, L.; Feron, M.; Talon, S.; Brand, M.; Megeney, L.A. Quantitative proteomic analysis of dystrophic dog muscle. J. Proteome Res. 2011, 10, 2465-2478.
26. Rayavarapu, S.; Coley, W.; Cakir, E.; Jahnke, V.; Takeda, S.; Aoki, Y.; Grodish-Dressman, H.; Jaiswal, J.K.; Hoffman, E.P.; Brown, K.J.; et al. Identification of disease specific pathways using in vivo SILAC proteomics in dystrophin deficient mdx mouse. Mol. Cell. Proteomics 2013, 12, 1061-1073.
27. Duguez, S.; Duddy, W.; Johnston, H.; Lainé, J.; Le Bihan, M.C.; Brown, K.J.; Bigot, A.; Hathout, Y.; Butler-Browne, G.; Partridge, T. Dystrophin deficiency leads to disturbance of LAMP1-vesicle-associated protein secretion. Cell. Mol. Life Sci. 2013, 70, 2159-2174.
28. Malm, C.; Hadrevi, J.; Bergström, S.A.; Pedrosa-Domellöf, F.; Antti, H.; Svensson, M.; Frängsmyr, L. Evaluation of 2-D DIGE for skeletal muscle: Protocol and repeatability. Scand. J. Clin. Lab. Invest. 2008, 68, 793-800.
29. Unlü, M.; Morgan, M.E.; Minden, J.S. Difference gel electrophoresis: A single gel method for detecting changes in protein extracts. Electrophoresis 1997, 18, 2071-2077.
30. Alban, A.; David, S.O.; Bjorkesten, L.; Andersson, C.; Sloge, E.; Lewis, S.; Currie, I. 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.
31. Viswanathan, S.; Unlü, M.; Minden, J.S. Two-dimensional difference gel electrophoresis. Nat. Protoc. 2006, 1, 1351-1358.
32. Minden, J.S. Two-dimensional difference gel electrophoresis. Methods Mol. Biol. 2012, 869, 287-304.
33. Tonge, R.; Shaw, J.; Middleton, B.; Rowlinson, R.; Rayner, S.; Young, J.; Pognan, F.; Hawkins, E.; Currie, I.; Davison, M. Validation and development of fluorescence two-dimensional differential gel electrophoresis proteomics technology. Proteomics 2001, 1, 377-396.
34. Marouga, R.; David, S.; Hawkins, E. The development of the DIGE system: 2D fluorescence difference gel analysis technology. Anal. Bioanal. Chem. 2005, 382, 669-678.
35. Karp, N.A.; Kreil, D.P.; Lilley, K.S. Determining a significant change in protein expression with DeCyder during a pair-wise comparison using two-dimensional difference gel electrophoresis. Proteomics 2004, 4, 1421-1432.
36. Karp, N.A.; Lilley, K.S. Maximising sensitivity for detecting changes in protein expression: Experimental design using minimal CyDyes. Proteomics 2005, 5, 3105-3115.
37. 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, 4610-4621.
38. Corzett, T.H.; Fodor, I.K.; Choi, M.W.; Walsworth, V.L.; Chromy, B.A.; Turteltaub, K.W.; McCutchen-Maloney, S.L. Statistical analysis of the experimental variation in the proteomic characterization of human plasma by two-dimensional difference gel electrophoresis. J. Proteome Res. 2006, 5, 2611-2619.
39. Guenet, J.L. Animal models of human genetic diseases: Do they need to be faithful to be useful? Mol. Genet. Genomics 2011, 286, 1-20.
40. Vainzof, M.; Ayub-Guerrieri, D.; Onofre, P.C.; Martins, P.C.; Lopes, V.F.; Zilberztajn, D.; Maia, L.S.; Sell, K.; Yamamoto, L.U. Animal models for genetic neuromuscular diseases. J. Mol. Neurosci. 2008, 34, 241-248.
41. Doran, P.; O'Connell, K.; Gannon, J.; Ohlendieck, K. Proteomic profiling of animal models mimicking skeletal muscle disorders. Proteomics Clin. Appl. 2007, 1, 1169-1184.
42. Koenig, M.; Hoffman, E.P.; Bertelson, C.J.; Monaco, A.P.; Feener, C.; Kunkel, L.M. Complete cloning of the Duchenne muscular dystrophy (DMD) cDNA and preliminary genomic organization of the DMD gene in normal and affected individuals. Cell 1987, 50, 509-517.
43. Nakamura, A.; Takeda, S. Mammalian models of Duchenne Muscular Dystrophy: Pathological characteristics and therapeutic applications. J. Biomed. Biotechnol. 2011, 2011, Article ID 184393.
44. Ng, R.; Banks, G.B.; Hall, J.K.; Muir, L.A.; Ramos, J.N.; Wicki, J.; Odom, G.L.; Konieczny, P.; Seto, J.; Chamberlain, J.R.; et al. Animal models of muscular dystrophy. Prog. Mol. Biol. Transl. Sci. 2012, 105, 83-111.
45. Banks, G.B.; Chamberlain, J.S. The value of mammalian models for Duchenne muscular dystrophy in developing therapeutic strategies. Curr. Top. Dev. Biol. 2008, 84, 431-453.
46. Kornegay, J.N.; Bogan, J.R.; Bogan, D.J.; Childers, M.K.; Li, J.; Nghiem, P.; Detwiler, D.A.; Larsen, C.A.; Grange, R.W.; Bhavaraju-Sanka, R.K.; et al. Canine models of Duchenne muscular dystrophy and their use in therapeutic strategies. Mamm. Genome 2012, 23, 85-108.
47. Ge, Y.; Molloy, M.P.; Chamberlain, J.S.; Andrews, P.C. Proteomic analysis of mdx skeletal muscle: Great reduction of adenylate kinase 1 expression and enzymatic activity. Proteomics 2003, 3, 1895-1903.
48. Holland, A.; Dowling, P.; Zweyer, M.; Swandulla, D.; Henry, M.; Clynes, M.; Ohlendieck, K. Proteomic profiling of cardiomyopathic tissue from the aged mdx model of Duchenne muscular dystrophy reveals a drastic decrease in laminin, nidogen and annexin. Proteomics 2013, 13, 2312-2323.
49. Doran, P.; Wilton, S.D.; Fletcher, S.; Ohlendieck, K. Proteomic profiling of antisense-induced exon skipping reveals reversal of pathobiochemical abnormalities in dystrophic mdx diaphragm. Proteomics 2009, 9, 671-685.
50. Lewis, C.; Carberry, S.; Ohlendieck, K. Proteomic profiling of x-linked muscular dystrophy. J. Muscle Res. Cell Motil. 2009, 30, 267-269.
51. Lefaucheur, J.P.; Pastoret, C.; Sebille, A. Phenotype of dystrophinopathy in old mdx mice. Anat. Rec. 1995, 242, 70-76.
52. 2+ homeostasis during fatigue. Exp. Physiol. 2010, 95, 641-656.
53. Chamberlain, J.S.; Metzger, J.; Reyes, M.; Townsend, D.; Faulkner, J.A. Dystrophin-deficient mdx mice display a reduced life span and are susceptible to spontaneous rhabdomyosarcoma. FASEB J. 2007, 21, 2195-2204.
54. Mouisel, E.; Vignaud, A.; Hourde, C.; Butler-Browne, G.; Ferry, A. Muscle weakness and atrophy are associated with decreased regenerative capacity and changes in mTOR signaling in skeletal muscles of venerable (18-24-month-old) dystrophic mdx mice. Muscle Nerve 2010, 41, 809-818.
55. Carberry, S.; Zweyer, M.; Swandulla, D.; Ohlendieck, K. Proteomics reveals drastic increase of extracellular matrix proteins collagen and dermatopontin in aged mdx diaphragm muscle. Int. J. Mol. Med. 2012, 30, 229-234.
56. Carberry, S.; Zweyer, M.; Swandulla, D.; Ohlendieck, K. Profiling of age-related changes in the tibialis anterior muscle proteome of the mdx mouse model of dystrophinopathy. J. Biomed. Biotechnol. 2012, 2012, 691641.
57. Sicinski, P.; Geng, Y.; Ryder-Cook, A.S.; Barnard, E.A.; Darlison, M.G.; Barnard, P.J. The molecular basis of muscular dystrophy in the mdx mouse: A point mutation. Science 1989, 244, 1578-1580.
58. Stedman, H.H.; Sweeney, H.L.; Shrager, J.B.; Maguire, H.C.; Panettieri, R.A.; Petrof, B.; Narusawa, M.; Leferovich, J.M.; Sladky, J.T.; Kell, A.M. The mdx mouse diaphragm reproduces the degenerative changes of Duchenne muscular dystrophy. Nature 1991, 352, 536-539.
59. Staunton, L.; Jockusch, H.; Ohlendieck, K. Proteomic analysis of muscle affected by motor neuron degeneration: The wobbler mouse model of amyotrophic lateral sclerosis. Biochem. Biophys. Res. Commun. 2011, 406, 595-600.
60. O'Connell, K.; Ohlendieck, K. Proteomic DIGE analysis of the mitochondria-enriched fraction from aged rat skeletal muscle. Proteomics 2009, 9, 5509-5524.
61. Kang, Y.; Techanukul, T.; Mantalaris, A.; Nagy, J.M. Comparison of three commercially available DIGE analysis software packages: Minimal user intervention in gel-based proteomics. J. Proteome Res. 2009, 8, 1077-1084.
62. Carberry, S.; Ohlendieck, K. Gel electrophoresis-based proteomics of senescent tissues. Methods Mol. Biol. 2013, 1048, 229-246.
63. Staunton, L.; Jockusch, H.; Wiegand, C.; Albrecht, T.; Ohlendieck, K. Identification of secondary effects of hyperexcitability by proteomic profiling of myotonic mouse muscle. Mol. Biosyst. 2011, 7, 2480-2489.
64. PANTHER Gene List Analysis. Available online: http://pantherdb.org/ (accessed on 15 November 2013).
65. Mi, H.; Muruganujan, A.; Thomas, P.D. PANTHER in 2013: Modeling the evolution of gene function, and other gene attributes, in the context of phylogenetic trees. Nucleic Acids Res. 2013, 41, D377-D386.
66. STRING Functional Protein Association Network. Available online: http://string-db.org/ (accessed on 17 November 2013).
67. Franceschini, A.; Szklarczyk, D.; Frankild, S.; Kuhn, M.; Simonovic, M.; Roth, A.; Lin, J.; Minguez, P.; Bork, P.; von Mering, C.; et al. STRING v9.1: Protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res. 2013, 41, D808-D815.
68. Staunton, L.; Zweyer, M.; Swandulla, D.; Ohlendieck, K. Mass spectrometry-based proteomic analysis of middle-aged vs. aged vastus lateralis reveals increased levels of carbonic anhydrase isoform 3 in senescent human skeletal muscle. Int. J. Mol. Med. 2012, 30, 723-733.
69. Holland, A.; Carberry, S.; Ohlendieck, K. Proteomics of the dystrophin-glycoprotein complex and dystrophinopathy. Curr. Protein Pep. Sci. 2013, in press.
70. Culligan, K.; Banville, N.; Dowling, P.; Ohlendieck, K. Drastic reduction of calsequestrin-like proteins and impaired calcium binding in dystrophic mdx muscle. J. Appl. Physiol. 2002, 92, 435-445.
71. Davey, J.W.; Hohenlohe, P.A.; Etter, P.D.; Boone, J.Q.; Catchen, J.M.; Blaxter, M.L. Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat. Rev. Genet. 2011, 12, 499-510.
72. Pontén, F.; Schwenk, J.M.; Asplund, A.; Edqvist, P.H. The Human Protein Atlas as a proteomic resource for biomarker discovery. J. Intern. Med. 2011, 270, 428-446.
73. Theodoridis, G.A.; Gika, H.G.; Want, E.J.; Wilson, I.D. Liquid chromatography-mass spectrometry based global metabolite profiling: A review. Anal. Chim. Acta 2012, 711, 7-16.
74. Cox, J.; Mann, M. Quantitative, high-resolution proteomics for data-driven systems biology. Annu. Rev. Biochem. 2011, 80, 273-299.
75. Stastna, M.; van Eyk, J.E. Secreted proteins as a fundamental source for biomarker discovery. Proteomics 2012, 12, 722-735.
76. Mallick, P.; Kuster, B. Proteomics: A pragmatic perspective. Nat. Biotechnol. 2010, 28, 695-709.
77. Graham, K.M.; Singh, R.; Millman, G.; Malnassy, G.; Gatti, F.; Bruemmer, K.; Stefanski, C.; Curtis, H.; Sesti, J.; Carlson, C.G. Excessive collagen accumulation in dystrophic (mdx) respiratory musculature is independent of enhanced activation of the NF-kappaB pathway. J. Neurol. Sci. 2010, 294, 43-50.
78. Wang, J.; Pantopoulos, K. Regulation of cellular iron metabolism. Biochem. J. 2011, 434, 365-381.
79. Kuznetsov, A.V.; Winkler, K.; Wiedemann, F.R.; von Bossanyi, P.; Dietzmann, K.; Kunz, W.S. Impaired mitochondrial oxidative phosphorylation in skeletal muscle of the dystrophin-deficient mdx mouse. Mol. Cell. Biochem. 1998, 183, 87-96.
80. Percival, J.M.; Siegel, M.P.; Knowels, G.; Marcinek, D.J. Defects in mitochondrial localization and ATP synthesis in the mdx mouse model of Duchenne muscular dystrophy are not alleviated by PDE5 inhibition. Hum. Mol. Genet. 2013, 22, 153-167.
81. Doran, P.; Dowling, P.; Donoghue, P.; Buffini, M.; Ohlendieck, K. Reduced expression of regucalcin in young and aged mdx diaphragm indicates abnormal cytosolic calcium handling in dystrophin-deficient muscle. Biochim. Biophys. Acta 2006, 1764, 773-785.
82. 2+-binding proteins demonstrates decreased calsequestrin expression in dystrophic mouse skeletal muscle. Eur. J. Biochem. 2004, 271, 3943-3952.
83. Carberry, S.; Brinkmeier, H.; Zhang, Y.; Winkler, C.K.; Ohlendieck, K. Comparative proteomic profiling of soleus, extensor digitorum longus, flexor digitorum brevis and interosseus muscle from the mdx mouse model of Duchenne muscular dystrophy. Int. J. Mol. Med. 2013, 32, 544-556.
84. Gardan-Salmon, D.; Dixon, J.M.; Lonergan, S.M.; Selsby, J.T. Proteomic assessment of the acute phase of dystrophin deficiency in mdx mice. Eur. J. Appl. Physiol. 2011, 111, 2763-2773.
85. Carberry, S.; Zweyer, M.; Swandulla, D.; Ohlendieck, K. Comparative proteomic analysis of the contractile protein-depleted fraction from normal versus dystrophic skeletal muscle. Anal. Biochem. 2013, doi:10.1016/j.ab.2013.08.004.