Proteomic profiling of cardiomyopathic tissue from the aged mdx model of Duchenne muscular dystrophy reveals a drastic decrease in laminin, nidogen and annexin

Proteomics

Volumn 13, Issue 15, 2013, Pages 2312-2323

  Holland, Ashling ^a   Dowling, Paul ^b   Zweyer, Margit ^c   Swandulla, Dieter ^c   Henry, Michael ^b   Clynes, Martin ^b   Ohlendieck, Kay ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^b DUBLIN CITY UNIVERSITY   (Ireland)

^c UNIVERSITY OF BONN   (Germany)

Author keywords

Animal proteomics; Annexin; Cardiomyopathy; Laminin; Muscular dystrophy; Nidogen

Indexed keywords

2,4 DIENOYL COENZYME A REDUCTASE (NADPH); 3 HYDROXYACYL COENZYME A DEHYDROGENASE; 6 PHOSPHOFRUCTOKINASE; ACETYL COENZYME A ACETYLTRANSFERASE; ACETYL COENZYME A ACYLTRANSFERASE; ALDEHYDE REDUCTASE; ALPHA ACTIN; ANNEXIN; BETA ACTIN; BIGLYCAN; CALPHOBINDIN II; CALRETICULIN; CATALASE; DYSTROPHIN; ENTACTIN; GLUCOSE 6 PHOSPHATE ISOMERASE; GLUTAMATE DEHYDROGENASE; GLUTATHIONE TRANSFERASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; IMMUNOGLOBULIN; ISOCITRATE DEHYDROGENASE; LAMININ; MYOGLOBIN; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; OXOGLUTARATE DEHYDROGENASE; PROTEIN DISULFIDE ISOMERASE; SELENIUM BINDING PROTEIN; TRANSFERRIN; TRIOSEPHOSPHATE ISOMERASE; VIMENTIN;

AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; CARDIOMYOPATHY; CONTROLLED STUDY; CYTOSKELETON; DUCHENNE MUSCULAR DYSTROPHY; IMMUNOBLOTTING; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLISM; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; UNINDEXED SEQUENCE; WILD TYPE;

EID: 84881229184     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201200578     Document Type: Article

References (68)

1. Dalkilic, I., Kunkel, L. M., Muscular dystrophies: genes to pathogenesis. Curr. Opin. Genet. Dev. 2003, 13, 231-238.
2. Lewis, C., Carberry, S., Ohlendieck, K., Proteomic profiling of x-linked muscular dystrophy. J. Muscle Res. Cell. Motil. 2009, 30, 267-279.
3. Morrison, L. A., Dystrophinopathies. Handb. Clin. Neurol. 2011, 101, 11-39.
4. Hermans, M. C., Pinto, Y. M., Merkies, I. S., de Die-Smulders, C. E. et al., Hereditary muscular dystrophies and the heart. Neuromuscul. Disord. 2010, 20, 479-492.
5. Verhaert, D., Richards, K., Rafael-Fortney, J. A., Raman, S. V., Cardiac involvement in patients with muscular dystrophies: magnetic resonance imaging phenotype and genotypic considerations. Circ. Cardiovasc. Imaging. 2011, 4, 67-76.
6. Judge, D. P., Kass, D. A., Thompson, W. R., Wagner, K. R., Pathophysiology and therapy of cardiac dysfunction in Duchenne muscular dystrophy. Am. J. Cardiovasc. Drugs. 2011, 11, 287-294.
7. Romfh, A., McNally, E. M., Cardiac assessment in Duchenne and Becker muscular dystrophies. Curr. Heart Fail Rep. 2010, 7, 212-218.
8. Kaspar, R. W., Allen, H. D., Montanaro, F., Current understanding and management of dilated cardiomyopathy in Duchenne and Becker muscular dystrophy. J. Am. Acad. Nurse Pract. 2009, 21, 241-249.
9. Cox, G. F., Kunkel, L. M., Dystrophies and heart disease. Curr. Opin. Cardiol. 1997, 12, 329-343.
10. Finsterer, J., Stöllberger, C., The heart in human dystrophinopathies. Cardiology 2003, 99, 1-19.
11. 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.
12. Rayavarapu, S., Coley, W., Cakir, E., Jahnke, V. et al., Identification of disease specific pathways using in vivo SILAC proteomics in dystrophin deficient mdx mouse. Mol. Cell. Proteomics 2013, 12, 1061-1073.
13. Sicinski, P., Geng, Y., Ryder-Cook, A. S., Barnard, E. A. et al., The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science 1989, 244, 1578-1580.
14. Johnson, E. K., Zhang, L., Adams, M. E., Phillips, A. et al., Proteomic analysis reveals new cardiac-specific dystrophin-associated proteins. PLoS One 2012, 7, e43515.
15. Gulston, M. K., Rubtsov, D. V., Atherton, H. J., Clarke, K. et al., A combined metabolomic and proteomic investigation of the effects of a failure to express dystrophin in the mouse heart. J. Proteome Res. 2008, 7, 2069-2077.
16. Lewis, C., Jockusch, H., Ohlendieck, K., Proteomic profiling of the dystrophin-deficient mdx heart reveals drastically altered levels of key metabolic and contractile proteins. J. Biomed. Biotechnol. 2010, 2010, 648501.
17. Shioi, T., Inuzuka, Y., Aging as a substrate of heart failure. J. Cardiol. 2012, 60, 423-428.
18. Richardson, M. R., Lai, X., Mason, S. B., Miller, S. J. et al., Differential protein expression during aging in ventricular myocardium of Fischer 344 x Brown Norway hybrid rats. Exp. Gerontol. 2008, 43, 909-918.
19. Dai, Q., Escobar, G. P., Hakala, K. W., Lambert, J. M. et al., The left ventricle proteome differentiates middle-aged and old left ventricles in mice. J. Proteome Res. 2008, 7, 756-765.
20. Grant, J. E., Bradshaw, A. D., Schwacke, J. H., Baicu, C. F. et al., Quantification of protein expression changes in the aging left ventricle of Rattus norvegicus. J. Proteome Res. 2009, 8, 4252-4263.
21. Carberry, S., Zweyer, M., Swandulla, D., Ohlendieck, K., Proteomics reveals drastic increase of extracellular matrix proteins collagen and dermatopontin in the aged mdx diaphragm model of Duchenne muscular dystrophy. Int. J. Mol. Med. 2012, 30, 229-234.
22. 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.
23. Meleady, P., Gallagher, M., Clarke, C., Henry, M. et al., Impact of miR-7 over-expression on the proteome of Chinese hamster ovary cells. J. Biotechnol. 2012, 160, 251-262.
24. Meleady, P., Hoffrogge, R., Henry, M., Rupp, O. et al. Utilization and evaluation of CHO-specific sequence databases for mass spectrometry based proteomics. Biotechnol. Bioeng. 2012, 109, 1386-1394.
25. O'Connell, K., Ohlendieck, K., Proteomic DIGE analysis of the mitochondria-enriched fraction from aged rat skeletal muscle. Proteomics 2009, 9, 5509-5524.
26. Partridge, T. A., Impending therapies for Duchenne muscular dystrophy. Curr. Opin. Neurol. 2011, 24, 415-422.
27. Ameen, V., Robson, L. G., Experimental models of Duchenne muscular dystrophy: relationship with cardiovascular disease. Open Cardiovasc. Med. J. 2010, 4, 265-77.
28. De Luca, A., Pre-clinical drug tests in the mdx mouse as a model of dystrophinopathies: an overview. Acta Myol. 2012, 31, 40-47.
29. Durbeej, M., Campbell, K. P., Muscular dystrophies involving the dystrophin-glycoprotein complex: an overview of current mouse models. Curr. Opin. Genet. Dev. 2002, 12, 349-361.
30. Bia, B. L., Cassidy, P. J., Young, M. E., Rafael, J. A. et al., Decreased myocardial nNOS, increased iNOS and abnormal ECGs in mouse models of Duchenne muscular dystrophy. J. Mol. Cell. Cardiol. 1999, 31, 1857-1862.
31. Lohan, J., Culligan, K., Ohlendieck, K., Deficiency in cardiac dystrophin affects the abundance of the alpha/beta-dystroglycan complex. J. Biomed. Biotechnol. 2005, 2005, 28-36.
32. 2+-binding proteins calsequestrin and sarcalumenin in dystrophin-deficient cardiac muscle. Biochim. Biophys. Acta. 2004, 1689, 252-258.
33. 2+ signalling and reactive oxygen species-generating pathways. Cardiovasc. Res. 2008, 77, 766-773.
34. 2+ influx into dystrophic mdx cardiomyocytes. Cell Calcium 2009, 46, 114-121.
35. Au, C. G., Butler, T. L., Sherwood, M. C., Egan, J. R. et al., Increased connective tissue growth factor associated with cardiac fibrosis in the mdx mouse model of dystrophic cardiomyopathy. Int. J. Exp. Pathol. 2011, 92, 57-65.
36. Koenig, X., Dysek, S., Kimbacher, S., Mike, A. K. et al., Voltage-gated ion channel dysfunction precedes cardiomyopathy development in the dystrophic heart. PLoS One 2011, 6, e20300.
37. Barnabei, M. S., Metzgerm, J. M., Ex vivo stretch reveals altered mechanical properties of isolated dystrophin-deficient hearts. PLoS One 2012, 7, e32880.
38. Stuckey, D. J., Carr, C. A., Camelliti, P., Tyler, D. J. et al., In vivo MRI characterization of progressive cardiac dysfunction in the mdx mouse model of muscular dystrophy. PLoS One 2012, 7, e28569.
39. Quinlan, J. G., Hahn, H. S., Wong, B. L., Lorenz, S. N. et al., Evolution of the mdx mouse cardiomyopathy: physiological and morphological findings. Neuromuscul. Disord. 2004, 14, 491-496.
40. Spurney, C. F., Knoblach, S., Pistilli, E. E., Nagaraju, K. et al., Dystrophin-deficient cardiomyopathy in mouse: expression of Nox4 and Lox are associated with fibrosis and altered functional parameters in the heart. Neuromuscul. Disord. 2008, 18, 371-381.
41. Van Erp, C., Loch, D., Laws, N., Trebbin, A. et al., Timeline of cardiac dystrophy in 3-18-month-old MDX mice. Muscle Nerve 2010, 42, 504-513.
42. Klietsch, R., Ervasti, J. M., Arnold, W., Campbell, K. P. et al., Dystrophin-glycoprotein complex and laminin colocalize to the sarcolemma and transverse tubules of cardiac muscle. Circ. Res. 1993, 72, 349-360.
43. Zhao, P., Sharma, A. C., Ren, J., Pathogenesis and therapy of autoimmunity-induced dilated cardiomyopathy. Front. Biosci. 2009, 14, 1708-1715.
44. Szoke, D., Panteghini, M., Diagnostic value of transferrin. Clin. Chim. Acta. 2012, 413, 1184-1189.
45. Wang, J., Pantopoulos, K., Regulation of cellular iron metabolism. Biochem. J. 2011, 434, 365-381.
46. Crichton, R. R., Declercq, J. P., X-ray structures of ferritins and related proteins. Biochim. Biophys. Acta 2010, 1800, 706-718.
47. Harrison, P. M., Arosio, P., The ferritins: molecular properties, iron storage function and cellular regulation. Biochim. Biophys. Acta 1996, 1275, 161-203.
48. Board, P. G., Menon, D., Glutathione transferases, regulators of cellular metabolism and physiology. Biochim. Biophys. Acta. 2013, 1830, 3267-3288.
49. Dulhunty, A. F., Hewawasam, R., Liu, D., Casarotto, M. G. et al., Regulation of the cardiac muscle ryanodine receptor by glutathione transferases. Drug Metab. Rev. 2011, 43, 236-252.
50. Haycock, J. W., MacNeil, S., Jones, P., Harris, J. B. et al., Oxidative damage to muscle protein in Duchenne muscular dystrophy. Neuroreport 1996, 8, 357-361.
51. Hauser, E., Höger, H., Bittner, R., Widhalm, K. et al., Oxyradical damage and mitochondrial enzyme activities in the mdx mouse. Neuropediatrics 1995, 26, 260-272.
52. Renjini, R., Gayathri, N., Nalini, A., Srinivas Bharath, M. M. Oxidative damage in muscular dystrophy correlates with the severity of the pathology: role of glutathione metabolism. Neurochem. Res. 2012, 37, 885-898.
53. Tidball, J. G., Wehling-Henricks, M., The role of free radicals in the pathophysiology of muscular dystrophy. J. Appl. Physiol. 2007, 102, 1677-1686.
54. Williams, I.A., Allen, D. G., The role of reactive oxygen species in the hearts of dystrophin-deficient mdx mice. Am. J. Physiol. Heart. Circ. Physiol. 2007, 293, H1969-H1977.
55. Selsby, J. T., Increased catalase expression improves muscle function in mdx mice. Exp. Physiol. 2011, 96, 194-202.
56. Domogatskaya, A., Rodin, S., Tryggvason, K., Functional diversity of laminins. Annu. Rev. Cell Dev. Biol. 2012, 28, 523-553.
57. Carmignac, V., Durbeej, M., Cell-matrix interactions in muscle disease. J. Pathol. 2012, 226, 200-218.
58. Dziadek, M., Role of laminin-nidogen complexes in basement membrane formation during embryonic development. Experientia 1995, 51, 901-913.
59. Ho, M.S., Böse, K., Mokkapati, S., Nischt, R. et al., Nidogens-extracellular matrix linker molecules. Microsc. Res. Tech. 2008, 71, 387-395.
60. Kruegel, J., Miosge, N., Basement membrane components are key players in specialized extracellular matrices. Cell. Mol. Life Sci. 2010, 67, 2879-2895.
61. Bizzarro, V., Petrella, A., Parente, L., Annexin A1: novel roles in skeletal muscle biology. J. Cell Physiol. 2012, 227, 3007-3015.
62. 2+ handling in the heart. Cardiovasc. Res. 2005, 65, 793-802.
63. Selbert, S., Fischer, P., Menke, A., Jockusch, H. et al., Annexin VII relocalization as a result of dystrophin deficiency. Exp. Cell Res. 1996, 222, 199-208.
64. Broers, J. L., Ramaekers, F. C., Bonne, G., Yaou, R. B. et al., Nuclear lamins: laminopathies and their role in premature ageing. Physiol. Rev. 2006, 86, 967-1008.
65. Reddy, S., Comai, L., Lamin A, farnesylation and aging. Exp. Cell Res. 2012, 318, 1-7.
66. Zhang, W., ten Hove, M., Schneider, J. E., Stuckey, D. J. et al., Abnormal cardiac morphology, function and energy metabolism in the dystrophic mdx mouse: an MRI and MRS study. J. Mol. Cell. Cardiol. 2008, 45, 754-760.
67. Kuznetsov, A. V., Winkler, K., Wiedemann, F. R., von Bossanyi, P. et al., Impaired mitochondrial oxidative phosphorylation in skeletal muscle of the dystrophin-deficient mdx mouse. Mol. Cell. Biochem. 1998, 183, 87-96.
68. 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.