Comparative proteomic profiling of soleus, extensor digitorum longus, flexor digitorum brevis and interosseus muscles from the mdx mouse model of Duchenne muscular dystrophy

International Journal of Molecular Medicine

Volumn 32, Issue 3, 2013, Pages 544-556

  Carberry, Steven ^a   Brinkmeier, Heinrich ^b   Zhang, Yaxin ^b   Winkler, Claudia K ^b   Ohlendieck, Kay ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^b UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

Dystrophinopathy; Flexor digitorum brevis muscle; Interosseus muscle; Muscle dystrophic x linked; Muscular dystrophy

Indexed keywords

ACTIN; DESMIN; DYSTROPHIN; FRUCTOSE BISPHOSPHATE ALDOLASE; FRUCTOSE BISPHOSPHATE ALDOLASE ISOENZYME; GLUTATHIONE TRANSFERASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GLYCOGEN PHOSPHORYLASE; LEUKOCYTE ELASTASE INHIBITOR; LEUKOCYTE ELASTASE INHIBITOR A; MALATE DEHYDROGENASE; MUSCLE PROTEIN; MYOGLOBIN; MYOSIN BINDING PROTEIN C; MYOSIN LIGHT CHAIN; MYOSIN LIGHT CHAIN 2; MYOSIN LIGHT CHAIN 3; PARVALBUMIN; PARVALBUMIN ALPHA; PEROXIREDOXIN 1; PHOSPHOGLYCERATE KINASE; PHOSPHOGLYCERATE MUTASE; PHOSPHOGLYCERATE MUTASE 2; PROTEIN 14 3 3; TRIOSEPHOSPHATE ISOMERASE; TROPOMYOSIN; TROPONIN C; TROPONIN I; TROPONIN T; UNCLASSIFIED DRUG; VIMENTIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELLULAR STRESS RESPONSE; DUCHENNE MUSCULAR DYSTROPHY; EXTENSOR DIGITORUM LONGUS MUSCLE; FLEXOR DIGITORUM BREVIS; FLUORESCENCE; IMMUNOBLOTTING; INTEROSSEUS MUSCLE; MALE; MASS SPECTROMETRY; METABOLITE; MOUSE; MUSCLE CONTRACTION; MUSCLE HYPERTROPHY; MUSCLE METABOLISM; MUSCLE RELAXATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; SKELETAL MUSCLE; SOLEUS MUSCLE; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ANIMALS; MALE; MICE; MICE, INBRED MDX; MUSCLE PROTEINS; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, DUCHENNE; PROTEOME; PROTEOMICS;

EID: 84880404341     PISSN: 11073756     EISSN: 1791244X     Source Type: Journal    
DOI: 10.3892/ijmm.2013.1429     Document Type: Article

References (77)

1. Bushby K, Finkel R, Birnkrant DJ, Case LE, Clemens PR, Cripe L, Kaul A, Kinnett K, McDonald C, Pandya S, Poysky J, Shapiro F, Tomezsko J and Constantin C: Diagnosis and management of Duchenne muscular dystrophy, part 1: diagnosis, and pharmacological and psychosocial management. Lancet Neurol 9: 77-93, 2010.
2. Dalkilic I and Kunkel LM: Muscular dystrophies: genes to pathogenesis. Curr Opin Genet Dev 13: 231-238, 2003.
3. Guglieri M and Bushby K: Molecular treatments in Duchenne muscular dystrophy. Curr Opin Pharmacol 10: 331-337, 2010.
4. Mosqueira M, Zeiger U, Förderer M, Brinkmeier H and Fink RH: Cardiac and respiratory dysfunction in Duchenne muscular dystrophy and the role of second messengers. Med Res Rev: April 30, 2013 (Epub ahead of print).
5. Partridge TA: Impending therapies for Duchenne muscular dystrophy. Curr Opin Neurol 24: 415-422, 2011.
6. Spurney CF, Gordish-Dressman H, Guerron AD, Sali A, Pandey GS, Rawat R, Van Der Meulen JH, Cha HJ, Pistilli EE, Partridge TA, Hoffman EP and Nagaraju K: Preclinical drug trials in the mdx mouse: assessment of reliable and sensitive outcome measures. Muscle Nerve 39: 591-602, 2009.
7. Banks GB and Chamberlain JS: The value of mammalian models for duchenne muscular dystrophy in developing therapeutic strategies. Curr Top Dev Biol 84: 431-453, 2008.
8. Durbeej M and Campbell KP: Muscular dystrophies involving the dystrophin-glycoprotein complex: an overview of current mouse models. Curr Opin Genet Dev 12: 349-361, 2002.
9. Tutdibi O, Brinkmeier H, Rüdel R and Föhr KJ: Increased calcium entry into dystrophin-deficient muscle fibres of MDX and ADR-MDX mice is reduced by ion channel blockers. J Physiol 515: 859-868, 1999.
10. Wells DJ and Wells KE: What do animal models have to tell us regarding Duchenne muscular dystrophy? Acta Myol 24: 172-180, 2005.
11. Sicinski P, Geng Y, Ryder-Cook AS, Barnard EA, Darlison MG and Barnard PJ: The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science 244: 1578-1580, 1989.
12. Dowling P, Lohan J and Ohlendieck K: Comparative analysis of Dp427-deficient mdx tissues shows that the milder dystrophic phenotype of extraocular and toe muscle fibres is associated with a persistent expression of beta-dystroglycan. Eur J Cell Biol 82: 222-230, 2003.
13. Marques MJ, Ferretti R, Vomero VU, Minatel E and Neto HS: Intrinsic laryngeal muscles are spared from myonecrosis in the mdx mouse model of Duchenne muscular dystrophy. Muscle Nerve 35: 349-353, 2007.
14. Porter JD, Merriam AP, Khanna S, Andrade FH, Richmonds CR, Leahy P, Cheng G, Karathanasis P, Zhou X, Kusner LL, Adams ME, Willem M, Mayer U and Kaminski HJ: Constitutive properties, not molecular adaptations, mediate extraocular muscle sparing in dystrophic mdx mice. FASEB J 17: 893-895, 2003.
15. Carnwath JW and Shotton DM: Muscular dystrophy in the mdx mouse: histopathology of the soleus and extensor digitorum longus muscles. J Neurol Sci 80: 39-54, 1987.
16. Coulton GR, Morgan JE, Partridge TA and Sloper JC: The mdx mouse skeletal muscle myopathy: I. A histological, morphometric and biochemical investigation. Neuropathol Appl Neurobiol 14: 53-70, 1988.
17. Torres LF and Duchen LW: The mutant mdx: inherited myopathy in the mouse. Morphological studies of nerves, muscles and end-plates. Brain 110: 269-299, 1987.
18. Stedman HH, Sweeney HL, Shrager JB, Maguire HC, Panettieri RA, Petrof B, Narusawa M, Leferovich JM, Sladky JT and Kelly AM: The mdx mouse diaphragm reproduces the degenerative changes of Duchenne muscular dystrophy. Nature 352: 536-539, 1991.
19. Dupont-Versteegden EE and McCarter RJ: Differential expression of muscular dystrophy in diaphragm versus hindlimb muscles of mdx mice. Muscle Nerve 15: 1105-1110, 1992.
20. Lynch GS, Rafael JA, Hinkle RT, Cole NM, Chamberlain JS and Faulkner JA: Contractile properties of diaphragm muscle segments from old mdx and old transgenic mdx mice. Am J Physiol 272: C2063-C2068, 1997.
21. Ohlendieck K: Proteomics of skeletal muscle differentiation, neuromuscular disorders and fiber aging. Expert Rev Proteomics 7: 283-296, 2010.
22. Gelfi C, Vasso M and Cerretelli P: Diversity of human skeletal muscle in health and disease: contribution of proteomics. J Proteomics 74: 774-795, 2011.
23. Ohlendieck K: Skeletal muscle proteomics: current approaches, technical challenges and emerging techniques. Skelet Muscle 1: 6, 2011.
24. Ohlendieck K: Proteomic identification of biomarkers of skeletal muscle disorders. Biomark Med 7: 169-186, 2013.
25. Lewis C, Carberry S and Ohlendieck K: Proteomic profiling of x-linked muscular dystrophy. J Muscle Res Cell Motil 30: 267-269, 2009.
26. Ge Y, Molloy MP, Chamberlain JS and Andrews PC: Proteomic analysis of mdx skeletal muscle: great reduction of adenylate kinase 1 expression and enzymatic activity. Proteomics 3: 1895-1903, 2003.
27. Ge Y, Molloy MP, Chamberlain JS and Andrews PC: Differential expression of the skeletal muscle proteome in mdx mice at different ages. Electrophoresis 25: 2576-2585, 2004.
28. Doran P, Dowling P, Lohan J, McDonnell K, Poetsch S and Ohlendieck K: Subproteomics analysis of Ca+-binding proteins demonstrates decreased calsequestrin expression in dystrophic mouse skeletal muscle. Eur J Biochem 271: 3943-3952, 2004.
29. Doran P, Dowling P, Donoghue P, Buffini M and Ohlendieck K: Reduced expression of regucalcin in young and aged mdx diaphragm indicates abnormal cytosolic calcium handling in dystrophin-deficient muscle. Biochim Biophys Acta 1764: 773-785, 2006.
30. Doran P, Martin G, Dowling P, Jockusch H and Ohlendieck K: Proteome analysis of the dystrophin-deficient MDX diaphragm reveals a drastic increase in the heat shock protein cvHSP. Proteomics 6: 4610-4621, 2006.
31. Doran P, Wilton SD, Fletcher S and Ohlendieck K: Proteomic profiling of antisense-induced exon skipping reveals reversal of pathobiochemical abnormalities in dystrophic mdx diaphragm. Proteomics 9: 671-685, 2009.
32. Gardan-Salmon D, Dixon JM, Lonergan SM and Selsby JT: Proteomic assessment of the acute phase of dystrophin deficiency in mdx mice. Eur J Appl Physiol 111: 2763-2773, 2011.
33. Carberry S, Zweyer M, Swandulla D and 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 30: 229-234, 2012.
34. Carberry S, Zweyer M, Swandulla D and Ohlendieck K: Profiling of age-related changes in the tibialis anterior muscle proteome of the mdx mouse model of dystrophinopathy. J Biomed Biotechnol 2012: 691641, 2012.
35. Lewis C and Ohlendieck K: Proteomic profiling of naturally protected extraocular muscles from the dystrophin-deficient mdx mouse. Biochem Biophys Res Commun 396: 1024-1029, 2010.
36. Rayavarapu S, Coley W, Cakir E, Jahnke V, Takeda S, Aoki Y, Gordish-Dressman H, Jaiswal JK, Hoffman EP, Brown KJ, Hathout Y and Nagaraju K: Identification of disease specific pathways using in vivo SILAC proteomics in dystrophin deficient mdx mouse. Mol Cell Proteomics 12:1061-1073, 2013.
37. Alagaratnam S, Mertens BJ, Dalebout JC, Deelder AM, van Ommen GJ, den Dunnen JT and 't Hoen PA: Serum protein profiling in mice: identification of Factor XIIIa as a potential biomarker for muscular dystrophy. Proteomics 8: 1552-1563, 2008.
38. Colussi C, Banfi C, Brioschi M, Tremoli E, Straino S, Spallotta F, Mai A, Rotili D, Capogrossi MC and Gaetano C: Proteomic profile of differentially expressed plasma proteins from dystrophic mice and following suberoylanilide hydroxamic acid treatment. Proteomics Clin Appl 4: 71-83, 2010.
39. Gulston MK, Rubtsov DV, Atherton HJ, Clarke K, Davies KE, Lilley KS and Griffin JL: A combined metabolomic and proteomic investigation of the effects of a failure to express dystrophin in the mouse heart. J Proteome Res 7: 2069-2077, 2008.
40. Johnson EK, Zhang L, Adams ME, Phillips A, Freitas MA, Froehner SC, Green-Church KB and Montanaro F: Proteomic analysis reveals new cardiac-specific dystrophin-associated proteins. PLoS One 7: e43515, 2012.
41. Lewis C, Jockusch H and Ohlendieck K: Proteomic profiling of the Dystrophin-deficient MDX heart reveals drastically altered levels of key metabolic and contractile proteins. J Biomed Biotechnol 2010: 648501, 2010.
42. Holland A, Dowling P, Zweyer M, Swandulla D, Henry M, Clynes M and 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: May 23, 2013 (Epub ahead of print).
43. Jarmey C: The Atlas of Musculo-skeletal Anatomy. Lotus Publishing, Chichester, 2004.
44. Lieber RL: Skeletal muscle Structure, Function, and Plasticity. 3rd edition, Lippincott Williams & Wilkins, Baltimore, MD, 2009.
45. Stal P, Eriksson PO, Eriksson A and Thornell LE: Enzyme-histochemical differences in fibre-type between the human major and minor zygomatic and the first dorsal interosseus muscles. Arch Oral Biol 32: 833-841, 1987.
46. Staron RS: Human skeletal muscle fiber types: delineation, development, and distribution. Can J Appl Physiol 22: 307-327, 1997.
47. + channels. Proc Natl Acad Sci USA 97: 4950-4955, 2000.
48. 2+ influx and muscle fatigue. Pflügers Arch 461: 115-122, 2011.
49. 2+ entry in dystrophic skeletal muscle fibers. Biochem Biophys Res Commun 391: 401-406, 2010.
50. 2+ sparks via mechanosensitive channels is disrupted in dystrophin deficient muscle but restored by mini-dystrophin expression. PLoS One 3: e3644, 2008.
51. Ohlendieck K and Campbell KP: Dystrophin-associated proteins are greatly reduced in skeletal muscle from mdx mice. J Cell Biol 115: 1685-1694, 1991.
52. Krüger J, Kunert-Keil C, Bisping F and Brinkmeier H: Transient receptor potential cation channels in normal and dystrophic mdx muscle. Neuromuscul Disord 18: 501-513, 2008.
53. Bradford MM: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254, 1976.
54. Gannon J, Staunton L, O'Connell K, Doran P and Ohlendieck K: Phosphoproteomic analysis of aged skeletal muscle. Int J Mol Med 22: 33-42, 2008.
55. Rabilloud T, Strub JM, Luche S, van Dorsselaer A and Lunardi J: A comparison between Sypro Ruby and ruthenium II tris (bathophenanthroline disulfonate) as fluorescent stains for protein detection in gels. Proteomics 1: 699-704, 2001.
56. Lewis C and Ohlendieck K: Mass spectrometric identification of dystrophin isoform Dp427 by on-membrane digestion of sarcolemma from skeletal muscle. Anal Biochem 404: 197-203, 2010.
57. Donoghue P, Doran P, Wynne K, Pedersen K, Dunn MJ and Ohlendieck K: Proteomic profiling of chronic low-frequency stimulated fast muscle. Proteomics 7: 3417-3430, 2007.
58. Staunton L, Jockusch H, Wiegand C, Albrecht T and Ohlendieck K: Identification of secondary effects of hyperexcitability by proteomic profiling of myotonic mouse muscle. Mol Biosyst 7: 2480-2489, 2011.
59. Kornegay JN, Childers MK, Bogan DJ, Bogan JR, Nghiem P, Wang J, Fan Z, Howard JF Jr, Schatzberg SJ, Dow JL, Grange RW, Styner MA, Hoffman EP and Wagner KR: The paradox of muscle hypertrophy in muscular dystrophy. Phys Med Rehabil Clin N Am 23: 149-172, 2012.
60. Andres-Mateos E, Brinkmeier H, Burks TN, Mejias R, Files DC, Steinberger M, Soleimani A, Marx R, Simmers JL, Lin B, Finanger Hedderick E, Marr TG, Lin BM, Hourde C, Leinwand LA, Kuhl D, Foller M, Vogelsang S, Hernandez-Diaz I, Vaughan DK, Alvarez de la Rosa D, Lang F and Cohn RD: Activation of serum/glucocorticoid-induced kinase 1 (SGK1) is important to maintain skeletal muscle homeostasis and prevent atrophy. EMBO Mol Med 5: 80-91, 2013.
61. Gundersen K: Excitation-transcription coupling in skeletal muscle: the molecular pathways of exercise. Biol Rev Camb Philos Soc 86: 564-600, 2011.
62. Zeiger U, Mitchell CH and Khurana TS: Superior calcium homeostasis of extraocular muscles. Exp Eye Res 91: 613-622, 2010.
63. Swartz DR, Yang Z, Sen A, Tikunova SB and Davis JP: Myofibrillar troponin exists in three states and there is signal transduction along skeletal myofibrillar thin filaments. J Mol Biol 361: 420-435, 2006.
64. Gordon AM, Homsher E and Regnier M: Regulation of contraction in striated muscle. Physiol Rev 80: 853-924, 2000.
65. Gonzalez B, Negredo P, Hernando R and Manso R: Protein variants of skeletal muscle regulatory myosin light chain isoforms: prevalence in mammals, generation and transitions during muscle remodelling. Pflügers Arch 443: 377-386, 2002.
66. Bozzo C, Spolaore B, Toniolo L, Stevens L, Bastide B, Cieniewski-Bernard C, Fontana A, Mounier Y and Reggiani C: Nerve influence on myosin light chain phosphorylation in slow and fast skeletal muscles. FEBS J 272: 5771-5785, 2005.
67. Clark KA, McElhinny AS, Beckerle MC and Gregorio CC: Striated muscle cytoarchitecture: an intricate web of form and function. Annu Rev Cell Dev Biol 18: 637-706, 2002.
68. Pette D and Staron RS: Myosin isoforms, muscle fiber types, and transitions. Microsc Res Tech 50: 500-509, 2000.
69. Holland A and Ohlendieck K: Proteomic profiling of the contractile apparatus from skeletal muscle. Expert Rev Proteomics (In press).
70. Donoghue P, Doran P, Dowling P and Ohlendieck K: Differential expression of the fast skeletal muscle proteome following chronic low-frequency stimulation. Biochim Biophys Acta 1752: 166-176, 2005.
71. Philippova M, Banfi A, Ivanov D, Gianni-Barrera R, Allenspach R, Erne P and Resink T: Atypical GPI-anchored T-cadherin stimulates angiogenesis in vitro and in vivo. Arterioscler Thromb Vasc Biol 26: 2222-2230, 2006.
72. Steinacker P, Aitken A and Otto M: 14-3-3 proteins in neurodegeneration. Semin Cell Dev Biol 22: 696-704, 2011.
73. Ohlendieck K: Proteomics of skeletal muscle glycolysis. Biochim Biophys Acta 1804: 2089-2101, 2010.
74. Gelfi C, Vigano A, De Palma S, Ripamonti M, Begum S, Cerretelli P and Wait R: 2-D protein maps of rat gastrocnemius and soleus muscles: a tool for muscle plasticity assessment. Proteomics 6: 321-340, 2006.
75. Wells GD, Selvadurai H and Tein I: Bioenergetic provision of energy for muscular activity. Paediatr Respir Rev 10: 83-90, 2009.
76. Rakus D, Pasek M, Krotkiewski H and Dzugaj A: Interaction between muscle aldolase and muscle fructose 1,6-bisphosphatase results in the substrate channeling. Biochemistry 43: 14948-14957, 2004.
77. Kim JW and Dang CV: Multifaceted roles of glycolytic enzymes. Trends Biochem Sci 30: 142-150, 2005.