Use of quantitative membrane proteomics identifies a novel role of mitochondria in healing injured muscles

Journal of Biological Chemistry

Volumn 287, Issue 36, 2012, Pages 30455-30467

  Sharma, Nimisha ^a,c   Medikayala, Sushma ^a   Defour, Aurelia ^a   Rayavarapu, Sree ^a,b   Brown, Kristy J ^a   Hathout, Yetrib ^a   Jaiswal, Jyoti K ^a,b  

^a CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

^b GEORGE WASHINGTON UNIVERSITY   (United States)

^c GURU GOBIND SINGH INDRAPRASTHA UNIVERSITY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

IN-VIVO; INFLAMMATORY CELLS; MITOCHONDRIAL FUNCTION; MODIFIED AMINO ACIDS; MOLECULAR PROCESS; MUSCLE INJURIES; MYOBLASTS; MYOFIBERS; PHASE RESPONSE; PROTEOMICS; REALTIME IMAGING; SKELETAL MUSCLE;

AMINO ACIDS; MOLECULAR BIOLOGY; MUSCLE; PROTEINS;

MITOCHONDRIA;

PROTEOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SURFACE; CHEMICAL LABELING; CONTROLLED STUDY; HEALING; IMAGING; IN VIVO STUDY; INTRACELLULAR TRANSPORT; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MOUSE; MUSCLE INJURY; MYOBLAST; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEOMICS; QUANTITATIVE ANALYSIS; SARCOLEMMA;

ANIMALS; CELL LINE, TRANSFORMED; FEMALE; MALE; MICE; MITOCHONDRIA, MUSCLE; MUSCLE FIBERS, SKELETAL; MUSCLE PROTEINS; PROTEOMICS; SARCOLEMMA; WOUND HEALING;

MUS;

EID: 84865731321     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.354415     Document Type: Article

References (54)

1. Bansal, D., Miyake, K., Vogel, S. S., Groh, S., Chen, C. C., Williamson, R., McNeil, P. L., and Campbell, K. P. (2003) Defective membrane repair in dysferlin-deficient muscular dystrophy. Nature 423, 168-172
2. Carpenter, S., and Karpati, G. (1989) Segmental necrosis and its demarcation in experimental micropuncture injury of skeletal muscle fibers. J. Neuropathol. Exp. Neurol. 48, 154-170
3. Papadimitriou, J. M., Robertson, T. A., Mitchell, C. A., and Grounds, M. D. (1990) The process of new plasmalemma formation in focally injured skeletal muscle fibers. J. Struct. Biol. 103, 124-134
4. Faulkner, J. A., Brooks, S. V., and Opiteck, J. A. (1993) Injury to skeletal muscle fibers during contractions. Conditions of occurrence and prevention. Phys. Ther. 73, 911-921
5. Grounds, M. D. (1991) Toward understanding skeletal muscle regeneration. Pathol. Res. Pract. 187, 1-22
6. Wallace, G. Q., and McNally, E. M. (2009) Mechanisms of muscle degeneration, regeneration, and repair in the muscular dystrophies. Annu. Rev. Physiol. 71, 37-57
7. Bansal, D., and Campbell, K. P. (2004) Dysferlin and the plasma membrane repair in muscular dystrophy. Trends Cell Biol. 14, 206-213
8. Chargé, S. B., and Rudnicki, M. A. (2004) Cellular and molecular regulation of muscle regeneration. Physiol. Rev. 84, 209-238
9. Cohn, R. D., and Campbell, K. P. (2000) Molecular basis of muscular dystrophies. Muscle Nerve 23, 1456-1471
10. Gelfi, C., Vasso, M., and Cerretelli, P. (2011) Diversity of human skeletal muscle in health and disease. Contribution of proteomics. J. Proteomics 74, 774-795
11. Ohlendieck, K. (2011) Skeletal muscle proteomics. Current approaches, technical challenges, and emerging techniques. Skelet. Muscle 1, 6
12. Raddatz, K., Albrecht, D., Hochgräfe, F., Hecker, M., and Gotthardt, M. (2008)Aproteome map of murine heart and skeletal muscle. Proteomics 8, 1885-1897
13. Vitorino, R., Ferreira, R., Neuparth, M., Guedes, S., Williams, J., Tomer, K. B., Domingues, P. M., Appell, H. J., Duarte, J. A., and Amado, F. M. (2007) Subcellular proteomics of mice gastrocnemius and soleus muscles. Anal. Biochem. 366, 156-169
14. Tannu, N. S., Rao, V. K., Chaudhary, R. M., Giorgianni, F., Saeed, A. E., Gao, Y., and Raghow, R. (2004) Comparative proteomes of the proliferating C2C12 myoblasts and fully differentiated myotubes reveal the complexity of the skeletal muscle differentiation program. Mol. Cell Proteomics 3, 1065-1082
15. Kislinger, T., Gramolini, A. O., Pan, Y., Rahman, K., MacLennan, D. H., and Emili, A. (2005) Proteome dynamics during C2C12 myoblast differentiation. Mol. Cell Proteomics 4, 887-901
16. Gundry, R. L., Raginski, K., Tarasova, Y., Tchernyshyov, I., Bausch-Fluck, D., Elliott, S. T., Boheler, K. R., Van Eyk, J. E., and Wollscheid, B. (2009) The mouse C2C12 myoblast cell surface N-linked glycoproteome. Identification, glycosite occupancy, and membrane orientation. Mol. Cell Proteomics 8, 2555-2569
17. Seiler, S., and Fleischer, S. (1982) Isolation of plasma membrane vesicles from rabbit skeletal muscle and their use in ion transport studies. J. Biol. Chem. 257, 13862-13871
18. Seiler, S., and Fleischer, S. (1988) Isolation and characterization of sarcolemmal vesicles from rabbit fast skeletal muscle. Methods Enzymol. 157, 26-36
19. Lewis, C., and Ohlendieck, K. (2010) Mass spectrometric identification of dystrophin isoform Dp427 by on-membrane digestion of sarcolemma from skeletal muscle. Anal. Biochem. 404, 197-203
20. Ohlendieck, K., Ervasti, J. M., Snook, J. B., and Campbell, K. P. (1991) Dystrophin-glycoprotein complex is highly enriched in isolated skeletal muscle sarcolemma. J. Cell Biol. 112, 135-148
21. Charuk, J. H., Howlett, S., and Michalak, M. (1989) Subfractionation of cardiac sarcolemma with wheat germ agglutinin. Biochem. J. 264, 885-892
22. Elschenbroich, S., Kim, Y., Medin, J. A., and Kislinger, T. (2010) Isolation of cell surface proteins for mass spectrometry-based proteomics. Expert Rev. Proteomics 7, 141-154
23. Jarrold, B., DeMuth, J., Greis, K., Burt, T., and Wang, F. (2005) An effective skeletal muscle prefractionation method to remove abundant structural proteins for optimized two-dimensional gel electrophoresis. Electrophoresis 26, 2269-2278
24. Huber, L. A., Pfaller, K., and Vietor, I. (2003) Organelle proteomics. Implications for subcellular fractionation in proteomics. Circ. Res. 92, 962-968
25. Elia, G. (2008) Biotinylation reagents for the study of cell surface proteins. Proteomics 8, 4012-4024
26. Peirce, M. J., Cope, A. P., and Wait, R. (2009) Proteomic analysis of the lymphocyte plasma membrane using cell surface biotinylation and solution- phase isoelectric focusing. Methods Mol. Biol. 528, 135-140
27. Ghosh, D., Krokhin, O., Antonovici, M., Ens, W., Standing, K. G., Beavis, R. C., and Wilkins, J. A. (2004) Lectin affinity as an approach to the proteomic analysis of membrane glycoproteins. J. Proteome Res. 3, 841-850
28. Wollscheid, B., Bausch-Fluck, D., Henderson, C., O'Brien, R., Bibel, M., Schiess, R., Aebersold, R., and Watts, J. D. (2009) Mass spectrometric identification and relative quantification of N-linked cell surface glycoproteins. Nat. Biotechnol. 27, 378-386
29. Chaney, L. K., and Jacobson, B. S. (1983) Coating cells with colloidal silica for high yield isolation of plasma membrane sheets and identification of transmembrane proteins. J. Biol. Chem. 258, 10062-10072
30. Kline, K. G., and Sussman, M. R. (2010) Protein quantitation using isotope- assisted mass spectrometry. Annu. Rev. Biophys. 39, 291-308
31. Brewis, I. A., and Brennan, P. (2010) Proteomics technologies for the global identification and quantification of proteins. Adv. Protein Chem. Struct. Biol. 80, 1-44
32. Krüger, M., Moser, M., Ussar, S., Thievessen, I., Luber, C. A., Forner, F., Schmidt, S., Zanivan, S., Fässler, R., and Mann, M. (2008) SILAC mouse for quantitative proteomics uncovers kindlin-3 as an essential factor for red blood cell function. Cell 134, 353-364
33. McClatchy, D. B., Liao, L., Park, S. K., Xu, T., Lu, B., and Yates Iii, J. R. (2011) Differential proteomic analysis of mammalian tissues using SILAM. PLoS One 6, e16039
34. Zanivan, S., Krueger, M., and Mann, M. (2012) In vivo quantitative proteomics. The SILAC mouse. Methods Mol. Biol. 757, 435-450
35. Donoghue, P., Staunton, L., Mullen, E., Manning, G., and Ohlendieck, K. (2010) DIGE analysis of rat skeletal muscle proteins using nonionic detergent phase extraction of young adult versus aged gastrocnemius tissue. J. Proteomics 73, 1441-1453
36. Nagaraj, N., Lu, A., Mann, M., and Wiśniewski, J. R. (2008) Detergent-based but gel-free method allows identification of several hundred membrane proteins in single LC-MS runs. J. Proteome Res. 7, 5028-5032
37. Zhao, Y., Zhang, W., Kho, Y., and Zhao, Y. (2004) Proteomic analysis of integral plasma membrane proteins. Anal. Chem. 76, 1817-1823
38. Zhang, Z., Zhang, L., Hua, Y., Jia, X., Li, J., Hu, S., Peng, X., Yang, P., Sun, M., Ma, F., and Cai, Z. (2010) Comparative proteomic analysis of plasma membrane proteins between human osteosarcoma and normal osteoblastic cell lines. BMC Cancer 10, 206
39. Weekes, M. P., Antrobus, R., Lill, J. R., Duncan, L. M., Hör, S., and Lehner, P. J. (2010) Comparative analysis of techniques to purify plasma membrane proteins. J. Biomol. Tech. 21, 108-115
40. Morgan, J. E., Beauchamp, J. R., Pagel, C. N., Peckham, M., Ataliotis, P., Jat, P. S., Noble, M. D., Farmer, K., and Partridge, T. A. (1994) Myogenic cell lines derived from transgenic mice carrying a thermolabile T antigen. A model system for the derivation of tissue-specific and mutation-specific cell lines. Dev. Biol. 162, 486-498
41. McNeil, A. K., Rescher, U., Gerke, V., and McNeil, P. L. (2006) Requirement for annexin A1 in plasma membrane repair. J. Biol. Chem. 281, 35202-35207
42. Cai, C., Masumiya, H., Weisleder, N., Matsuda, N., Nishi, M., Hwang, M., Ko, J. K., Lin, P., Thornton, A., Zhao, X., Pan, Z., Komazaki, S., Brotto, M., Takeshima, H., and Ma, J. (2009) MG53 nucleates assembly of cell membrane repair machinery. Nat. Cell Biol. 11, 56-64
43. Zhu, H., Lin, P., De, G., Choi, K. H., Takeshima, H., Weisleder, N., and Ma, J. (2011) Polymerase transcriptase release factor (PTRF) anchors MG53 protein to cell injury site for initiation of membrane repair. J. Biol. Chem. 286, 12820-12824
44. Lennon, N. J., Kho, A., Bacskai, B. J., Perlmutter, S. L., Hyman, B. T., and Brown, R. H., Jr. (2003) Dysferlin interacts with annexins A1 and A2 and mediates sarcolemmal wound healing. J. Biol. Chem. 278, 50466-50473
45. Mellgren, R. L. (2010) A plasma membrane wound proteome. Reversible externalization of intracellular proteins following reparable mechanical damage. J. Biol. Chem. 285, 36597-36607
46. Honscha, W., Ottallah, M., Kistner, A., Platte, H., and Petzinger, E. (1993) A membrane-bound form of protein-disulfide isomerase (PDI) and the hepatic uptake of organic anions. Biochim. Biophys. Acta 1153, 175-183
47. Shin, B. K., Wang, H., Yim, A. M., Le Naour, F., Brichory, F., Jang, J. H., Zhao, R., Puravs, E., Tra, J., Michael, C. W., Misek, D. E., and Hanash, S. M. (2003) Global profiling of the cell surface proteome of cancer cells uncovers an abundance of proteins with chaperone function. J. Biol. Chem. 278, 7607-7616
48. Negrutskii, B. S., and El'skaya, A. V. (1998) Eukaryotic translation elongation factor 1α. Structure, expression, functions, and possible role in aminoacyl- tRNA channeling. Prog. Nucleic Acid Res. Mol. Biol. 60, 47-78
49. Doran, P., Martin, G., Dowling, P., Jockusch, H., and Ohlendieck, K. (2006) Proteome analysis of the dystrophin-deficient MDX diaphragm reveals a drastic increase in the heat shock protein cvHSP. Proteomics 6, 4610-4621
50. Sonnemann, K. J., and Bement, W. M. (2011) Wound repair. Toward understanding and integration of single-cell and multicellular wound responses. Annu. Rev. Cell Dev. Biol. 27, 237-263
51. McNeil, P. L., and Steinhardt, R. A. (2003) Plasma membrane disruption. Repair, prevention, and adaptation. Annu. Rev. Cell Dev. Biol. 19, 697-731
52. Kim, B. W., Lee, J. W., Choo, H. J., Lee, C. S., Jung, S. Y., Yi, J. S., Ham, Y. M., Lee, J. H., Hong, J., Kang, M. J., Chi, S. G., Hyung, S. W., Lee, S. W., Kim, H. M., Cho, B. R., Min, D. S., Yoon, G., and Ko, Y. G. (2010) Mitochondrial oxidative phosphorylation system is recruited to detergent-resistant lipid rafts during myogenesis. Proteomics 10, 2498-2515
53. Tarnopolsky, M. A., and Raha, S. (2005) Mitochondrial myopathies. Diagnosis, exercise intolerance, and treatment options. Med. Sci. Sports Exerc. 37, 2086-2093
54. Howard, A. C., McNeil, A. K., and McNeil, P. L. (2011) Promotion of plasma membrane repair by vitamin E. Nat. Commun. 2, 597