The integrin-adhesome is required to maintain muscle structure, mitochondrial ATP production, and movement forces in Caenorhabditis elegans

FASEB Journal

Volumn 29, Issue 4, 2015, Pages 1235-1246

  Etheridge, Timothy ^a   Rahman, Mizanur ^b   Gaffney, Christopher J ^c   Shaw, Debra ^a,c   Shephard, Freya ^d   Magudia, Jignesh ^c   Solomon, Deepak E ^b   Milne, Thomas ^c   Blawzdziewicz, Jerzy ^b   Constantin Teodosiu, Dumitru ^c   Greenhaff, Paul L ^c   Vanapalli, Siva A ^b   Szewczyk, Nathaniel J ^c  

^a UNIVERSITY OF EXETER   (United Kingdom)

^b Department of Electrical and Computer Engineering   (United States)

^c UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^d UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Calpain; Dystrophy; Focal adhesion; Mitochondria

Indexed keywords

ADENOSINE TRIPHOSPHATE; INTEGRIN; CAENORHABDITIS ELEGANS PROTEIN; MUSCLE PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; CELL FUNCTION; CELL STRUCTURE; CONTROLLED STUDY; ESCHERICHIA COLI; GENE SILENCING; IN VIVO STUDY; MUSCLE ADHESOME; MUSCLE CELL; MUSCLE MITOCHONDRION; MUSCLE STRENGTH; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN HOMEOSTASIS; PROTEIN INTERACTION; PROTEIN LOCALIZATION; RNA INTERFERENCE; SARCOMERE; VECTOR CONTROL; ANATOMY AND HISTOLOGY; ANIMAL; BIOSYNTHESIS; GENE; GENETICS; MECHANOTRANSDUCTION; METABOLISM; MOVEMENT (PHYSIOLOGY); MUSCLE; PHYSIOLOGY;

ANIMALIA; CAENORHABDITIS ELEGANS; MAMMALIA;

ADENOSINE TRIPHOSPHATE; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; GENE KNOCKDOWN TECHNIQUES; GENES, HELMINTH; INTEGRINS; MECHANOTRANSDUCTION, CELLULAR; MITOCHONDRIA, MUSCLE; MOVEMENT; MUSCLE PROTEINS; MUSCLES; PHENOTYPE; RNA INTERFERENCE;

EID: 84937394344     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-259119     Document Type: Article

References (57)

1. Geiger, B., and Bershadsky, A. (2002) Exploring the neighborhood: adhesion-coupled cell mechanosensors. Cell 110, 139-142
2. Lo, C. M., Wang, H. B., Dembo, M., and Wang, Y. L. (2000) Cell movement is guided by the rigidity of the substrate. Biophys. J. 79, 144-152
3. Mayer, U., Saher, G., Fässler, R., Bornemann, A., Echtermeyer, F., von der Mark, H., Miosge, N., Pöschl, E., and von der Mark, K. (1997) Absence of integrin alpha 7 causes a novel form of muscular dystrophy. Nat. Genet. 17, 318-323
4. Beckmann, J. S., Richard, I., Hillaire, D., Broux, O., Antignac, C., Bois, E., Cann, H., Cottingham, R. W., Jr., Feingold, N., and Feingold, J. (1991) A gene for limb-girdle muscular dystrophy maps to chromosome 15 by linkage. C. R. Acad. Sci. III 312, 141-148
5. Minetti, C., Sotgia, F., Bruno, C., Scartezzini, P., Broda, P., Bado, M., Masetti, E., Mazzocco, M., Egeo, A., Donati, M. A., Volonte, D., Galbiati, F., Cordone, G., Bricarelli, F. D., Lisanti, M. P., and Zara, F. (1998) Mutations in the caveolin-3 gene cause autosomal dominant limb-girdle muscular dystrophy. Nat. Genet. 18, 365-368
6. Klossner, S., Durieux, A. C., Freyssenet, D., and Flueck, M. (2009) Mechano-transduction to muscle protein synthesis is modulated by FAK. Eur. J. Appl. Physiol. 106, 389-398
7. Flück, M., Carson, J. A., Gordon, S. E., Ziemiecki, A., and Booth, F. W. (1999) Focal adhesion proteins FAK and paxillin increase in hypertrophied skeletal muscle. Am. J. Physiol. 277, C152-C162
8. De Boer, M. D., Selby, A., Atherton, P., Smith, K., Seynnes, O. R., Maganaris, C. N., Maffulli, N., Movin, T., Narici, M. V., and Rennie, M. J. (2007) The temporal responses of protein synthesis, gene expression and cell signalling in human quadriceps muscle and patellar tendon to disuse. J. Physiol. 585, 241-251
9. Moerman, D. G., and Williams, B. D. (2006) Sarcomere assembly in C. elegans muscle. WormBook 16, 1-16
10. Hobert, O., Moerman, D. G., Clark, K. A., Beckerle, M. C., and Ruvkun, G. (1999) A conserved LIM protein that affects muscular adherens junction integrity and mechanosensory function in Caenorhabditis elegans. J. Cell Biol. 144, 45-57
11. Rogalski, T. M., Mullen, G. P., Gilbert, M. M., Williams, B. D., and Moerman, D. G. (2000) The UNC-112 gene in Caenorhabditis elegans encodes a novel component of cell-matrix adhesion structures required for integrin localization in the muscle cell membrane. J. Cell Biol. 150, 253-264
12. Etheridge, T., Oczypok, E. A., Lehmann, S., Fields, B. D., Shephard, F., Jacobson, L. A., and Szewczyk, N. J. (2012) Calpains mediate integrin attachment complex maintenance of adult muscle in Caenorhabditis elegans. PLoS Genet. 8, e1002471
13. Francis, G. R., and Waterston, R. H. (1985) Muscle organization in Caenorhabditis elegans: localization of proteins implicated in thin filament attachment and I-band organization. J. Cell Biol. 101, 1532-1549
14. Mackey, A. L., Bojsen-Moller, J., Qvortrup, K., Langberg, H., Suetta, C., Kalliokoski, K. K., Kjaer, M., and Magnusson, S. P. (2008) Evidence of skeletal muscle damage following electrically stimulated isometric muscle contractions in humans. J. Appl. Physiol. 105, 1620-1627
15. Zaidel-Bar, R., Itzkovitz, S., Ma'ayan, A., Iyengar, R., and Geiger, B. (2007) Functional atlas of the integrin adhesome. Nat. Cell Biol. 9, 858-867
16. Lecroisey, C., Ségalat, L., and Gieseler, K. (2007) The C. elegans dense body: anchoring and signaling structure of the muscle. J. Muscle Res. Cell Motil. 28, 79-87
17. Sparrow, J. C., and Schöck, F. (2009) The initial steps of myofibril assembly: integrins pave the way. Nat. Rev. Mol. Cell Biol. 10, 293-298
18. Shephard, F., Adenle, A. A., Jacobson, L. A., and Szewczyk, N. J. (2011) Identification and functional clustering of genes regulating muscle protein degradation from amongst the known C. elegans muscle mutants. PLoS ONE 6, e24686
19. Brenner, S. (1974) The genetics of Caenorhabditis elegans. Genetics 77, 71-94
20. Zdinak, L. A., Greenberg, I. B., Szewczyk, N. J., Barmada, S. J., Cardamone-Rayner, M., Hartman, J. J., and Jacobson, L. A. (1997) Transgene-coded chimeric proteins as reporters of intracellular proteolysis: starvation-induced catabolism of a lacZ fusion protein in muscle cells of Caenorhabditis elegans. J. Cell. Biochem. 67, 143-153
21. Fraser, A. G., Kamath, R. S., Zipperlen, P., Martinez-Campos, M., Sohrmann, M., and Ahringer, J. (2000) Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 408, 325-330
22. Flicek, P., Ahmed, I., Amode, M. R., Barrell, D., Beal, K., Brent, S., Carvalho-Silva, D., Clapham, P., Coates, G., Fairley, S., Fitzgerald, S., Gil, L., García-Girón, C., Gordon, L., Hourlier, T., Hunt, S., Juettemann, T., Kähäri, A. K., Keenan, S., Komorowska, M., Kulesha, E., Longden, I., Maurel, T., McLaren, W. M., Muffato, M., Nag, R., Overduin, B., Pignatelli, M., Pritchard, B., Pritchard, E., Riat, H. S., Ritchie, G. R., Ruffier, M., Schuster, M., Sheppard, D., Sobral, D., Taylor, K., Thormann, A., Trevanion, S., White, S., Wilder, S. P., Aken, B. L., Birney, E., Cunningham, F., Dunham, I., Harrow, J., Herrero, J., Hubbard, T. J., Johnson, N., Kinsella, R., Parker, A., Spudich, G., Yates, A., Zadissa, A., and Searle, S. M. (2013) Ensembl 2013. Nucleic Acids Res. 41, D48-D55
23. Harris, T. W., Antoshechkin, I., Bieri, T., Blasiar, D., Chan, J., Chen, W. J., De La Cruz, N., Davis, P., Duesbury, M., Fang, R., Fernandes, J., Han, M., Kishore, R., Lee, R., Müller, H. M., Nakamura, C., Ozersky, P., Petcherski, A., Rangarajan, A., Rogers, A., Schindelman, G., Schwarz, E. M., Tuli, M. A., Van Auken, K., Wang, D., Wang, X., Williams, G., Yook, K., Durbin, R., Stein, L. D., Spieth, J., and Sternberg, P. W. (2010) WormBase: a comprehensive resource for nematode research. Nucleic Acids Res. 38, D463-D467
24. Shaye, D. D., and Greenwald, I. (2011) OrthoList: a compendium of C. elegans genes with human orthologs. PLoS ONE 6, e20085
25. Uhlén, M., Björling, E., Agaton, C., Szigyarto, C. A., Amini, B., Andersen, E., Andersson, A. C., Angelidou, P., Asplund, A., Asplund, C., Berglund, L., Bergström, K., Brumer, H., Cerjan, D., Ekström, M., Elobeid, A., Eriksson, C., Fagerberg, L., Falk, R., Fall, J., Forsberg, M., Björklund, M. G., Gumbel, K., Halimi, A., Hallin, I., Hamsten, C., Hansson, M., Hedhammar, M., Hercules, G., Kampf, C., Larsson, K., Lindskog, M., Lodewyckx, W., Lund, J., Lundeberg, J., Magnusson, K., Malm, E., Nilsson, P., Odling, J., Oksvold, P., Olsson, I., Oster, E., Ottosson, J., Paavilainen, L., Persson, A., Rimini, R., Rockberg, J., Runeson, M., Sivertsson, A., Sköllermo, A., Steen, J., Stenvall, M., Sterky, F., Strömberg, S., Sundberg, M., Tegel, H., Tourle, S., Wahlund, E., Waldén, A., Wan, J., Wernérus, H., Westberg, J., Wester, K., Wrethagen, U., Xu, L. L., Hober, S., and Pontén, F. (2005) A human protein atlas for normal and cancer tissues based on antibody proteomics. Mol. Cell. Proteomics 4, 1920-1932
26. Meissner, B., Rogalski, T., Viveiros, R., Warner, A., Plastino, L., Lorch, A., Granger, L., Segalat, L., and Moerman, D. G. (2011) Determining the sub-cellular localization of proteins within Caenorhabditis elegans body wall muscle. PLoS ONE 6, e19937
27. Hoehndorf, R., Hardy, N. W., Osumi-Sutherland, D., Tweedie, S., Schofield, P. N., and Gkoutos, G. V. (2013) Systematic analysis of experimental phenotype data reveals gene functions. PLoS ONE 8, e60847
28. Lehmann, S., Shephard, F., Jacobson, L. A., and Szewczyk, N. J. (2012) Using multiple phenotype assays and epistasis testing to enhance the reliability of RNAi screening and identify regulators of muscle protein degradation. Genes (Basel) 3, 686-701
29. Koller, A., and Wätzig, H. (2005) Precision and variance components in quantitative gel electrophoresis. Electrophoresis 26, 2470-2475
30. Lehmann, S., Bass, J. J., and Szewczyk, N. J. (2013) Knockdown of the C. elegans kinome identifies kinases required for normal protein homeostasis, mitochondrial network structure, and sarcomere structure in muscle. Cell Commun. Signal. 11, 71-88
31. Meissner, B., Warner, A., Wong, K., Dube, N., Lorch, A., McKay, S. J., Khattra, J., Rogalski, T., Somasiri, A., Chaudhry, I., Fox, R. M., Miller D. M., Baillie, D. L., Holt, R. A., Jones, S. J., Marra, M. A., and Moerman, D. G. (2009) An integrated strategy to study muscle development and myofilament structure in Caenorhabditis elegans. PLoS Genet. 5, e1000537
32. Wibom, R., Hagenfeldt, L., and von Döbeln, U. (2002) Measurement of ATP production and respiratory chain enzyme activities in mitochondria isolated from small muscle biopsy samples. Anal. Biochem. 311, 139-151
33. Alp, P. R., Newsholme, E. A., and Zammit, V. A. (1976) Activities of citrate synthase and NAD+-linked and NADP+-linked isocitrate dehydrogenase in muscle from vertebrates and invertebrates. Biochem. J. 154, 689-700
34. Ghanbari, A., Nock, V., Johari, S., Blaickie, R., Chen, X., and Wang, W. (2012) A micro-pillar based on-chip system for continuous force measurement of C. elegans. J. Micromech. Microeng. 22, 095009
35. Johari, S., Nock, V., Alkaisi, M. M., and Wang, W. (2013) On-chip analysis of C. elegans muscular forces and locomotion patterns in microstructured environments. Lab Chip 13, 1699-1707
36. Ugural, A. C., Fenster, S. K. (2003) Advanced Strength and Applied Elasticity, Prentice Hall, Upper Saddle River, NJ, USA
37. Fisher, K., Gee, F., Wang, S., Xue, F., Knapp, S., Philpott, M., Wells, C., Rodriguez, M., Snoek, L. B., Kammenga, J., and Poulin, G. B. (2013) Maintenance of muscle myosin levels in adult C. elegans requires both the double bromodomain protein BET-1 and sumoylation. Biol. Open 2, 1354-1363
38. Piekny, A. J., Wissmann, A., and Mains, P. E. (2000) Embryonic morphogenesis in Caenorhabditis elegans integrates the activity of LET-502 Rho-binding kinase, MEL-11 myosin phosphatase, DAF-2 insulin receptor and FEM-2 PP2c phosphatase. Genetics 156, 1671-1689
39. Xu, X., Guo, H., Wycuff, D. L., and Lee, M. (2007) Role of phosphatidylinositol-4-phosphate 5′ kinase (ppk-1) in ovulation of Caenorhabditis elegans. Exp. Cell Res. 313, 2465-2475
40. Konieczny, P., Fuchs, P., Reipert, S., Kunz, W. S., Zeöld, A., Fischer, I., Paulin, D., Schröder, R., and Wiche, G. (2008) Myofiber integrity depends on desmin network targeting to Z-disks and costameres via distinct plectin isoforms. J. Cell Biol. 181, 667-681
41. Crossland, H., Kazi, A. A., Lang, C. H., Timmons, J. A., Pierre, P., Wilkinson, D. J., Smith, K., Szewczyk, N. J., and Atherton, P. J. (2013) Focal adhesion kinase is required for IGF-I-mediated growth of skeletal muscle cells via a TSC2/mTOR/S6K1-associated pathway. Am. J. Physiol. Endocrinol. Metab. 305, E183-E193
42. Wang, H. V., Chang, L. W., Brixius, K., Wickström, S. A., Montanez, E., Thievessen, I., Schwander, M., Müller, U., Bloch, W., Mayer, U., and Fässler, R. (2008) Integrin-linked kinase stabilizes myotendinous junctions and protects muscle from stress-induced damage. J. Cell Biol. 180, 1037-1049
43. Kramerova, I., Kudryashova, E., Wu, B., Germain, S., Vandenborne, K., Romain, N., Haller, R. G., Verity, M. A., and Spencer, M. J. (2009) Mitochondrial abnormalities, energy deficit and oxidative stress are features of calpain 3 deficiency in skeletal muscle. Hum. Mol. Genet. 18, 3194-3205
44. Moulder, G. L., Cremona, G. H., Duerr, J., Stirman, J. N., Fields, S. D., Martin, W., Qadota, H., Benian, G. M., Lu, H., and Barstead, R. J. (2010) a-actinin is required for the proper assembly of Z-disk/focal-adhesion-like structures and for efficient locomotion in Caenorhabditis elegans. J. Mol. Biol. 403, 516-528
45. Ono, K., Parast, M., Alberico, C., Benian, G. M., and Ono, S. (2003) Specific requirement for two ADF/cofilin isoforms in distinct actin-dependent processes in Caenorhabditis elegans. J. Cell Sci. 116, 2073-2085
46. Warner, A., Qadota, H., Benian, G. M., Vogl, A. W., and Moerman, D. G. (2011) The Caenorhabditis elegans paxillin orthologue, PXL-1, is required for pharyngeal muscle contraction and for viability. Mol. Biol. Cell 22, 2551-2563
47. Lebart, M. C., and Benyamin, Y. (2006) Calpain involvement in the remodeling of cytoskeletal anchorage complexes. FEBS J. 273, 3415-3426
48. Kramerova, I., Kudryashova, E., Wu, B., Ottenheijm, C., Granzier, H., and Spencer, M. J. (2008) Novel role of calpain-3 in the triad-associated protein complex regulating calcium release in skeletal muscle. Hum. Mol. Genet. 17, 3271-3280
49. Ojima, K., Kawabata, Y., Nakao, H., Nakao, K., Doi, N., Kitamura, F., Ono, Y., Hata, S., Suzuki, H., Kawahara, H., Bogomolovas, J., Witt, C., Ottenheijm, C., Labeit, S., Granzier, H., Toyama-Sorimachi, N., Sorimachi, M., Suzuki, K., Maeda, T., Abe, K., Aiba, A., and Sorimachi, H. (2010) Dynamic distribution of muscle-specific calpain in mice has a key role in physical-stress adaptation and is impaired in muscular dystrophy. J. Clin. Invest. 120, 2672-2683
50. Ermolova, N., Kudryashova, E., DiFranco, M., Vergara, J., Kramerova, I., and Spencer, M. J. (2011) Pathogenity of some limb girdle muscular dystrophy mutations can result from reduced anchorage to myofibrils and altered stability of calpain 3. Hum. Mol. Genet. 20, 3331-3345
51. Ojima, K., Ono, Y., Ottenheijm, C., Hata, S., Suzuki, H., Granzier, H., and Sorimachi, H. (2011) Non-proteolytic functions of calpain-3 in sarcoplasmic reticulum in skeletal muscles. J. Mol. Biol. 407, 439-449
52. Hauerslev, S., Sveen, M. L., Duno, M., Angelini, C., Vissing, J., and Krag, T. O. (2012) Calpain 3 is important for muscle regeneration: evidence from patients with limb girdle muscular dystrophies. BMC Musculoskelet. Disord. 13, 43
53. Rogalski, T. M., Gilbert, M. M., Devenport, D., Norman, K. R., and Moerman, D. G. (2003) DIM-1, a novel immunoglobulin superfamily protein in Caenorhabditis elegans, is necessary for maintaining bodywall muscle integrity. Genetics 163, 905-915
54. Plenefisch, J. D., Zhu, X., and Hedgecock, E. M. (2000) Fragile skeletal muscle attachments in dystrophic mutants of Caenorhabditis elegans: isolation and characterization of the mua genes. Development 127, 1197-1207
55. Nahabedian, J. F., Qadota, H., Stirman, J. N., Lu, H., and Benian, G. M. (2012) Bending amplitude - a new quantitative assay of C. elegans locomotion: identification of phenotypes for mutants in genes encoding muscle focal adhesion components. Methods 56, 95-102
56. Ervasti, J. M. (2003) Costameres: the Achilles' heel of Herculean muscle. J. Biol. Chem. 278, 13591-13594
57. Zaidel-Bar, R., and Geiger, B. (2010) The switchable integrin adhesome. J. Cell Sci. 123, 1385-1388