γ-Sarcoglycan deficiency increases cell contractility, apoptosis and MAPK pathway activation but does not affect adhesion

Journal of Cell Science

Volumn 118, Issue 7, 2005, Pages 1405-1416

  Griffin, Maureen A ^a,b   Feng, Huisheng ^a   Tewari, Manorama ^a,b   Acosta, Pedro ^a   Kawana, Masataka ^a   Sweeney, H Lee ^a   Discher, Dennis E ^a,b  

^a HOSPITAL OF THE UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Differentation; Limb girdle muscular dystrophy; Muscular dystrophy; Sarcoglycan

Indexed keywords

GAMMA SARCOGLYCAN; MITOGEN ACTIVATED PROTEIN KINASE; MYOSIN ADENOSINE TRIPHOSPHATASE; SARCOGLYCAN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL CELL CULTURE; APOPTOSIS; ARTICLE; CELL ADHESION; CELL MEMBRANE; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME ACTIVATION; HYPERTENSION; MICROPIPETTE; MOUSE; MUSCLE CONTRACTION; MUSCLE DEVELOPMENT; MUSCLE FIBER CONTRACTION; MUSCLE STRETCHING; MYOTUBE; NEWBORN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN PHOSPHORYLATION; SARCOMERE; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; STRESS;

ANIMALS; APOPTOSIS; CELL ADHESION; CELL MOVEMENT; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASES; MODELS, BIOLOGICAL; MYOBLASTS, SKELETAL; SARCOGLYCANS; SIGNAL TRANSDUCTION;

EID: 17844404025     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01717     Document Type: Article

References (75)

1. Awata, H., Huang, C., Handlogten, M. E. and Miller, R. T. (2001). Interaction of the calcium-sensing receptor and filamin, a potential scaffolding protein. J. Biol. Chem. 276, 34871-34879.
2. Azuma, N., Akasaka, N., Kito, H., Ikeda, M., Gahtan, V., Sasajima, T. and Sumpio, B. E. (2001). Role of p38 MAP kinase in endothelial cell alignment induced by fluid shear stress. Am. J. Physiol. Heart Circ. Physiol. 280, H189-H197.
3. Bellanger, J. M., Astier, C., Sardet, C., Ohta, Y., Stossel, T. P. and Debant, A. (2000). The Rac1- and RhoG-specific GEF domain of Trio targets filamin to remodel cytoskeletal actin. Nat. Cell Biol. 2, 888-892.
4. Bradley, W. G. and Fulthorpe, J. J. (1978). Studies of sarcolemmal integrity in myopathic muscle. Neurology 28, 670-677.
5. Bushby, K. M. (1999). The limb-girdle muscular dystrophies-multiple genes, multiple mechanisms. Hum. Mol. Genet. 8, 1875-1882.
6. Carragher, N. O., Westhoff, M. A., Fincham, V. J., Schaller, M. D. and Frame, M. C. (2003). A novel role for FAK as a protease-targeting adaptor protein: regulation by p42 ERK and Src. Curr. Biol. 13, 1442-1450.
7. Cavaldesi, M., Macchia, G., Barca, S., Defilippi, P., Tarone, G. and Petrucci, T. C. (1999). Association of the dystroglycan complex isolated from bovine brain synaptosomes with proteins involved in signal transduction. J. Neurochem. 72, 1648-1655.
8. Cheung, E. C. and Slack, R. S. (2004). Emerging role for ERK as a key regulator of neuronal apoptosis. Sci. STKE 2004 PE45.
9. Deschesnes, R. G., Huot, J., Valerie, K. and Landry, J. (2001). Involvement of p38 in apoptosis-associated membrane blebbing and nuclear condensation. Mol. Biol. Cell 12, 1569-1582.
10. Engler, A., Bacakova, L., Newman, C., Hategan, A., Griffin, M. and Discher, D. (2004a). Substrate compliance versus ligand density in cell on gel responses. Biophys. J. 86, 617-628.
11. Engler, A. J., Griffin, M. A., Sen, S., Bonnemann, C. G., Sweeney, H. L. and Discher, D. E. (2004b). Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments. J. Cell Biol. 166, 877-887.
12. Fanning, P. J., Emkey, G., Smith, R. J., Grodzinsky, A. J., Szasz, N. and Trippel, S. B. (2003). Mechanical regulation of mitogen-activated protein kinase signaling in articular cartilage. J. Biol. Chem. 278, 50940-50948.
13. Fong, P. Y., Turner, P. R., Denetclaw, W. F. and Steinhardt, R. A. (1990). Increased activity of calcium leak channels in myotubes of Duchenne human and mdx mouse origin. Science 250 673-676.
14. Frisch, S. M., Vuori, K., Ruoslahti, E. and Chan-Hui, P. Y. (1996). Control of adhesion-dependent cell survival by focal adhesion kinase. J. Cell Biol. 134, 793-799.
15. Grace, E. A. and Busciglio, J. (2003). Aberrant activation of focal adhesion proteins mediates fibrillar amyloid beta-induced neuronal dystrophy. J. Neurosci. 23, 493-502.
16. Grady, R. M., Merlie, J. P. and Sanes, J. R. (1997). Subtle neuromuscular defects in utrophin-deficient mice. J. Cell Biol. 136, 871-882.
17. Griffin, M. A., Engler, A. J., Barber, T. A., Healy, K. E., Sweeney, H. L. and Discher, D. E. (2004a). Patterning, prestress, and peeling dynamics of myocytes. Biophys. J. 86, 1209-1222.
18. Griffin, M. A., Sen, S., Sweeney, H. L. and Discher, D. E. (2004b). Adhesion-contractile balance in myocyte differentiation. J. Cell Sci. 117, 5855-5863.
19. Hack, A. A., Cordier, L., Shoturma, D. I., Lam, M. Y., Sweeney, H. L. and McNally, E. M. (1999). Muscle degeneration without mechanical injury in sarcoglycan deficiency. Proc. Natl. Acad. Sci. USA 96, 10723-10728.
20. Hack, A. A., Ly, C. T., Jiang, F., Clendenin, C. J., Sigrist, K. S., Wollmann, R. L. and McNally, E. M. (1998). Gamma-sarcoglycan deficiency leads to muscle membrane defects and apoptosis independent of dystrophin. J. Cell Biol. 142, 1279-1287.
21. Hornberger, T. A., Armstrong, D. D., Koh, T. J., Burkholder, T. J. and Esser, K. A. (2005). Intracellular signaling specificity in response to uniaxial vs. multiaxial stretch: implications for mechanotransduction. Am. J. Physiol. Cell Physiol. 288, C185-C194.
22. Hubmayr, R. D., Shore, S. A., Fredberg, J. J., Planus, E., Panettieri, R. A., Jr, Moller, W., Heyder, J. and Wang, N. (1996). Pharmacological activation changes stiffness of cultured human airway smooth muscle cells. Am. J. Physiol. 271, C1660-C1668.
23. Ibitayo, A. I., Sladick, J., Tuteja, S., Louis-Jacques, O., Yamada, H., Groblewski, G., Welsh, M. and Bitar, K. N. (1999). HSP27 in signal transduction and association with contractile proteins in smooth muscle cells. Am. J. Physiol. 277, G445-G454.
24. Imamdi, R., de Graauw, M. and van de Water, B. (2004). Protein kinase C mediates cisplatin-induced loss of adherens junctions followed by apoptosis of renal proximal tubular epithelial cells. J. Pharmacol. Exp. Ther. 311, 892-903.
25. Jansen, J. H., Weyts, F. A., Westbroek, I., Jahr, H., Chiba, H., Pols, H. A., Verhaar, J. A., van Leeuwen, J. P. and Weinans, H. (2004). Stretch-induced phosphorylation of ERK1/2 depends on differentiation stage of osteoblasts. J. Cell. Biochem. 93, 542-551.
26. Je, H. D., Gallant, C., Leavis, P. C. and Morgan, K. G. (2004). Caveolin-1 regulates contractility in differentiated vascular smooth muscle. Am. J. Physiol. Heart Circ. Physiol. 286, H91-H98.
27. Jung, Y. S., Ryu, B. R., Lee, B. K., Mook-Jung, I., Kim, S. U., Lee, S. H., Baik, E. J. and Moon, C. H. (2004). Role for PKC-epsilon in neuronal death induced by oxidative stress. Biochem. Biophys. Res. Commun. 320, 789-794.
28. Kaariainen, M., Kaariainen, J., Jarvinen, T. L., Nissinen, L., Heino, J., Jarvinen, M. and Kalimo, H. (2000). Integrin and dystrophin associated adhesion protein complexes during regeneration of shearing-type muscle injury. Neuromuscul. Disord. 10, 121-132.
29. Kainulainen, T., Pender, A., D'Addario, M., Feng, Y., Lekic, P. and McCulloch, C. A. (2002). Cell death and mechanoprotection by filamin a in connective tissues after challenge by applied tensile forces. J. Biol. Chem. 277, 21998-22009.
30. Kramarcy, N. R. and Sealock, R. (1990). Dystrophin as a focal adhesion protein. Collocalization with talin and the Mr 48,000 sarcolemmal protein in cultured Xenopus muscle. FEBS Lett. 274 171-174.
31. Krief, S., Faivre, J. F., Robert, P., le Douarin, B., Brument-Larignon, N., Lefrere, I., Bouzyk, M. M., Anderson, K. M., Greller, L. D., Tobin, F. L. et al. (1999). Identification and characterization of cvHsp. A novel human small stress protein selectively expressed in cardiovascular and insulin-sensitive tissues. J. Biol. Chem. 274, 36592-36600.
32. Krook, A., Widegren, U., Jiang, X. J., Henriksson, J., Wallberg-Henriksson, H., Alessi, D. and Zierath, J. R. (2000). Effects of exercise on mitogen- and stress-activated kinase signal transduction in human skeletal muscle. Am. J. Physiol. Regul. Integr. Comp. Physiol. 279, R1716-R1721.
33. Kumar, A., Chaudhry, I., Reid, M. B. and Boriek, A. M. (2002). Distinct signaling pathways are activated in response to mechanical stress applied axially and transversely to skeletal muscle fibers. J. Biol. Chem. 277, 46493-46503.
34. Kumar, A., Khandelwal, N., Malya, R., Reid, M. B. and Boriek, A. M. (2004). Loss of dystrophin causes aberrant mechanotransduction in skeletal muscle fibers. FASEB J. 18, 102-113.
35. Kurenova, E., Xu, L. H., Yang, X., Baldwin, A. S., Jr, Craven, R. J., Hanks, S. K., Liu, Z. G. and Cance, W. G. (2004). Focal adhesion kinase suppresses apoptosis by binding to the death domain of receptor-interacting protein. Mol. Cell. Biol. 24, 4361-4371.
36. Lakonishok, M., Muschler, J. and Horwitz, A. F. (1992). The alpha 5 beta 1 integrin associates with a dystrophin-containing lattice during muscle development. Dev. Biol. 152, 209-220.
37. Laprise, P., Poirier, E. M., Vezina, A., Rivard, N. and Vachon, P. H. (2002). Merosin-integrin promotion of skeletal myofiber cell survival: Differentiation state-distinct involvement of p60Fyn tyrosine kinase and p38alpha stress-activated MAP kinase. J. Cell Physiol. 191, 69-81.
38. Lee, K. M., Tsai, K. Y., Wang, N. and Ingber, D. E. (1998). Extracellular matrix and pulmonary hypertension: control of vascular smooth muscle cell contractility. Am. J. Physiol. 274 H76-H82.
39. Leonardi, A., Ellinger-Ziegelbauer, H., Franzoso, G., Brown, K. and Siebenlist, U. (2000). Physical and functional interaction of filamin (actin-binding protein-280) and tumor necrosis factor receptor-associated factor 2. J. Biol. Chem. 275, 271-278.
40. Lesay, A., Hickman, J. A. and Gibson, R. M. (2001). Disruption of focal adhesions mediates detachment during neuronal apoptosis. Neuroreport 12, 2111-2115.
41. Lin, E. H., Hui, A. Y., Meens, J. A., Tremblay, E. A., Schaefer, E. and Elliott, B. E. (2004). Disruption of Ca2+-dependent cell-matrix adhesion enhances c-Src kinase activity, but causes dissociation of the c-Src/FAK complex and dephosphorylation of tyrosine-577 of FAK in carcinoma cells. Exp. Cell Res. 293, 1-13.
42. Liu, Q. and Hofmann, P. A. (2004). Protein phosphatase 2A-mediated crosstalk between p38 MAPK and ERK in apoptosis of cardiac myocytes. Am. J. Physiol. Heart Circ. Physiol. 286, H2204-H2212.
43. Loth, F., Fischer, P. F., Arslan, N., Bertram, C. D., Lee, S. E., Royston, T. J., Shaalan, W. E. and Bassiouny, H. S. (2003). Transitional flow at the venous anastomosis of an arteriovenous graft: potential activation of the ERK1/2 mechanotransduction pathway. J. Biomech. Eng. 125, 49-61.
44. Lunn, J. A. and Rozengurt, E. (2004). Hyperosmotic stress induces rapid focal adhesion kinase phosphorylation at tyrosines 397 and 577. Role of Src family kinases and Rho family GTPases. J. Biol. Chem. 279, 45266-45278.
45. Mansour, H., de Tombe, P. P., Samarel, A. M. and Russell, B. (2004). Restoration of resting sarcomere length after uniaxial static strain is regulated by protein kinase Cepsilon and focal adhesion kinase. Circ. Res. 94, 642-649.
46. Martineau, L. C. and Gardiner, P. F. (2001). Insight into skeletal muscle mechanotransduction: MAPK activation is quantitatively related to tension. J. Appl. Physiol. 91, 693-702.
47. Matassa, A. A., Kalkofen, R. L., Carpenter, L., Biden, T. J. and Reyland, M. E. (2003). Inhibition of PKCalpha induces a PKCdelta-dependent apoptotic program in salivary epithelia] cells. Cell Death Differ. 10, 269-277.
48. Matsuoka, Y., Li, X. and Bennett, V. (2000). Adducin: structure, function and regulation. Cell. Mol. Life Sci. 57, 884-895.
49. Mizutani, T., Fukushi, S., Saijo, M., Kurane, I. and Morikawa, S. (2004). Phosphorylation of p38 MAPK and its downstream targets in SARS coronavirus-infected cells. Biochem. Biophys. Res. Commun. 319, 1228-1234.
50. Neville, C., Rosenthal, N., McGraw, M., Bogdanova, N. and Hauschka, S. D. (1998). Skeletal muscle cultures. San Diego, CA: Academic Press.
51. Ni, C. W., Wang, D. L., Lien, S. C., Cheng, J. J., Chao, Y. J. and Hsieh, H. J. (2003). Activation of PKC-epsilon and ERK1/2 participates in shear-induced endothelial MCP-1 expression that is repressed by nitric oxide. J. Cell. Physiol. 195, 428-434.
52. Noguchi, S., McNally, E. M., Ben Othmane, K., Hagiwara, Y., Mizuno, Y., Yoshida, M., Yamamoto, H., Bonnemann, C. G., Gussoni, E., Denton, P. H. et al. (1995). Mutations in the dystrophin-associated protein gamma-sarcoglycan in chromosome 13 muscular dystrophy. Science 270, 819-822.
53. Oak, S. A., Zhou, Y. W. and Jarrett, H. W. (2003). Skeletal muscle signaling pathway through the dystrophin glycoprotein complex and Rac1. J. Biol. Chem. 278, 39287-39295.
54. Paul, A. C., Sheard, P. W., Kaufman, S. J. and Duxson, M. J. (2002). Localization of alpha 7 integrins and dystrophin suggests potential for both lateral and longitudinal transmission of tension in large mammalian muscles. Cell Tissue Res. 308, 255-265.
55. Pelech, S., Sutter, C. and Zhang, H. (2003). Kinetworks™ Protein Kinase Multiblot Analysis. In Cancer Cell Signaling: Methods and Protocols, vol. 218 (ed. D. M. Terrian), pp. 99-111. Totowa, N.J.: Humana Press.
56. Potard, U. S., Butler, J. P. and Wang, N. (1997). Cytoskeletal mechanics in confluent epithelial cells probed through integrins and E-cadherins. Am. J. Physiol. 272, C1654-C1663.
57. Radojevic, V., Lin, S. and Burgunder, J. M. (2000). Differential expression of dystrophin, utrophin, and dystrophin-associated proteins in human muscle culture. Cell Tissue Res. 300, 447-457.
58. Rando, T. A. (2001). The dystrophin-glycoprotein complex, cellular signaling, and the regulation of cell survival in the muscular dystrophies. Muscle Nerve 24, 1575-1594.
59. Ryder, J. W., Fahlman, R., Wallberg-Henriksson, H., Alessi, D. R., Krook, A. and Zierath, J. R. (2000). Effect of contraction on mitogen-activated protein kinase signal transduction in skeletal muscle. Involvement Of the mitogen- and stress-activated protein kinase 1. J. Biol. Chem. 275, 1457-1462.
60. Scherer, A. and Graff, J. M. (2000). Calmodulin differentially modulates Smad1 and Smad2 signaling. J. Biol. Chem. 275, 41430-41438.
61. Stamenovic, D., Liang, Z., Chen, J. and Wang, N. (2002). Effect of the cytoskeletal prestress on the mechanical impedance of cultured airway smooth muscle cells. J. Appl. Physiol. 92, 1443-1450.
62. Straub, V., Rafael, J. A., Chamberlain, J. S. and Campbell, K. P. (1997). Animal models for muscular dystrophy show different patterns of sarcolemmal disruption. J. Cell Biol. 139 375-385.
63. Subramaniam, S., Zirrgiebel, U., von Bohlen Und Halbach, O., Strelau, J., Laliberte, C., Kaplan, D. R. and Unsicker, K. (2004). ERK activation promotes neuronal degeneration predominantly through plasma membrane damage and independently of caspase-3. J. Cell Biol. 165, 357-369.
64. Suzawa, M., Tamura, Y., Fukumoto, S., Miyazono, K., Fujita, T., Kato, S. and Takeuchi, Y. (2002). Stimulation of Smad1 transcriptional activity by Ras-extracellular signal-regulated kinase pathway: a possible mechanism for collagen-dependent osteoblastic differentiation. J. Bone Miner. Res. 17, 240-248.
65. Sward, K., Dreja, K., Susnjar, M., Hellstrand, P., Hartshorne, D. J. and Walsh, M. P. (2000). Inhibition of Rho-associated kinase blocks agonist-induced Ca2+ sensitization of myosin phosphorylation and force in guineapig ileum. J. Physiol. 522 33-49.
66. Thompson, T. G., Chan, Y. M., Hack, A. A., Brosius, M., Rajala, M., Lidov, H. G., McNally, E. M., Watkins, S. and Kunkel, L. M. (2000). Filamin 2 (FLN2): A muscle-specific sarcoglycan interacting protein. J. Cell Biol. 148, 115-126.
67. Trevisan, R., Daprai, L., Acquasaliente, L., Ciminale, V., Chieco-Bianchi, L. and Saggioro, D. (2004). Relevance of CREB phosphorylation in the anti-apoptotic function of human T-lymphotropic virus type 1 tax protein in serum-deprived murine fibroblasts. Exp. Cell Res. 299, 57-67.
68. van de Water, B., Tijdens, I. B., Verbrugge, A., Huigsloot, M., Dihal, A. A., Stevens, J. L., Jaken, S. and Mulder, G. J. (2000). Cleavage of the actin-capping protein alpha-adducin at Asp-Asp-Ser-Asp633-Ala by caspase-3 is preceded by its phosphorylation on serine 726 in cisplatin-induced apoptosis of renal epithelial cells. J. Biol. Chem. 275, 25805-25813.
69. van der Flier, A., Kuikman, I., Kramer, D., Geerts, D., Kreft, M., Takafuta, T., Shapiro, S. S. and Sonnenberg, A. (2002). Different splice variants of filamin-B affect myogenesis, subcellular distribution, and determine binding to integrin [beta] subunits. J. Cell Biol. 156, 361-376.
70. Wang, N., Butler, J. P. and Ingber, D. E. (1993). Mechanotransduction across the cell surface and through the cytoskeleton. Science 260, 1124-1127.
71. Wang, N., Tolic-Norrelykke, I. M., Chen, J., Mijailovich, S. M., Butler, J. P., Fredberg, J. J. and Stamenovic, D. (2002). Cell prestress. I. Stiffness and prestress are closely associated in adherent contractile cells. Am. J. Physiol. Cell Physiol. 282, C606-C616.
72. Xia, Z., Dickens, M., Raingeaud, J., Davis, R. J. and Greenberg, M. E. (1995). Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270, 1326-1331.
73. Yoshida, T., Hanada, H., Iwata, Y., Pan, Y. and Sigekawa, M. (1996). Expression of a dystrophin-sarcoglycan complex in serum-deprived BC3H1 cells and involvement of alpha-sarcoglycan in substrate attachment. Biochem. Biophys. Res. Commun. 225, 11-15.
74. Yoshida, T., Pan, Y., Hanada, H., Iwata, Y. and Shigekawa, M. (1998). Bidirectional signaling between sarcoglycans and the integrin adhesion system in cultured L6 myocytes. J. Biol. Chem. 273, 1583-1590.
75. Zechner, D., Thuerauf, D. J., Hanford, D. S., McDonough, P. M. and Glembotski, C. C. (1997). A role for the p38 mitogen-activated protein kinase pathway in myocardial cell growth, sarcomeric organization, and cardiac-specific gene expression. J. Cell Biol. 139, 115-127.