Vesicle budding from endoplasmic reticulum is involved in calsequestrin routing to sarcoplasmic reticulum of skeletal muscles

Biochemical Journal

Volumn 379, Issue 2, 2004, Pages 505-512

  Nori, Alessandra ^a   Bortoloso, Elena ^a   Frasson, Federica ^a   Valle, Giorgia ^a   Volpe, Pompeo ^a  

^a UNIVERSITY OF PADOVA   (Italy)

Author keywords

Calsequestrin; Sarcoplasmic reticulum; Skeletal muscle; Targeting

Indexed keywords

ACIDITY; AMINO ACIDS; FIBERS; MUTAGENESIS; PROTEINS; SENSITIVITY ANALYSIS;

ENDOPLASMIC RETICULUM; INTRACELLULAR VESICLE TRAFFICKING; MYOTUBES; SUBCELLULAR LOCALIZATIONS;

MUSCLE;

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; AMINO ACID; CALSEQUESTRIN; EPITOPE; MUTANT PROTEIN; VIRUS HEMAGGLUTININ;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; MALE; MOUSE; MUSCLE CELL; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SARCOPLASMIC RETICULUM; SKELETAL MUSCLE;

ADP-RIBOSYLATION FACTOR 1; ANIMALS; ANIMALS, GENETICALLY MODIFIED; AUTOANTIGENS; CALSEQUESTRIN; CELL LINE; ENDOPLASMIC RETICULUM; HEMAGGLUTININS, VIRAL; MALE; MEMBRANE PROTEINS; MICE; MICROSCOPY, FLUORESCENCE; MONOMERIC GTP-BINDING PROTEINS; MUSCLE FIBERS; MUSCLE, SKELETAL; PROTEIN TRANSPORT; RATS; RATS, WISTAR; RECOMBINANT FUSION PROTEINS; SARCOPLASMIC RETICULUM; TRANSPORT VESICLES;

ANIMALIA;

EID: 2342620103     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20031875     Document Type: Article

References (53)

1. 2+ release units in skeletal and cardiac muscle. Ann. N.Y. Acad. Sci. 85, 20-30
2. Volpe, P., Villa, A., Podini, P., Martini, A., Nori, A., Panzeri, M. C. and Meldolesi, J. (1992) The endoplasmic reticulum-sarcoplasmic reticulum connection: distribution of endoplasmlc reticulum markers in the sarcoplasmic reticulum of skeletal muscle fibers. Proc. Natl. Acad. Sci. U.S.A. 89, 6142-6146
3. Fliegel, L., Ohnishi, M., Carpenter, M. R., Khanna, V. K., Reithmeier, R. A. F. and MacLennan, D. H. (1987) Amino acid sequence of rabbit fast-twitch skeletal muscle calsequestrin deduced from cDNA and peptide sequence. Proc. Natl. Acad. Sci. U.S.A. 84, 1167-1171
4. Jorgensen, A. O., Kalnins, V. I., Zubrzycka, E. and MacLennan, D. H. (1977) Assembly of the sarcoplasmic reticulum proteins in differentiating rat skeletal muscle cell cultures. J. Cell Biol. 74, 287-298
5. Franzini-Armstrong, C., Kenney, L. J. and Varriano-Marston, M. (1987) The structure of calsequestrin in triads of vertebrate skeletal muscle: a deep-etch study. J. Cell Biol. 105, 49-56
6. Kawasaki, T. and Kasai, M. (1994) Regulation of calcium channel of sarcoplasmic reticulum by calsequestrin. Biochem. Biophys. Res. Commun. 199, 1120-1127
7. 2+ release channel activity by phosphorylation of the skeletal muscle ryanodine receptor. FEBS Lett. 332, 237-242
8. 2+ buffer inside the sarcoplasmic reticulum. Biochem. J. 337, 19-22
9. Flucher, B. E. (1992) Structural analysis of muscle development: transverse tubules, sarcoplasmic reticulum and the triad. Dev. Biol. 154, 245-260
10. Villa, A., Podini, P., Nori, A., Panzeri, C., Martini, A., Meldolesi, J. and Volpe, P. (1993) The endoplasmic reticulum-sarcoplasmic reticulum connection II. Postnatal differentiation of the sarcoplasmic reticulum in skeletal muscle fibers. Exp. Cell Res. 209, 140-148
11. O'Brian, J. J., Ram, M. L., Kiarash, A. and Cala, S. E. (2002) Mass spectrometry of cardiac calsequestrin characterizes microheterogeneity unique to heart and indicative of complex intracellular transit. J. Biol. Chem. 277, 37154-37160
12. Campbell, K. P., MacLennan, D. H., Jorgensen, A. O. and Mintzer, M. C. (1983) Purification and characterization of calsequestrin from canine cardiac sarcoplasmic reticulum and identification of the 53,000 dalton glycoprotein. J. Biol. Chem. 258, 1197-1204
13. Thomas, K., Navarro, L. R., Benson, R. J. J., Campbell, K. P., Rotundo, R. L. and Fine, R. E. (1989) Newly synthesized calsequestrin, destined for the sarcoplasmic reticulum, is contained in early/intermediate Golgi-derived clathrin-coated vesicles. J. Biol. Chem. 264, 3140-3145
14. Gatti, G., Podini, P. and Meldolesi, J. (1997) Overexpression of calsequestrin in L6 myoblasts: formation of endoplasmic reticulum subdomains and their evolution into discrete vacuoles where aggregates of the protein are specifically accumulated. Mol. Biol. Cell 8, 1789-1803
15. Nori, A., Valle, G., Massimino, M. L. and Volpe, P. (2001) Targeting of calsequestrin to the sarcoplasmic reticulum of skeletal muscle upon deletion of its glycosylation site. Exp. Cell Res. 265, 104-113
16. Dascher, C. and Balch, W. E. (1994) Dominant inhibitory mutants of ARF1 block endoplasmic reticulum to Golgi transport and trigger disassembly of the Golgi apparatus. J. Biol. Chem. 269, 1437-1448
17. Lippincott-Schwartz, J., Roberts, T. H. and Hirschberg, K. (2000) Secretory protein trafficking and organelle dynamics in living cells. Annu. Rev. Cell Dev. Biol. 16, 557-589
18. Presley, J. F., Ward, T. H., Pfeifer, A. C., Siggia, E. D., Phair, R. D. and Lippincott-Schwartz, J. (2002) Dissection of COPI and Arf1 dynamics in vivo and role in Golgi membrane transport. Nature (London) 417, 187-193
19. Pepperkok, R., Whitney, J. A., Gomez, M. and Kreis, T. E. (2000) COPI vesicles accumulating In the presence of a GTP restricted arf1 mutant are depleted of anteretrograde and retrograde cargo. J. Cell Sci. 113, 135-144
20. Takatsu, H., Yoscino, K., Toda, K. and Nakayama, K. (2002) GGA proteins associate with Golgi membranes through interaction between their GGAH domains and ADP-ribosylation factors. Biochem. J. 365, 369-378
21. Aridor, M., Bannykh, S. I., Rowe, T. and Balch, W. E. (1995) Sequential coupling between COPII and COPI vesicle coats in endoplasmic reticulum to Golgi transport. J. Cell Biol. 131, 875-893
22. Bannykh, S. I. and Balch, W. E. (1998) Selective transport of cargo between the endoplasmic reticulum and Golgi compartments. Histochem. Cell Biol. 109, 463-475
23. Rahkila, P., Takala, T. E., Parton, R. G. and Metsikkö, K. (2001) Protein targeting to the plasma membrane of adult skeletal muscle fiber: an organized mosaic of functional domains. Exp. Cell Res. 267, 61-72
24. Norl, A., Nadalini, K. A., Martini, A., Rizzuto, R., Villa, A. and Volpe, P. (1997) Chimeric calsequestrin and its targeting to the functional sarcoplasmic reticulum of skeletal muscle. Am. J. Physiol. 272, C1420-C1428
25. Blau, H. M., Chiu, C. P. and Webster, C. (1983) Cytoplasmic activation of human nuclear genes in stable heterocaryons. Cell (Cambridge, Mass.) 32, 1171-1180
26. Lu, Z., Joseph, D., Bugnard, E., Zaal, K. J. M. and Ralston, E. (2001) Golgi complex reorganization during muscle differentiation: visualization in living cells and mechanism. Mol. Biol. Cell 12, 795-808
27. Mathiesen, I. (1999) Electropermeabilization of skeletal muscle enhances gene transfer in vivo. Gene Ther. 6, 508-514
28. Nori, A., Lin, P.-J., Cassetti, A., Villa, A., Bayer, K.-U. and Volpe, P. (2003) Targeting of αKAP to sarcoplasmic reticulum and nuclei of skeletal muscle. Biochem. J. 370, 873-880
29. Lahtinen, U., Dahllof, B. and Saraste, J. (1992) Characterization of a 58 kDa cis-Golgi protein in pancreatic exocrine cells. J. Cell Sci. 103, 321-333
30. Sandri, M., Bortoloso, E., Nori, A. and Volpe, P. (2003) Electrotransfer in differentiated myotubes: a novel, efficient procedure for functional gene transfer. Exp. Cell Res. 286, 87-95
31. Ralston, E., Lu, Z. and Ploug, T. (1999) The organization of the Golgi complex and microtubules in skeletal muscle is fiber type-dependent. J. Neurosci. 19, 10694-10705
32. Plutner, H., Davidson, H. W., Saraste, J. and Balch, W. E. (1992) Morphological analysis of protein transport from the ER to Golgi membranes in digitonin-permeabilized cells: role of the p58 containing compartment. J. Cell Biol. 119, 1097-1116
33. Rahkila, P., Luukela, V., Väänänen, K. and Metsikkö, K. (1998) Differential targeting of vesicular stomatitis virus G protein and influenza virus hemagglutinin appears during myogenesis of L6 muscle cells. J. Cell Biol. 140, 1101-1111
34. Kaisto, T. and Metsikkö, K. (2003) Distribution of the endoplasmic reticulum and its relationship with the sarcoplasmic reticulum in skeletal myofibers. Exp. Cell Res. 289, 47-57
35. Ralston, E., Ploug, T., Kalhovde, J. and Lomo, T. (2001) Golgi complex, endoplasmic reticulum exit sites, and microtubules in skeletal muscle fibers are organized by patterned activity. J. Neurosci. 21, 875-883
36. Seemann, J., Jokitalo, E., Pypaert, M. and Warren, G. (2000) Matrix proteins can generate the higher order architecture of the Golgi apparatus. Nature (London) 407, 1022-1026
37. Tharin, S., Hamel, P. A., Conway, E. M., Michalak, M. and Opas, M. (1996) Regulation of calcium binding proteins calreticulin and calsequestrin during differentiation in the myogenic cell line L6. J. Cell. Physiol. 166, 547-560
38. Ralston, E. (1993) Changes in architecture of the Golgi complex and other subcellular organelles during myogenesis. J. Cell Biol. 120, 399-409
39. Ralston, E. and Ploug, T. (1996) GLUT4 in cultured skeletal myotubes is segregated from the transferring receptor and stored in vesicles associated with TGN. J. Cell Sci. 109, 2967-2978
40. Stearns, T., Willingham, M. C., Botstein, D. and Kahn, R. A. (1990) ADP-ribosylation factor is functionally and physically associated with the Golgi complex. Proc. Natl. Acad. Sci. U.S.A. 87, 1238-1242
41. Hosaka, M., Toda, K., Takatsu, H., Torii, S., Muratami, K. and Nakayama, K. (1996) Structure and intracellular localization of mouse ADP-ribosylation factors type 1 to type 6. J. Biochem. (Tokyo) 120, 813-819
42. Stamnes, M. A. and Rothman, J. E. (1993) The binding of AP-1 clathrin adaptor particles to Golgi membranes requires ADP-ribosylation factor, a small GTP-binding protein. Cell (Cambridge, Mass.) 73, 999-1005
43. Rahkila, P., Väänänen, K., Saraste, J. and Metsikkö, K. (1997) Endoplasmic reticulum to Golgi trafficking in multinucleated skeletal muscle fibers. Exp. Cell Res. 234, 452-464
44. Rahkila, P., Alakangas, A., Väänänen, K. and Metsikkö, K. (1996) Transport pathway, maturation, and targeting of the vesicular stomatitis virus glycoprotein in skeletal muscle fibers. J. Cell Sci. 109, 1585-1596
45. Kaisto, T., Luukela, V., Birr, E. and Metsikkö, K. (2002) Retargeting of viral glycoproteins into a non-exporting compartment during the myogenic differentiation of rat L6 cells. Cell Tissue Res. 308, 381-390
46. Liu, S. H., Towler, M. C., Chen, E., Chen, C. Y., Song, W., Apodaca, G. and Brodsky, F. M. (2001) A novel clathrin homolog that co-distributes with cytoskeletal components functions in the trans-Golgi network. EMBO J. 20, 272-284
47. Shugrue, C. A., Kolen, E. R., Peters, H., Czernik, A., Kaiser, C., Matovcik, L., Hubbard, A. L. and Gorelick, F. (1999) Identification of the putative mammalian orthologue of Sec31P, a component of the COPII coat. J. Cell Sci. 112, 4547-4556
48. Tang, B. L., Ong, Y. S., Huang, B., Wei, S., Wong, E. T., Qi, R., Horstmann, H. and Hong, W. (2001) A membrane protein enriched in endoplasmic reticulum exit sites interacts with COPII. J. Biol. Chem. 276, 40008-40017
49. Butler, M. H., David, C., Ochoa, G. C., Freyberg, Z., Daniell, L., Grabs, D., Cremona, O. and DeCamilli, P. (1997) Amphiphysin II (SH3P9; BIN1), a member of the amphiphysin/Rvs family, is concentrated in the cortical cytomatrix of axon initial segments and nodes of Ranvier in brain and around T tubules in skeletal muscle. J. Cell Biol. 137, 1355-1367
50. Parton, R. G., Way, M., Zorzi, N. and Stang, E. (1997) Caveolin-3 associates with developing T-tubules during muscle differentiation. J. Cell Biol. 136, 137-154
51. Simpson, F., Whitehead, J. P. and James, D. E. (2001) GLUT4 - at the cross roads between membrane trafficking and signal transduction. Traffic 2, 2-11
52. 2+ homeostasis proteins. J. Cell Biol. 147, 995-1008
53. Gagelin, C., Constantin, B., Deprette, C., Ludosky, M. A., Recouvreur, M., Cartaud, J., Cognard, C., Raymond, G. and Kordeli, E. (2002) Identification of Ank (G107), a muscle-specific ankyrin-G isoform. J. Biol. Chem. 277, 12978-12987