Myosin Va facilitates the distribution of secretory granules in the F-actin rich cortex of PC12 cells

Journal of Cell Science

Volumn 116, Issue 7, 2003, Pages 1339-1348

  Rudolf, Rüdiger ^a   Kögel, Tanja ^a   Kuznetsov, Sergei A ^a,c   Salm, Thorsten ^a   Schlicker, Oliver ^a   Hellwig, Andrea ^a   Hammer III, John A ^b   Gerdes, Hans Hermann ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^c UNIVERSITY OF ROSTOCK   (Germany)

Author keywords

Cell cortex; F actin; hCgB GFP; Myosin Va; Organelle transport; Secretory granules

Indexed keywords

F ACTIN; MYOSIN V;

ANIMAL CELL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; INTRACELLULAR TRANSPORT; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN STRUCTURE; RAT; REVIEW; SECRETORY GRANULE;

ACTINS; ANIMALS; CELL COMPARTMENTATION; CYTOPLASM; CYTOSKELETON; MICROSCOPY, ELECTRON; MICROTUBULES; MYOSIN HEAVY CHAINS; MYOSIN TYPE V; PC12 CELLS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RATS; SECRETORY VESICLES;

ANIMALIA;

EID: 0037383440     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.00317     Document Type: Review

References (43)

1. Al-Haddad, A., Shonn, M. A., Redlich, B., Blocker, A., Burkhardt, J. K., Yu, H., Hammer, J. A., 3rd, Weiss, D. G., Steffen, W., Griffiths, G. and Kuznetsov, S. A. (2001). Myosin Va bound to phagosomes binds to F-actin and delays microtubule-dependent motility. Mol. Biol. Cell 12, 2742-2755.
2. Bauerfeind, R., Régnier-Vigouroux, A., Flatmark, T. and Huttner, W. B. (1993). Selective storage of acetylcholine, but not catecholamines, in neuroendocrine synaptic-like microvesicles of early endosomal origin. Neuron 11, 105-121.
3. Brown, S. S. (1999). Cooperation between microtubule- and actin-based motor proteins. Annu. Rev. Cell Dev. Biol. 15, 63-80.
4. Burke, N. V., Han, W., Li, D., Takimoto, K., Watkins, S. C. and Levitan, E. S. (1997). Neuronal peptide release is limited by secretory granule mobility. Neuron 19, 1095-1102.
5. Cheney, R. E., O'Shea, M. K., Heuser, J. E., Coelho, M. V., Wolenski, J. S., Espreafico, E. M., Forscher, P., Larson, R. E. and Mooseker, M. S. (1993). Brain myosin-V is a two-headed unconventional myosin with motor activity. Cell 75, 13-23.
6. Darchen, F., Senyshyn, J., Brondyk, W. H., Taatjes, D. J., Holz, R. W., Henry, J. P., Denizot, J. P. and Macara, I. G. (1995). The GTPase Rab3a is associated with large dense core vesicles in bovine chromaffin cells and rat PC12 cells. J. Cell Sci. 108, 1639-1649.
7. Deacon, S. W. and Gelfand, V. I. (2001). Of yeast, mice, and men: rab proteins and organelle transport. J. Cell Biol. 152, F21-F24.
8. Espindola, F. S., Suter, D. M., Partata, L. B., Cao, T., Wolenski, J. S., Cheney, R. E., King, S. M. and Mooseker, M. S. (2000). The light chain composition of chicken brain myosin-Va: calmodulin, myosin-II essential light chains, and 8-kDa dynein light chain/PIN. Cell Motil. Cytoskeleton 47, 269-281.
9. Evans, L. L., Lee, A. J., Bridgman, P. C. and Mooseker, M. S. (1998). Vesicle-associated brain myosin-V can be activated to catalyze actin-based transport. J. Cell Sci. 111, 2055-2066.
10. Fischer von Mollard, G., Mignery, G. A., Baumert, M., Perin, M. S., Hanson, T. J., Burger, P. M., Jahn, R. and Sudhof, T. C. (1990). Rab3 is a small GTP-binding protein exclusively localized to synaptic vesicles. Proc. Natl. Acad. Sci. USA 87, 1988-1992.
11. Gerdes, H.-H. and Rudolf, R. (1999). Green light for the secretory pathway. Protoplasma 209, 1-8.
12. Heumann, R., Kachel, V. and Thoenen, H. (1983). Relationship between NGF-mediated volume increase and "priming effect" in fast and slow reacting clones of PC12 pheochromocytoma cells. Exp. Cell Res. 145, 179-190.
13. Huang, J. D., Brady, S. T., Richards, B. W., Stenolen, D., Resau, J. H., Copeland, N. G. and Jenkins, N. A. (1999). Direct interaction of microtubule- and actin-based transport motors. Nature 397, 267-270.
14. Huttner, W. B., Gerdes, H.-H. and Rosa, P. (1991). The granin (chromogranin/secretogranin) family. Trends Biochem. Sci. 16, 27-30.
15. Kaether, C. and Gerdes, H.-H. (1995). Visualization of protein transport along the secretory pathway using green fluorescent protein. FEBS Lett. 369, 267-271.
16. Kaether, C., Salm, T., Glombik, M., Almers, W. and Gerdes, H.-H. (1997). Targeting of green fluorescent protein to neuroendocrine secretory granules: a new tool for real time studies of regulated protein secretion. Eur. J. Cell Biol. 74, 133-142.
17. Kelly, R. B. (1993). Storage and release of neurotransmitters. Cell 72, 43-53.
18. Krömer, A., Glombik, M. M., Huttner, W. B. and Gerdes, H.-H. (1998). Essential role of the disulfide-bonded loop of chromogranin B for sorting to secretory granules is revealed by expression of a deletion mutant in the absence of endogenous granin synthesis. J. Cell Biol. 140, 1331-1346.
19. 2+-triggered peptide secretion in single cells imaged with green fluorescent protein and evanescent-wave microscopy. Neuron 18, 857-863.
20. Lang, T., Wacker, I., Wunderlich, I., Rohrbach, A., Giese, G., Soldati, T. and Almers, W. (2000). Role of actin cortex in the subplasmalemmal transport of secretory granules in PC-12 cells. Biophys. J 78, 2863-2877.
21. Lochner, J. E., Kingma, M., Kuhn, S., Meliza, C. D., Cutler, B. and Scalettar, B. A. (1998). Real-time imaging of the axonal transport of granules containing a tissue plasminogen activator/green fluorescent protein hybrid. Mol. Biol. Cell 9, 2463-2476.
22. Martelli, A. M., Baldini, G., Tabellini, G., Koticha, D. and Bareggi, R. (2000). Rab3A and Rab3D control the total granule number and the fraction of granules docked at the plasma membrane in PC12 cells. Traffic 1, 976-986.
23. Mercer, J. A., Seperack, P. K., Strobel, M. C., Copeland, N. G. and Jenkins, N. A. (1991). Novel myosin heavy chain encoded by murine dilute coat colour locus [published erratum appears in Nature 1991 Aug 8; 352(6335):547]. Nature 349, 709-713.
24. Mermall, V., Post, P. and Mooseker, M. (1998). Unconventional myosins in cell movement, membrane traffic, and signal transduction. Science 279, 527-533.
25. Nakata, T., and Hirokawa, N. (1992). Organization of cortical cytoskeleton of cultured chromaffin cells and involvement in secretion as revealed by quick-freeze, deep-etching, and double-label immunoelectron microscopy. J. Neurosci. 12, 2186-2197.
26. Ohashi, M. and Huttner, W. B. (1994). An elevation of cytosolic protein phosphorylation modulates trimeric G-protein regulation of secretory vesicle formation from the trans-Golgi network. J. Biol. Chem. 269, 24897-24905.
27. Ong, L. L., Lim, A. P., Er, C. P., Kuznetsov, S. A. and Yu, H. (2000). Kinectin-kinesin binding domains and their effects on organelle motility. J. Biol. Chem. 275, 32854-32860.
28. 2+-dependent interaction with the synaptobrevin-synaptophysin complex. J. Cell Biol. 137, 1589-1601.
29. Rapp, S., Saffrich, R., Anton, M., Jäkle, U., Ansorge, W., Gorgas, K. and Just, W. W. (1996). Microtubule-based peroxisome movement. J. Cell Sci. 109, 837-849.
30. Reck-Peterson, S. L., Provance, D. W., Jr., Mooseker, M. S. and Mercer, J. A. (2000). Class V myosins. Biochim. Biophys. Acta. 1496, 36-51.
31. Rogers, S. L. and Gelfand, V. I. (1998). Myosin cooperates with microtubule motors during organelle transport in melanophores. Curr. Biol. 8, 161-164.
32. Rudolf, R., Salm, T., Rustom, A. and Gerdes, H.-H. (2001). Dynamics of immature secretory granules: role of cytoskeletal elements during transport, cortical restriction and F-actin-dependent tethering. Mol. Biol. Cell. 12, 1353-1365.
33. Schliwa, M. (1999). Molecular motors join forces. Nature 397, 204-205.
34. Tabb, J. S., Molyneaux, B. J., Cohen, D. L., Kuznetsov, S. A. and Langford, G. M. (1998). Transport of ER vesicles on actin filaments in neurons by myosin V. J. Cell Sci. 111, 3221-3234.
35. Tai, A. W., Chuang, J. Z., Bode, C., Wolfrum, U. and Sung, C. H. (1999). Rhodopsin's carboxy-terminal cytoplasmic tail acts as a membrane receptor for cytoplasmic dynein by binding to the dynein light chain Tctex-1. Cell 97, 877-887.
36. Tooze, S. A., Flatmark, T., Tooze, J. and Huttner, W. B. (1991). Characterization of the immature secretory granule, an intermediate in granule biogenesis. J. Cell Biol. 115, 1491-1503.
37. Tvaruskó, W., Bentele, M., Misteli, T., Rudolf, R., Kaether, C., Spector, D. L. Gerdes, H.-H. and Eils, R. (1999). Time-resolved analysis and visualization of dynamic processes in living cells. Proc. Natl. Acad. Sci. USA 96, 7950-7955.
38. Vallee, R. B. and Sheetz, M. P. (1996). Targeting of motor proteins. Science 271, 1539-1544.
39. Wang, F. S., Wolenski, J. S., Cheney, R. E., Mooseker, M. S. and Jay, D. G. (1996). Function of myosin-V in filopodial extension of neuronal growth cones. Science 273, 660-663.
40. Wang, F., Chen, L., Arcucci, O., Harvey, E. V., Bowers, B., Xu, Y., Hammer, J. A., 3rd and Sellers, J. R. (2000). Effect of ADP and ionic strength on the kinetic and motile properties of recombinant mouse myosin V. J. Biol. Chem. 275, 4329-4335.
41. Wu, X., Bowers, B., Wei, Q., Kocher, B. and Hammer, J. A., 3rd (1997). Myosin V associates with melanosomes in mouse melanocytes: evidence that myosin V is an organelle motor. J. Cell Sci. 110, 847-859.
42. Wu, X., Bowers, B., Rao, K., Wei, Q. and Hammer, J. A., 3rd (1998). Visualization of melanosome dynamics within wild-type and dilute melanocytes suggests a paradigm for myosin V function In vivo. J. Cell Biol. 143, 1899-1918.
43. Wu, X., Rao, K., Bowers, M. B., Copeland, N. G., Jenkins, N. A. and Hammer, J. A., 3rd (2001). Rab27a enables myosin Va-dependent melanosome capture by recruiting the myosin to the organelle. J. Cell Sci. 114, 1091-1100.