A newly identified myomegalin isoform functions in Golgi microtubule organization and ER-Golgi transport

Journal of Cell Science

Volumn 127, Issue 22, 2014, Pages 4904-4917

  Wang, Zhe ^a   Zhang, Chao ^a   Qi, Robert Z ^a  

^a HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

Author keywords

Golgi; Microtubule; Myomegalin; Protein trafficking

Indexed keywords

A KINASE ANCHORING PROTEIN 9; GAMMA TUBULIN; MICROTUBULE PLUS END TRACKING PROTEIN EB1; MUSCLE PROTEIN; MYOMEGALIN VARIANT 8; PEPTIDES AND PROTEINS; UNCLASSIFIED DRUG; ISOPROTEIN; NUCLEAR PROTEIN; PDE4DIP PROTEIN, HUMAN;

ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; FEMALE; GOLGI COMPLEX; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MASS SPECTROMETRY; MICROTUBULE; NUCLEOTIDE SEQUENCE; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; ANIMAL; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; MOUSE;

MAMMALIA;

ANIMALS; ENDOPLASMIC RETICULUM; GOLGI APPARATUS; HEK293 CELLS; HELA CELLS; HUMANS; MICE; MICROTUBULES; MUSCLE PROTEINS; NUCLEAR PROTEINS; PROTEIN ISOFORMS;

EID: 84911956027     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.155408     Document Type: Article

References (34)

1. Akhmanova, A. and Steinmetz, M. O. (2008). Tracking the ends: a dynamic protein network controls the fate of microtubule tips. Nat. Rev. Mol. Cell Biol. 9, 309-322.
2. Bejarano, E., Cabrera, M., Vega, L., Hidalgo, J. and Velasco, A. (2006). Golgi structural stability and biogenesis depend on associated PKA activity. J. Cell Sci. 119, 3764-3775.
3. Chabin-Brion, K., Marceiller, J., Perez, F., Settegrana, C., Drechou, A., Durand, G. and Poüs, C. (2001). The Golgi complex is a microtubuleorganizing organelle. Mol. Biol. Cell 12, 2047-2060.
4. Choi, Y. K., Liu, P., Sze, S. K., Dai, C. and Qi, R. Z. (2010). CDK5RAP2 stimulates microtubule nucleation by the gamma-tubulin ring complex. J. Cell Biol. 191, 1089-1095.
5. Cole, N. B., Sciaky, N., Marotta, A., Song, J. and Lippincott-Schwartz, J. (1996). Golgi dispersal during microtubule disruption: regeneration of Golgi stacks at peripheral endoplasmic reticulum exit sites. Mol. Biol. Cell 7, 631-650.
6. Diao, A., Frost, L., Morohashi, Y. and Lowe, M. (2008). Coordination of golgin tethering and SNARE assembly: GM130 binds syntaxin 5 in a p115-regulated manner. J. Biol. Chem. 283, 6957-6967.
7. Efimov, A., Kharitonov, A., Efimova, N., Loncarek, J., Miller, P. M., Andreyeva, N., Gleeson, P., Galjart, N., Maia, A. R., McLeod, I. X. et al. (2007). Asymmetric CLASP-dependent nucleation of noncentrosomal microtubules at the trans-Golgi network. Dev. Cell 12, 917-930.
8. Fong, K. W., Choi, Y. K., Rattner, J. B. and Qi, R. Z. (2008). CDK5RAP2 is a pericentriolar protein that functions in centrosomal attachment of the gammatubulin ring complex. Mol. Biol. Cell 19, 115-125.
9. Fong, K. W., Hau, S. Y., Kho, Y. S., Jia, Y., He, L. and Qi, R. Z. (2009). Interaction of CDK5RAP2 with EB1 to track growing microtubule tips and to regulate microtubule dynamics. Mol. Biol. Cell 20, 3660-3670.
10. Grigoriev, I., Gouveia, S. M., van der Vaart, B., Demmers, J., Smyth, J. T., Honnappa, S., Splinter, D., Steinmetz, M. O., Putney, J. W., Jr, Hoogenraad, C. C. et al. (2008). STIM1 is a MT-plus-end-tracking protein involved in remodeling of the ER. Curr. Biol. 18, 177-182.
11. Honnappa, S., Gouveia, S. M., Weisbrich, A., Damberger, F. F., Bhavesh, N. S., Jawhari, H., Grigoriev, I., van Rijssel, F. J., Buey, R. M., Lawera, A. et al. (2009). An EB1-binding motif acts as a microtubule tip localization signal. Cell 138, 366-376.
12. Hurtado, L., Caballero, C., Gavilan, M. P., Cardenas, J., Bornens, M. and Rios, R. M. (2011). Disconnecting the Golgi ribbon from the centrosome prevents directional cell migration and ciliogenesis. J. Cell Biol. 193, 917-933.
13. Keryer, G., Rios, R. M., Landmark, B. F., Skalhegg, B., Lohmann, S. M. and Bornens, M. (1993). A high-affinity binding protein for the regulatory subunit of cAMP-dependent protein kinase II in the centrosome of human cells. Exp. Cell Res. 204, 230-240.
14. Komarova, Y., De Groot, C. O., Grigoriev, I., Gouveia, S. M., Munteanu, E. L., Schober, J. M., Honnappa, S., Buey, R. M., Hoogenraad, C. C., Dogterom, M. et al. (2009). Mammalian end binding proteins control persistent microtubule growth. J. Cell Biol. 184, 691-706.
15. Lippincott-Schwartz, J. (1998). Cytoskeletal proteins and Golgi dynamics. Curr. Opin. Cell Biol. 10, 52-59.
16. Malhotra, V., Serafini, T., Orci, L., Shepherd, J. C. and Rothman, J. E. (1989). Purification of a novel class of coated vesicles mediating biosynthetic protein transport through the Golgi stack. Cell 58, 329-336.
17. Marra, P., Salvatore, L., Mironov, A., Jr, Di Campli, A., Di Tullio, G., Trucco, A., Beznoussenko, G., Mironov, A. and De Matteis, M. A. (2007). The biogenesis of the Golgi ribbon: the roles of membrane input from the ER and of GM130. Mol. Biol. Cell 18, 1595-1608.
18. Mavillard, F., Hidalgo, J., Megias, D., Levitsky, K. L. and Velasco, A. (2010). PKA-mediated Golgi remodeling during cAMP signal transmission. Traffic 11, 90-109.
19. Miller, P. M., Folkmann, A. W., Maia, A. R., Efimova, N., Efimov, A. and Kaverina, I. (2009). Golgi-derived CLASP-dependent microtubules control Golgi organization and polarized trafficking in motile cells. Nat. Cell Biol. 11, 1069-1080.
20. Presley, J. F., Cole, N. B., Schroer, T. A., Hirschberg, K., Zaal, K. J. and Lippincott-Schwartz, J. (1997). ER-to-Golgi transport visualized in living cells. Nature 389, 81-85.
21. Rios, R. M. and Bornens, M. (2003). The Golgi apparatus at the cell centre. Curr. Opin. Cell Biol. 15, 60-66.
22. Ríos, R. M., Sanchís, A., Tassin, A. M., Fedriani, C. and Bornens, M. (2004). GMAP-210 recruits gamma-tubulin complexes to cis-Golgi membranes and is required for Golgi ribbon formation. Cell 118, 323-335.
23. Rivero, S., Cardenas, J., Bornens, M. and Rios, R. M. (2009). Microtubule nucleation at the cis-side of the Golgi apparatus requires AKAP450 and GM130. EMBO J. 28, 1016-1028.
24. Scales, S. J., Pepperkok, R. and Kreis, T. E. (1997). Visualization of ER-to-Golgi transport in living cells reveals a sequential mode of action for COPII and COPI. Cell 90, 1137-1148.
25. Schmidt, P. H., Dransfield, D. T., Claudio, J. O., Hawley, R. G., Trotter, K. W., Milgram, S. L. and Goldenring, J. R. (1999). AKAP350, a multiply spliced protein kinase A-anchoring protein associated with centrosomes. J. Biol. Chem. 274, 3055-3066.
26. Sütterlin, C. and Colanzi, A. (2010). The Golgi and the centrosome: building a functional partnership. J. Cell Biol. 188, 621-628.
27. Svitkina, T. M., Verkhovsky, A. B. and Borisy, G. G. (1996). Plectin sidearms mediate interaction of intermediate filaments with microtubules and other components of the cytoskeleton. J. Cell Biol. 135, 991-1007.
28. Takahashi, M., Shibata, H., Shimakawa, M., Miyamoto, M., Mukai, H. and Ono, Y. (1999). Characterization of a novel giant scaffolding protein, CG-NAP, that anchors multiple signaling enzymes to centrosome and the golgi apparatus. J. Biol. Chem. 274, 17267-17274.
29. Takahashi, M., Yamagiwa, A., Nishimura, T., Mukai, H. and Ono, Y. (2002). Centrosomal proteins CG-NAP and kendrin provide microtubule nucleation sites by anchoring gamma-tubulin ring complex. Mol. Biol. Cell 13, 3235-3245.
30. Verde, I., Pahlke, G., Salanova, M., Zhang, G., Wang, S., Coletti, D., Onuffer, J., Jin, S. L. and Conti, M. (2001). Myomegalin is a novel protein of the golgi/ centrosome that interacts with a cyclic nucleotide phosphodiesterase. J. Biol. Chem. 276, 11189-11198.
31. Vinogradova, T., Paul, R., Grimaldi, A. D., Loncarek, J., Miller, P. M., Yampolsky, D.,Magidson, V., Khodjakov, A., Mogilner, A. and Kaverina, I. (2012). Concerted effort of centrosomal and Golgi-derived microtubules is required for proper Golgi complex assembly but not for maintenance. Mol. Biol. Cell 23, 820-833.
32. Wang, Z., Wu, T., Shi, L., Zhang, L., Zheng, W., Qu, J. Y., Niu, R. and Qi, R. Z. (2010). Conserved motif of CDK5RAP2 mediates its localization to centrosomes and the Golgi complex. J. Biol. Chem. 285, 22658-22665.
33. Watson, P., Forster, R., Palmer, K. J., Pepperkok, R. and Stephens, D. J. (2005). Coupling of ER exit to microtubules through direct interaction of COPII with dynactin. Nat. Cell Biol. 7, 48-55.
34. Witczak, O., Skalhegg, B. S., Keryer, G., Bornens, M., Taskén, K., Jahnsen, T. and Orstavik, S. (1999). Cloning and characterization of a cDNA encoding an A-kinase anchoring protein located in the centrosome, AKAP450. EMBO J. 18, 1858-1868.