CAMSAP3-dependent microtubule dynamics regulates Golgi assembly in epithelial cells

Jing Wang; Honglin Xu; Yuqiang Jiang; Mikiko Takahashi; Masatoshi Takeichi; Wenxiang Meng

doi:10.1016/j.jgg.2016.11.005

Volume 44 Issue 1

Jan. 2017

Turn off MathJax

Article Contents

Article Navigation > Journal of Genetics and Genomics > 2017 > 44(1): 39-49

PDF( 5482 KB)

CAMSAP3-dependent microtubule dynamics regulates Golgi assembly in epithelial cells

doi: 10.1016/j.jgg.2016.11.005

a
State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China
b
University of Chinese Academy of Sciences, No. 19A Yuquan Road, Beijing 100049, China
c
Faculty of Pharmaceutical Sciences, Teikyo Heisei University, 4-21-2 Nakano, Nakano-ku, Tokyo 164-8530, Japan
d
RIKEN Center for Developmental Biology, 2-2-3 Chuo-ku, Kobe 650-0047, Japan

More Information

Corresponding author: E-mail address: wxmeng@genetics.ac.cn (Wenxiang Meng)
Received Date: 2016-07-07
Accepted Date: 2016-11-30
Rev Recd Date: 2016-11-19

Available Online: 2016-12-26

Publish Date: 2017-01-20

Abstract

Abstract

The Golgi assembly pattern varies among cell types. In fibroblast cells, the Golgi apparatus concentrates around the centrosome that radiates microtubules; whereas in epithelial cells, whose microtubules are mainly noncentrosomal, the Golgi apparatus accumulates around the nucleus independently of centrosome. Little is known about the mechanisms behind such cell type-specific Golgi and microtubule organization. Here, we show that the microtubule minus-end binding protein Nezha/CAMSAP3 (calmodulin-regulated spectrin-associated protein 3) plays a role in translocation of Golgi vesicles in epithelial cells. This function of CAMSAP3 is supported by CG-NAP (centrosome and Golgi localized PKN-associated protein) through their binding. Depletion of either one of these proteins similarly induces fragmentation of Golgi membranes. Furthermore, we find that stathmin-dependent microtubule dynamics is graded along the radial axis of cells with highest activity at the perinuclear region, and inhibition of this gradient disrupts perinuclear distribution of the Golgi apparatus. We propose that the assembly of the Golgi apparatus in epithelial cells is induced by a multi-step process, which includes CAMSAP3-dependent Golgi vesicle clustering and graded microtubule dynamics.
- CG-NAP,
- Nezha/CAMSAP3,
- Golgi,
- Noncentrosomal microtubules,
- Stathmin

FullText(HTML)

References(33)

References

[1]	Allan, V.J., Thompson, H.M., McNiven, M.A. Motoring around the Golgi Nat. Cell Biol., 4 (2002),pp. E236-E242
[2]	Andersen, S.S. Spindle assembly and the art of regulating microtubule dynamics by MAPs and Stathmin/Op18 Trends Cell Biol., 10 (2000),pp. 261-267
[3]	Burkhardt, J.K. The role of microtubule-based motor proteins in maintaining the structure and function of the Golgi complex Biochim. Biophys. Acta, 1404 (1998),pp. 113-126
[4]	Cassimeris, L. The oncoprotein 18/stathmin family of microtubule destabilizers Curr. Opin. Cell Biol., 14 (2002),pp. 18-24
[5]	Colanzi, A., Suetterlin, C., Malhotra, V. Cell-cycle-specific Golgi fragmentation: how and why? Curr. Opin. Cell Biol., 15 (2003),pp. 462-467
[6]	Cole, N.B., Sciaky, N., Marotta, A. et al. Golgi dispersal during microtubule disruption: regeneration of Golgi stacks at peripheral endoplasmic reticulum exit sites Mol. Biol. Cell, 7 (1996),pp. 631-650
[7]	Efimov, A., Kharitonov, A., Efimova, N. et al. Asymmetric CLASP-dependent nucleation of noncentrosomal microtubules at the trans-Golgi network Dev. Cell, 12 (2007),pp. 917-930
[8]	Gillingham, A.K., Munro, S. The PACT domain, a conserved centrosomal targeting motif in the coiled-coil proteins AKAP450 and pericentrin EMBO Rep., 1 (2000),pp. 524-529
[9]	Horwitz, S.B., Shen, H.J., He, L. et al. The microtubule-destabilizing activity of metablastin (p19) is controlled by phosphorylation J. Biol. Chem., 272 (1997),pp. 8129-8132
[10]	Jiang, K., Hua, S., Mohan, R. et al. Microtubule minus-end stabilization by polymerization-driven CAMSAP deposition Dev. Cell, 28 (2014),pp. 295-309
[11]	Kim, H.S., Takahashi, M., Matsuo, K. et al. Recruitment of CG-NAP to the Golgi apparatus through interaction with dynein-dynactin complex Genes Cells, 12 (2007),pp. 421-434
[12]	Larocca, M.C., Shanks, R.A., Tian, L. et al. AKAP350 interaction with cdc42 interacting protein 4 at the Golgi apparatus Mol. Biol. Cell, 15 (2004),pp. 2771-2781
[13]	Larsson, N., Marklund, U., Gradin, H.M. et al. Control of microtubule dynamics by oncoprotein 18: dissection of the regulatory role of multisite phosphorylation during mitosis Mol. Cell. Biol., 17 (1997),pp. 5530-5539
[14]	Lowe, M. Structural organization of the Golgi apparatus Curr. Opin. Cell Biol., 23 (2011),pp. 85-93
[15]	Meng, W., Mushika, Y., Ichii, T. et al. Anchorage of microtubule minus ends to adherens junctions regulates epithelial cell-cell contacts Cell, 135 (2008),pp. 948-959
[16]	Miller, P.M., Folkmann, A.W., Maia, A.R. et al. Golgi-derived CLASP-dependent microtubules control Golgi organization and polarized trafficking in motile cells Nat. Cell Biol., 11 (2009),pp. 1069-1080
[17]	Mimori-Kiyosue, Y., Shiina, N., Tsukita, S. The dynamic behavior of the APC-binding protein EB1 on the distal ends of microtubules Curr. Biol., 10 (2000),pp. 865-868
[18]	Nagae, S., Meng, W., Takeichi, M. Non-centrosomal microtubules regulate F-actin organization through the suppression of GEF-H1 activity Genes Cells, 18 (2013),pp. 387-396
[19]	Nishimura, T., Takahashi, M., Kim, H.S. et al. Centrosome-targeting region of CG-NAP causes centrosome amplification by recruiting cyclin E-cdk2 complex Genes Cells, 10 (2005),pp. 75-86
[20]	Rivero, S., Cardenas, J., Bornens, M. et al. EMBO J., 28 (2009),pp. 1016-1028
[21]	Schmidt, P.H., Dransfield, D.T., Claudio, J.O. et al. AKAP350, a multiply spliced protein kinase A-anchoring protein associated with centrosomes J. Biol. Chem., 274 (1999),pp. 3055-3066
[22]	Schulze, E., Kirschner, M. Microtubule dynamics in interphase cells J. Cell Biol., 102 (1986),pp. 1020-1031
[23]	Sillibourne, J.E., Milne, D.M., Takahashi, M. et al. Centrosomal anchoring of the protein kinase CK1delta mediated by attachment to the large, coiled-coil scaffolding protein CG-NAP/AKAP450 J. Mol. Biol., 322 (2002),pp. 785-797
[24]	Sobel, A., Boutterin, M.C., Beretta, L. et al. Intracellular substrates for extracellular signaling. Characterization of a ubiquitous, neuron-enriched phosphoprotein (stathmin) J. Biol. Chem., 264 (1989),pp. 3765-3772
[25]	Sutterlin, C., Colanzi, A. The Golgi and the centrosome: building a functional partnership J. Cell Biol., 188 (2010),pp. 621-628
[26]	Takahashi, M., Shibata, H., Shimakawa, M. et al. Characterization of a novel giant scaffolding protein, CG-NAP, that anchors multiple signaling enzymes to centrosome and the golgi apparatus J. Biol. Chem., 274 (1999),pp. 17267-17274
[27]	Takahashi, M., Yamagiwa, A., Nishimura, T. et al. Centrosomal proteins CG-NAP and kendrin provide microtubule nucleation sites by anchoring gamma-tubulin ring complex Mol. Biol. Cell, 13 (2002),pp. 3235-3245
[28]	Tanaka, N., Meng, W., Nagae, S. et al. Nezha/CAMSAP3 and CAMSAP2 cooperate in epithelial-specific organization of noncentrosomal microtubules Proc. Natl. Acad. Sci. U. S. A., 109 (2012),pp. 20029-20034
[29]	Thyberg, J., Moskalewski, S. Role of microtubules in the organization of the Golgi complex Exp. Cell Res., 246 (1999),pp. 263-279
[30]	Toya, M., Kobayashi, S., Kawasaki, M. et al. CAMSAP3 orients the apical-to-basal polarity of microtubule arrays in epithelial cells Proc. Natl. Acad. Sci. U. S. A., 113 (2016),pp. 332-337
[31]	Witczak, O., Skalhegg, B.S., Keryer, G. et al. Cloning and characterization of a cDNA encoding an A-kinase anchoring protein located in the centrosome, AKAP450 EMBO J., 18 (1999),pp. 1858-1868
[32]	Wu, J., de Heus, C., Liu, Q. et al. Molecular pathway of microtubule organization at the Golgi apparatus Dev. Cell, 39 (2016),pp. 44-60
[33]	Yau, K.W., van Beuningen, S.F., Cunha-Ferreira, I. et al. Microtubule minus-end binding protein CAMSAP2 controls axon specification and dendrite development Neuron, 82 (2014),pp. 1058-1073