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J. Cell Biol. 149 (7): 1455-1472

Copyright © 2000 by the Rockefeller University Press.

Original Article

Gap43, Marcks, and Cap23 Modulate Pi(4,5)p2 at Plasmalemmal Rafts, and Regulate Cell Cortex Actin Dynamics through a Common Mechanism

Thorsten Lauxa, Kiyoko Fukamib, Marcus Thelenc, Tamara Goluba, Dunja Freya, , and Pico Caronia

a Friedrich Miescher Institute, CH-4058 Basel, Switzerland
b Department of Biochemistry, Institute of Medical Sciences, Tokyo, Japan
c Theodor Kocher Institut, Bern, Switzerland
Friedrich Miescher Institute, Maulbeerstrasse 66, CH-4058 Basel, Switzerland.41-61-697-397641-61-697-3727

caroni{at}fmi.ch

Abstract: The dynamic properties of the cell cortex and its actin cytoskeleton determine important aspects of cell behavior and are a major target of cell regulation. GAP43, myristoylated alanine-rich C kinase substrate (MARCKS), and CAP23 (GMC) are locally abundant, plasmalemma-associated PKC substrates that affect actin cytoskeleton. Their expression correlates with morphogenic processes and cell motility, but their role in cortex regulation has been difficult to define mechanistically. We now show that the three proteins accumulate at rafts, where they codistribute with PI(4,5)P2, and promote its retention and clustering. Binding and modulation of PI(4,5)P2 depended on the basic effector domain (ED) of these proteins, and constructs lacking the ED functioned as dominant inhibitors of plasmalemmal PI(4,5)P2 modulation. In the neuronlike cell line, PC12, NGF- and substrate-induced peripheral actin structures, and neurite outgrowth were greatly augmented by any of the three proteins, and suppressed by {Delta}ED mutants. Agents that globally mask PI(4,5)P2 mimicked the effects of GMC on peripheral actin recruitment and cell spreading, but interfered with polarization and process formation. Dominant negative GAP43({Delta}ED) also interfered with peripheral nerve regeneration, stimulus-induced nerve sprouting and control of anatomical plasticity at the neuromuscular junction of transgenic mice. These results suggest that GMC are functionally and mechanistically related PI(4,5)P2 modulating proteins, upstream of actin and cell cortex dynamics regulation.

Key Words: neurite outgrowth • cell spreading • anatomical plasticity • actin recruitment • lipid microdomain

Abbreviations used in this paper: CaM, calmodulin; GMC, GAP23, MARCKS, and CAP23; MARCKS, myristoylated alanine-rich C kinase substrate; ED, effector domain; PKC, protein kinase C; PLC, phospholipase C.

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Intracytoplasmic domains of MHC class II molecules are essential for lipid-raft-dependent signaling.
S. Becart, N. Setterblad, S. Ostrand-Rosenberg, S. J. Ono, D. Charron, and N. Mooney (2003)
J. Cell Sci. 116, 2565-2575
   Abstract »    Full Text »    PDF »
The 43,000 Growth-associated Protein Functions as a Negative Growth Regulator in Glioma.
Z.-y. Huang, Y. Wu, S. P. Burke, and D. H. Gutmann (2003)
Cancer Res. 63, 2933-2939
   Abstract »    Full Text »    PDF »
Neural cell adhesion molecule (NCAM) association with PKC{beta}2 via {beta}I spectrin is implicated in NCAM-mediated neurite outgrowth.
I. Leshchyns'ka, V. Sytnyk, J. S. Morrow, and M. Schachner (2003)
J. Cell Biol. 161, 625-639
   Abstract »    Full Text »    PDF »
Membrane Lipid Organization Is Critical for Human Neutrophil Polarization.
L. M. Pierini, R. J. Eddy, M. Fuortes, S. Seveau, C. Casulo, and F. R. Maxfield (2003)
J. Biol. Chem. 278, 10831-10841
   Abstract »    Full Text »    PDF »
Increased Electrotonic Coupling in Spinal Motoneurons After Transient Botulinum Neurotoxin Paralysis in the Neonatal Rat.
A. M. Pastor, G. Z. Mentis, R. R. De la Cruz, E. Diaz, and R. Navarrete (2003)
J Neurophysiol 89, 793-805
   Abstract »    Full Text »    PDF »
Nerve growth factor controls GAP-43 mRNA stability via the phosphoprotein ARPP-19.
N. Irwin, S. Chao, L. Goritchenko, A. Horiuchi, P. Greengard, A. C. Nairn, and L. I. Benowitz (2002)
PNAS 99, 12427-12431
   Abstract »    Full Text »    PDF »
Lateral Sequestration of Phosphatidylinositol 4,5-Bisphosphate by the Basic Effector Domain of Myristoylated Alanine-rich C Kinase Substrate Is Due to Nonspecific Electrostatic Interactions.
J. Wang, A. Gambhir, G. Hangyas-Mihalyne, D. Murray, U. Golebiewska, and S. McLaughlin (2002)
J. Biol. Chem. 277, 34401-34412
   Abstract »    Full Text »    PDF »
Agonist-induced PIP2 Hydrolysis Inhibits Cortical Actin Dynamics: Regulation at a Global but not at a Micrometer Scale.
J. van Rheenen and K. Jalink (2002)
Mol. Biol. Cell 13, 3257-3267
   Abstract »    Full Text »    PDF »
A Novel Strategy to Engineer Functional Fluorescent Inhibitory G-protein alpha Subunits.
J. L. Leaney, A. Benians, F. M. Graves, and A. Tinker (2002)
J. Biol. Chem. 277, 28803-28809
   Abstract »    Full Text »    PDF »
Growth Cone Collapse Induced by Semaphorin 3A Requires 12/15-Lipoxygenase.
K. Mikule, J. C. Gatlin, B. A. de la Houssaye, and K. H. Pfenninger (2002)
J. Neurosci. 22, 4932-4941
   Abstract »    Full Text »    PDF »
Cosignaling of NCAM via lipid rafts and the FGF receptor is required for neuritogenesis.
P. Niethammer, M. Delling, V. Sytnyk, A. Dityatev, K. Fukami, and M. Schachner (2002)
J. Cell Biol. 157, 521-532
   Abstract »    Full Text »    PDF »
Myristoylated Alanine-rich C Kinase Substrate (MARCKS) Sequesters Spin-labeled Phosphatidylinositol 4,5-Bisphosphate in Lipid Bilayers.
M. E. Rauch, C. G. Ferguson, G. D. Prestwich, and D. S. Cafiso (2002)
J. Biol. Chem. 277, 14068-14076
   Abstract »    Full Text »    PDF »
Comparative Gene Expression Profile Analysis of Neurofibromatosis 1-associated and Sporadic Pilocytic Astrocytomas.
D. H. Gutmann, N. M. Hedrick, J. Li, R. Nagarajan, A. Perry, and M. A. Watson (2002)
Cancer Res. 62, 2085-2091
   Abstract »    Full Text »    PDF »
Regulation of Protein Kinase C in Escherichia coli K1 Invasion of Human Brain Microvascular Endothelial Cells.
S. K. Sukumaran and N. V. Prasadarao (2002)
J. Biol. Chem. 277, 12253-12262
   Abstract »    Full Text »    PDF »
A Lipid-regulated Docking Site on Vinculin for Protein Kinase C.
W. H. Ziegler, U. Tigges, A. Zieseniss, and B. M. Jockusch (2002)
J. Biol. Chem. 277, 7396-7404
   Abstract »    Full Text »    PDF »
Growth-Associated Protein-43 Is Required for Commissural Axon Guidance in the Developing Vertebrate Nervous System.
Y. Shen, S. Mani, S. L. Donovan, J. E. Schwob, and K. F. Meiri (2002)
J. Neurosci. 22, 239-247
   Abstract »    Full Text »    PDF »
Heterozygosity for the neurofibromatosis 1 (NF1) tumor suppressor results in abnormalities in cell attachment, spreading and motility in astrocytes.
D. H. Gutmann, Y. L. Wu, N. M. Hedrick, Y. Zhu, A. Guha, and L. F. Parada (2001)
Hum. Mol. Genet. 10, 3009-3016
   Abstract »    Full Text »    PDF »
Amoeboid leukocyte crawling through extracellular matrix: lessons from the Dictyostelium paradigm of cell movement.
P. Friedl, S. Borgmann, and E.-B. Brocker (2001)
J. Leukoc. Biol. 70, 491-509
   Abstract »    Full Text »    PDF »

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