Fluorescence approaches to the study of the actin-nucleating and bundling activities of synapsin I

doi:10.1016/0928-4257(93)90005-E

Journal of Physiology-Paris

Volume 87, Issue 2, 1993, Pages 117-122

https://doi.org/10.1016/0928-4257(93)90005-E Get rights and content

Abstract

Synapsin I is a neuron-specific phosphoprotein which binds to small synaptic vesicles and actin in a phosphorylation-dependent fashion. We have analyzed the ability of synapsin I to interact with actin monomers and filaments using purified proteins derivatized with fluorescent probes. Synapsin I accelerates the initial rate of actin polymerization and increases the final steady-state levels of polymerized actin. The fraction of total actin polymerized by synapsin I strongly depends on the synapsin I-actin ratio. We have visualized the actin-bundling activity of synapsin I using a non-perturbing method, video-enhanced microscopy of fluoresceinated synapsin I and actin filaments. Our findings suggest that synapsin I exerts a control on the physical characteristics of the cytoskeletal network of the nerve terminal and are consistent with the proposed role of synapsin I in mediating the interaction of synaptic vesicles with actin.

References (19)

F. Benfenati et al.
Interaction of free and synaptic vesicle-bound synapsin I with F-actin
Neuron
(1992)
R. Fesce et al.
Effects of the neuronal phosphoprotein synapsin I on actin polymerization. II. Analytical interpretation of kinetic curves
J Biol Chem
(1992)
O.H. Lowry et al.
Protein measurement with the Folin phenol reagent
J Biol Chem
(1951)
T.L. McGuinness et al.
Ca²⁺/calmodulin-dependent protein kinase II isozymic forms from rat forebrain and cerebellum
J Biol Chem
(1985)
M.A.K. Markwell et al.
A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples
Anal Biochem
(1978)
W. Schiebler et al.
Characterization of synapsin I binding to small synaptic vesicles
J Biol Chem
(1986)
J.A. Spudich et al.
The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosin-troponin complex with actin and the proteolytic fragments of myosin
J Biol Chem
(1971)
T. Ueda et al.
Adenosine 3′:5′-monophosphate-regulated phosphoprotein system of neuronal membranes. I. Solubilization, purification, and some properties of an endogenous phosphoprotein
J Biol Chem
(1977)
F. Valtorta et al.
Structure and function of the synapsins
J Biol Chem
(1992)

There are more references available in the full text version of this article.

Cited by (4)

Effects of synaptic vesicles on actin polymerization
1996, FEBS Letters
We have analyzed the effects of synaptic vesicles on actin polymerization by using a time-resolved spectrofluorometric assay. We have found that synaptic vesicles have complex effects on the kinetics of actin polymerization, which vary depending on whether the synaptic vesicle-specific phosphoprotein synapsin I is absent or present on their membrane. Synapsin I bound either to synaptic vesicles or to pure phospholipid vesicles exhibits phosphorylation-dependent actin-nucleating activity. Synaptic vesicles depleted of endogenous synapsin I decrease the rate and the final extent of actin polymerization, an effect which is not observed with pure phospholipid vesicles. Thus, the state of association of synapsin I with synaptic vesicles, which is modulated by its state of phosphorylation, may affect actin assembly and the physico-chemical characteristics of the synaptic vesicle microenvironment.
Membrane Trafficking in Nerve Terminals
1995, Advances in Pharmacology
Most exocytotic release of neurotransmitters occurs in the nerve terminal, which can be envisaged as a dedicated secretory compartment. Thus, the nerve terminal is the most interesting compartment from the point of view of membrane trafficking, also because it is indirectly involved in a large part of the membrane trafficking events occurring in other neuronal compartments; most membrane-bound organelles found in axons are actually traveling to or from the nerve ending, and sorting of proteins destined to exocytosis from nerve endings is a major task of the Golgi complex. In recent times, intense research on the mechanism of neurotransmitter release has been done. The basic features of the release process are shared with other kinds of exocytosis, such as exocytosis of synaptic vesicles—mechanisms of fusion. Membrane fusion is a ubiquitous process characterizing membrane traffic among the various intracellular compartments and with the plasma membrane. In regulated exocytosis, membrane fusion must be governed so that it is triggered only in response to the specific stimulus. Two possibilities exist: either biological membranes are keen to fuse with each other and specific proteins have the ability to keep this spontaneous process under control or biological membranes are intrinsically resistant to fusing with each other and therefore constitutive and regulated fusion occurs with the intervention of fusion proteins. This chapter describes the life cycle of the neurotransmitter storage organelles and the release process that occurs at the nerve terminal level, underlining the features shared with exocytosis in other cells as well as those peculiar to neuronal cells.
Synapsin I, an actin-binding protein regulating synaptic vesicle traffic in the nerve terminal
1994, Advances in Second Messenger and Phosphoprotein Research
Cdk5 in neuroskeletal dynamics
2003, NeuroSignals

^∗: Present address: Unité de la Rage, Institut Pasteur, Paris, France.

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Fluorescence approaches to the study of the actin-nucleating and bundling activities of synapsin I

Abstract

Neuron

J Biol Chem

J Biol Chem

J Biol Chem

Anal Biochem

J Biol Chem

J Biol Chem

J Biol Chem

J Biol Chem