Common and distinct tubulin binding sites for microtubule-associated proteins.

Littauer, Uriel Z.; Giveon, David; Thierauf, Marion; Ginzburg, Irith; Ponstingl, Herwig

doi:10.1073/pnas.83.19.7162

Cited by 210 publications

(146 citation statements)

References 29 publications

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“…Tau binds to the acidic COOH terminus of tubulin (Littauer et al, 1986) so that from charge complementarity one would expect the COOH-terminal part of tau to interact with tubu- Figure 7. End region of a paracrystal stained with ammonium molybdate.…”

Section: Influence Of Phosphorylation On Length and Elasticity Of Taumentioning

confidence: 99%

Tau protein becomes long and stiff upon phosphorylation: correlation between paracrystalline structure and degree of phosphorylation.

Hagestedt

Lichtenberg

Wille

et al. 1989

The Journal of Cell Biology

189

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Abstract. In a previous report we have shown that microtubule-associated protein tau can be induced to form paracrystals (Lichtenberg, B., E.-M. Mandelkow, T. Hagestedt, and E. . Nature [Lond.]. 334:359-362). A striking feature was the high degree of elasticity of the molecules. We now report that this property is related to the state of phosphorylation. When tau is dephosphorylated by alkaline phosphatase, it becomes shorter and more elastic; when it is phosphorylated by Ca++/calmodulin-dependent kinase, it becomes longer and stiffer. This may provide a model for the control of structural properties of tau-like molecules by phosphorylation.T AU is one of the microtubule-associated proteins (MAPs)' in mammalian brain (Weingarten et al., 1975). When isolated from brain tissue it is a mixture of several polypeptides of apparent molecule mass values between 50 and 70 kD. The sequence oftau protein from mouse containing 364 amino acid residues has been reported (Lee et al., 1988a). A highly homologous human form oftau has been found in the neurofibrillary tangles of Alzheimer's disease (Goedert et al., 1988). The COOH-terminal part oftau contains three internal repeats and seems to be responsible for the binding to microtubules (Aizawa et al., 1988). This part is also homologous to the COOH-terminal region of microtubule-associated protein 2 (MAP2), another brain MAP (Lewis et all., 1988), suggesting that it might serve as a microtubule-binding domain for a family of proteins.Tau is heat stable and soluble in perchloric acid (Cleveland et al., 1977;Lindwall and Cole, 1984b); this forms the basis for the isolation procedure (see Materials and Methods). Cole and co-workers showed that the apparent heterogeneity oftau can be reduced by controlling the state of phosphorylation (Lindwall and Cole, 1984b;Baudier and Cole, 1987a). Tan treated by alkaline phosphatase shows four main isoforms on SDS gels, termed taul--4. All of them can be phosphorylated by several kinases. In particular, the Ca++/calmodulin-dependent kinase (CaMK) induces a conformational change that results in an upward shift of the bands in the gel. Thus, when the protein is isolated in a mixed state of phosphorylation the number of observed bands is greater than four. The change in electrophoretic mobility is a convenient assay to monitor phosphorylation by CaMK; it is not observed 1. Abbreviations used in this paper: CaMK, Ca++/calmodulin-dependent protein kinase; MAP, microtubule-associated protein; MAP2, microtubuleassociated protein 2.after phosphorylation with other kinases such as protein kinase C.Structural information on tau or other MAPs is limited so far. Hydrodynamic data (Cleveland et al., 1977) and metal shadowing (Hirokawa et al., 1988) suggest a rod-like shape. In our attempts to crystallize tau we have recently obtained paracrystals suitable for electron microscopy and image processing (Lichtenberg et al., 1988). They show distinct transverse banding and polarity, indicating that the protein subunits are aligned with the same orientation...

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Section: Influence Of Phosphorylation On Length and Elasticity Of Taumentioning

confidence: 99%

Tau protein becomes long and stiff upon phosphorylation: correlation between paracrystalline structure and degree of phosphorylation.

Hagestedt

Lichtenberg

Wille

et al. 1989

The Journal of Cell Biology

189

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“…Several isogenes (-6 in higher eukaryotes), encoding for each a or A subunit, and a number of different posttranslational modifications (PTMs)1 have been evidenced (for review see Sullivan, 1988;Joshi and Cleveland, 1990;Murphy, (the last 15 residues of the C-terminal sequence) of a-and f-tubulin, which extends out of the microtubular lattice. This region is likely involved in the interactions with microtubule-associated proteins (MAPs), although accurate localization of the binding site remains a controversial question (Serrano et al, 1985;Littauer et al, 1986;Maccioni et al, 1988;Paschal et al, 1989;Goldsmith et al, 1991).…”

Section: Introductionmentioning

confidence: 99%

Reversible polyglutamylation of alpha- and beta-tubulin and microtubule dynamics in mouse brain neurons.

Audebert

Desbruyères

Gruszczynski

et al. 1993

MBoC

125

114

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The relationship between microtubule dynamics and polyglutamylation of [3H]glutamate into a-and 3-tubulin, whereas taxol had no effect for a-tubulin and a stimulating effect for f-tubulin. These results strongly suggest that microtubule polymers are the preferred substrate for polyglutamylation. Chase experiments revealed the existence of a reversal reaction that, in the case of a-tubulin, was not affected by microtubule drugs, suggesting that deglutamylation of this subunit can occur on both polymers and soluble tubulin. Evidence was obtained that deglutamylation of a-tubulin operates following two distinct rates depending on the length of the polyglutamyl chain, the distal units (4th-6th) being removed rapidly whereas the proximal ones (lst-3rd) appearing much more resistant to deglutamylation. Partition of glutamylated a-tubulin isoforms was also correlated with the length of the polyglutamyl chain. Forms bearing four to six units were recovered specifically in the polymeric fraction, whereas those bearing one to three units were distributed evenly between polymeric and soluble fractions. It thus appears that the slow rate component of the deglutamylation reaction offers to neurons the possibility to maintain a basal level of glutamylated a-tubulin in the soluble pool independently of microtubule dynamics. Finally, some differences observed in the glutamylation of a-and ,B-tubulin suggest that distinct enzymes are involved.

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“…Assuming a receptor/ligand relationship between high-Mr MAP molecules and their interacting molecules, the goal is to narrow down the interaction site to the essential amino acid sequences. In this approach it should also be possible to establish whether certain high-Mr MAP species show preferences in binding to particular tubulin isoforms and their peptides (Littauer et al, 1986;Maccioni et al, 1988). Major advances in the understanding of MAP functions are expected to be made using experimental strategies based on recombinant DNA technology.…”

Section: Discussionmentioning

confidence: 99%

“…Using solid phase binding assays, a number of proteins have been shown to interact with MAP 2. These include the 68 kDa (Heimann et al, 1985;Furtner & Wiche, 1987) as well as the 160 kDa and the 200 kDa neurofilament proteins (Furtner & Wiche, 1987), intact and fragmented tubulin subunits (Littauer et al, 1986;Furtner & Wiche, 1987), plectin and MAP 2 itself (Furtner & Wiche, 1987), the latter indicating self-association of MAP 2 (see also Foisner & Wiche, 1985). Furthermore, it was shown in previous studies that MAP 2 binds to neurofilaments (Leterrier et al, 1982) and to actin filaments (see Pollard et al, 1984, and references therein), the latter being affected by Ca2+/phospholipid-dependent kinase (see above) and Ca2+/calmodulin (Kotani et al, 1985;Sobue et al, 1985).…”

Section: Mapmentioning

confidence: 99%