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Originally published In Press as doi:10.1074/jbc.M005693200 on October 2, 2000

J. Biol. Chem., Vol. 276, Issue 1, 583-592, January 5, 2001
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The N-terminal End of Nebulin Interacts with Tropomodulin at the Pointed Ends of the Thin Filaments*

Abigail S. McElhinnyDagger , Bernhard Kolmerer§, Velia M. Fowler, Siegfried Labeit§, and Carol C. GregorioDagger ||**

From the Departments of Dagger  Cell Biology and Anatomy and || Cellular and Molecular Biology, University of Arizona, Tucson, Arizona 85724, the § European Molecular Biology Laboratory, Heidelberg 69012, Germany, and the  Department of Cell Biology, The Scripps Research Institute, La Jolla, California 92037

Strict regulation of actin thin filament length is critical for the proper functioning of sarcomeres, the basic contractile units of myofibrils. It has been hypothesized that a molecular template works with actin filament capping proteins to regulate thin filament lengths. Nebulin is a giant protein (~800 kDa) in skeletal muscle that has been proposed to act as a molecular ruler to specify the thin filament lengths characteristic of different muscles. Tropomodulin (Tmod), a pointed end thin filament capping protein, has been shown to maintain the final length of the thin filaments. Immunofluorescence microscopy revealed that the N-terminal end of nebulin colocalizes with Tmod at the pointed ends of thin filaments. The three extreme N-terminal modules (M1-M2-M3) of nebulin bind specifically to Tmod as demonstrated by blot overlay, bead binding, and solid phase binding assays. These data demonstrate that the N terminus of the nebulin molecule extends to the extreme end of the thin filament and also establish a novel biochemical function for this end. Two Tmod isoforms, erythrocyte Tmod (E-Tmod), expressed in embryonic and slow skeletal muscle, and skeletal Tmod (Sk-Tmod), expressed late in fast skeletal muscle differentiation, bind on overlapping sites to recombinant N-terminal nebulin fragments. Sk-Tmod binds nebulin with higher affinity than E-Tmod does, suggesting that the Tmod/nebulin interaction exhibits isoform specificity. These data provide evidence that Tmod and nebulin may work together as a linked mechanism to control thin filament lengths in skeletal muscle.

* This work was supported by the National Institutes of Health Grants HL57461 and HL03985 (to C. C. G.), HL07249 (to A. S. M.), and GM3425 (to V. M. F.), Deutsche Forschungsgemeinschaft Grant La 668/3-3 (to S. L.), and an award from the Human Frontier Science Program (to C. C. G., V. M. F., and S. L.).The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBankTM/EMBL Data Bank with accession number(s) X83957.

** To whom correspondence should be addressed: Dept. of Cell Biology and Anatomy, LSN455, The University of Arizona, 1501 N. Campbell Ave., Tucson, AZ 85724. Tel.: 520-626-8113; Fax: 520-626-2097; E-mail: gregorio@u.arizona.edu.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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