Differential targeting of nNOS and AQP4 to dystrophin-deficient sarcolemma by membrane-directed alpha-dystrobrevin

J Cell Sci. 2008 Jan 1;121(Pt 1):48-54. doi: 10.1242/jcs.020701. Epub 2007 Dec 4.

Abstract

alpha-Dystrobrevin associates with and is a homologue of dystrophin, the protein linked to Duchenne and Becker muscular dystrophies. We used a transgenic approach to restore alpha-dystrobrevin to the sarcolemma in mice that lack dystrophin (mdx mice) to study two interrelated functions: (1) the ability of alpha-dystrobrevin to rescue components of the dystrophin complex in the absence of dystrophin and (2) the ability of sarcolemmal alpha-dystrobrevin to ameliorate the dystrophic phenotype. We generated transgenic mice expressing alpha-dystrobrevin-2a linked to a palmitoylation signal sequence and bred them onto the alpha-dystrobrevin-null and mdx backgrounds. Expression of palmitoylated alpha-dystrobrevin prevented the muscular dystrophy observed in the alpha-dystrobrevin-null mice, demonstrating that the altered form of alpha-dystrobrevin was functional. On the mdx background, the palmitoylated form of alpha-dystrobrevin was expressed on the sarcolemma but did not significantly ameliorate the muscular dystrophy phenotype. Palmitoylated dystrobrevin restored alpha-syntrophin and aquaporin-4 (AQP4) to the mdx sarcolemma but was unable to recruit beta-dystroglycan or the sarcoglycans. Despite restoration of sarcolemmal alpha-syntrophin, neuronal nitric oxide synthase (nNOS) was not localized to the sarcolemma, suggesting that nNOS requires both dystrophin and alpha-syntrophin for correct localization. Thus, although nNOS and AQP4 both require interaction with the PDZ domain of alpha-syntrophin for sarcolemmal association, their localization is regulated differentially.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Aquaporin 4 / genetics*
  • Dystrophin / chemistry
  • Dystrophin / genetics*
  • Dystrophin / metabolism
  • Dystrophin-Associated Proteins / genetics*
  • Dystrophin-Associated Proteins / metabolism
  • Lipoylation
  • Mice
  • Mice, Inbred mdx
  • Mice, Knockout
  • Mice, Transgenic
  • Microscopy, Fluorescence
  • Muscles / metabolism
  • Muscles / pathology
  • Muscular Dystrophy, Animal / genetics
  • Muscular Dystrophy, Animal / pathology
  • Neuropeptides / genetics*
  • Neuropeptides / metabolism
  • Nitric Oxide Synthase Type I / genetics*
  • Nitric Oxide Synthase Type I / metabolism
  • PDZ Domains
  • Protein Binding
  • Sarcolemma / chemistry
  • Sarcolemma / metabolism*

Substances

  • Aqp4 protein, mouse
  • Aquaporin 4
  • Dtna protein, mouse
  • Dystrophin
  • Dystrophin-Associated Proteins
  • Neuropeptides
  • syntrophin
  • Nitric Oxide Synthase Type I
  • Nos1 protein, mouse