Unconventional roles for membrane traffic proteins in response to muscle membrane stress

https://doi.org/10.1016/j.ceb.2020.02.007Get rights and content

Abstract

In skeletal muscle fibers, ubiquitous membrane trafficking pathways responsible for transporting newly synthesized proteins, recycling cell surface receptors, and organizing membrane compartmentation have adapted to the high needs of an extremely specialized cell under constant mechanical stress. Membrane remodeling proteins involved in ubiquitous mechanisms such as clathrin-mediated endocytosis, caveolae formation, and membrane fusion have evolved to produce new pathways with sometimes completely different functions such as adhesion and mechanoprotection. In this review, I discuss recent advances in understanding the specialized features of skeletal muscle clathrin-coated plaques, caveolae, and dysferlin-mediated membrane repair. A special emphasis is given on recent findings suggesting that membrane trafficking pathways have evolved to participate into the mechanisms responsible for sarcolemma resistance to mechanical stress and discuss how defects in these pathways result in muscle disease.

Section snippets

The sarcolemma

The plasma membrane of skeletal muscle fibers, the sarcolemma, is repeatedly submitted to intense mechanical stress. To ensure their integrity, muscle fibers have developed an extraordinary compartmentation of their plasma membrane. By linking the extracellular matrix to the contractile apparatus, the myotendinous junction and lateral junctions called costameres, integrate adhesion to the propagation of forces. Although both have similar junctional anchoring structures, this review focuses on

Costameres

Costameres were originally described as electron-dense circumferential structures enriched in the focal adhesion protein vinculin and involved in attachment of the peripheral Z-disks of sarcomeres to the plasma membrane [3, 4, 5]. They are composed of several protein complexes which all share a common feature: they link the sarcolemma with the intracellular cytoskeleton (Figure 1). The first costamere complex corresponds to classical focal adhesion complexes and is centered on integrins,

Dynamin 2 and centronuclear myopathies

Centronuclear myopathy (CNM) is a rare neuromuscular disorder characterized by the presence of centrally located nuclei in a large number of nonregenerating muscle fibers and disorganization of intracellular compartments [54]. Three main forms of CNM have been distinguished corresponding to three modes of inheritance [54]. The X-linked recessive myotubular myopathy is characterized by severe hypotonia and generalized muscle weakness at birth [55]. The MTM1 gene responsible for the X-linked form

Caveolinopathies

Mutations of muscle-specific caveolin-3, cavin-1, and cavin-4 have been associated with a number of muscle diseases including limb girdle muscular dystrophies, rippling muscle disease, and cardiomyopathies [66,67]. The observed symptoms could be ascribed to several defects in muscle physiology. A lack of functional caveolae could lead to defective formation of the excitation contraction coupling machinery and disorganization of the T-tubule network [47,67]. It could also result in abnormal

Conclusion/Perspectives

While in recent years, a wealth of information has emerged regarding the mechanisms that control response to mechanical stress, there is still a lot to learn from studying skeletal muscle. The recent explosion in the interest of the scientific community for mechanobiology has steered great interest in the skeletal muscle fiber as a model system. A better understanding of the key flat to curved transition observed for both clathrin-coated structures and caveolae will likely deepen our knowledge

Conflict of interest statement

Nothing declared.

Acknowledgments

The author apologizes to all the colleagues whose work could not be extensively quoted in this short review. The author would like to thank Robyn Roth and the Washington University Center for Cellular Imaging (St. Louis, MO) for their assistance with deep-etch electron microscopy and the IBPS cryo-EM facility for EM equipment. Some illustrations accompanying figures of the present manuscript were partially generated using the BioRender.com online tool. The author acknowledges the institutional

References (67)

  • R.G. Parton et al.

    The multiple faces of caveolae

    Nat Rev Mol Cell Biol

    (2007)
  • M. Stoeber et al.

    Oligomers of the ATPase EHD2 confine caveolae to the plasma membrane through association with actin

    EMBO J

    (2012)
  • D. Bansal et al.

    Defective membrane repair in dysferlin-deficient muscular dystrophy

    Nature

    (2003)
  • J.P. Kerr et al.

    Dysferlin at transverse tubules regulates Ca2+ homeostasis in skeletal muscle

    Front Physiol

    (2014)
  • J.E. Heuser et al.

    Introducing a mammalian nerve-muscle preparation ideal for physiology and microscopy, the transverse auricular muscle in the ear of the mouse

    Neuroscience

    (2019)
  • B.S. Cowling et al.

    Amphiphysin (BIN1) negatively regulates dynamin 2 for normal muscle maturation

    J Clin Invest

    (2017)
  • B. Charvet et al.

    The development of the myotendinous junction. A review

    Muscles Ligaments Tendons J

    (2012)
  • M. Valdivia et al.

    Mechanical control of myotendinous junction formation and tendon differentiation during development

    Front Cell Dev Biol

    (2017)
  • B.A. Danowski et al.

    Costameres are sites of force transmission to the substratum in adult rat cardiomyocytes

    J Cell Biol

    (1992)
  • C.R. Shear et al.

    Vinculin in subsarcolemmal densities in chicken skeletal muscle: localization and relationship to intracellular and extracellular structures

    J Cell Biol

    (1985)
  • J.V. Pardo et al.

    Vinculin is a component of an extensive network of myofibril-sarcolemma attachment regions in cardiac muscle fibers

    J Cell Biol

    (1983)
  • R. Barresi et al.

    Dystroglycan: from biosynthesis to pathogenesis of human disease

    J Cell Sci

    (2006)
  • A. Franck et al.

    Clathrin plaques and associated actin anchor intermediate filaments in skeletal muscle

    Mol Biol Cell

    (2019)
  • S. Vassilopoulos et al.

    Actin scaffolding by clathrin heavy chain is required for skeletal muscle sarcomere organization

    J Cell Biol

    (2014)
  • P. Maupin et al.

    Improved preservation and staining of HeLa cell actin filaments, clathrin-coated membranes, and other cytoplasmic structures by tannic acid-glutaraldehyde-saponin fixation

    J Cell Biol

    (1983)
  • P.G. De Deyne et al.

    The vitronectin receptor associates with clathrin-coated membrane domains via the cytoplasmic domain of its beta5 subunit

    J Cell Sci

    (1998)
  • D. Li et al.

    ADVANCED IMAGING. Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics

    Science

    (2015)
  • S. Saffarian et al.

    Distinct dynamics of endocytic clathrin-coated pits and coated plaques

    PLoS Biol

    (2009)
  • D. Leyton-Puig et al.

    Flat clathrin lattices are dynamic actin-controlled hubs for clathrin-mediated endocytosis and signalling of specific receptors

    Nat Commun

    (2017)
  • F. Baschieri et al.

    Frustrated endocytosis controls contractility-independent mechanotransduction at clathrin-coated structures

    Nat Commun

    (2018)
  • K.D. Bellve et al.

    Plasma membrane domains specialized for clathrin-mediated endocytosis in primary cells

    J Biol Chem

    (2006)
  • M.J. Taylor et al.

    A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis

    PLoS Biol

    (2011)
  • J.G. Lock et al.

    Reticular adhesions are a distinct class of cell-matrix adhesions that mediate attachment during mitosis

    Nat Cell Biol

    (2018)

    • Cited by (7)

    View all citing articles on Scopus
    View full text
    © 2020 Elsevier Ltd. All rights reserved.