The Basement Membrane/Basal Lamina of Skeletal Muscle
Year: 2003
Type: review
Abstract: basement membrane basal lamina acetylcholinesterase acetylcholine receptor muscle-specific kinase Many cells, including skeletal muscle fibers, are coated by a layer of extracellular matrix material called the basement membrane (BM).1 The BM, in turn, is composed of two layers: an internal, felt-like basal lamina (BL) directly linked to the plasma membrane, and an external, fibrillar reticular lamina. BMs contain protein and carbohydrate but no lipid or nucleic acid. Virtually all the protein is glycosylated, and nearly all the carbohydrate is covalently bound to protein. The fibrils of the reticular lamina are collagenous, and they are embedded in an amorphous proteoglycan-rich ground substance. The BL contains non-fibrillar collagen, non-collagenous glycoproteins, and proteoglycans (1Timpl, R., and Rohrbach, O. (eds) Molecular and Cellular Aspects of Basement Membranes, Academic Press, New York.Google Scholar). Initially, the BM was viewed as a static structure that provides mechanical support; essentially something for the cells to sit on. A key advance was the discovery that, because the acellular BM survives injury to associated cells, it can provide a scaffold to orient and constrain cells during regeneration (2Vracko R. Benditt E.P. J. Cell Biol. 1972; 55: 406-419Crossref PubMed Scopus (276) Google Scholar). A more radical transformation over the past few decades was the realization that BM components play active roles and that these roles extend to developmental as well as regenerative processes (1Timpl, R., and Rohrbach, O. (eds) Molecular and Cellular Aspects of Basement Membranes, Academic Press, New York.Google Scholar). In skeletal muscle, these processes include myogenesis and synaptogenesis. Most recently, emphasis has shifted to a search for the matrix-associated signals and membrane-associated receptors that underlie cell-matrix interactions. The purpose of this minireview is to relate results from the new molecular analyses to the early cellular observations that motivated them. For more detailed descriptions of what happened in between, see Refs. 3Sanes J.R. Engel A.G. Franzini-Armstrong C. Mycology. McGraw Hill, New York1994: 242-260Google Scholar, 4Sanes J.R. Semin. Dev. Biol. 1995; 6: 163-173Crossref Scopus (28) Google Scholar, 5Sanes J.R. Lichtman J.W. Annu. Rev. Neurosci. 1999; 22: 389-442Crossref PubMed Scopus (1209) Google Scholar. Although we now know that BMs are present in nearly all tissues, their existence was first appreciated in muscle. In his 1840 report “On the Minute Structure and Movements of Voluntary Muscle,” Bowman (6Bowman W. Philos. Trans. R. Soc. Lond. Biol. Sci. 1840; 130: 457-494Crossref Google Scholar) described a “highly delicate, transparent, and probably elastic” sheath encircling individual muscle fibers. This sheath, which he called the sarcolemma, became apparent when muscle fibers were injured during dissection; the cell itself lysed and retracted, leaving the sarcolemma behind (Fig.1). Over a century later, electron microscopy revealed that the BM is the main component of such tubes and that the BL is a main component of the BM. Today the term sarcolemma is often used to refer to the plasma membrane alone, although only fragments of it were present in Bowman's tubes (3Sanes J.R. Engel A.G. Franzini-Armstrong C. Mycology. McGraw Hill, New York1994: 242-260Google Scholar). The terms BL and BM are often used interchangeably, but should not be; I will attempt to use them appropriately here. Bowman's view of what we now know to be BM and particularly his evidence for its “strength and tenacity” (6Bowman W. Philos. Trans. R. Soc. Lond. Biol. Sci. 1840; 130: 457-494Crossref Google Scholar) led directly to appreciation of its role in muscle function. Muscles are strong, flexible, and stress-resistant. Formal models of their mechanical properties include both contractile and elastic elements. The contractile element is, of course, the sarcomere, and extracellular matrix accounts for much of the elasticity. In fact, several matrix-rich structures contribute to muscle strength and elasticity, but a sizable fraction has been shown to reside in the BM (7Tidball J.G. Biophys. J. 1986; 50: 1127-1138Abstract Full Text PDF PubMed Scopus (35) Google Scholar). Direct biophysical analysis of BM is lacking, but keys to its strength most likely are its major structural components (8Timpl R. Brown J.C. Bioessays. 1996; 18: 123-132Crossref PubMed Scopus (575) Google Scholar, 9Colognato H. Yurchenco P.D. Dev. Dyn. 2000; 218: 213-234Crossref PubMed Scopus (1024) Google Scholar). The most abundant protein of the BL is triple-helical collagen IV, the subunits of which, called α chains, have prominent terminal non-collagenous domains. The major non-collagenous protein is laminin, which is also a heterotrimer of related chains, in this case called α, β, and γ. Both collagens IV and laminins exist in multiple isoforms, with the most abundant in muscle being collagen (α1(IV))2(α2(IV))1 and laminin α2β1γ1 (also called laminin-2). The basic structure of BLs appears to involve distinct networks of collagens IV and laminin, each of which is capable of self-assembly. The collagen network becomes cemented by covalent cross-links, and the two networks are linked to each other by another non-collagenous glycoprotein, entactin/nidogen. These core components bear a multitude of recognition sites that bind other BL components, anchor reticular lamina components to the BL, and serve as ligands for membrane-associated receptors. Among the transmembrane receptors are the integrins and dystroglycans, both of which interact with the cytoskeleton (10Michele D.E. Campbell K.P. J. Biol. Chem. 2003; 278 (January 29, 10.1074/jbc.R200031200)Abstract Full Text Full Text PDF Scopus (366) Google Scholar, 11Mayer U.R. J. Biol. Chem. 2003; 278: 14587-14590Abstract Full Text Full Text PDF PubMed Scopus (138) Google Scholar). Thus, one can envision a series of direct linkages that together span the distance from reticular lamina to BL to plasma membrane to cytoskeleton. The BM provides a significant fraction of the tensile strength of the whole structure (3Sanes J.R. Engel A.G. Franzini-Armstrong C. Mycology. McGraw Hill, New York1994: 242-260Google Scholar), presumably via the collagen/laminin networks of BL, which run orthogonal to this axis. Genetic studies of muscle disease show that the BM is critical for the maintenance of muscle integrity. Positional cloning in humans and analysis of naturally occurring and targeted mutants in mice have revealed that muscular dystrophy can arise from loss of any of several components in the reticular lamina-BL-membrane-cytoskeleton linkage. These include laminin α2 (congenital muscular dystrophy), its major transemembrane receptors, integrin α7 and dystroglycan; dystrophin, which links dystroglycan to the cytoskeleton (Duchenne muscular dystrophy); the dystroglycan- and dystrophin-associated sarcoglycans (limb-girdle muscular dystrophies); and the α chains of collagen VI, which help connect the BL to the reticular lamina (Bethlem myopathy) (10Michele D.E. Campbell K.P. J. Biol. Chem. 2003; 278 (January 29, 10.1074/jbc.R200031200)Abstract Full Text Full Text PDF Scopus (366) Google Scholar, 11Mayer U.R. J. Biol. Chem. 2003; 278: 14587-14590Abstract Full Text Full Text PDF PubMed Scopus (138) Google Scholar, 12Helbling-Leclerc A. Zhang X. Topaloglu H. Cruaud C. Tesson F. Weissenbach J. Tome F.M. Schwartz K. Fardeau M. Tryggvason K. et al.Nat. Genet. 1995; 11: 216-218Crossref PubMed Scopus (558) Google Scholar, 13Xu H. Wu X.R. Wewer U.M. Engvall E. Nat. Genet. 1994; 8: 297-302Crossref PubMed Scopus (320) Google Scholar, 14Blake D.J. Weir A. Newey S.E. Davies K.E. Physiol. Rev. 2002; 82: 291-329Crossref PubMed Scopus (886) Google Scholar, 15Jobsis G.J. Keizers H. Vreijling J.P. de Visser M. Speer M.C. Wolterman R.A. Baas F. Bolhuis P.A. Nat. Genet. 1996; 14: 113-115Crossref PubMed Scopus (215) Google Scholar). Importantly, in all of these diseases, muscles develop normally but then degenerate. Thus, even though the BL does play roles in myogenesis (see below) it is separately required for muscle maintenance. In part, this requirement may be a passive, mechanical one, but more active mechanisms also contribute. The core BL components, laminin and collagen IV, are signaling as well as structural molecules, and their receptors, dystroglycan and integrins, are signal transducers. For example, active signaling from laminin α2 may provide a survival signal for muscle, and its absence in congenital dystrophy is associated with particularly high levels of apoptosis (16Vachon P.H. Loechel F. Xu H. Wewer U.M. Engvall E. J. Cell Biol. 1996; 134: 1483-1497Crossref PubMed Scopus (193) Google Scholar). In short, muscle maintenance requires both the structural and signaling properties of BL. In one of the first clear demonstrations that extracellular matrix influences cellular differentiation, Hauschka and Konigsberg (17Hauschka S.D. Konigsberg I.R. Proc. Natl. Acad. Sci. U. S. A. 1966; 55: 119-126Crossref PubMed Scopus (332) Google Scholar) showed that substrate-bound collagen could replace “conditioned medium” factors in promoting the formation of myotubes from cultured myoblasts. Subsequent work showed that several matrix components affect myogenesis. Of these, laminin appears to be particularly critical. Laminin enhances proliferation of myoblasts, stimulates their motility, and leads them to assume the bipolar shape characteristic of fusing cells (18Foster R.F. Thompson J.M. Kaufman S.J. Dev. Biol. 1987; 122: 11-20Crossref PubMed Scopus (133) Google Scholar). Myotube formation is decreased, although not abolished, in the absence of laminin (19Smyth N. Vatansever H.S. Murray P. Meyer M. Frie C. Paulsson M. Edgar D. J. Cell Biol. 1999; 144: 151-160Crossref PubMed Scopus (408) Google Scholar). In contrast, fibronectin selectively promotes adhesion of fibroblasts and may lead to dedifferentiation of myoblasts (20von der Mark K. Ocalan M. Differentiation. 1989; 40: 150-157Crossref PubMed Scopus (108) Google Scholar). The locations of these proteins also differ; laminin adjoins myotubes whereas fibronectin is initially excluded from myogenic regions (20von der Mark K. Ocalan M. Differentiation. 1989; 40: 150-157Crossref PubMed Scopus (108) Google Scholar). Therefore, laminin and fibronectin may be involved in sorting myoblasts from fibroblasts as well as in orchestrating their differentiation. In addition, laminin and collagen IV provide binding sites for proteoglycans, the principal one in muscle being perlecan (8Timpl R. Brown J.C. Bioessays. 1996; 18: 123-132Crossref PubMed Scopus (575) Google Scholar). The glycosaminoglycan chains of the proteoglycans, in turn, provide binding sites that concentrate and present bioactive polypeptides such as fibroblast growth factors and transforming growth factors, which are critical for myogenesis (21Pirskanen A. Kiefer J.C. Hauschka S.D. Dev. Biol. 2000; 224: 189-203Crossref PubMed Scopus (57) Google Scholar, 22Baeg G.H. Perrimon N. Curr. Opin. Cell Biol. 2000; 12: 575-580Crossref PubMed Scopus (94) Google Scholar). Indeed, these nominally soluble factors are predominantly matrix-associated in vivo. Thus, major BL components not only promote myogenesis directly but also orchestrate muscle development by presentation of morphogenic, mitogenic, and trophic factors. Bowman's discovery of the BM arose from its persistence following injury during dissection. When injury occurs in vivo, new muscle fibers regenerate from a resident population of stem cells, called satellite cells, which are wedged between muscle fiber and BL. Bowman (6Bowman W. Philos. Trans. R. Soc. Lond. Biol. Sci. 1840; 130: 457-494Crossref Google Scholar) noted that the BM “provides an effectual barrier between the parts within and those without”; as predicted from this property, most satellite cells remain within the BL as they divide and form myotubes (2Vracko R. Benditt E.P. J. Cell Biol. 1972; 55: 406-419Crossref PubMed Scopus (276) Google Scholar, 23Sanes J.R. Marshall L.M. McMahan U.J. J. Cell Biol. 1978; 78: 176-198Crossref PubMed Scopus (397) Google Scholar). Thus, by constraining the growth and migration of activated satellite cells, BL orients the regeneration of new muscle fibers. From what we know about myogenesis, it seems likely that the BL also actively promotes regeneration. In addition, BL acts as a mechanical barrier to prevent migratory loss of satellite cells from normal muscle and could be involved in repressing satellite cell mitosis and differentiation in the absence of damage. The guidance that BL provides is of Muscles regenerate the BL is but myotubes are not in the regenerate as a whole may develop (3Sanes J.R. Engel A.G. Franzini-Armstrong C. Mycology. McGraw Hill, New York1994: 242-260Google Scholar). because BLs of and also as for regeneration (2Vracko R. Benditt E.P. J. 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Biol. 1996; PubMed Scopus Google Scholar). are the the of the muscle fiber is that but are BL these and is to the plasma membrane by M. J.R. Rev. 2000; PubMed Google Scholar). These fibrils and the of by the are for the of from muscle to molecular have been noted between the BL the and that regions of the sarcolemma 2000; PubMed Scopus Google Scholar, F. D. J. 2000; PubMed Scopus Google Scholar), but the of these is The key in are of acetylcholine from the terminal and of acetylcholine receptors in the that the BL of acetylcholine the but studies show that its to receptors is Proc. Natl. Acad. Sci. U. S. A. PubMed Google Scholar). This is with from analysis of BL in which is an only for K. J. Curr. Opin. PubMed Scopus Google Scholar). 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When they form that contain of and membrane-associated sites called active J.R. Lichtman J.W. Annu. Rev. Neurosci. 1999; 22: 389-442Crossref PubMed Scopus (1209) Google Scholar). Importantly, these only in the fraction of the that directly the that factors differentiation. of BL from which muscle fibers been (see also active and as well as the to when new active in these in with of BL that sites active been J.R. Marshall L.M. McMahan U.J. J. Cell Biol. 1978; 78: 176-198Crossref PubMed Scopus (397) Google Scholar). This showed that of differentiation were within the BL. Among the of differentiation are the The laminin was initially by of its in BL J.P. J.R. 1989; PubMed Scopus Google Scholar). are to to J.R. 1995; PubMed Scopus Google Scholar), to formation of a BL in which sites bear whereas regions are in fragments or in to and to J. J.R. 1995; 14: Full Text PDF PubMed Scopus Google Scholar, J.R. J. Neurosci. 1999; 11: PubMed Scopus (28) Google Scholar). This with the that these results a for the existence of multiple they in a structural In direct of this differentiation is in few active is decreased, cell processes the and of the of M. J. J.R. J.P. 1995; PubMed Scopus Google Scholar, J.R. PubMed Scopus Google Scholar). Thus, laminins as of differentiation. the other the that differentiation to a in the absence of that analysis of muscle laminins revealed the of α chains in BL and but only one J.R. J. Cell Biol. PubMed Scopus (366) Google Scholar). Thus, BL may contain and and all of which be involved in differentiation. Genetic studies and analyses in distinct roles for each promotes differentiation and cell promotes the of and and may be for structural as is 2000; PubMed Scopus Google Scholar, J.R. J. Cell Biol. PubMed Scopus (366) Google Scholar, J.M. J. J. H. Tryggvason K. J.R. Nat. Neurosci. PubMed Scopus Google Scholar, J.P. P.A. PubMed Scopus Google Scholar). Thus, of the to and differentiation. The distinct of laminins that they have multiple receptors and presumably include integrins, which bind laminins integrin is active J. Neurosci. 2000; PubMed Google Scholar). In addition, and with distinct membrane components, the that and the S.J. J.R. J. Biol. Chem. 2000; Full Text Full Text PDF PubMed Scopus Google Scholar, J.R. J. Neurosci. 2000; PubMed Google Scholar). These the that laminins could differentiation in by direct with critical components of the receptors are in myotubes but in the membrane of muscle can their but studies a of to including sites of J.R. Lichtman J.W. Annu. Rev. Neurosci. 1999; 22: 389-442Crossref PubMed Scopus (1209) Google Scholar, J.R. Lichtman J.W. Nat. Rev. Neurosci. PubMed Scopus Google Scholar). are of associated with and BL components, sites for following The of BL that it play a role in and BL this When myotubes in these following and (see new including in to BL, even though the was S.J. McMahan U.J. J. Cell Biol. 82: PubMed Scopus Google Scholar). These results the that of the of differentiation be in or by the BL. In fact, of only one has been shown to play a vivo, and this is a BL was by McMahan and U.J. Biol. Scopus Google Scholar) in a search for bioactive components of BL. is a with that interact with the muscle membrane and an that binding to laminin in the BL U.J. Biol. Scopus Google Scholar, F. C. 6: Full Text PDF PubMed Scopus Google Scholar, R. M. M. J. Cell Biol. PubMed Scopus Google Scholar). is by and the C. McMahan U.J. J. Cell Biol. 1987; PubMed Scopus Google Scholar). and studies the that is and for differentiation. of the in mice leads to in and of in muscle leads to of a M. McMahan U.J. Neurosci. PubMed Scopus Google Scholar, M. Proc. Natl. Acad. Sci. U. S. A. PubMed Scopus Google Scholar, M. F. J.P. J.R. 1996; Full Text Full Text PDF PubMed Scopus Google Scholar). A is that muscles as well as only the by of called are more active and targeted of the leads to as as those in the absence of all Lichtman J.W. J.R. 1999; Full Text Full Text PDF PubMed Scopus Google Scholar). a it is not that with cellular receptors, including the cell adhesion molecules, and integrins J.R. Lichtman J.W. Annu. Rev. Neurosci. 1999; 22: 389-442Crossref PubMed Scopus (1209) Google Scholar). Genetic analysis has that of these are required for the critical receptor of for this is a receptor kinase called of in turn, leads to of with the cytoskeleton via a protein called J.R. Lichtman J.W. Nat. Rev. Neurosci. PubMed Scopus Google Scholar). binding the BL both the signal and its persistence by the In addition, dystroglycan and proteins associated with it are involved in the and maintenance of the membrane in J.R. Lichtman J.W. Nat. Rev. Neurosci. PubMed Scopus Google Scholar, M. S. J.R. Lichtman J.W. 2002; Full Text Full Text PDF PubMed Scopus Google it seems likely that the dystroglycan ligands in BL, and laminin, are involved in the of the The BL of skeletal muscle a of roles during development and in is in but all have been and molecular analysis is now well as one of the in which we are to relate the molecular of BL to its function. which may be to other tissues, are as The view of the BL as a mechanical has been not by the realization that it also has and by individual The major components of BL, laminins and collagens IV, are not only structural which form networks within BL and links to but they are also signaling that receptors in the Both laminins and collagens IV are of that cells can to within a BL. This provides a for of signals within a structural sites the core BL components of abundant components such as The glycosaminoglycan components of the proteoglycans, in turn, and present nominally soluble signaling molecules, such as growth factors. the structural and roles of BL can be its to serve as a in which cells can that direct the differentiation and of the
Source: Journal of Biological Chemistry
Author: Joshua R. Sanes
Institution: Washington University in St. Louis
Language: English
Subfield: Molecular Biology
Domain: Life Sciences
Open Access status: hybrid
Estimated APC paid: $3,430
OpenAlex ID: W2075303668