© The Rockefeller University Press,
0021-9525/1999//619 $5.00
The Journal of Cell Biology, Volume 145, Number 3,
, 1999 619-631
Laminin Polymerization Induces a Receptor–Cytoskeleton Network
Holly Colognato,
Donald A. Winkelmann, and
Peter D. Yurchenco
Department of Pathology and Laboratory Medicine, Robert Wood Johnson Medical School, Piscataway, New Jersey 08854
The transition of laminin from a monomeric to a polymerized state is thought to be a crucial step in the development of basement membranes and in the case of skeletal muscle, mutations in laminin can result in severe muscular dystrophies with basement membrane defects. We have evaluated laminin polymer and receptor interactions to determine the requirements for laminin assembly on a cell surface and investigated what cellular responses might be mediated by this transition. We found that on muscle cell surfaces, laminins preferentially polymerize while bound to receptors that included dystroglycan and
7β1 integrin. These receptor interactions are mediated through laminin COOH-terminal domains that are spatially and functionally distinct from NH2-terminal polymer binding sites. This receptor-facilitated self-assembly drives rearrangement of laminin into a cell-associated polygonal network, a process that also requires actin reorganization and tyrosine phosphorylation. As a result, dystroglycan and integrin redistribute into a reciprocal network as do cortical cytoskeleton components vinculin and dystrophin. Cytoskeletal and receptor reorganization is dependent on laminin polymerization and fails in response to receptor occupancy alone (nonpolymerizing laminin). Preferential polymerization of laminin on cell surfaces, and the resulting induction of cortical architecture, is a cooperative process requiring laminin– receptor ligation, receptor-facilitated self-assembly, actin reorganization, and signaling events.
Key Words: laminin matrix assembly muscular dystrophy dystroglycan integrin
Abbreviations used in this paper: AEBSF, p-aminoethylbenzenesulfonyl fluoride; CMD, congenital muscular dystrophy.
This project was supported by National Institutes of Health grants R01-DK36425 (to P.D. Yurchenco) and R01-AR38454 (to D.A. Winkelmann).

CiteULike
Complore
Connotea
Del.icio.us
Digg
Facebook
Reddit
Technorati
Twitter What's this?
This article has been cited by other articles:
-
Jacoby, A. S., Busch-Nentwich, E., Bryson-Richardson, R. J., Hall, T. E., Berger, J., Berger, S., Sonntag, C., Sachs, C., Geisler, R., Stemple, D. L., Currie, P. D.
(2009). The zebrafish dystrophic mutant softy maintains muscle fibre viability despite basement membrane rupture and muscle detachment. Development
136: 3367-3376
[Abstract]
[Full Text]
-
Masuda-Hirata, M., Suzuki, A., Amano, Y., Yamashita, K., Ide, M., Yamanaka, T., Sakai, M., Imamura, M., Ohno, S.
(2009). Intracellular polarity protein PAR-1 regulates extracellular laminin assembly by regulating the dystroglycan complex. GENES CELLS
14: 835-850
[Abstract]
[Full Text]
-
Court, F. A., Hewitt, J. E., Davies, K., Patton, B. L., Uncini, A., Wrabetz, L., Feltri, M. L.
(2009). A Laminin-2, Dystroglycan, Utrophin Axis Is Required for Compartmentalization and Elongation of Myelin Segments. J. Neurosci.
29: 3908-3919
[Abstract]
[Full Text]
-
Nie, J., Sage, E. H.
(2009). SPARC Inhibits Adipogenesis by Its Enhancement of {beta}-Catenin Signaling. J. Biol. Chem.
284: 1279-1290
[Abstract]
[Full Text]
-
Rooney, J. E., Gurpur, P. B., Yablonka-Reuveni, Z., Burkin, D. J.
(2009). Laminin-111 Restores Regenerative Capacity in a Mouse Model for {alpha}7 Integrin Congenital Myopathy. Am. J. Pathol.
174: 256-264
[Abstract]
[Full Text]
-
Nishimune, H., Valdez, G., Jarad, G., Moulson, C. L., Muller, U., Miner, J. H., Sanes, J. R.
(2008). Laminins promote postsynaptic maturation by an autocrine mechanism at the neuromuscular junction. JCB
182: 1201-1215
[Abstract]
[Full Text]
-
Harrison, D., Hussain, S.-A., Combs, A. C., Ervasti, J. M., Yurchenco, P. D., Hohenester, E.
(2007). Crystal Structure and Cell Surface Anchorage Sites of Laminin {alpha}1LG4-5. J. Biol. Chem.
282: 11573-11581
[Abstract]
[Full Text]
-
Knoblauch, A., Will, C., Goncharenko, G., Ludwig, S., Wixler, V.
(2007). The binding of Mss4 to {alpha}-integrin subunits regulates matrix metalloproteinase activation and fibronectin remodeling. FASEB J.
21: 497-510
[Abstract]
[Full Text]
-
Sehgal, B. U., DeBiase, P. J., Matzno, S., Chew, T.-L., Claiborne, J. N., Hopkinson, S. B., Russell, A., Marinkovich, M. P., Jones, J. C. R.
(2006). Integrin beta4 Regulates Migratory Behavior of Keratinocytes by Determining Laminin-332 Organization. J. Biol. Chem.
281: 35487-35498
[Abstract]
[Full Text]
-
Weir, M. L., Oppizzi, M. L., Henry, M. D., Onishi, A., Campbell, K. P., Bissell, M. J., Muschler, J. L.
(2006). Dystroglycan loss disrupts polarity and {beta}-casein induction in mammary epithelial cells by perturbing laminin anchoring. J. Cell Sci.
119: 4047-4058
[Abstract]
[Full Text]
-
Poulton, J. S., Deng, W.-M.
(2006). Dystroglycan down-regulation links EGF receptor signaling and anterior-posterior polarity formation in the Drosophila oocyte. Proc. Natl. Acad. Sci. USA
103: 12775-12780
[Abstract]
[Full Text]
-
Mak, G. Z., Kavanaugh, G. M., Buschmann, M. M., Stickley, S. M., Koch, M., Goss, K. H., Waechter, H., Zuk, A., Matlin, K. S.
(2006). Regulated Synthesis and Functions of Laminin 5 in Polarized Madin-Darby Canine Kidney Epithelial Cells. Mol. Biol. Cell
17: 3664-3677
[Abstract]
[Full Text]
-
DeBiase, P. J., Lane, K., Budinger, S., Ridge, K., Wilson, M., Jones, J. C.R.
(2006). Laminin-311 (Laminin-6) Fiber Assembly by Type I-like Alveolar Cells. J. Histochem. Cytochem.
54: 665-672
[Abstract]
[Full Text]
-
Bajanca, F., Luz, M., Raymond, K., Martins, G. G., Sonnenberg, A., Tajbakhsh, S., Buckingham, M., Thorsteinsdottir, S.
(2006). Integrin {alpha}6{beta}1-laminin interactions regulate early myotome formation in the mouse embryo. Development
133: 1635-1644
[Abstract]
[Full Text]
-
Smirnov, S. P., Barzaghi, P., McKee, K. K., Ruegg, M. A., Yurchenco, P. D.
(2005). Conjugation of LG Domains of Agrins and Perlecan to Polymerizing Laminin-2 Promotes Acetylcholine Receptor Clustering. J. Biol. Chem.
280: 41449-41457
[Abstract]
[Full Text]
-
Occhi, S., Zambroni, D., Del Carro, U., Amadio, S., Sirkowski, E. E., Scherer, S. S., Campbell, K. P., Moore, S. A., Chen, Z.-L., Strickland, S., Di Muzio, A., Uncini, A., Wrabetz, L., Feltri, M. L.
(2005). Both Laminin and Schwann Cell Dystroglycan Are Necessary for Proper Clustering of Sodium Channels at Nodes of Ranvier. J. Neurosci.
25: 9418-9427
[Abstract]
[Full Text]
-
Fan, X., She, Y.-M., Bagshaw, R. D., Callahan, J. W., Schachter, H., Mahuran, D. J.
(2005). Identification of the hydrophobic glycoproteins of Caenorhabditis elegans. Glycobiology
15: 952-964
[Abstract]
[Full Text]
-
Niewmierzycka, A., Mills, J., St-Arnaud, R., Dedhar, S., Reichardt, L. F.
(2005). Integrin-Linked Kinase Deletion from Mouse Cortex Results in Cortical Lamination Defects Resembling Cobblestone Lissencephaly. J. Neurosci.
25: 7022-7031
[Abstract]
[Full Text]
-
Hallmann, R., Horn, N., Selg, M., Wendler, O., Pausch, F., Sorokin, L. M.
(2005). Expression and Function of Laminins in the Embryonic and Mature Vasculature. Physiol. Rev.
85: 979-1000
[Abstract]
[Full Text]
-
Jones, J. C. R., Lane, K., Hopkinson, S. B., Lecuona, E., Geiger, R. C., Dean, D. A., Correa-Meyer, E., Gonzales, M., Campbell, K., Sznajder, J. I., Budinger, S.
(2005). Laminin-6 assembles into multimolecular fibrillar complexes with perlecan and participates in mechanical-signal transduction via a dystroglycan-dependent, integrin-independent mechanism. J. Cell Sci.
118: 2557-2566
[Abstract]
[Full Text]
-
Li, S., Liquari, P., McKee, K. K., Harrison, D., Patel, R., Lee, S., Yurchenco, P. D.
(2005). Laminin-sulfatide binding initiates basement membrane assembly and enables receptor signaling in Schwann cells and fibroblasts. JCB
169: 179-189
[Abstract]
[Full Text]
-
Halfter, W., Willem, M., Mayer, U.
(2005). Basement Membrane-Dependent Survival of Retinal Ganglion Cells. IOVS
46: 1000-1009
[Abstract]
[Full Text]
-
Yu, W., Datta, A., Leroy, P., O'Brien, L. E., Mak, G., Jou, T.-S., Matlin, K. S., Mostov, K. E., Zegers, M. M.P.
(2005). {beta}1-Integrin Orients Epithelial Polarity via Rac1 and Laminin. Mol. Biol. Cell
16: 433-445
[Abstract]
[Full Text]
-
Burkin, D. J., Wallace, G. Q., Milner, D. J., Chaney, E. J., Mulligan, J. A., Kaufman, S. J.
(2005). Transgenic Expression of {alpha}7{beta}1 Integrin Maintains Muscle Integrity, Increases Regenerative Capacity, Promotes Hypertrophy, and Reduces Cardiomyopathy in Dystrophic Mice. Am. J. Pathol.
166: 253-263
[Abstract]
[Full Text]
-
Zenker, M., Aigner, T., Wendler, O., Tralau, T., Muntefering, H., Fenski, R., Pitz, S., Schumacher, V., Royer-Pokora, B., Wuhl, E., Cochat, P., Bouvier, R., Kraus, C., Mark, K., Madlon, H., Dotsch, J., Rascher, W., Maruniak-Chudek, I., Lennert, T., Neumann, L. M., Reis, A.
(2004). Human laminin {beta}2 deficiency causes congenital nephrosis with mesangial sclerosis and distinct eye abnormalities. Hum Mol Genet
13: 2625-2632
[Abstract]
[Full Text]
-
Odenthal, U., Haehn, S., Tunggal, P., Merkl, B., Schomburg, D., Frie, C., Paulsson, M., Smyth, N.
(2004). Molecular Analysis of Laminin N-terminal Domains Mediating Self-interactions. J. Biol. Chem.
279: 44504-44512
[Abstract]
[Full Text]
-
Kojima, K., Davidovits, A., Poczewski, H., Langer, B., Uchida, S., Nagy-Bojarski, K., Hovorka, A., Sedivy, R., Kerjaschki, D.
(2004). Podocyte Flattening and Disorder of Glomerular Basement Membrane Are Associated with Splitting of Dystroglycan-Matrix Interaction. J. Am. Soc. Nephrol.
15: 2079-2089
[Abstract]
[Full Text]
-
Miner, J. H., Li, C., Mudd, J. L., Go, G., Sutherland, A. E.
(2004). Compositional and structural requirements for laminin and basement membranes during mouse embryo implantation and gastrulation. Development
131: 2247-2256
[Abstract]
[Full Text]
-
Yurchenco, P. D., Cheng, Y.-S., Campbell, K., Li, S.
(2004). Loss of basement membrane, receptor and cytoskeletal lattices in a laminin-deficient muscular dystrophy. J. Cell Sci.
117: 735-742
[Abstract]
[Full Text]
-
Srikakulam, R., Winkelmann, D. A.
(2004). Chaperone-mediated folding and assembly of myosin in striated muscle. J. Cell Sci.
117: 641-652
[Abstract]
[Full Text]
-
Brown, S. C., Torelli, S., Brockington, M., Yuva, Y., Jimenez, C., Feng, L., Anderson, L., Ugo, I., Kroger, S., Bushby, K., Voit, T., Sewry, C., Muntoni, F.
(2004). Abnormalities in {alpha}-Dystroglycan Expression in MDC1C and LGMD2I Muscular Dystrophies. Am. J. Pathol.
164: 727-737
[Abstract]
[Full Text]
-
Rambukkana, A., Kunz, S., Min, J., Campbell, K. P., Oldstone, M. B. A.
(2003). Targeting Schwann cells by nonlytic arenaviral infection selectively inhibits myelination. Proc. Natl. Acad. Sci. USA
100: 16071-16076
[Abstract]
[Full Text]
-
McDearmon, E. L., Combs, A. C., Ervasti, J. M.
(2003). Core 1 Glycans on {alpha}-Dystroglycan Mediate Laminin-induced Acetylcholine Receptor Clustering but Not Laminin Binding. J. Biol. Chem.
278: 44868-44873
[Abstract]
[Full Text]
-
Wang, Q., Moncman, C. L., Winkelmann, D. A.
(2003). Mutations in the motor domain modulate myosin activity and myofibril organization. J. Cell Sci.
116: 4227-4238
[Abstract]
[Full Text]
-
Huang, C.-c., Hall, D. H., Hedgecock, E. M., Kao, G., Karantza, V., Vogel, B. E., Hutter, H., Chisholm, A. D., Yurchenco, P. D., Wadsworth, W. G.
(2003). Laminin {alpha} subunits and their role in C. elegans development. Development
130: 3343-3358
[Abstract]
[Full Text]
-
Previtali, S. C., Nodari, A., Taveggia, C., Pardini, C., Dina, G., Villa, A., Wrabetz, L., Quattrini, A., Feltri, M. L.
(2003). Expression of Laminin Receptors in Schwann Cell Differentiation: Evidence for Distinct Roles. J. Neurosci.
23: 5520-5530
[Abstract]
[Full Text]
-
Michele, D. E., Campbell, K. P.
(2003). Dystrophin-Glycoprotein Complex: Post-translational Processing and Dystroglycan Function. J. Biol. Chem.
278: 15457-15460
[Full Text]
-
Freire, E., Gomes, F. C. A., Linden, R., Neto, V. M., Coelho-Sampaio, T.
(2003). Structure of laminin substrate modulates cellular signaling for neuritogenesis. J. Cell Sci.
115: 4867-4876
[Abstract]
[Full Text]
-
Zhu, J., Motejlek, K., Wang, D., Zang, K., Schmidt, A., Reichardt, L. F.
(2003). {beta}8 integrins are required for vascular morphogenesis in mouse embryos. Development
129: 2891-2903
[Abstract]
[Full Text]
-
Deng, W.-M., Schneider, M., Frock, R., Castillejo-Lopez, C., Gaman, E. A., Baumgartner, S., Ruohola-Baker, H.
(2003). Dystroglycan is required for polarizing the epithelial cells and the oocyte in Drosophila. Development
130: 173-184
[Abstract]
[Full Text]
-
Wang, F., Hansen, R. K., Radisky, D., Yoneda, T., Barcellos-Hoff, M. H., Petersen, O. W., Turley, E. A., Bissell, M. J.
(2002). Phenotypic Reversion or Death of Cancer Cells by Altering Signaling Pathways in Three-Dimensional Contexts. JNCI J Natl Cancer Inst
94: 1494-1503
[Abstract]
[Full Text]
-
Velling, T., Risteli, J., Wennerberg, K., Mosher, D. F., Johansson, S.
(2002). Polymerization of Type I and III Collagens Is Dependent On Fibronectin and Enhanced By Integrins alpha 11beta 1 and alpha 2beta 1. J. Biol. Chem.
277: 37377-37381
[Abstract]
[Full Text]
-
Petajaniemi, N., Korhonen, M., Kortesmaa, J., Tryggvason, K., Sekiguchi, K., Fujiwara, H., Sorokin, L., Thornell, L.-E., Wondimu, Z., Assefa, D., Patarroyo, M., Virtanen, I.
(2002). Localization of Laminin {alpha}4-Chain in Developing and Adult Human Tissues. J. Histochem. Cytochem.
50: 1113-1130
[Abstract]
[Full Text]
-
Gloe, T., Pohl, U.
(2002). Laminin Binding Conveys Mechanosensing in Endothelial Cells. Physiology
17: 166-169
[Abstract]
[Full Text]
-
Li, S., Harrison, D., Carbonetto, S., Fassler, R., Smyth, N., Edgar, D., Yurchenco, P. D.
(2002). Matrix assembly, regulation, and survival functions of laminin and its receptors in embryonic stem cell differentiation. JCB
157: 1279-1290
[Abstract]
[Full Text]
-
Marangi, P. A., Wieland, S. T., Fuhrer, C.
(2002). Laminin-1 redistributes postsynaptic proteins and requires rapsyn, tyrosine phosphorylation, and Src and Fyn to stably cluster acetylcholine receptors. JCB
157: 883-895
[Abstract]
[Full Text]
-
Smirnov, S. P., McDearmon, E. L., Li, S., Ervasti, J. M., Tryggvason, K., Yurchenco, P. D.
(2002). Contributions of the LG Modules and Furin Processing to Laminin-2 Functions. J. Biol. Chem.
277: 18928-18937
[Abstract]
[Full Text]
-
Ardini, E., Sporchia, B., Pollegioni, L., Modugno, M., Ghirelli, C., Castiglioni, F., Tagliabue, E., Menard, S.
(2002). Identification of a Novel Function for 67-kDa Laminin Receptor: Increase in Laminin Degradation Rate and Release of Motility Fragments. Cancer Res.
62: 1321-1325
[Abstract]
[Full Text]
-
Cote, P. D., Moukhles, H., Carbonetto, S.
(2002). Dystroglycan Is Not Required for Localization of Dystrophin, Syntrophin, and Neuronal Nitric-oxide Synthase at the Sarcolemma but Regulates Integrin alpha 7B Expression and Caveolin-3 Distribution. J. Biol. Chem.
277: 4672-4679
[Abstract]
[Full Text]
-
Rozovsky, I., Wei, M., Stone, D. J., Zanjani, H., Anderson, C. P., Morgan, T. E., Finch, C. E.
(2002). Estradiol (E2) Enhances Neurite Outgrowth by Repressing Glial Fibrillary Acidic Protein Expression and Reorganizing Laminin. Endocrinology
143: 636-646
[Abstract]
[Full Text]
-
Parsons, M. J., Pollard, S. M., Saude, L., Feldman, B., Coutinho, P., Hirst, E. M. A., Stemple, D. L.
(2002). Zebrafish mutants identify an essential role for laminins in notochord formation. Development
129: 3137-3146
[Abstract]
[Full Text]
-
Tsiper, M. V., Yurchenco, P. D.
(2002). Laminin assembles into separate basement membrane and fibrillar matrices in Schwann cells. J. Cell Sci.
115: 1005-1015
[Abstract]
[Full Text]
-
Li, X., Talts, U., Talts, J. F., Arman, E., Ekblom, P., Lonai, P.
(2001). Akt/PKB regulates laminin and collagen IV isotypes of the basement membrane. Proc. Natl. Acad. Sci. USA
98: 14416-14421
[Abstract]
[Full Text]
-
Rabinovitz, I., Gipson, I. K., Mercurio, A. M.
(2001). Traction Forces Mediated by alpha 6beta 4 Integrin: Implications for Basement Membrane Organization and Tumor Invasion. Mol. Biol. Cell
12: 4030-4043
[Abstract]
[Full Text]
-
Moiseeva, E. P.
(2001). Adhesion receptors of vascular smooth muscle cells and their functions. Cardiovasc Res
52: 372-386
[Abstract]
[Full Text]
-
Guo, L., Sanders, P. W., Woods, A., Wu, C.
(2001). The Distribution and Regulation of Integrin-Linked Kinase in Normal and Diabetic Kidneys. Am. J. Pathol.
159: 1735-1742
[Abstract]
[Full Text]
-
Yamada, H., Saito, F., Fukuta-Ohi, H., Zhong, D., Hase, A., Arai, K., Okuyama, A., Maekawa, R., Shimizu, T., Matsumura, K.
(2001). Processing of {beta}-dystroglycan by matrix metalloproteinase disrupts the link between the extracellular matrix and cell membrane via the dystroglycan complex. Hum Mol Genet
10: 1563-1569
[Abstract]
[Full Text]
-
Bezakova, G., Lomo, T.
(2001). Muscle Activity and Muscle Agrin Regulate the Organization of Cytoskeletal Proteins and Attached Acetylcholine Receptor (Achr) Aggregates in Skeletal Muscle Fibers. JCB
153: 1453-1464
[Abstract]
[Full Text]
-
Burkin, D. J., Wallace, G. Q., Nicol, K. J., Kaufman, D. J., Kaufman, S. J.
(2001). Enhanced Expression of the {alpha}7{beta}1 Integrin Reduces Muscular Dystrophy and Restores Viability in Dystrophic Mice. JCB
152: 1207-1218
[Abstract]
[Full Text]
-
Jacobson, C., Cote, P. D., Rossi, S. G., Rotundo, R. L., Carbonetto, S.
(2001). The Dystroglycan Complex Is Necessary for Stabilization of Acetylcholine Receptor Clusters at Neuromuscular Junctions and Formation of the Synaptic Basement Membrane. JCB
152: 435-450
[Abstract]
[Full Text]
-
Henry, M., Satz, J., Brakebusch, C, Costell, M, Gustafsson, E, Fassler, R, Campbell, K.
(2001). Distinct roles for dystroglycan, (&bgr;)1 integrin and perlecan in cell surface laminin organization. J. Cell Sci.
114: 1137-1144
[Abstract]
-
Williams, M., Resneck, W., Kaysser, T, Ursitti, J., Birkenmeier, C., Barker, J., Bloch, R.
(2001). Na,K-ATPase in skeletal muscle: two populations of beta-spectrin control localization in the sarcolemma but not partitioning between the sarcolemma and the transverse tubules. J. Cell Sci.
114: 751-762
[Abstract]
-
DiPersio, C., van der Neut, R, Georges-Labouesse, E, Kreidberg, J., Sonnenberg, A, Hynes, R.
(2000). alpha3beta1 and alpha6beta4 integrin receptors for laminin-5 are not essential for epidermal morphogenesis and homeostasis during skin development. J. Cell Sci.
113: 3051-3062
[Abstract]
-
Burkin, D., Kim, J., Gu, M, Kaufman, S.
(2000). Laminin and alpha7beta1 integrin regulate agrin-induced clustering of acetylcholine receptors. J. Cell Sci.
113: 2877-2886
[Abstract]
-
Aumailley, M, Pesch, M, Tunggal, L, Gaill, F, Fassler, R
(2000). Altered synthesis of laminin 1 and absence of basement membrane component deposition in (beta)1 integrin-deficient embryoid bodies. J. Cell Sci.
113: 259-268
[Abstract]
-
Liu, L. A., Engvall, E.
(1999). Sarcoglycan Isoforms in Skeletal Muscle. J. Biol. Chem.
274: 38171-38176
[Abstract]
[Full Text]