Laminin deposition in the extracellular matrix: A complex picture emerges

Journal of Cell Science

Volumn 122, Issue 24, 2009, Pages 4409-4417

  Hamill, Kevin J ^a   Kligys, Kristina ^a   Hopkinson, Susan B ^a   Jones, Jonathan C R ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Extracellular matrix; Integrins; Matrix receptors

Indexed keywords

ALPHA DYSTROGLYCAN; CELL SURFACE RECEPTOR; COLLAGEN TYPE 7; ENTACTIN; HEPARAN SULFATE; INTEGRIN; LAMININ; NETRIN; RAC1 PROTEIN;

ARTICLE; CELL FUNCTION; CELL MIGRATION; EXTRACELLULAR MATRIX; HUMAN; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; CELL MOVEMENT; CELLS; DIMERIZATION; EXTRACELLULAR MATRIX; HUMANS; LAMININ; PROTEIN SUBUNITS;

EID: 71449090226     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.041095     Document Type: Article

References (109)

1. Amano, S., Scott, I. A., Takahara, K., Koch, M., Gerecke, D. R., Keene, D. R., Hudson, D. L., Nishiyama, T., Lee, S., Greenspan, D. S. et al. (2000). Bone morphogenetic protein-1 (BMP-1) is an extracellular processing enzyme of the laminin 5 g2 chain. J. Biol. Chem. 275, 22728-22735.
2. Aumailley, M., Bruckner-Tuderman, L., Carter, W. G., Deutzmann, R., Edgar, D., Ekblom, P., Engel, J., Engvall, E., Hohenester, E., Jones, J. C. R. et al. (2005). A simplified laminin nomenclature. Matrix Biol. 24, 326-332.
3. Bader, B. L., Smyth, N., Nedbal, S., Miosge, N., Baranowsky, A., Mokkapati, S., Murshed, M. and Nischt, R. (2005). Compound genetic ablation of nidogen 1 and 2 causes basement membrane defects and perinatal lethality in mice. Mol. Cell. Biol. 25, 6846-6856.
4. Beck, K., Hunter, I. and Engel, J. (1990). Structure and function of laminin: anatomy of a multidomain glycoprotein. FASEB J. 4, 148-160.
5. Bezakova, G. and Ruegg, M. A. (2003). New insights into the roles of agrin. Nat. Rev. Mol. Cell. Biol. 4, 295-308.
6. Bose, K., Nischt, R., Page, A., Bader, B. L., Paulsson, M. and Smyth, N. (2006). Loss of nidogen-1 and -2 results in syndactyly changes in limb development. J. Biol. Chem. 281, 39620-39629.
7. Breitkreutz, D., Mirancea, N., Schmidt, C., Beck, R. and Werner, U. (2004). Inhibition of basement membrane formation by a nidogen-binding laminin γ1-chain fragment in human skin-organotypic cocultures. J. Cell Sci. 117, 2611-2622.
8. Burgess, R. W., Skarnes, W. C. and Sanes, J. R. (2000). Agrin isoforms with distinct amino termini: differential expression, localization, and function. J. Cell Biol. 151, 41-52.
9. Champliaud, M. F., Lunstrum, G. P., Rousselle, P., Nishiyama, T., Keene, D. R. and Burgeson, R. E. (1996). Human amnion contains a novel laminin variant, laminin-7, which like laminin-6, covalently associates with laminin-5 to promote stable epithelial-stromal attachment. J. Cell Biol. 132, 1189-1198.
10. Chen, M., Marinkovich, P. M., Jones, J. C. R., O'Toole, E. A., Li, Y.-Y. and Woodley, D. T. (1999). NC1 domain of type VII collagen binds to the β3 chain of laminin 5 via a unique subdomain within the fibrogenic-like repeats. J. Invest. Dermatol. 112, 177-183.
11. Chen, M., Kasahara, N., Keene, D. R., Chan, L., Hoeffler, W. K., Finlay, D., Barcova, M., Cannon, P. M., Mazurek, C. and Woodley, D. T. (2002). Restoration of type VII collagen expression and function in dystrophic epidermolysis bullosa. Nat. Genet. 32, 670-675.
12. Cheng, Y. S., Champliaud, M. F., Burgeson, R. E., Marinkovich, M. P. and Yurchenco, P. D. (1997). Self-assembly of laminin isoforms. J. Biol. Chem. 272, 31525-31532.
13. Church, H. J. and Aplin, J. D. (1998). BeWo choriocarcinoma cells produce laminin 10. Biochem. J. 332, 491-498.
14. Cohen, M. W., Jacobson, C., Yurchenco, P. D., Morris, G. E. and Carbonetto, S. (1997). Laminin-induced clustering of dystroglycan on embryonic muscle cells: comparison with agrin-induced clustering. J. Cell Biol. 136, 1047-1058.
15. Colognato, H. and Yurchenco, P. D. (1999). The laminin alpha2 expressed by dystrophic dy(2J) mice is defective in its ability to form polymers. Curr. Biol. 18, 1327-1330.
16. Costell, M., Gustafsson, E., Aszódi, A., Mörgelin, M., Bloch, W., Hunziker, E., Addicks, K., Timpl, R. and Fässler, R. (1999). Perlecan maintains the integrity of cartilage and some basement membranes. J. Cell Biol. 147, 1109-1122.
17. Dabadie, M., Valli, N., Jacobin, M. J., Laroche-Traineau, J., Barat, J. L., Ducassou, D., Nurden, A. T. and Clofent-Sanchez, G. (2001). Characterisation, cloning and sequencing of a conformation-dependent monoclonal antibody to the αIIbβ3 integrin: interest for use in thrombus detection. Platelets 12, 395-405.
18. DeBiase, P. J., Lane, K., Budinger, S., Ridge, K., Wilson, M. and Jones, J. C. R. (2006). Laminin-311 (laminin-6) fiber assembly by type I-like alveolar cells. J. Histo. Cytochem. 54, 665-672.
19. deHart, G. W. and Jones, J. C. R. (2004). Myosin-mediated cytoskeleton contraction and Rho GTPases regulate laminin-5 matrix assembly. Cell Motil. Cyto. 57, 107-117.
20. deHart, G. W., Healy, K. E. and Jones, J. C. R. (2003). The role of α3β1 integrin in determining the supramolecular organization of laminin-5 in the extracellular matrix of keratinocytes. Exp. Cell Res. 283, 67-79.
21. Denzer, A. J., Gesemann, M., Schumacher, B. and Ruegg, M. A. (1995). An amino-terminal extension is required for the secretion of chick agrin and its binding to extracellular matrix. J. Cell Biol. 131, 1547-1560.
22. Denzer, A. J., Schulthess, T., Fauser, C., Schumacher, B., Kammerer, R. A., Engel, J. and Ruegg, M. A. (1998). Electron microscopic structure of agrin and mapping of its binding site in laminin-1. EMBO J. 17, 335-343.
23. Ekbloom, P., Ekbloom, M., Fecker, L., Klein, G., Zhang, H. Y., Kadoya, Y., Chu, M. L., Mayer, U. and Timpl, R. (1994). Role of mesenchymal nidogen for epithelial morphogenesis in vitro. Development 120, 2003-2014.
24. Frank, D. E. and Carter, W. G. (2004). Laminin 5 deposition regulates keratinocyte polarization and persistent migration. J. Cell Sci. 117, 1351-1363.
25. Gagnoux-Palacios, L., Allegra, M., Spirito, F., Pommeret, O., Romero, C., Ortonne, J. P. and Meneguzzi, G. (2001). The short arm of the laminin gamma2 chain plays a pivotal role in the incorporation of laminin 5 into the extracellular matrix and in cell adhesion. J. Cell Biol. 153, 835-850.
26. Gesemann, M., Brancaccio, A., Schumacher, B. and Ruegg, M. A. (1998). Agrin Is a high-affinity binding protein of dystroglycan in non-muscle tissue. J. Biol. Chem. 273, 600-605.
27. Giannelli, G., Falk-Marzillier, J., Schiraldi, O., Stetler-Stevenson, W. G. and Quaranta, V. (1997). Induction of cell migration by matrix metalloprotease-2 cleavage of laminin-5. Science 277, 225-228.
28. Gipson, I. K., Grill, S. M., Spurr, S. J. and Brennan, S. J. (1983). Hemidesmosome formation in vitro. J. Cell Biol., 97, 849-857.
29. Goldfinger, L. E., Stack, M. S. and Jones, J. C. R. (1998). Processing of laminin-5 and its functional consequences: role of plasmin and tissue-type plasminogen activator. J. Cell Biol. 141, 255-265.
30. Gonzales, M., Haan, K., Baker, S. E., Fitchmun, M. I., Todorov, I., Weitzman, S. and Jones, J. C. R. (1999). A cell signal pathway involving laminin-5, α3β1 integrin, and mitogen-activated protein kinase can regulate epithelial cell proliferation. Mol. Biol. Cell 10, 259-270.
31. Gonzales, M., Weksler, B., Tsuruta, D., Goldman, R. D., Yoon, K. J., Hopkinson, S. B., Flitney, F. W. and Jones, J. C. R. (2001). Structure and function of a vimentin-associated matrix adhesion in endothelial cells. Mol. Biol. Cell 12, 85-100.
32. Hamelers, I. H. L., Olivo, C., Mertens, A. E. E., Pegtel, D. M., van der Kammen, R. A., Sonnenberg, A. and Collard, J. G. (2005). The Rac activator Tiam1 is required for α3β1-mediated laminin-5 deposition, cell spreading, and cell migration. J. Cell Biol. 171, 871-881.
33. Hamill, K. J., Langbein, L., Jones, J. C. R. and McLean, W. H. I. (2009). Identification of a novel family of laminin N-terminal alternate splice isoforms: structural and functional characterization. J. Biol. Chem. [Epub ahead of print] doi; 10.1074/jbc.M109.052811
34. Hashimoto, J., Kariya, Y. and Miyazaki, K. (2006). Regulation of proliferation and chondrogenic differentiation of human mesenchymal stem cells by laminin-5 (laminin-332). Stem Cells 24, 2346-2354.
35. Henry, M. D. and Campbell, K. P. (1998). A role for dystroglycan in basement membrane assembly. Cell 95, 859-870.
36. Henry, M. D., Satz, J. S., Brakebusch, C., Costell, M., Gustafsson, E., Fassler, R. and Campbell, K. P. (2001). Distinct roles for dystroglycan, β1 integrin and perlecan in cell surface laminin organization. J. Cell Sci. 114, 1137-1144.
37. Hopf, M., Goring, W., Kohfeldt, E., Yamada, Y. and Timpl, R. (1999). Recombinant domain IV of perlecan binds to nidogens, laminin-nidogen complex, fibronectin, fibulin-2, and heparin. Eur. J. Biochem. 259, 917-926.
38. Hopkinson, S. B., DeBiase, P. J., Kligys, K. H. K. and Jones, J. C. R. (2008). Fluorescently tagged laminin subunits facilitate analyses of the properties, assembly and processing of laminins in live and fixed lung epithelial cells and keratinocytes. Matrix Biol. 27, 640-647.
39. Jones, J. C. R., Asmuth, J., Baker, S. E., Langhofer, M., Roth, S. I. and Hopkinson, S. B. (1994). Hemidesmosomes: Extracellular Matrix/ Intermediate Filament Connectors. Exp. Cell Res. 213, 1-11.
40. Jones, J. C. R., Hopkinson, S. B. and Goldfinger, L. E. (1998). Structure and assembly of hemidesmosomes. BioEssays 20, 488-494.
41. 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. et al. (2005). Laminin-6 assembles into multimolecular fibrillar complexes with perlecan and participates in mechano-signal transduction via a dystroglycan-dependent, integrin-independent, mechanism. J. Cell Sci. 118, 2557-2565.
42. Kadoya, Y., Salmwirta, K., Talts, J. F., Kadoya, K., Mayer, U., Timpl, R. and Ekbloom, P. (1997). Importance of nidogen binding to laminin gamma 1 for branching morphogenesis in the submadibular gland. Development 124, 683-691.
43. Kallunki, P. and Tryggvason, K. (1992). Human basement membrane heparan sulfate proteoglycan core protein: a 467-kD protein containing multiple domains resembling elements of the low density lipoprotein receptor, laminin, neural cell adhesion molecules, and epidermal growth factor. J. Cell Biol. 116, 559-571.
44. Kallunki, P., Sainio, K., Eddy, R., Byers, M., Kallunki, T., Sariola, H., Beck, K., Hirvonen, H., Shows, T. B. and Tryggvason, K. (1992). A truncated laminin chain homologous to the B2 chain: structure, spatial expression, and chromosomal assignment. J. Cell Biol. 119, 679-693.
45. Klass, C. M., Couchman, J. R. and Woods, A. (2000). Control of extracellular matrix assembly by syndecan-2 proteoglycan. J. Cell Sci. 113, 493-506.
46. Kligys, K., Claiborne, J. N., DeBiase, P., Hopkinson, S. B., Mizuno, K. and Jones, J. C. R. (2007). The Slingshot family of phosphatases mediates Rac1 regulation of cofilin phosphorylation, laminin-332 organization and motility behavior of keratinocytes. J. Biol. Chem. 282, 32520-32528.
47. Kohfeldt, E., Sasaki, T., Göhring, W. and Timpl, R. (1998). Nidogen-2: a new basement membrane protein with diverse binding properties. J. Mol. Biol. 282, 99-109.
48. Kunneken, K., Pohlentz, G., Schmidt-Hederich, A., Odenthal, U., Smyth, N., Peter-Katalinic, J., Bruckner, P. and Eble, J. A. (2004). Recombinant human laminin-5 domains - effects of heterotrimerization, proteolytic processing, and N-glycosylation on α3β1 integrin binding. J. Biol. Chem. 279, 5184-5193.
49. Leiss, M., Beckmann, K., Giros, A., Costell, M. and Fassler, R. (2008). The role of integrin binding sites in fibronectin matrix assembly in vivo. Curr. Opin. Cell Biol. 20, 502-507.
50. Li, S., Harrison, D., Carbonetto, S., Fassler, R., Smyth, N. and Edgar, D. (2002). Matrix assembly, regulation, and survival functions of laminin and its receptors in embryonic stem cell differentiation. J. Cell Biol. 157, 1279-1290.
51. Lohikangas, L., Gullberg, D. and Johansson, S. (2001). Assembly of laminin polymers is dependent on β1-integrins. Exp. Cell Res. 265, 135-144.
52. Ma, W., Tavakoli, T., Derby, E., Serebryakova, Y., Rao, M. and Mattson, M. (2008). Cell-extracellular matrix interactions regulate neural differentiation of human embryonic stem cells. BMC Dev. Biol. 8, 90.
53. Mainiero, F., Murgia, C., Wary, K. K., Curatola, A. M., Pepe, A., Blumenberg, M., Westwick, J. K., Der, C. J. and Giancotti, F. G. (1997). The coupling of α6β4 integrin to the Ras-MAP kinase pathways mediated by Shc controls keratinocyte proliferation. EMBO J. 16, 2365-2375.
54. Mann, K., Deutzmann, R., Aumailley, M., Timpl, R., Raimondi, L., Yamada, Y., Pan, T.-C., Conway, D. and Chu, M.-L. (1989). Amino acid sequence of mouse nidogen, a multidomain basement membrane protein with binding activity for laminin, collagen IV and cells. EMBO J. 8, 65-72.
55. Margadant, C., Raymond, K., Kreft, M., Sachs, N., Janssen, H. and Sonnenberg, A. (2009). Integrin α3β1 inhibits directional migration and wound re-epithelialization in the skin. J. Cell Sci. 122, 278-288.
56. Marinkovich, M. P., Lunstrum, G. P. and Burgeson, R. E. (1992). The anchoring filament protein kalinin is synthesized and secreted as a high molecular weight precursor. J. Biol. Chem. 267, 17900-17906.
57. Mascarenhas, J. B., Rüegg, M. A., Winzen, U., Halfter, W., Engel, J. and Stetefeld, J. (1993). Mapping of the laminin-binding site of the N-terminal agrin domain (NtA). EMBO J. 22, 529-536.
58. Matsui, C., Wang, C. K., Nelson, C. F., Bauer, E. A. and Hoeffler, W. K. (1995). The assembly of laminin-5 subunits. J. Biol. Chem. 270, 23496-23503.
59. Mayer, U., Nischt, R., Poschl, E., Mann, K., Fukuda, K., Gerl, M., Yamada, Y. and Timpl, R. (1993). A single EGF-like motif of laminin is responsible for high affinity nidogen binding. EMBO J. 12, 1879-1885.
60. McGowan, K. and Marinkovich, M. P. (2000). Laminins and human disease. Micro. Res. Tech. 51, 262-279.
61. McKee, K. K., Harrison, D., Capizzi, S. and Yurchenco, P. D. (2007). Role of laminin terminal globular domains in basement membrane assembly. J. Biol. Chem. 282, 21437-21447.
62. McKee, K. K., Capizzi, S. and Yurchenco, P. D. (2009). Scaffold-forming and adhesive contributions of synthetic laminin-binding proteins to basement membrane assembly. J. Biol. Chem. 284, 8984-8994.
63. Miner, J. H. and Yurchenco, P. D. (2004). Laminin function in tissue morphogenesis. Ann. Rev. Cell Dev. Biol. 20, 255-284.
64. Mokkapati, S., Baranowsky, A., Mirancea, N. and Smyth, N. (2008). Basement membranes in skin are differently affected by lack of nidogen 1 and 2. J. Invest. Dermatol. 128, 2259-2267.
65. Moll, J., Barzaghi, P., Lin, S., Bezakova, G., Lochmüller, H., Engvall, E., Müller, U. and Ruegg, M. A. (2001). An agrin minigene rescues dystrophic symptoms in a mouse model for congenital muscular dystrophy. Nature 413, 302-307.
66. Montanaro, F., Lindenbaum, M. and Carbonetto, S. (1999). α-Dystroglycan is a laminin receptor involved in extracellular matrix assembly on myotubes and muscle cell viability. J. Cell Biol. 145, 1325-1340.
67. Murshed, M., Smyth, N., Miosge, N., Karolat, T., Krieg, M., Paulsson, M. and Nischt, R. (2000). The absence of nidogen 1 does not affect murine basement membrane formation. Mol. Cell. Biol. 20, 7007-7012.
68. Nomizu, M., Utani, A., Beck, K., Otaka, A., Roller, P. P. and Yamada, Y. (1996). Mechanism of laminin chain assembly into a triple-stranded coiled-coil structure. Biochem. 35, 2885-2893.
69. Noonan, D. M., Fulle, A., Valente, P., Cai, S., Horigan, E., Sasaki, M., Yamada, Y. and Hassell, J. R. (1991). The complete sequence of perlecan, a basement membrane heparan sulfate proteoglycan, reveals extensive similarity with laminin A chain, low density lipoprotein-receptor, and the neural cell adhesion molecule. J. Biol. Chem. 266, 22939-22947.
70. O'Brien, L. E., Jou, T. S., Pollack, A. L., Zhang, Q., Hansen, S. H., Yurchenco, P. and Mostov, K. E. (2001). Rac1 orientates epithelial apical polarity through effects on basolateral laminin assembly. Nat. Cell Biol. 3, 831-838.
71. Odenthal, U., Haehn, S., Tunggal., P, Merkl, B., Schomburg, D., Frie, C., Paulsson, M. and Smyth, N. (2004). Molecular analysis of laminin N-terminal domains mediating self-interactions. J. Biol. Chem. 279, 44504-44512.
72. Patton, B. L., Miner, J. H., Chiu, A. Y. and Sanes, J. (1997). Distribution and function of laminins in the neuromuscular system of developing, adult, and mutant mice. J. Cell Biol. 139, 1507-1521.
73. Poschl, E., Fox, J. W., Block, D., Mayer, U. and Timpl, R. (1994). Two non-contiguous regions contribute to nidogen binding to a single EGF-like motif on the laminin gamma 1 chain. EMBO J. 13, 3741-3747.
74. Raftopoulou, M. and Hall, A. (2004). Cell migration: Rho GTPases lead the way. Dev. Biol. 265, 23-32.
75. Ridley, A. J. (2001a). Rho family proteins: coordinating cell responses. Trends Cell Biol. 11, 471-477.
76. Ridley, A. J. (2001b). Rho GTPases and cell migration. J. Cell Sci. 114, 2713-2722.
77. Rousselle, P., Keene, D. R., Ruggiero, F., Champliaud, M. F., Rest, M. and Burgeson, R. E. (1997). Laminin 5 binds the NC-1 domain of type VII collagen J. Cell Biol. 138, 719-728.
78. Ruegg, M. A. and Bixby, J. L. (1998). Agrin orchestrates synaptic differentiation at the vertebrate neuromuscular junction. Trends Neurosci. 21, 22-27.
79. Russell, A. J., Fincher, E. F., Millman, L., Smith, R., Vela, V., Waterman, E. A., Dey, C. N., Guide, S., Weaver, V. M. and Marinkovich, M. P. (2003). α6β4 integrin regulates keratinocyte chemotaxis through differential GTPase activation and antagonism of α3β1 integrin. J. Cell Sci. 116, 3543-3556.
80. Schittny, J. C. and Yurchenco, P. D. (1990). Terminal short arm domains of basement membrane laminin are critical for its self-assembly. J. Cell Biol. 110, 825-832.
81. Schneiders, F. I., Maertens, B., Böse, K., Li, Y., Brunken, W. J., Paulsson, M., Smyth, N. and Koch, M. (2007). Binding of netrin-4 to laminin short arms regulates basement membrane assembly. J. Biol. Chem. 282, 23750-23758.
82. Schymeinsky, J., Nedbal, S., Miosge, N., Poschl, E., Rao, C., Beier, D. R., Skarnes, W. C., Timpl, R. and Bader, B. (2002). Gene structure and functional analysis of the mouse nidogen-2 gene: nidogen-2 is not essential for basement membrane formation in mice. Mol. Cell. Biol. 22, 6820-6830.
83. Sehgal, B. U., Debiase, P., Matzno, S., Chew, T.-L., Claiborne, J. N., Hopkinson, S. B., Russell, A., Marinkovich, P. M. and Jones, J. C. R. (2006). Integrin β4 regulates migratory behavior of keratinocytes by determining laminin-332 (laminin-5) matrix organization. J. Biol. Chem. 281, 35487-35498.
84. Sher, I., Zisman-Rozen, S., Eliahu, L., Whitelock, J. M., Maas-Szabowski, N., Yamada, Y., Breitkreutz, D., Fusenig, N. E., Arikawa-Hirasawa, E., Iozzo, R. V. et al. (2006). Targeting perlecan in human keratinocytes reveals novel roles for perlecan in epidermal formation. J. Biol. Chem. 281, 5178-5187.
85. Sigle, R. O., Gil, S. G., Bhattacharya, M., Ryan, M. C., Yang, T.-M., Brown, T. A., Boutaud, A., Miyashita, Y., Olerud, J. and Carter, W. G. (2004). Globular domains 4/5 of the laminin α3 chain mediate deposition of precursor laminin 5. J. Cell Sci. 11, 4481-4494.
86. Staquicini, F. I., Dias-Neto, E., Li, J., Snyder, E. Y., Sidman, R. L., Pasqualini, R. and Arap, W. (2009). Discovery of a functional protein complex of netrin-4, laminin γ1 chain, and integrin α6β1 in mouse neural stem cells. Proc. Natl. Acad. Sci. USA 106, 2903-2908.
87. Stepp, M. A., Liu, Y., Pal-Ghosh, S., Jurjus, R. A., Tadvalkar, G., Sekaran, A., LoSicco, K., Jiang, L., Larsen, M., Li, L. et al. (2007). Reduced migration, altered matrix and enhanced TGF1 signaling are signatures of mouse keratinocytes lacking Sdc1. J. Cell Sci. 120, 2851-2863.
88. Stetefeld, J., Jenny, M., Schulthess, T., Landwehr, R., Schumacher, B., Frank, S., Rüegg, M. A., Engel, J. and Kammerer, R. A. (2001). The laminin-binding domain of agrin is structurally related to N-TIMP-1. Nat. Struct. Biol. 8, 705-709.
89. Takagi, J., Yang, T., Liu, J., Wang, J. and Springer, T. A. (2003). Complex between nidogen and laminin fragments reveals a paradigmatic β-propellor interface. Nature 424, 969-974.
90. Talts, J. F., Sasaki, T., Miosge, N., Gohring, W., Mann, K., Mayne, R. and Timpl, R. (2000). Structural and functional analysis of the recombinant G domain of the laminin α4 chain and its proteolytic processing in tissues. J. Biol. Chem. 275, 35192-35199.
91. Timpl, R., Tisi, D., Talts, J. F., Andac, Z., Sasaki, T. and Hohenester, E. (2000). Structure and function of laminin LG modules. Matrix Biol. 19, 309-317.
92. Tisi, D., Talts, J. F., Timpl, R. and Hohenester, E. (2000). Structure of the C-terminal laminin G-like domain pair of the laminin alpha2 chain harbouring binding sites for alpha-dystroglycan and heparin. EMBO J. 19, 1432-1440.
93. Tran, M., Rousselle, P., Nokelainen, P., Tallapragada, S., Nguyen, N. T., Fincher, E. F. and Marinkovich, M. P. (2008). Targeting a tumor-specific laminin domain critical for human carcinogenesis. Cancer Res. 68, 2885-2894.
94. Tsiper, M. V. and Yurchenco, P. D. (2002). Laminin assembles into separate basement membrane and fibrillar matrices in Schwann cells. J. Cell Sci. 115, 1005-1015.
95. Tsubota, Y., Mizushima, H., Hirosaki, T., Higashi, S., Yasumitsu, H. and Miyazaki, K. (2000). Isolation and activity of proteolytic fragment of laminin-5 α3 chain. Biochem. Biophys. Res. Commun. 278, 614-620.
96. Tunggal, P., Smyth, N., Paulsson, M. and Ott, M. C. (2000). Laminins: structural and genetic regulation. Micro. Res. Tech. 51, 214-227.
97. Tunggal, P., Wartenberg, M., Paulsson, M. and Smyth, N. (2003). Expression of the nidogen-binding site on laminin γ1 chain disturbs basement membrane formation and maintenance in F9 embryoid bodies. J. Cell Sci. 116, 803-812.
98. Tzu, J. and Marinkovich, M. P. (2008). Bridging structure with function: Structural, regulatory, and developmental role of laminins. Int. J. Biochem. Cell Biol. 40, 199-214.
99. Udayakumar, T. S., Chen, M. L., Bair, E. L., Von Bredow, D. C., Cress, A. E., Nagle, R. B. and Bowden, G. T. (2003). Membrane type-1-matrix metalloproteinase expressed by prostate carcinoma cells cleaves human laminin-5 beta3 chain and induces cell migration. Cancer Res. 63, 2292-2299.
100. Utani, A., Nomizu, M., Timpl, R., Roller, P. P. and Yamada, Y. (1994). Laminin chain assembly. Specific sequences at the C terminus of the long arm are required for the formation of specific double- and triple-stranded coiled-coil structures. J. Biol. Chem. 269, 19167-19175.
101. Vidal, F., Aberdam, D., Miquel, C., Christiano, A. M., Pulkkinen, L., Uitto, J., Ortonne, J.-P. and Meneguzzi, G. (1995). Integrin β4 mutations associated with junctional epidermolysis bullosa with pyloric atresia. Nat. Genet. 10, 229-234.
102. Weir, L., Oppizzi, M. L., Henry, M. D., Onishi, A., Campbell, K. P., Bissell, M. J. and Muschler, J. (2006). Dystroglycan loss disrupts polarity and beta-casein induction in mammary epithelial cells by perturbing laminin anchoring. J. Cell Sci. 119, 4047-4058.
103. Wierzbicka-Patynowski, I. and Schwarzbauer, J. E. (2003). The ins and outs of fibronectin matrix assembly. J. Cell Sci. 116, 3269-3276.
104. Williamson, R. A., Henry, M. D., Daniels, K. J., Hrstka, R. F., Sunada, Y., Ibraghimov-Beskrovnaya, O. and Campbell, K. P. (1997). Dystroglycan is essential for early embryonic development: disruption of Reichert's membrane in Dag1-null mice. Hum. Mol. Genet. 6, 831-841.
105. Wolozin, B. L., Pruchnicki, A., Dickson, D. W. and Davies, P. (1986). A neuronal antigen in the brains of Alzheimer patients. Science 232, 648-650.
106. Yurchenco, P. D., Quan, Y., Colognato, P., Mathus, T., Harrison, D., Yamada, Y. and O'Rear, J. (1997). The α chain of laminin 1 is independently secreted and drives secretion of its β and γ chain partners. Proc. Natl. Acac. Sci. USA 94, 10189-10194.
107. Yurchenco, P. D., Amenta, P. S. and Patton, B. L. (2004). Basement membrane assembly, stability and activities through the developmental lens.. Matrix Biol. 22, 521-538.
108. Yurchenco, P. D. and Wadsworth, W. G. (2004). Assembly and tissue functions of early embryonic laminins and netrins. Curr. Op. Cell Biol. 6, 572-579.
109. Zahir, N., Lakins, J. N., Russell, A., Ming, W., Chatterjee, C., Rozenberg, G. I., Marinkovich, M. P. and Weaver, V. M. (2003). Autocrine laminin-5 ligates α6β4 integrin and activates RAC and NFκB to mediate anchorage-independent survival of mammary tumors. J. Cell Biol. 163, 1397-1407.