Identification of α-dystroglycan binding sequences in the laminin α2 chain LG4-5 module

Matrix Biology

Volumn 29, Issue 2, 2010, Pages 143-151

  Suzuki, Nobuharu ^a,b   Hozumi, Kentaro ^a,b   Urushibata, Shunsuke ^a   Yoshimura, Takashi ^a   Kikkawa, Yamato ^a   Gumerson, Jessica D ^c   Michele, Daniel E ^c   Hoffman, Matthew P ^b   Yamada, Yoshihiko ^b   Nomizu, Motoyoshi ^a  

^a TOKYO UNIVERSITY OF PHARMACY AND LIFE SCIENCES   (Japan)

^b NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Dystroglycan; Basement membrane; Heparin; Laminin; Synthetic peptide

Indexed keywords

ALANINE; ALPHA DYSTROGLYCAN; ARGININE; CELL SURFACE RECEPTOR; HEPARIN; LAMININ ALPHA2; PROTEOHEPARAN SULFATE; RECOMBINANT PROTEIN; SYNTHETIC PEPTIDE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CONTROLLED STUDY; EXPLANT; INHIBITION KINETICS; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; SUBMANDIBULAR GLAND; TISSUE CULTURE;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; DNA MUTATIONAL ANALYSIS; DYSTROGLYCANS; HEPARIN; HUMANS; LAMININ; MICE; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; PEPTIDES; PROTEIN BINDING; RECOMBINANT PROTEINS; SUBMANDIBULAR GLAND;

EID: 76549083174     PISSN: 0945053X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.matbio.2009.09.006     Document Type: Article

References (36)

1. Aumailley M., Bruckner-Tuderman L., Carter W.G., Deutzmann R., Edgar D., Ekblom P., Engel J., Engvall E., Hohenester E., Jones J.C.R., Kleinman H.K., Marinkovich M.P., Martin G.R., Mayer U., Meneguzzi G., Miner J.H., Miyazaki K., Patarroyo M., Paulsson M., Quaranta V., Sanes J.R., Sasaki T., Sekiguchi K., Sorokin L.M., Talts J.F., Tryggvason K., Uitto J., Virtanen I., von der Mark K., Wewer U.M., Yamada Y., and Yurchenco P.D. A simplified laminin nomenclature. Matrix Biol. 24 (2005) 326-332
2. Combs A.C., and Ervasti J.M. Enhanced laminin binding by alpha-dystroglycan after enzymatic deglycosylation. Biochem. J. 390 (2005) 303-309
3. Couchman J.R. Syndecans: proteoglycan regulators of cell-surface microdomains?. Nat. Rev., Mol. Cell Biol. 4 (2003) 926-937
4. Durbeej M., Talts J.F., Henry M.D., Yurchenco P.D., Campbell K.P., and Ekblom P. Dystroglycan binding to laminin alpha1LG4 module influences epithelial morphogenesis of salivary gland and lung in vitro. Differentiation 69 (2001) 121-134
5. Helbling-Leclerc A., Zhang X., Topaloglu H., Cruaud C., Tesson F., Weissenbach J., Tome F.M., Schwartz K., Fardeau M., and Tryggvason K. Mutations in the laminin alpha 2-chain gene (LAMA2) cause merosin-deficient congenital muscular dystrophy. Nat. Genet. 11 (1995) 216-218
6. Hoffman M.P., Nomizu M., Roque E., Lee S., Jung D.W., Yamada Y., and Kleinman H.K. Laminin-1 and laminin-2 G-domain synthetic peptides bind syndecan-1 and are involved in acinar formation of a human submandibular gland cell line. J. Biol. Chem. 273 (1998) 28633-28641
7. Hoffman M.P., Engbring J.A., Nielsen P.K., Vargas J., Steinberg Z., Karmand A.J., Nomizu M., Yamada Y., and Kleinman H.K. Cell type-specific differences in glycosaminoglycans modulate the biological activity of a heparin-binding peptide (RKRLQVQLSIRT) from the G domain of the laminin alpha1 chain. J. Biol. Chem. 276 (2001) 22077-22085
8. Hohenester E., Tisi D., Talts J.F., and Timpl R. The crystal structure of a laminin G-like module reveals the molecular basis of alpha-dystroglycan binding to laminins, perlecan, and agrin. Mol. Cell 4 (1999) 783-792
9. Hozumi K., Suzuki N., Nielsen P.K., Nomizu M., and Yamada Y. Laminin alpha1 chain LG4 module promotes cell attachment through syndecans and cell spreading through integrin alpha2beta1. J. Biol. Chem. 281 (2006) 32929-32940
10. Hozumi K., Suzuki N., Uchiyama Y., Katagiri F., Kikkawa Y., and Nomizu M. Chain-specific heparin-binding sequences in the laminin alpha chain LG45 modules. Biochemistry 48 (2009) 5375-5381
11. Hozumi K., Yamagata N., Otagiri D., Fujimori C., Kikkawa Y., Kadoya Y., and Nomizu M. Mixed peptide-chitosan membranes to mimic the biological activities of a multifunctional laminin alpha1 chain LG4 module. Biomaterials 30 (2009) 1596-1603
12. Kadoya Y., and Yamashina S. Salivary gland morphogenesis and basement membranes. Anat. Sci. Int. 80 (2005) 71-79
13. Kadoya Y., Nomizu M., Sorokin L.M., Yamashina S., and Yamada Y. Laminin alpha1 chain G domain peptide, RKRLQVQLSIRT, inhibits epithelial branching morphogenesis of cultured embryonic mouse submandibular gland. Dev. Dyn. 212 (1998) 394-402
14. Kato K., Utani A., Suzuki N., Mochizuki M., Yamada M., Nishi N., Matsuura H., Shinkai H., and Nomizu M. Identification of neurite outgrowth promoting sites on the laminin alpha 3 chain G domain. Biochemistry 41 (2002) 10747-10753
15. Kim W.H., Nomizu M., Song S.Y., Tanaka K., Kuratomi Y., Kleinman H.K., and Yamada Y. Laminin-alpha1-chain sequence Leu-Gln-Val-Gln-Leu-Ser-Ile-Arg (LQVQLSIR) enhances murine melanoma cell metastases. Int. J. Cancer 77 (1998) 632-639
16. Kuang W., Xu H., Vachon P.H., Liu L., Loechel F., Wewer U.M., and Engvall E. Merosin-deficient congenital muscular dystrophy. Partial genetic correction in two mouse models. J. Clin. Invest. 102 (1998) 844-852
17. Miner J.H., and Yurchenco P.D. Laminin functions in tissue morphogenesis. Annu. Rev. Cell Dev. Biol. 20 (2004) 255-284
18. Miyagoe Y., Hanaoka K., Nonaka I., Hayasaka M., Nabeshima Y., Arahata K., and Takeda S. Laminin alpha2 chain-null mutant mice by targeted disruption of the Lama2 gene: a new model of merosin (laminin 2)-deficient congenital muscular dystrophy. FEBS Lett. 415 (1997) 33-39
19. Nomizu M., Kim W.H., Yamamura K., Utani A., Song S.Y., Otaka A., Roller P.P., Kleinman H.K., and Yamada Y. Identification of cell binding sites in the laminin alpha 1 chain carboxyl-terminal globular domain by systematic screening of synthetic peptides. J. Biol. Chem. 270 (1995) 20583-20590
20. Nomizu M., Kuratomi Y., Malinda K.M., Song S.Y., Miyoshi K., Otaka A., Powell S.K., Hoffman M.P., Kleinman H.K., and Yamada Y. Cell binding sequences in mouse laminin alpha1 chain. J. Biol. Chem. 273 (1998) 32491-32499
21. Okazaki I., Suzuki N., Nishi N., Utani A., Matsuura H., Shinkai H., Yamashita H., Kitagawa Y., and Nomizu M. Identification of biologically active sequences in the laminin alpha 4 chain G domain. J. Biol. Chem. 277 (2002) 37070-37078
22. Patel V.N., Rebustini I.T., and Hoffman M.P. Salivary gland branching morphogenesis. Differentiation 74 (2006) 349-364
23. Patel V.N., Knox S.M., Likar K.M., Lathrop C.A., Hossain R., Eftekhari S., Whitelock J.M., Elkin M., Vlodavsky I., and Hoffman M.P. Heparanase cleavage of perlecan heparan sulfate modulates FGF10 activity during ex vivo submandibular gland branching morphogenesis. Development 134 (2007) 4177-4186
24. Rebustini I.T., Patel V.N., Stewart J.S., Layvey A., Georges-Labouesse E., Miner J.H., and Hoffman M.P. Laminin alpha5 is necessary for submandibular gland epithelial morphogenesis and influences FGFR expression through beta1 integrin signaling. Dev. Biol. 308 (2007) 15-29
25. Richard B.L., Nomizu M., Yamada Y., and Kleinman H.K. Identification of synthetic peptides derived from laminin alpha1 and alpha2 chains with cell type specificity for neurite outgrowth. Exp. Cell Res. 228 (1996) 98-105
26. Suzuki N., Ichikawa N., Kasai S., Yamada M., Nishi N., Morioka H., Yamashita H., Kitagawa Y., Utani A., Hoffman M.P., and Nomizu M. Syndecan binding sites in the laminin alpha1 chain G domain. Biochemistry 42 (2003) 12625-12633
27. Suzuki N., Nakatsuka H., Mochizuki M., Nishi N., Kadoya Y., Utani A., Oishi S., Fujii N., Kleinman H.K., and Nomizu M. Biological activities of homologous loop regions in the laminin alpha chain G domains. J. Biol. Chem. 278 (2003) 45697-45705
28. Suzuki N., Yokoyama F., and Nomizu M. Functional sites in the laminin alpha chains. Connect. Tissue Res. 46 (2005) 142-152
29. Talts J.F., Andac Z., Gohring W., Brancaccio A., and Timpl R. Binding of the G domains of laminin alpha1 and alpha2 chains and perlecan to heparin, sulfatides, alpha-dystroglycan and several extracellular matrix proteins. EMBO J. 18 (1999) 863-870
30. Utani A., Nomizu M., Matsuura H., Kato K., Kobayashi T., Takeda U., Aota S., Nielsen P.K., and Shinkai H. A unique sequence of the laminin alpha 3 G domain binds to heparin and promotes cell adhesion through syndecan-2 and -4. J. Biol. Chem. 276 (2001) 28779-28788
31. Utani A., Momota Y., Endo H., Kasuya Y., Beck K., Suzuki N., Nomizu M., and Shinkai H. Laminin alpha 3 LG4 module induces matrix metalloproteinase-1 through mitogen-activated protein kinase signaling. J. Biol. Chem. 278 (2003) 34483-34490
32. Williamson R.A., Henry M.D., Daniels K.J., Hrstka R.F., Lee J.C., Sunada Y., Ibraghimov-Beskrovnaya O., and Campbell K.P. Dystroglycan is essential for early embryonic development: disruption of Reichert's membrane in Dag1-null mice. Hum. Mol. Genet. 6 (1997) 831-841
33. Wizemann H., Garbe J.H.O., Friedrich M.V.K., Timpl R., Sasaki T., and Hohenester E. Distinct requirements for heparin and alpha-dystroglycan binding revealed by structure-based mutagenesis of the laminin alpha2 LG4-LG5 domain pair. J. Mol. Biol. 332 (2003) 635-642
34. Yamada H., Chiba A., Endo T., Kobata A., Anderson L.V., Hori H., Fukuta-Ohi H., Kanazawa I., Campbell K.P., Shimizu T., and Matsumura K. Characterization of dp6troglycan-laminin interaction in peripheral nerve. J. Neurochem. 66 (1996) 1518-1524
35. Yamaguchi H., Yamashita H., Mori H., Okazaki I., Nomizu M., Beck K., and Kitagawa Y. High and low affinity heparin-binding sites in the G domain of the mouse laminin alpha 4 chain. J. Biol. Chem. 275 (2000) 29458-29465
36. Yan H.H.N., and Cheng C.Y. Laminin alpha 3 forms a complex with beta3 and gamma3 chains that serves as the ligand for alpha 6beta1-integrin at the apical ectoplasmic specialization in adult rat testes. J. Biol. Chem. 281 (2006) 17286-17303