Differential regulation of cellular adhesion and migration by recombinant laminin-5 forms with partial deletion or mutation within the G3 domain of α3 chain

Journal of Cellular Biochemistry

Volumn 88, Issue 3, 2003, Pages 506-520

  Kariya, Yoshinobu ^a   Tsubota, Yoshiaki ^a   Hirosaki, Tomomi ^a   Mizushima, Hiroto ^a   Puzon McLaughlin, Wilma ^b   Takada, Yoshikazu ^b   Miyazaki, Kaoru ^a  

^a YOKOHAMA CITY UNIVERSITY   (Japan)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Cell adhesion; Cell migration; G3 domain; Integrin; Laminin 5

Indexed keywords

COMPLEMENTARY DNA; INTEGRIN; KALININ; LAMININ RECEPTOR;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; BASEMENT MEMBRANE; BLADDER CARCINOMA; CARBOXY TERMINAL SEQUENCE; CELL ADHESION; CELL MIGRATION; CELL MOTILITY; CHO CELL; CONTROLLED STUDY; DELETION MUTANT; FIBROSARCOMA; HUMAN; HUMAN CELL; IMMUNOBLOTTING; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; RAT;

AMINO ACID SEQUENCE; ANIMALS; CELL ADHESION; CELL LINE; CELL MOVEMENT; CELL SIZE; HUMANS; INTEGRINS; LAMININ; MICE; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS;

EID: 0037441482     PISSN: 07302312     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcb.10350     Document Type: Article

References (41)

1. Aumailley M, Krieg T. 1996. Laminins: A family of diverse multifunctional molecules of basement membranes. J Invest Dermatol 106:209-214.
2. Aumailley M, Rousselle P. 1999. Laminins of the dermo-epidermal junction. Matrix Biol 18:19-28.
3. Carter WG, Ryan MC, Gahr PJ. 1991. Epiligrin, a new cell adhesion ligand for integrin α3β1 in epithelial basement membranes. Cell 65:599-610.
4. Colognato H, Yurchenco PD. 2000. Form and function: The laminin family of heterotrimers. Dev Dyn 218:213-234.
5. Faull RJ, Kovach NL, Harlan V, Ginsberg MH. 1993. Affinity modulation of integrin α5β1: Regulation of the functional response by soluble fibronectin. J Cell Biol 121:155-162.
6. Fujiwara H, Kikkawa Y, Sanzen N, Sekiguchi K. 2001. Purification and characterization of human laminin-8. Laminin-8 stimulates cell adhesion and migration through α3β1 and α6β1 integrins. J Biol Chem 276:17550-17558.
7. Giancotti FG, Ruoslahti E. 1999. Integrin signaling. Science 285:1028-1032.
8. Giannelli G, Falk-Marzillier J, Schiraldi O, Stetler-Stevenson WG, Quaranta V. 1997. Induction of cell migration by matrix metalloprotease-2 cleavage of laminin-5. Science 277:225-228.
9. Goldfinger LE, Stack MS, Jones JC. 1998. Processing of laminin-5 and its functional consequences: Role of plasmin and tissue-type plasminogen activator. J Cell Biol 141:255-265.
10. Grishkovskaya I, Avvakumov GV, Sklenar G, Dales D, Hammond GL, Muller YA. 2000. Crystal structure of human sex hormone-binding globulin: Steroid transport by a laminin G-like domain. Embo J 19:504-512.
11. Hirosaki T, Mizushima H, Tsubota Y, Moriyama K, Miyazaki K. 2000. Structural requirement of carboxyl-terminal globular domains of laminin α3 chain for promotion of rapid cell adhesion and migration by laminin-5. J Biol Chem 275:22495-22502.
12. Hohenester E, Tisi D, Talts JF, Timpl R. 1999. The crystal structure of a laminin G-like module reveals the molecular basis of α-dystroglycan binding to laminins, perlecan, and agrin. Mol Cell 4:783-792.
13. Howe A, Aplin AE, Alahari SK, Juliano RL. 1998. Integrin signaling and cell growth control. Curr Opin Cell Biol 10:220-231.
14. Kikkawa Y, Umeda M, Miyazaki K. 1994. Marked stimulation of cell adhesion and motility by ladsin, a laminin-like scatter factor. J Biochem (Tokyo) 116:862-869.
15. Koshikawa N, Moriyama K, Takamura H, Mizushima H, Nagashima Y, Yanoma S, Miyazaki K. 1999. Overexpression of laminin γ2 chain monomer in invading gastric carcinoma cells. Cancer Res 59:5596-5601.
16. Koshikawa N, Giannelli G, Cirulli V, Miyazaki K, Quaranta V. 2000. Role of cell surface metalloprotease MT1-MMP in epithelial cell migration over laminin-5. J Cell Biol 148:615-624.
17. Lampe PD, Nguyen BP, Gil S, Usui M, Olerud J, Takada Y, Carter WG. 1998. Cellular interaction of integrin α3β1 with laminin 5 promotes gap junctional communication. J Cell Biol 143:1735-1747.
18. Matsui C, Wang CK, Nelson CF, Bauer EA, Hoeffler WK. 1995. The assembly of laminin-5 subunits. J Biol Chem 270:23496-23503.
19. Miyata S, Miyagi Y, Koshikawa N, Nagashima Y, Kato Y, Yasumitsu H, Hirahara F, Misugi K, Miyazaki K. 1998. Stimulation of cellular growth and adhesion to fibronectin and vitronectin in culture and tumorigenicity in nude mice by overexpression of trypsinogen in human gastric cancer cells. Clin Exp Metastasis 16:6136-6222.
20. Miyazaki K, Kikkawa Y, Nakamura A, Yasumitsu H, Umeda M. 1993. A large cell-adhesive scatter factor secreted by human gastric carcinoma cells. Proc Natl Acad Sci USA 90:11767-11771.
21. Mizushima H, Miyagi Y, Kikkawa Y, Yamanaka N, Yasumitsu H, Misugi K, Miyazaki K. 1996. Differential expression of laminin-5/ladsin subunits in human tissues and cancer cell lines and their induction by tumor promoter and growth factors. J Biochem (Tokyo) 120:1196-1202.
22. Mizushima H, Takamura H, Miyagi Y, Kikkawa Y, Yamanaka N, Yasumitsu H, Misugi K, Miyazaki K. 1997. Identification of integrin-dependent and -independent cell adhesion domains in COOH-terminal globular region of laminin-5 α3 chain. Cell Growth Differ 8:979-987.
23. Mizushima H, Koshikawa N, Moriyama K, Takamura H, Nagashima Y, Hirahara F, Miyazaki K. 1998. Wide distribution of laminin-5 γ2 chain in basement membranes of various human tissues. Horm Res 50(Suppl 2):7-14.
24. Nielsen PK, Gho YS, Hoffman MP, Watanabe H, Makino M, Nomizu M, Yamada Y. 2000. Identification of a major heparin and cell binding site in the LG4 module of the laminin α5 chain. J Biol Chem 275:14517-14523.
25. Niessen CM, Hogervorst F, Jaspars LH, de Melker AA, Delwel GO, Hulsman EH, Kuikman I, Sonnenberg A. 1994. The α6β4 integrin is a receptor for both laminin and kalinin. Exp Cell Res 211:360-367.
26. Nievers MG, Schaapveld RQ, Sonnenberg A. 1999. Biology and function of hemidesmosomes. Matrix Biol 18:5-17.
27. Nomizu M, Kim WH, Yamamura K, Utani A, Song SY, Otaka A, Roller PP, Kleinman HK, Yamada Y. 1995. Identification of cell binding sites in the laminin α1 chain carboxyl-terminal globular domain by systematic screening of synthetic peptides. J Biol Chem 270:20583-20590.
28. Pyke C, Salo S, Raltkiaer E, Romer J, Dano K, Tryggvason K. 1995. Laminin-5 is a marker of invading cancer cells in some human carcinomas and is coexpressed with the receptor for urokinase plasminogen activator in budding cancer cells in colon adenocarcinomas. Cancer Res 55:4132-4139.
29. Rousselle P, Aumailley M. 1994. Kalinin is more efficient than laminin in promoting adhesion of primary keratinocytes and some other epithelial cells and has a different requirement for integrin receptors. J Cell Biol 125:205-214.
30. Rudenko G, Nguyen T, Chelliah Y, Sudhof TC, Deisenhofer J. 1999. The structure of the ligand-binding domain of neurexin Iβ: Regulation of LNS domain function by alternative splicing. Cell 99:93-101.
31. Ryan MC, Tizard R, VanDevanter DR, Carter WG. 1994. Cloning of the LamA3 gene encoding the α3 chain of the adhesive ligand epiligrin. Expression in wound repair. J Biol Chem 269:22779-22787.
32. Shang M, Koshikawa N, Schenk S, Quaranta V. 2001. The LG3 module of laminin-5 harbors a binding site for integrin α3β1 that promotes cell adhesion, spreading, and migration. J Biol Chem 276:33045-33053.
33. Smirnov S, McDearmon E, Li S, Ervasti J, Tryggvason K, Yurchenco PD. 2002. Contributions of the LG modules and furin-processing to laminin-2 functions. J Biol Chem 277:18928-18937.
34. Symington BE, Takada Y, Carter WG. 1993. Interaction of integrins α3β1 and α2β1: Potential role in keratinocyte intercellular adhesion. J Cell Biol 120:523-535.
35. Talts JF, Timpl R. 1999b. Mutation of a basic sequence in the laminin α2LG3 module leads to a lack of proteolytic processing and has different effects on β1 integrin-mediated cell adhesion and α-dystroglycan binding. FEBS Lett 458:319-323.
36. Talts JF, Andac Z, Gohring W, Brancaccio A, Timpl R. 1999a. Binding of the G domains of laminin α1 and α2 chains and perlecan to heparin, sulfatides, α-dystroglycan, and several extracellular matrix proteins. Embo J 18:863-870.
37. Timpl R, Tisi D, Talts JF, Andac Z, Sasaki T, Hohenester E. 2000. Structure and function of laminin LG modules. Matrix Biol 19:309-317.
38. Tisi D, Talts JF, Timpl R, Hohenester E. 2000. Structure of the C-terminal laminin G-like domain pair of the laminin α2 chain harbouring binding sites for α-dystroglycan and heparin. Embo J 19:1432-1440.
39. Tsubota Y, Mizushima H, Hirosaki T, Higashi S, Yasumitsu H, Miyazaki K. 2000. Isolation and activity of proteolytic fragment of laminin-5 α3 chain. Biochem Biophys Res Commun 278:614-620.
40. Utani A, Nomizu M, Matsuura H, Kato K, Kobayashi T, Takeda U, Aota S, Nielsen PK, Shinkai H. 2001. A unique sequence of the laminin α3 G domain binds to heparin and promotes cell adhesion through syndecan-2 and -4. J Biol Chem 276:28779-28788.
41. Zhang XP, Puzon-McLaughlin W, Irie A, Kovach N, Prokopishyn NL, Lafert S, Takeuchi K, Tsuji T, Takada Y. 1999. α3β1 adhesion to laminin-5 and invasin: Critical and differential role of integrin residues clustered at the.boundary between α3 N-terminal repeats 2 and 3. Biochemistry 38:14424-14431.