Polymerized laminin-332 matrix supports rapid and tight adhesion of keratinocytes, suppressing cell migration

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Kariya, Yoshinobu ^a,b,c   Sato, Hiroki ^a   Katou, Naoko ^a   Kariya, Yukiko ^a,c   Miyazaki, Kaoru ^a  

^a YOKOHAMA CITY UNIVERSITY   (Japan)

^b Kihara Memorial Yokohama Foundation for the Advancement of Life Sciences   (Japan)

^c FUKUSHIMA MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA3 INTEGRIN; ALPHA6 INTEGRIN; ALPHA6BETA4 INTEGRIN; KALININ; LAMININ; LAMININ 10; LAMININ 311; LAMININ BETA1; LAMININ GAMMA1; SELENATE; UNCLASSIFIED DRUG; CELL ADHESION MOLECULE; INTEGRIN; POLYMER;

ARTICLE; BIOLOGICAL ACTIVITY; CELL ADHESION; CELL INTERACTION; CELL MIGRATION; CELL TYPE; CONTROLLED STUDY; CULTURE MEDIUM; EMBRYO; EXTRACELLULAR MATRIX; GENE OVEREXPRESSION; HEMIDESMOSOME; HUMAN; HUMAN CELL; KERATINOCYTE; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN POLYMERIZATION; PROTEIN PURIFICATION; PROTEIN SECRETION; PROTEIN STABILITY; PROTEIN STRUCTURE; CELL CULTURE; CELL MOTION; CELL STRAIN HEK293; CONFOCAL MICROSCOPY; CYTOLOGY; FLUORESCENCE MICROSCOPY; GENETICS; IMMUNOBLOTTING; METABOLISM; NEOPLASM; PATHOLOGY; PROTEIN BINDING; TRANSMISSION ELECTRON MICROSCOPY; TUMOR CELL LINE; ULTRASTRUCTURE;

CELL ADHESION; CELL ADHESION MOLECULES; CELL LINE, TUMOR; CELL MOVEMENT; CELLS, CULTURED; EXTRACELLULAR MATRIX; HEK293 CELLS; HUMANS; IMMUNOBLOTTING; INTEGRINS; KERATINOCYTES; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; NEOPLASMS; POLYMERS; PROTEIN BINDING;

EID: 84860476724     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035546     Document Type: Article

References (49)

1. Adams JC, Watt FM, (1993) Regulation of development and differentiation by the extracellular matrix. Development 117: 1183-1198.
2. Giancotti FG, Ruoslahti E, (1999) Integrin signaling. Science 285: 1028-1032.
3. Kalluri R, (2003) Basement membranes: structure, assembly and role in tumour angiogenesis. Nat Rev Cancer 3: 422-433.
4. Colognato H, Yurchenco PD, (2000) Form and function: the laminin family of heterotrimers. Dev Dyn 218: 213-234.
5. Cukierman E, Pankov R, Stevens DR, Yamada KM, (2001) Taking cell-matrix adhesions to the third dimension. Science 294: 1708-1712.
6. Aumailley M, Bruckner-Tuderman L, Carter WG, Deutzmann R, Edgar D, et al. (2005) A simplified laminin nomenclature. Matrix Biol 24: 326-332.
7. Baker SE, Hopkinson SB, Fitchmun M, Andreason GL, Frasier F, et al. (1996) Laminin-5 and hemidesmosomes: role of the alpha 3 chain subunit in hemidesmosome stability and assembly. J Cell Sci 109 (Pt 10): 2509-2520.
8. Nievers MG, Schaapveld RQ, Sonnenberg A, (1999) Biology and function of hemidesmosomes. Matrix Biol 18: 5-17.
9. Pulkkinen L, Christiano AM, Gerecke D, Wagman DW, Burgeson RE, et al. (1994) A homozygous nonsense mutation in the beta 3 chain gene of laminin 5 (LAMB3) in Herlitz junctional epidermolysis bullosa. Genomics 24: 357-360.
10. Aberdam D, Galliano MF, Vailly J, Pulkkinen L, Bonifas J, et al. (1994) Herlitz's junctional epidermolysis bullosa is linked to mutations in the gene (LAMC2) for the gamma 2 subunit of nicein/kalinin (laminin-5). Nat Genet 6: 299-304.
11. 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.
12. Kikkawa Y, Umeda M, Miyazaki K, (1994) Marked stimulation of cell adhesion and motility by ladsin, a laminin-like scatter factor. J Biochem 116: 862-869.
13. 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.
14. Hirosaki T, Mizushima H, Tsubota Y, Moriyama K, Miyazaki K, (2000) Structural requirement of carboxyl-terminal globular domains of laminin alpha 3 chain for promotion of rapid cell adhesion and migration by laminin-5. J Biol Chem 275: 22495-22502.
15. Kariya Y, Tsubota Y, Hirosaki T, Mizushima H, Puzon-McLaughlin W, et al. (2003) Differential regulation of cellular adhesion and migration by recombinant laminin-5 forms with partial deletion or mutation within the G3 domain of alpha3 chain. J Cell Biochem 88: 506-520.
16. Kariya Y, Miyazaki K, (2004) The basement membrane protein laminin-5 acts as a soluble cell motility factor. Exp Cell Res 297: 508-520.
17. Ryan MC, Tizard R, VanDevanter DR, Carter WG, (1994) Cloning of the LamA3 gene encoding the alpha 3 chain of the adhesive ligand epiligrin. Expression in wound repair. J Biol Chem 269: 22779-22787.
18. Nguyen BP, Ryan MC, Gil SG, Carter WG, (2000) Deposition of laminin 5 in epidermal wounds regulates integrin signaling and adhesion. Curr Opin Cell Biol 12: 554-562.
19. Pyke C, Salo S, Ralfkiaer E, Romer J, Dano K, et al. (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.
20. Lohi J, (2001) Laminin-5 in the progression of carcinomas. Int J Cancer 94: 763-767.
21. Kariya Y, Kawamura C, Tabei T, Gu J, (2010) Bisecting GlcNAc residues on laminin-332 down-regulate galectin-3-dependent keratinocyte motility. J Biol Chem 285: 3330-3340.
22. O'Toole EA, Marinkovich MP, Hoeffler WK, Furthmayr H, Woodley DT, (1997) Laminin-5 inhibits human keratinocyte migration. Exp Cell Res 233: 330-339.
23. 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.
24. Tsubota Y, Yasuda C, Kariya Y, Ogawa T, Hirosaki T, et al. (2005) Regulation of biological activity and matrix assembly of laminin-5 by COOH-terminal, LG4-5 domain of alpha3 chain. J Biol Chem 280: 14370-14377.
25. 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.
26. 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.
27. Ogawa T, Tsubota Y, Maeda M, Kariya Y, Miyazaki K, (2004) Regulation of biological activity of laminin-5 by proteolytic processing of gamma2 chain. J Cell Biochem 92: 701-714.
28. Miyazaki K, (2006) Laminin-5 (laminin-332): Unique biological activity and role in tumor growth and invasion. Cancer Sci 97: 91-98.
29. Hamill KJ, Kligys K, Hopkinson SB, Jones JC, (2009) Laminin deposition in the extracellular matrix: a complex picture emerges. J Cell Sci 122: 4409-4417.
30. Kariya Y, Ishida K, Tsubota Y, Nakashima Y, Hirosaki T, et al. (2002) Efficient expression system of human recombinant laminin-5. J Biochem 132: 607-612.
31. Kariya Y, Yasuda C, Nakashima Y, Ishida K, Tsubota Y, et al. (2004) Characterization of laminin 5B and NH2-terminal proteolytic fragment of its alpha3B chain: promotion of cellular adhesion, migration, and proliferation. J Biol Chem 279: 24774-24784.
32. Mizushima H, Miyagi Y, Kikkawa Y, Yamanaka N, Yasumitsu H, et al. (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 120: 1196-1202.
33. Gagnoux-Palacios L, Allegra M, Spirito F, Pommeret O, Romero C, et al. (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.
34. Sigle RO, Gil SG, Bhattacharya M, Ryan MC, Yang TM, et al. (2004) Globular domains 4/5 of the laminin alpha3 chain mediate deposition of precursor laminin 5. J Cell Sci 117: 4481-4494.
35. Frank DE, Carter WG, (2004) Laminin 5 deposition regulates keratinocyte polarization and persistent migration. J Cell Sci 117: 1351-1363.
36. deHart GW, Healy KE, Jones JC, (2003) The role of alpha3beta1 integrin in determining the supramolecular organization of laminin-5 in the extracellular matrix of keratinocytes. Exp Cell Res 283: 67-79.
37. Sehgal BU, DeBiase PJ, Matzno S, Chew TL, Claiborne JN, et al. (2006) Integrin beta4 regulates migratory behavior of keratinocytes by determining laminin-332 organization. J Biol Chem 281: 35487-35498.
38. Nakashima Y, Kariya Y, Miyazaki K, (2007) The beta3 chain short arm of laminin-332 (laminin-5) induces matrix assembly and cell adhesion activity of laminin-511 (laminin-10). J Cell Biochem 100: 545-556.
39. Sonnenberg A, Calafat J, Janssen H, Daams H, van der Raaij-Helmer LM, et al. (1991) Integrin alpha 6/beta 4 complex is located in hemidesmosomes, suggesting a major role in epidermal cell-basement membrane adhesion. J Cell Biol 113: 907-917.
40. Li S, Liquari P, McKee KK, Harrison D, Patel R, et al. (2005) Laminin-sulfatide binding initiates basement membrane assembly and enables receptor signaling in Schwann cells and fibroblasts. J Cell Biol 169: 179-189.
41. Dietrich CP, Nader HB, Buonassisi V, Colburn P, (1988) Inhibition of synthesis of heparan sulfate by selenate: possible dependence on sulfation for chain polymerization. FASEB J 2: 56-59.
42. Cheng YS, Champliaud MF, Burgeson RE, Marinkovich MP, Yurchenco PD, (1997) Self-assembly of laminin isoforms. J Biol Chem 272: 31525-31532.
43. Colognato H, Yurchenco PD, (1999) The laminin alpha2 expressed by dystrophic dy(2J) mice is defective in its ability to form polymers. Curr Biol 9: 1327-1330.
44. Nakashima Y, Kariya Y, Yasuda C, Miyazaki K, (2005) Regulation of cell adhesion and type VII collagen binding by the beta3 chain short arm of laminin-5: effect of its proteolytic cleavage. J Biochem 138: 539-552.
45. Kariya Y, Kariya Y, Gu J, (2009) Roles of laminin-332 and alpha6beta4 integrin in tumor progression. Mini Rev Med Chem 9: 1284-1291.
46. Kariya Y, Mori T, Yasuda C, Watanabe N, Kaneko Y, et al. (2008) Localization of laminin alpha3B chain in vascular and epithelial basement membranes of normal human tissues and its down-regulation in skin cancers. J Mol Histol 39: 435-446.
47. Mori T, Kariya Y, Ogawa T, Higashi S, Miyazaki K, (2010) Laminin-3B11, a novel vascular-type laminin capable of inducing prominent lamellipodial protrusions in microvascular endothelial cells. J Biol Chem 285: 35068-35078.
48. Arimura A, Nakamura Y, Shimizu A, Harada M, Yanoma S, (1991) Establishment and characterization of a CA19-9 producing human gastric cancer cell line, STKM-1. Hum Cell 4: 67-70.
49. Nishiuchi R, Murayama O, Fujiwara H, Gu J, Kawakami T, et al. (2003) Characterization of the ligand-binding specificities of integrin alpha3beta1 and alpha6beta1 using a panel of purified laminin isoforms containing distinct alpha chains. J Biochem 134: 497-504.