Plasmin induces degradation and dysfunction of laminin 332 (laminin 5) and impaired assembly of basement membrane at the dermal-epidermal junction

British Journal of Dermatology

Volumn 159, Issue 1, 2008, Pages 49-60

  Ogura, Y ^a   Matsunaga, Y ^a   Nishiyama, T ^b   Amano, S ^a  

^a SHISEIDO RESEARCH CENTER   (Japan)

^b TOKYO UNIVERSITY OF AGRICULTURE AND TECHNOLOGY   (Japan)

Author keywords

Basement membrane; Laminin 332; Laminin 5; Plasmin; Type VII collagen; Urokinase type plasminogen activator

Indexed keywords

APROTININ; COLLAGEN TYPE 7; GELATINASE; GELATINASE A; GELATINASE B; KALININ; PLASMIN; PLASMINOGEN; TRANEXAMIC ACID; UROKINASE;

AMINO TERMINAL SEQUENCE; ARTICLE; BASEMENT MEMBRANE; CELL ADHESION; COMPARATIVE STUDY; CONTROLLED STUDY; DERMOEPIDERMAL JUNCTION; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; KERATINOCYTE; PRIORITY JOURNAL; PROTEIN DEGRADATION; SEQUENCE ANALYSIS; SKIN STRUCTURE; ULTRAVIOLET RADIATION; ZYMOGRAPHY;

BASEMENT MEMBRANE; CELL ADHESION MOLECULES; CELLS, CULTURED; COLLAGEN TYPE VII; DERMIS; EPIDERMIS; FIBRINOLYTIC AGENTS; HUMANS; MATRIX METALLOPROTEINASE 2; MICROSCOPY, ELECTRON; PLASMIN; TISSUE INHIBITOR OF METALLOPROTEINASE-2;

EID: 45749136698     PISSN: 00070963     EISSN: 13652133     Source Type: Journal    
DOI: 10.1111/j.1365-2133.2008.08576.x     Document Type: Article

References (67)

1. De Arcangelis A, Neuville P, Boukamel R et al. Inhibition of laminin alpha 1-chain expression leads to alteration of basement membrane assembly and cell differentiation. J Cell Biol 1996 133 : 417 30.
2. Inoue S. Ultrastructure of basement membranes. Int Rev Cytol 1989 117 : 57 98.
3. Marinkovich MP, Keene DR, Rimberg CS et al. Cellular origin of the dermal-epidermal basement membrane. Dev Dyn 1993 197 : 255 67.
4. Kikkawa Y, Sanzen N, Sekiguchi K. Isolation and characterization of laminin-10/11 secreted by human lung carcinoma cells. Laminin-10/11 mediates cell adhesion through integrin alpha3 beta1. J Biol Chem 1998 273 : 15854 9.
5. Kikkawa Y, Sanzen N, Fujiwara H et al. Integrin binding specificity of laminin-10/11: laminin-10/11 are recognized by alpha 3 beta 1, alpha 6 beta 1 and alpha 6 beta 4 integrins. J Cell Sci 2000 113 : 869 76.
6. Hirako Y, Owaribe K. Hemidesmosomes and their unique transmembrane protein BP180. Microsc Res Tech 1998 43 : 207 17.
7. Rousselle P, Lunstrum GP, Keene DR et al. Kalinin: an epithelium-specific basement membrane adhesion molecule that is a component of anchoring filaments. J Cell Biol 1991 114 : 567 76.
8. Sakai LY, Keene DR, Morris NP et al. Type VII collagen is a major structural component of anchoring fibrils. J Cell Biol 1986 103 : 1577 86.
9. Lunstrum GP, Sakai LY, Keene DR et al. Large complex globular domains of type VII procollagen contribute to the structure of anchoring fibrils. J Biol Chem 1986 261 : 9042 8.
10. Uitto J, Pulkkinen L, Christiano AM. Molecular basis of the dystrophic and junctional forms of epidermolysis bullosa: mutations in the type VII collagen and kalinin (laminin 5) genes. J Invest Dermatol 1994 103 : S39 46.
11. Niessen CM, van der Raaij-Helmer MH, Hulsman EH et al. Deficiency of the integrin beta 4 subunit in junctional epidermolysis bullosa with pyloric atresia: consequences for hemidesmosome formation and adhesion properties. J Cell Sci 1996 109 : 1695 706.
12. McGrath JA, Gatalica B, Christiano AM et al. Mutations in the 180-kD bullous pemphigoid antigen (BPAG2), a hemidesmosomal transmembrane collagen (COL17A1), in generalized atrophic benign epidermolysis bullosa. Nat Genet 1995 11 : 83 6.
13. Bell E, Ehrlich HP, Buttle DJ et al. Living tissue formed in vitro and accepted as skin-equivalent tissue of full thickness. Science 1981 211 : 1052 4.
14. Amano S, Akutsu N, Matsunaga Y et al. Importance of balance between extracellular matrix synthesis and degradation in basement membrane formation. Exp Cell Res 2001 271 : 249 62.
15. Tsunenaga M, Adachi E, Amano S et al. Laminin 5 can promote assembly of the lamina densa in the skin equivalent model. Matrix Biol 1998 17 : 603 13.
16. Tsunenaga M, Kohno Y, Horii I et al. Growth and differentiation properties of normal and transformed human keratinocytes in organotypic culture. Jpn J Cancer Res 1994 85 : 238 44.
17. Nishiyama T, Amano S, Tsunenaga M et al. The importance of laminin 5 in the dermal-epidermal basement membrane. J Dermatol Sci 2000 24 : S51 9.
18. Lavker RM. Structural alterations in exposed and unexposed aged skin. J Invest Dermatol 1979 73 : 59 66.
19. Lavker RM, Zheng PS, Dong G. Aged skin: a study by light, transmission electron, and scanning electron microscopy. J Invest Dermatol 1987 88 : S44 51.
20. Amano S, Matsunaga Y, Akutsu N et al. Basement membrane damage, a sign of skin early aging, and laminin 5, a key player in basement membrane care. IFSCC Magazine 2000 3 : 15 23.
21. Fisher GJ, Datta SC, Talwar HS et al. Molecular basis of sun-induced premature skin ageing and retinoid antagonism. Nature 1996 379 : 335 9.
22. Scharffetter K, Wlaschek M, Hogg A et al. UVA irradiation induces collagenase in human dermal fibroblasts in vitro and in vivo. Arch Dermatol Res 1991 283 : 506 11.
23. Miralles F, Parra M, Caelles C et al. UV irradiation induces the murine urokinase-type plasminogen activator gene via the c-Jun N-terminal kinase signaling pathway: requirement of an AP1 enhancer element. Mol Cell Biol 1998 18 : 4537 47.
24. Marschall C, Lengyel E, Nobutoh T et al. UVB increases urokinase-type plasminogen activator receptor (uPAR) expression. J Invest Dermatol 1999 113 : 69 76.
25. Saksela O. Plasminogen activation and regulation of pericellular proteolysis. Biochim Biophys Acta 1985 823 : 35 65.
26. Morioka S, Jensen PJ, Lazarus GS. Human epidermal plasminogen activator. Characterization, localization, and modulation. Exp Cell Res 1985 161 : 364 72.
27. Plow EF, Freaney DE, Plescia J et al. The plasminogen system and cell surfaces: evidence for plasminogen and urokinase receptors on the same cell type. J Cell Biol 1986 103 : 2411 20.
28. Katsuta Y, Yoshida Y, Kawai E et al. Urokinase-type plasminogen activator is activated in stratum corneum after barrier disruption. J Dermatol Sci 2003 32 : 55 7.
29. Denda M, Kitamura K, Elias PM et al. trans-4-(Aminomethyl)cyclohexane carboxylic acid (T-AMCHA), an anti-fibrinolytic agent, accelerates barrier recovery and prevents the epidermal hyperplasia induced by epidermal injury in hairless mice and humans. J Invest Dermatol 1997 109 : 84 90.
30. Marchisio PC, Cremona O, Savoia P et al. The basement membrane protein BM-600/nicein codistributes with kalinin and the integrin alpha 6 beta 4 in human cultured keratinocytes. Exp Cell Res 1993 205 : 205 12.
31. Kikkawa Y, Umeda M, Miyazaki K. Marked stimulation of cell adhesion and motility by ladsin, a laminin-like scatter factor. J Biochem (Tokyo) 1994 116 : 862 9.
32. Rousselle P, Keene DR, Ruggiero F et al. Laminin 5 binds the NC-1 domain of type VII collagen. J Cell Biol 1997 138 : 719 28.
33. Goldfinger LE, Jiang L, Hopkinson SB et al. Spatial regulation and activity modulation of plasmin by high affinity binding to the G domain of the alpha 3 subunit of laminin-5. J Biol Chem 2000 275 : 34887 93.
34. Goldfinger LE, Stack MS, Jones JC. Processing of laminin-5 and its functional consequences: role of plasmin and tissue-type plasminogen activator. J Cell Biol 1998 141 : 255 65.
35. Amano S, Scott IC, Takahara K et al. Bone morphogenetic protein 1 is an extracellular processing enzyme of the laminin 5 gamma 2 chain. J Biol Chem 2000 275 : 22728 35.
36. Veitch DP, Nokelainen P, McGowan KA et al. Mammalian tolloid metalloproteinase, and not matrix metalloprotease 2 or membrane type 1 metalloprotease, processes laminin-5 in keratinocytes and skin. J Biol Chem 2003 278 : 15661 8.
37. Baudoin C, Fantin L, Meneguzzi G. Proteolytic processing of the laminin alpha3 G domain mediates assembly of hemidesmosomes but has no role on keratinocyte migration. J Invest Dermatol 2005 125 : 883 8.
38. Gilles C, Polette M, Coraux C et al. Contribution of MT1-MMP and of human laminin-5 gamma2 chain degradation to mammary epithelial cell migration. J Cell Sci 2001 114 : 2967 76.
39. Koshikawa N, Minegishi T, Sharabi A et al. Membrane-type matrix metalloproteinase-1 (MT1-MMP) is a processing enzyme for human laminin gamma 2 chain. J Biol Chem 2005 280 : 88 93.
40. Tunggal L, Ravaux J, Pesch M et al. Defective laminin 5 processing in cylindroma cells. Am J Pathol 2002 160 : 459 68.
41. Giannelli G, Brassard J, Foti C et al. Altered expression of basement membrane proteins and their integrin receptors in lichen planus: possible pathogenetic role of gelatinases A and B. Lab Invest 1996 74 : 1091 104.
42. Kino J, Adachi E, Yoshida T et al. A novel chain of basement membrane-associated collagen as revealed by biochemical and immunohistochemical characterizations of the epitope recognized by a monoclonal antibody against human placenta basement membrane collagen. Am J Pathol 1991 138 : 911 20.
43. Lunstrum GP, Kuo HJ, Rosenbaum LM et al. Anchoring fibrils contain the carboxyl-terminal globular domain of type VII procollagen, but lack the amino-terminal globular domain. J Biol Chem 1987 262 : 13706 12.
44. Marinkovich MP, Lunstrum GP, Burgeson RE. The anchoring filament protein kalinin is synthesized and secreted as a high molecular weight precursor. J Biol Chem 1992 267 : 17900 6.
45. MacPherson LJ, Bayburt EK, Capparelli MP et al. Discovery of CGS 27023A, a non-peptidic, potent, and orally active stromelysin inhibitor that blocks cartilage degradation in rabbits. J Med Chem 1997 40 : 2525 32.
46. Yamamoto I, Muto N, Murakami K et al. Collagen synthesis in human skin fibroblasts is stimulated by a stable form of ascorbate, 2-O-alpha-d- glucopyranosyl-l-ascorbic acid. J Nutr 1992 122 : 871 7.
47. Amano S, Nishiyama T, Burgeson RE. A specific and sensitive ELISA for laminin 5. J Immunol Methods 1999 224 : 161 9.
48. Sato Y, Mukai K, Watanabe S et al. The AMeX method. A simplified technique of tissue processing and paraffin embedding with improved preservation of antigens for immunostaining. Am J Pathol 1986 125 : 431 5.
49. Herrmann G, Wlaschek M, Lange TS et al. UVA irradiation stimulates the synthesis of various matrix-metalloproteinases (MMPs) in cultured human fibroblasts. Exp Dermatol 1993 2 : 92 7.
50. Kong W, Longaker MT, Lorenz HP. Cyclophilin C-associated protein is a mediator for fibronectin fragment-induced matrix metalloproteinase-13 expression. J Biol Chem 2004 279 : 55334 40.
51. Liu Z, Li N, Diaz LA et al. Synergy between a plasminogen cascade and MMP-9 in autoimmune disease. J Clin Invest 2005 115 : 879 87.
52. Tsubota Y, Mizushima H, Hirosaki T et al. Isolation and activity of proteolytic fragment of laminin-5 alpha3 chain. Biochem Biophys Res Commun 2000 278 : 614 20.
53. Kariya Y, Tsubota Y, Hirosaki T et al. 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 2003 88 : 506 20.
54. Chen M, Marinkovich MP, Jones JC et al. NC1 domain of type VII collagen binds to the beta3 chain of laminin 5 via a unique subdomain within the fibronectin-like repeats. J Invest Dermatol 1999 112 : 177 83.
55. Inomata S, Matsunaga Y, Amano S et al. Possible involvement of gelatinases in basement membrane damage and wrinkle formation in chronically ultraviolet B-exposed hairless mouse. J Invest Dermatol 2003 120 : 128 34.
56. Bechtel MJ, Reinartz J, Rox JM et al. Upregulation of cell-surface-associated plasminogen activation in cultured keratinocytes by interleukin-1 beta and tumor necrosis factor-alpha. Exp Cell Res 1996 223 : 395 404.
57. Oxholm A, Oxholm P, Staberg B et al. Immunohistological detection of interleukin I-like molecules and tumour necrosis factor in human epidermis before and after UVB-irradiation in vivo. Br J Dermatol 1988 118 : 369 76.
58. Schaefer BM, Stark HJ, Fusenig NE et al. Differential expression of urokinase-type plasminogen activator (uPA), its receptor (uPA-R), and inhibitor type-2 (PAI-2) during differentiation of keratinocytes in an organotypic coculture system. Exp Cell Res 1995 220 : 415 23.
59. Isseroff RR, Rifkin DB. Plasminogen is present in the basal layer of the epidermis. J Invest Dermatol 1983 80 : 297 9.
60. Ellis V, Behrendt N, Dano K. Plasminogen activation by receptor-bound urokinase. A kinetic study with both cell-associated and isolated receptor. J Biol Chem 1991 266 : 12752 8.
61. Zhou HM, Nichols A, Meda P et al. Urokinase-type plasminogen activator and its receptor synergize to promote pathogenic proteolysis. EMBO J 2000 19 : 4817 26.
62. Del Rosso M, Fibbi G, Pucci M et al. Modulation of surface-associated urokinase: binding, interiorization, delivery to lysosomes, and degradation in human keratinocytes. Exp Cell Res 1991 193 : 346 55.
63. Boudreau N, Werb Z, Bissell MJ. Suppression of apoptosis by basement membrane requires three-dimensional tissue organization and withdrawal from the cell cycle. Proc Natl Acad Sci USA 1996 93 : 3509 13.
64. Ghosh S, Brown R, Jones JC et al. Urinary-type plasminogen activator (uPA) expression and uPA receptor localization are regulated by alpha 3 beta 1 integrin in oral keratinocytes. J Biol Chem 2000 275 : 23869 76.
65. Liotta LA, Goldfarb RH, Brundage R et al. Effect of plasminogen activator (urokinase), plasmin, and thrombin on glycoprotein and collagenous components of basement membrane. Cancer Res 1981 41 : 4629 36.
66. Nakashima Y, Kariya Y, Yasuda C et al. 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 (Tokyo) 2005 138 : 539 52.
67. Waterman EA, Sakai N, Nguyen NT et al. A laminin-collagen complex drives human epidermal carcinogenesis through phosphoinositol-3-kinase activation. Cancer Res 2007 67 : 4264 70.