Human skin and gingival keratinocytes show differential regulation of matrix metalloproteinases when combined with fibroblasts in 3-dimensional cultures

Journal of Periodontology

Volumn 76, Issue 7, 2005, Pages 1072-1083

  Chinnathambi, Sathivel ^a   Bickenbach, Jackie R ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

Fibroblasts, dermal; Fibroblasts, gingival; Keratinocytes, dermal; Keratinocytes, gingival; Metalloproteinases, matrix

Indexed keywords

GELATINASE A; GELATINASE B; INTERSTITIAL COLLAGENASE; MATRIX METALLOPROTEINASE; PROTEIN INHIBITOR;

ARTICLE; CELL CULTURE; CELL GROWTH; CELL INTERACTION; CELL ISOLATION; CELL TYPE; CONTROLLED STUDY; CULTURE MEDIUM; ENZYME ACTIVATION; ENZYME INHIBITION; EXPERIMENTAL DESIGN; FIBROBLAST; GINGIVA; HUMAN; HUMAN CELL; HUMAN TISSUE; KERATINOCYTE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTEIN SYNTHESIS; REGULATORY MECHANISM; SKIN CELL; SKIN FIBROBLAST; THREE DIMENSIONAL IMAGING; TISSUE GRAFT; UPREGULATION;

ANIMALS; BLOTTING, WESTERN; CELL CULTURE TECHNIQUES; CELLS, CULTURED; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENZYME-LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR MATRIX PROTEINS; FIBROBLASTS; GINGIVA; HUMANS; KERATINOCYTES; MATRIX METALLOPROTEINASE 1; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MATRIX METALLOPROTEINASES; RATS; SKIN;

EID: 23044442615     PISSN: 00223492     EISSN: None     Source Type: Journal    
DOI: 10.1902/jop.2005.76.7.1072     Document Type: Article

References (50)

1. Ueda M, Torri S, Nagayama M, Kaneda T, Oka T. The pectoralis major myocutaneous flap for intraoral reconstruction: Surgical complications and their treatment. J Maxillofac Surg 1985;13:9-13.
2. Tsai C, Ueda M, Hata K, et al. Clinical results of cultured epithelial cell grafting in the oral and maxillofacial region. J Craniomaxillofac Surg 1997;25:4-8.
3. De Luca M, Albanese E, Megna M, et al. Evidence that human oral epithelium reconstituted in vitro and transplanted onto patients with defects in the oral mucosa retains properties of the original donor site. Transplantation 1990;50:454-459.
4. Ueda M, Koji E, Kaneda T. In vitro fabrication of bioartificial mucosa for reconstruction of oral mucosa: Basic research and clinical application. Ann Plast Surg 1991; 27:540-549.
5. Shibahara T, Noma H, Takeda E, Hashimoto S. Morphologic changes in forearm flaps of the oral cavity. J Oral Maxillofac Surg 2000;58:495-499.
6. Ejeil AL, Igondjo-Tchen S, Ghomrasseni S, Pellat B, Godeau G, Gogly B. Expression of matrix metalloproteinases (MMPs) and tissue inhibitors of metalloproteinases (TIMPs) in healthy and diseased human gingiva. J Periodontol 2003;74:188-195.
7. Liotta LA, Steeg PS, Stetler-Stevenson WG. Cancer metastasis and angiogenesis: An imbalance of positive and negative regulation. Trends Genet 1991;6:121-125.
8. Al-Khateeb T, Stephens P, Shepherd J. An investigation of preferential fibroblast wound population using a novel in vitro wound model. J Periodontol 1997;68:1063-1069.
9. Gould L, Yager D, Cohen K. In vitro analysis of fetal fibroblast collagenolytic activity. Wound Repair Regen 1997;5:151-158.
10. Stephens P, Davies K, Occleston N, et al. Skin and oral fibroblasts exhibit phenotypic differences in extracellular matrix reorganization and matrix metalloproteinase activity. Br J Dermatol 2001;144:229-237.
11. Birkedal-Hansen H, Moore WG, Bodden WG. Matrix metalloproteinase: A review. Br J Plast Surg 1994;44:302-305.
12. Murray GI. Matrix metalloproteinase: A multifunctional group of molecules. J Pathol 2001;195:135-137.
13. Edwards DR. The Tissue Inhibitors of Metalloproteinases: Biology and Regulation. Totawa, NJ: Humana Press; 2000.
14. Hoekstra R, Eskens FA, Verweij J. Matrix metalloproteinase inhibitors: Current developments and future perspectives. Oncologist 2001;6:415-427.
15. Osborne CS, Schmid P. Epidermal-dermal interactions regulate gelatinase activity in Apligraf, a tissue-engineered human skin equivalent. Br J Dermatol 2002; 146:26-31.
16. Ito A, Nakajima S, Sasaguri Y, Nagase H, Mori Y. Co-culture of human breast adenocarcinoma MCF-7 cells and human dermal fibroblasts enhances the production of matrix metalloproteinases 1, 2 and 3 in fibroblasts. Br J Cancer 1995;71:1039-1045.
17. Kobayashi T, Hattori S, Nagai Y, Tajima S, Nishikawa T. Differential regulation of MMP-2 and MMP-9 gelatinases in cultured human keratinocytes. Dermatology 1998; 197:1-5.
18. Lee AY, Akers KT, Collier M. Intracellular activation of gelatinase A (72-kDa type IV collagenase) by normal fibroblasts. Proc Natl Acad Sci (USA) 1997;94:4424-4429.
19. Li L, Akers KT, Eisen AZ. Activation of gelatinase A (72-kDa type IV collagenase) induced by monensin in normal human fibroblasts. Exp Cell Res 1997;232:322-330.
20. Chinnathambi S, Tomanek-Chalkley A, Ludwig N, et al. Recapitulation of oral mucosal tissues in long term organotypic culture. Anat Rec 2003;270:162-174.
21. Rheinwald JG, Green H. Serial cultivation of strains of human epidermal keratinocytes: The formation of keratinizing colonies from single cells. Cell 1975;6:331-344.
22. Ponec M, Weerheim A. Retinoids and lipid changes in keratinocytes. Methods Enzymol 1990;190:30-41.
23. Chi Y, Zeigler M, Walker J, Perone P, Datta S, Varani J. Elaboration of matrix metalloproteinase inhibitors by human skin in organ culture and by skin cells in monolayer culture: Relationship to invasion. Invasion Metastasis 1998;18:27-34.
24. Gogly B, Groult N, Hornebeck W, Godeau G, Pellat B. Collagen zymography as a sensitive and specific technique for the determination of subpicogram levels of interstitial collagenase. Anal Biochem 1998;255:211-216.
25. Matrisian LM. Metalloproteinases and their inhibitors in matrix remodeling. Trends Genet 1990;6:121-125.
26. McCawley L, O'Brien P, Hudson L. Epidermal growth factor (EGF-) and scatter factor/hepatocyte growth factor (SF/HGF)-mediated keratinocyte migration is coincident with induction of matrix metalloproteinase (MMP)-9. J Cell Physiol 1998;176:255-265.
27. Makela M, Larjava H, Pirila E, et al. Matrix metalloproteinase 2 (gelatinase A) is related to migration of keratinocytes. Exp Cell Res 1999;251:67-78.
28. Makela M, Sorsa T, Uitto VJ, et al. The effects of chemically modified tetracyclines (CMTs) on human keratinocyte proliferation and migration. Adv Dent Res 1998;12:131-135.
29. Pilcher BK, Dumin JA, Sudbeck BD, et al. The activity of collagenase-1 is required for keratinocyte migration on a type I collagen matrix. J Cell Biol 1997;37:1445-1457.
30. Giannelli G, Falk-Marzillier J, Schiraldi O, Steder-Stevenson W, Quaranta V. Induction of cell migration by matrix metalloproteinase-2 cleavage of laminin-5. Science 1997;277: 225-228.
31. Parks W, Mecham R. Matrix Metalloproteinases. San Diego: Academic Press; 1998.
32. Lund L, Romer J, Bugge T, et al. Functional overlap between two classes of matrix-degrading proteases in wound healing. EMBO J 1999;18:4645-4656.
33. Legrand C, Gilles C, Zahm J, et al. Airway epithelial cell migration dynamics. MMP-9 role in cell-extracellular matrix remodeling. J Cell Biol 1999;146:517-529.
34. Betsuyaku T, Fukuda Y, Parks W, Shipley J, Senior R. Gelatinase B is required for alveolar bronchiolization after intratracheal bleomycin. Am J Pathol 2000;157: 525-535.
35. Mauch C, Herron GS, Bauer EA. Regulation of connective tissue turnover by matrix metalloproteinases. In: Freinkel EK, Woodley DT, eds. The Biology of the Skin. New York: Parthenon Publishing; 2001:353-364.
36. Lambert C, Soudant E, Nusgens B, Lapiere C. Pre-translational regulation of extracellular matrix molecules and collagenase expression in fibroblasts by mechanical forces. Lab Invest 1992;66:444-451.
37. Vaalamo M, Mattila L, Johansson N, et al. Distinct populations of stromal cells express collagenase-3 (MMP-13) and collagenase-1 (MMP-1) in chronic ulcers but not in normally healing wounds. J Invest Dermatol 1997;109: 96-101.
38. Ravanti L, Heino J, Lopez-Otin C, Kahari V-M. Induction of collagenase-3 (MMP-13) expression in human skin fibroblast three-dimensional collagen is mediated by p38 mitogen-activated protein kinase. J Biol Chem 1999;274: 2446-2455.
39. Seguier S, Godeau G, Brousse N. Collagen fibers and inflammatory cells in healthy and diseased human gingival tissues: A comparative and quantitative study by immunohistochemistry and automated image analysis. J Periodontol 2000;71:1079-1085.
40. Makela M, Salo T, Uitto V-J, Larjava H. Matrix metalloproteinase (MMP-2 and MMP-9) of the oral cavity: Cellular origin and relationship to periodontal status. J Dent Res 1994;73:1397-1406.
41. Tuan T-L, Keller L, Sun D, Nimni M, Cheung D. Dermal fibroblasts activate keratinocyte outgrowth on collagen gels. J Cell Sci 1994;107:2285-2289.
42. Luger T, Schwarz T. The role of cytokines and neuroendocrine hormones in cutaneous immunity and inflammation. Allergy 1995;50:292-302.
43. Garner W. Epidermal regulation of dermal fibroblast activity. Plast Reconstr Surg 1998;102:135-139.
44. Smola H, Stark H-J, Thiekotter G, Mirancea N, Krieg T, Fusenig NE. Dynamics of basement membrane formation by keratinocyte-fibroblast interactions in organotypic skin culture. Exp Cell Res 1998;239:399-410.
45. Maas-Szabowski N, Szabowski A, Stark H, et al. Organotypic cocultures with genetically modified mouse fibroblasts as a tool to dissect molecular mechanisms regulating keratinocyte growth and differentiation. J Invest Dermatol 2001;116:816-820.
46. Agren M, Mirastschijski U, Karismark T, Saarialho-Kere U. Topical synthetic inhibitor of matrix metalloproteinases delays epidermal regeneration of human wounds. Exp Dermatol 2001;10:337-348.
47. Mohan R, Chintala S, Jung J, et al. Matrix metalloproteinase gelatinase B (MMP-9) coordinates and affects epithelial regeneration. J Biol Chem 2002;277:2065-2072.
48. de Souza A, Gerlach R, Line S. Inhibition of human gingival gelatinases (MMP-2 and MMP-9) by metal salts. Dent Mater 2000;16:103-108.
49. Vaalamo M, Weckroth M, Puolakkainen P, et al. Patterns of matrix metalloproteinase and TIMP-1 expression in chronic and normally healing human cutaneous wounds. Br J Dermatol 1996;135:52-59.
50. Madlener M, Parks W, Werner S. Matrix metalloproteinases (MMP) and their physiological inhibitors (TIMP) are differentially expressed during excisional skin wound repair. Exp Cell Res 1998;242:201-210.