Expression of pro-inflammatory markers by human dermal fibroblasts in a three-dimensional culture model is mediated by an autocrine interleukin-1 loop

Biochemical Journal

Volumn 379, Issue 2, 2004, Pages 351-358

  Kessler Becker, Daniela ^a   Krieg, Thomas ^a   Eckes, Beate ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Cell matrix interaction; Collagen lattice; Differential gene expression; Fibroblast; Inflammation; Transcriptional profiling

Indexed keywords

COLLAGEN; GENES; LATTICE CONSTANTS; MATRIX ALGEBRA; TISSUE;

MATRIX SYNTHESIS; MECHANICAL TENSION; PROFILERATION; TRANSCRIPTIONAL PROFILE;

BIOCHEMISTRY;

BIOLOGICAL MARKER; CYCLOOXYGENASE 2; CYTOKINE; GROWTH FACTOR; INTERLEUKIN 1; INTERLEUKIN 6; INTERSTITIAL COLLAGENASE; KERATINOCYTE GROWTH FACTOR; MATRIX METALLOPROTEINASE;

ARTICLE; AUTOCRINE EFFECT; CELL CULTURE; CONTROLLED STUDY; DERMIS; DOWN REGULATION; ENZYME INDUCTION; EXTRACELLULAR MATRIX; FIBROBLAST; GENE INDUCTION; GENETIC CODE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; INFLAMMATION; MICROENVIRONMENT; MOLECULAR BIOLOGY; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; MOLECULAR MODEL; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN FIBROBLAST;

AUTOCRINE COMMUNICATION; BIOLOGICAL MARKERS; BLOTTING, NORTHERN; CELL CULTURE TECHNIQUES; COLLAGEN; CYCLOOXYGENASE 2; DERMIS; FIBROBLASTS; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; INFLAMMATION; INTERLEUKIN-1; INTERLEUKIN-6; ISOENZYMES; MEMBRANE PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES;

EID: 2342528447     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20031371     Document Type: Article

References (65)

1. Hynes, R. O. (1992) Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69, 11-25
2. Eckes, B., Kessler, D., Aumailley, M. and Krieg, T. (1999) Interactions of fibroblasts with the extracellular matrix: implications for the understanding of fibrosis. Springer Semin. Immunopathol. 21, 415-429
3. Mauch, C. (1998) Regulation of connective tissue turnover by cell-matrix interactions. Arch. Dermatol. Res. 290 (Suppl.), S30-S36
4. Cukierman, E., Pankov, R., Stevens, D. R. and Yamada, K. M. (2001) Taking cell-matrix adhesions to the third dimension. Science 294, 1708-1712
5. Hynes, R. (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110, 673-687
6. Chiquet, M. (1999) Regulation of extracellular matrix gene expression by mechanical stress. Matrix Biol. 18, 417-426
7. Jordana, M., Sarnstrand, B., Sime, P. J. and Ramis, I. (1994) Immune-inflammatory functions of fibroblasts. Eur. Respir. J. 7, 2212-2222
8. Gabbiani, G. (1981) The myofibroblast: a key cell for wound healing and fibrocontractive diseases. Prog. Clin. Biol. Res. 54, 183-194
9. Grinnell, F. (1994) Fibroblasts, myofibroblasts, and wound contraction. J. Cell Biol. 124, 401-404
10. Vaughan, M. B., Howard, E. W. and Tomasek, J. J. (2000) Transforming growth factor-β1 promotes the morphological and functional differentiation of the myofibroblast. Exp. Cell Res. 257, 180-189
11. Kessler, D., Dethlefsen, S., Haase, I., Plomann, M., Hirche, F., Krieg, T. and Eckes, B. (2001) Fibroblasts in mechanically stressed collagen lattices assume a "synthetic" phenotype. J. Biol. Chem. 276, 36575-36585
12. Bell, E., Ivarsson, B. and Merrill, C. (1979) Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferate potential in vitro. Proc. Natl. Acad. Sci. U.S.A. 76, 1274-1278
13. Lambert, C. A., Soudant, E. P., Nusgens, B. V. and Lapiere, C. M. (1992) Pretranslational regulation of extracellular matrix macromolecules and collagenase expression in fibroblasts by mechanical forces. Lab. Invest. 66, 444-451
14. Grinnell, F., Ho, C. H., Lin, Y. C. and Skuta, G. (1999) Signal transduction pathways activated during fibroblast contraction of collagen matrices. J. Biol. Chem. 274, 918-923
15. Nusgens, B., Merrill, C., Lapiere, C. and Bell, E. (1984) Collagen biosynthesis by cells in a tissue equivalent matrix in vitro. Collagen Relat. Res. 4, 351-363
16. Mauch, C., Adelmann-Grill, B., Hatamochi, A. and Krieg, T. (1989) Collagenase gene expression in fibroblasts is regulated by a three-dimensional contact with collagen. FEBS Lett 250, 301-305
17. Klein, C. E., Dressel, D., Steinmayer, T., Mauch, C., Eckes, B., Krieg, T., Bankert, R. B. and Weber, L. (1991) Integrin α2β1 is upregulated in fibroblasts and highly aggressive melanoma cells in three-dimensional collagen lattices and mediates the reorganization of collagen I fibrils. J. Cell Biol. 115, 1427-1436
18. Langholz, O., Rockel, D., Mauch, C., Kozlowska, E., Bank, I., Krieg, T. and Eckes, B. (1995) Collagen and collagenase gene expression in three-dimensional collagen lattices are differentially regulated by α1β1 and α2β1 integrins. J. Cell Biol. 131, 1903-1915
19. Riikonen, T., Westermarck, J., Koivisto, L., Broberg, A., Kahari, V. M. and Heino, J. (1995) Integrin α2β1 is a positive regulator of collagenase (MMP-1) and collagen α1(I) gene expression. J. Biol. Chem. 270, 13548-13552
20. Zigrino, P., Drescher, C. and Mauch, C. (2001) Collagen-induced proMMP-2 activation by MT1-MMP in human dermal fibroblasts and the possible role of α2β1 integrins. Eur. J. Cell Biol. 80, 68-77
21. Ruoslahti, E. (1997) Stretching is good for a cell. Science 276, 1345-1346
22. Chen, C. S., Mrksich, M., Huang, S., Whitesides, G. M. and Ingber, D. E. (1997) Geometric control of cell life and death. Science 276, 1425-1428
23. Grinnell, F., Zhu, M., Carlson, M. A. and Abrams, J. M. (1999) Release of mechanical tension triggers apoptosis of human fibroblasts in a model of regressing granulation tissue. Exp. Cell Res. 248, 608-619
24. Niland, S., Cremer, A., Fluck, J., Eble, J. A., Krieg, T. and Sollberg, S. (2001) Contraction-dependent apoptosis of normal dermal fibroblasts. J. Invest. Dermatol. 116, 686-692
25. Fringer, J. and Grinnell, F. (2003) Fibroblast quiescence in floating collagen matrices: decrease in serum activation of MEK and Raf but not Ras. J. Biol. Chem. 278, 20612-20617
26. Lambert, C. A., Lapiere, C. M. and Nusgens, B. V. (1998) An interleukin-1 loop is induced in human skin fibroblasts upon stress relaxation in a three-dimensional collagen gel but is not involved in the up-regulation of matrix metalloproteinase 1. J. Biol. Chem. 273, 23143-23149
27. Finch, P. W., Rubin, J. S., Miki, T., Ron, D. and Aaronson, S. A. (1989)Human KGF is FGF-related with properties of a paracrine effector of epithelial cell growth. Science 245, 752-755
28. May, L. T., Helfgott, D. C. and Sehgal, P. B. (1986) Anti-β- interferon antibodies inhibit the increased expression of HLA-B7 mRNA in tumor necrosis factor-treated human fibroblasts: structural studies of the β2 interferon involved. Proc. Natl. Acad. Sci. U.S.A. 83, 8957-8961
29. Hla, T. and Neilson, K. (1992) Human cyclooxygenase-2 cDNA Proc. Natl. Acad. Sci. U.S.A. 89, 7384-7388
30. Chang, A. C., Janosi, J., Hulsbeek, M., de Jong, D., Jeffrey, K. J., Noble, J. R. and Reddel, R. R. (1995) A novel human cDNA highly homologous to the fish hormone stanniocalcin. Mol. Cell. Endocrinol. 112, 241-247
31. Scanlan, M. J., Raj, B. K., Calvo, B., Garin-Chesa, P., Sanz-Moncasi, M. P., Healey, J. H., Old, L. J. and Rettig, W. J. (1994) Molecular cloning of fibroblast activation protein α, a member of the serine protease family selectively expressed in stromal fibroblasts of epithelial cancers. Proc. Natl. Acad. Sci. U.S.A. 91, 5657-5661
32. Auron, P. E., Webb, A. C., Rosenwasser, L. J., Mucci, S. F., Rich, A., Wolff, S. M. and Dinarello, C. A. (1984) Nucleotide sequence of human monocyte interleukin 1 precursor cDNA. Proc. Natl. Acad. Sci. U.S.A. 81, 7907-7911
33. Valtavaara, M., Papponen, H., Pirttila, A. M., Hiltunen, K., Helander, H. and Myttyla, R. (1997) Cloning and characterization of a novel human lysyl hydroxylase isoform highly expressed in pancreas and muscle. J. Biol. Chem. 272, 6831-6834
34. Carlson, S. G., Fawcett, T. W., Bartlett, J. D., Bernier, M. and Holbrook, N. J. (1993) Regulation of the C/EBP-related gene gadd153 by glucose deprivation. Mol. Cell. Biol. 13, 4736-4744
35. Rouault, J. P., Rimokh, R., Tessa, C., Paranhos, G., Ffrench, M., Duret, L., Garoccio, M., Germain, D., Samarut, J. and Magaud, J. P. (1992) BTG1, a member of a new family of antiproliferative genes. EMBO J. 11, 1663-1670
36. Peng, Y., Du, K., Ramirez, S., Diamond, R. H. and Taub, R. (1999) Mitogenic up-regulation of the PRL-1 protein-tyrosine phosphatase gene by Egr-1:Egr-1 activation is an early event in liver regeneration. J. Biol. Chem. 274, 4513-4520
37. Eckes, B., Hunzelmann, N., Ziegler-Heitbrock, H. W., Urbanski, A., Luger, T., Krieg, T. and Mauch, C. (1992) Interleukin-6 expression by fibroblasts grown in three-dimensional gel cultures. FEBS Lett 298, 229-232
38. Madsen, K. L., Tavernini, M. M., Yachimec, C., Mendrick, D. L., Alfonso, P. J., Buergin, M., Olsen, H. S., Antonaccio, M. J., Thomson, A. B. and Fedorak, R. N. (1998) Stanniocalcin: a novel protein regulating calcium and phosphate transport across mammalian intestine. Am. J. Physiol. 274, G96-G102
39. Leong, S. R., Baxter, R. C., Camerato, T., Dai, J. and Wood, W. I. (1992) Structure and functional expression of the acid-labile subunit of the insulin-like growth factor-binding protein complex. Mol. Endocrinol. 6, 870-876
40. Rajah, R., Valentinis, B. and Cohen, P. (1997) Insulin-like growth factor (IGF)-binding protein-3 induces apoptosis and mediates the effects of transforming growth factor-β1 on programmed cell death through a p53- and IGF-independent mechanism. J. Biol. Chem. 272, 12181-12188
41. Valentinis, B., Bhala, A., DeAngelis, T., Baserga, R. and Cohen, P. (1995) The human insulin-like growth factor (IGF) binding protein-3 inhibits the growth of fibroblasts with a targeted disruption of the IGF-I receptor gene. Mol. Endocrinol. 9, 361-367
42. Smith, T., McCracken, J., Shin, Y. K. and DeWitt, D. (2000) Arachidonic acid and nonsteroidal anti-inflammatory drugs induce conformational changes in the human prostaglandin endoperoxide H2 synthase-2 (cyclooxygenase-2). J. Biol. Chem. 275, 40407-40415
43. Diaz, A., Chepenik, K. P., Korn, J. H., Reginato, A. M. and Jimenez, S. A. (1998) Differential regulation of cyclooxygenases 1 and 2 by interleukin-1β, tumor necrosis factor-α, and transforming growth factor-β1 in human lung fibroblasts. Exp. Cell Res. 241, 222-229
44. Fluck, J., Querfeld, C., Cremer, A., Niland, S., Krieg, T. and Sollberg, S. (1998) Normal human primary fibroblasts undergo apoptosis in three-dimensional contractile collagen gels. J. Invest. Dermatol. 110, 153-157
45. Mauch, C., Hatamochi, A., Scharffetter, K. and Krieg, T. (1988) Regulation of collagen synthesis in fibroblasts within a three-dimensional collagen gel. Exp. Cell Res. 178, 493-503
46. Nakagawa, S., Pawelek, P. and Grinnell, F. (1989) Extracellular matrix organization modulates fibroblast growth and growth factor responsiveness. J. Invest. Dermatol. 93, 792-798
47. Kono, T., Tanii, T., Furukawa, M., Mizuno, N., Kitajima, J., Ishii, M., Hamada, T. and Yoshizato, K. (1990) Cell cycle analysis of human dermal fibroblasts cultured on or in hydrated type I collagen lattices. Arch. Dermatol. Res. 282, 258-262
48. Johnson, K. W. and Smith, K. A. (1991) Molecular cloning of a novel human cdc2/CDC28-like protein kinase. J. Biol. Chem. 266, 3402-3407
49. Rodier, A., Marchal-Victorion, S., Rochard, P., Casas, F., Cassar-Malek, I., Rouault, J. P., Magaud, J. P., Mason, D. Y., Wrutniak, C. and Cabello, G. (1999) BTG1: a triiodothyronine target involved in the myogenic influence of the hormone. Exp. Cell Res. 249, 337-348
50. Giguere, V., Tini, M., Flock, G., Ong, E., Evans, R. M. and Otulakowski, G. (1994) Isoform-specific amino-terminal domains dictate DNA-binding properties of RORα, a novel family of orphan hormone nuclear receptors. Genes Dev. 8, 538-553
51. Rosenfeldt, H. and Grinnell, F. (2000) Fibroblast quiescence and the disruption of ERK signaling in mechanically unloaded collagen matrices. J. Biol. Chem. 275, 3088-3092
52. Ingber, D. E. (1997) Tensegrity: the architectural basis of cellular mechanotransduction. Annu. Rev. Physiol. 59, 575-599
53. Ravanti, L., Heino, J., Lopez-Otin, C. and Kähäri, V. M. (1999) Induction of collagenase-3 (MMP-13) expression in human skin fibroblasts by three-dimensional collagen is mediated by p38 mitogen-activated protein kinase. J. Biol. Chem. 274, 2446-2455
54. Tomasek, J. J., Halliday, N. L., Updike, D. L., Ahern-Moore, J. S., Vu, T. K., Liu, R. W. and Howard, E. W. (1997) Gelatinase A activation is regulated by the organization of the polymerized actin cytoskeleton. J. Biol. Chem. 272, 7482-7487
55. Mathew, S., Scanlan, M. J., Mohan Raj, B. K., Murty, V. V., Garin-Chesa, P., Old, L. J., Rettig, W. J. and Chaganti, R. S. (1995) The gene for fibroblast activation protein α (FAP), a putative cell surface-bound serine protease expressed in cancer stroma and wound healing, maps to chromosome band 2q23. Genomics 25, 335-337
56. Chen, W. T. (1996) Proteases associated with invadopodia, and their role in degradation of extracellular matrix. Enzyme Protein 49, 59-71
57. Eckes, B., Mauch, C., Hüppe, G. and Krieg, T. (1993) Downregulation of collagen synthesis in fibroblasts within three-dimensional collagen lattices involves transcriptional and posttranscriptional mechanisms. FEBS Lett. 318, 129-133
58. Trächslin, J., Koch, M. and Chiquet, M. (1999) Rapid and reversible regulation of collagen XII expression by changes in tensile stress. Exp. Cell Res. 247, 320-328
59. Hatamochi, A., Aumailley, M., Mauch, C., Chu, M. L., Timpl, R. and Krieg, T. (1989) Regulation of collagen VI expression in fibroblasts: effects of cell density, cell-matrix interactions, and chemical transformation. J. Biol. Chem. 264, 3494-3499
60. Chiquet-Ehrismann, R., Tannheimer, M., Koch, M., Brunner, A., Spring, J., Martin, D., Baumgartner, S. and Chiquet, M. (1994) Tenascin-C expression by fibroblasts is elevated in stressed collagen gels. J. Cell Biol. 127, 2093-2101
61. Sarman, G., Shappell, S. B., Mason, E. O., Smith, C. W. and Kaplan, S. L. (1995) Susceptibility to local and systemic bacterial infections in intercellular adhesion molecule 1-deficient transgenic mice. J. Infect. Dis. 172, 1001-1008
62. Braun, S., Hanselmann, C., Gassmann, M. G., auf dem Keller, U., Born-Berclaz, C., Chan, K., Kan, Y. W. and Werner, S. (2002) Nrf2 transcription factor, a novel target of keratinocyte growth factor action which regulates gene expression and inflammation in the healing skin wound. Mol. Cell. Biol. 22, 5492-5505
63. Kawata, A. and Mikuni-Takagaki, Y. (1998) Mechanotransduction in stretched osteocytes - temporal expression of immediate early and other genes. Biochem. Biophys. Res. Commun. 246, 404-408
64. Subbaramaiah, K., Hart, J. C., Norton, L. and Dannenberg, A. J. (2000) Microtubule-interfering agents stimulate the transcription of cyclooxygenase-2: evidence for involvement of ERK1/2 and p38 mitogen-activated protein kinase pathways. J. Biol. Chem. 275, 14838-14845
65. Kheradmand, F., Werner, E., Tremble, P., Symons, M. and Werb, Z. (1998) Role of Rac1 and oxygen radicals in collagenase-1 expression induced by cell shape change. Science 280, 898-902