[en] In order to characterize a fibroblast cell line representing normal human skin fibroblasts in three-dimensional cultures, we compared the fibroblast line MSU-1.1, derived from human foreskin and immortalized by v-myc, to primary human dermal fibroblasts (NDF). Our results demonstrate that in contrast to NDF, all MSU-1.1 fibroblasts die within 3-4 d when cultured within three-dimensional contractile collagen matrices. Also, in contrast to NDF. MSU-1.1 cells die markedly in anchored collagen gels as well. Death is due to apoptosis and is attenuated by addition of antibodies against collagen-recognizing receptors alpha1beta1 and alpha2beta1. Apoptosis of NDF in collagen lattices was repressed by an inhibitor of caspase-1, which was ineffective on apoptosis of MSU-1.1. Further, apoptosis by MSU-1.l fibroblasts was also observed in anchored, i.e., restrained collagen lattices, an environment that supports proliferation of NDF.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Niland, S.; University of Cologne, Germany > Dept of Dermatology
Cremer, A.
Herzhoff, K.
Nusgens, Betty ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Laboratoire de Biologie des Tissus Conjonctifs
Lapiere, C. M.
Krieg, T.; University of Cologne - Germany > Dept of Dermatology and Center for Biochemistry
Eckes, B.; University of Cologne, Germany > Dept of Dermatology
Language :
English
Title :
Apoptosis in v-myc-transfected MSU-1.1 fibroblasts is induced by cell-matrix contact and differs from that of normal dermal fibroblasts.
Publication date :
2001
Journal title :
In Vitro Cellular and Developmental Biology. Animal
ISSN :
1071-2690
eISSN :
1543-706X
Publisher :
Society for in Vitro Biology, Columbia, United States - Maryland
Angel P., Baumann I., Stein B., Delius H., Rahmsdorf H.J., Herrlich P. (1987) 12-O-Tetradecanoyl-phorbol-13-acetate induction of the human collagenase gene is mediated by an inducible enhancer element located in the 5' flanking region. Mol. Cell. Biol. 7:2256-2266.
Bell E., Ivarsson B., Merill C. (1979) Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vitro. Proc. Natl. Acad. Sci. USA 76:1274-1278.
Chan B.M.C., Kassner P.D., Schiro J.A., Byers R., Kupper T.S., Hemler M.E. (1992) Distinct cellular functions mediated by different VLA integrin α subunit cytoplasmic domains. Cell 68:1051-1060.
Chomczynski P. (1993) A reagent for the single-step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples. Biotechniques 15:532-537.
Delic J., Coppeymoisan M., Magdelenat H. (1993) γ-ray-induced transcription and apoptosis-associated loss of 28S RNA in interphase human lymphocytes. Int. J. Radiat. Biol. 64:39-46.
Desmoulière A., Redard M., Darby I., Gabbiani G. (1995) Apoptosis mediates the decrease in cellularity during the transition between granulation tissue and scar. Am. J. Pathol. 146:56-66.
Eckes B., Krieg T., Nusgens B.V., Lapière C.M. (1995) In vitro reconstituted skin as a tool for biology, pharmacology and therapy: A review. Wound Rep. Reg. 3:248-257.
Evan G.I., Wyllie A.H., Gilbert C.S. (1992) Induction of apoptosis in fibroblasts by c-myc protein. Cell 69:119-128.
Feinberg A.P., Vogelstein B. (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132:6-13.
Fluck J., Querfeld C., Cremer A., Niland S., Krieg T., Sollberg S. (1998) Normal human primary fibroblasts undergo apoptosis in three-dimensional contractile collagen gels. J. Invest. Dermatol. 110:153-157.
Folkman J., Moscona A. (1978) A role of cell shape in growth control. Nature 273:345-349.
Frisch S.M., Francis H. (1994) Disruption of epithelial cell-matrix interactions induces apoptosis. J. Cell Biol. 124:619-626.
Frisch S.M., Ruoslahti E. (1997) Integrins and anoikis. Curr. Opin. Cell Biol. 9:701-706.
Gardner H., Broberg A., Pozzi A., Laato M., Heino J. (1999) Absence of integrin α1β1 in the mouse causes loss of feedback regulation of collagen synthesis in normal and wounded dermis. J. Cell Sci. 112:263-272.
Grinnell F. (1994) Fibroblasts, myofibroblasts and wound contraction. J. Cell Biol. 124:401-404.
Grinnell K. (1999) Signal transduction pathways activated during fibroblast contraction of collagen matrices. Tissue repair and fibrosis , Desmoulière, A.; Tuchweber, B., ed. Berlin: Springer; 61-74.
Harrington E.A., Bennett M.R., Fanidi A., Evan G.I. (1994) c-Myc-induced apoptosis in fibroblasts is inhibited by specific cytokines. EMBO J. 13:3286-3295.
Herzhoff K., Dissertation, University of Cologne; 1999.
Houge G., Døkeland S.O. (1996) Divergence towards a dead end? Cleavage of the divergent domains of ribosomal RNA in apoptosis. Experientia 52:963-967.
Houge G., Døkeland S.O., Bø R., Lanotte M. (1993) Selective cleavage of 28S rRNA variable Regions V3 and V13 in myeloid leukemia cell apoptosis. FEBS Lett. 315:16-20.
Houge G., Robaye B., Eikhom T.S., Golstein J., Melgren G., Gjertsen B.T., Lanotte M., Døkeland S.O. (1995) Fine mapping of 28S rRNA sites specifically cleaved in cells undergoing apoptosis. Mol. Cell. Biol. 15:2051-2062.
Jiang M.-C., Yang-Yen H.-F., Lin J.-K., Yen J.J.-Y. (1996) Differential regulation of p53, c-Myc, Bcl- 2 and Bax protein expression during apoptosis induced by widely divergent stimuli in human hepatoblastoma cells. Oncogene 13:609-616.
Jiménez B., Arends M., Esteve P., Perona R., Sánchez R., Ramón y Cajal S., Wyllie A., Lacal J.C. (1995) Induction of apoptosis in N1H3T3 cells after serum deprivation by overexpression of rho-p21, a GTPase protein of the ras superfamily. Oncogene 10:811-816.
Juliano R.L., Haskill S. (1993) Signal transduction from the extracellular matrix. J. Cell Biol. 120:577-585.
Klein C.E., Dressel D., Steinmayer T., Mauch C., Eckes B., Krieg T., Bankert R.B., 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.
Kühn K. (1997) Extracellular matrix constituents as integrin ligands. Integrin-ligand interaction , Eble, J. A.; Kühn, K., ed. Berlin: Springer; 41-84.
Lambert C.A., Soudant E.P., Nusgens B.V., Lapière C.M. (1992) Pretranslational regulation of extracellular matrix macromolecules and collagenase expression in fibroblasts by mechanical forces. Lab. Invest. 66:444-451.
Langholz O., Röckel D., Mauch C., Kozlowska E., Bank I., Krieg T., 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.
Los M., Wesselborg S., Schulze-Osthoff K. (1999) The role of caspases in development, immunity, and apoptotic signal transduction: Lessons from knockout mice. Immunity 10:629-639.
Mauch C., Adelmann-Grill B., Hatamochi A., Krieg T. (1989) Collagenase gene expression in fibroblasts is regulated by a three-dimensional contact with collagen. FEBS Lett. 250:301-305.
Mauch C., Hatamochi A., Scharffetter K., Krieg T. (1988) Regulation of collagen synthesis within a three-dimensional collagen gel. Exp. Cell Res. 178:493-503.
McCormick J.J., Maher V.M. (1946) Analysis of the multistep process of carcinogenesis using human fibroblasts. Risk Anal. 14:257-263.
McKenna W.G., Bernhard E.J., Markiewicz D.A., Rudoltz M.S., Maity A., Muschel R.J. (1996) Regulation of radiation-induced apoptosis in oncogene-transfected fibroblasts: Influence of H-ras on the G 2 delay. Oncogene 12:237-245.
Meredith J.E., Fazeli B., Schwartz M.A. (1993) The extracellular matrix as a cell survival factor. Mol. Biol. Cell 4:953-961.
Meredith J.E., Schwartz M.A. (1997) Integrins, adhesion and apoptosis. Trends Cell Biol. 7:146-150.
Miura M., Zhu H., Rotello R., Hartwieg E.A., Yuan J. (1993) Induction of apoptosis in fibroblasts by IL-1 β-converting enzyme, a mammalian homolog of the C. elegans cell death gene ced-3. Cell 75:653-660.
Morgan T.L., Yang D.J., Fry D.G., Hurlin P.J., Kohler S.K., Maher V.M., McCormick J.J. (1991) Characteristics of an infinite life span diploid human fibroblast cell strain and a near-diploid strain arising from a clone of cells expressing a transfected v-myc oncogene. Exp. Cell Res. 197:125-136.
Niland S., Cremer A., Kuckenberg M., Fluck J., Krieg T., Sollberg S. (1997) Induction of apoptosis in primary fibroblasts is mediated by distinct integrins. Wound Rep. Reg. , 7th Annual Meeting of the European Tissue Repair Society, Köln, 23- 26 August 1997; 5:A283.
Niland S., Cremer A., Fluck J., Eble J.A., Krieg T., Sollberg S. (2001) Contraction-dependent apoptosis of normal dermal fibroblasts. J. Invest. Dermatol. 116(5):686-692.
Petropoulos C.J., Givol I., Hughes S.H. (1996) Comparative analysis of the structure and function of the chicken c-myc and v-myc genes: v-myc is a more potent inducer of cell proliferation and apoptosis than c-myc. Oncogene 12:2611-2621.
Pozzi A., Wary K.K., Ciancotti F.G., Gardner H.A. (1998) Integrin α1β1 mediates a unique collagen-dependent proliferation pathway in vivo. J. Cell Biol. 142:587-594.
Riikonen T., Westermarck J., Koivisto L., Broberg A., Kahari V.M., 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.
Sambrook K.J., Fritsch E.F., Maniatis T. Molecular cloning - A laboratory manual. 2nd ed. , Cold Spring Harbor: Cold Spring Harbor Laboratory Press; 1989, 916-917.
Saoncella S., Echtermeyer F., Denhez F., Nowlen J.K., Mosher D.F., Robinson S.D., Hynes R.O., Goetinck P.F. (1999) Syndecan-4 signals cooperatively with integrins in a Rho-dependent manner in the assembly of focal adhesions and actin stress fibers. Proc. Natl. Acad. Sci. USA 96:2805-2810.
Thornberry N., Lazebnik Y. (1998) Caspases: Enemies within. Science 281:1312-1316.
Thornberry N.A., Peterson E.P., Zhao J.J., Howard A.D., Griffin R.P., Chapman K.T. (1994) Inactivation of interleukin-1β converting enzyme by peptide (acyloxy)methyl ketones. Biochemistry 33:3934-3940.
Vogel W. (1999) Discoidin domain receptors: Structural relations and functional implications. FASEB J 13:S77-S82.
Von der Mark K., Mollenhauer J. (1997) Annexin V interactions with collagen. Cell. Mol. Life Sci. 53:539-545.
Wang Y., Ramqvist T., Szekely L., Axelson H., Klein G., Wimann K.G. (1993) Reconstitution of wild-type p53 expression triggers apoptosis in a p53-negative v-myc retrovirus-induced T-cell lymphoma line. Cell Growth Differ 4:467-473.