Epidermal differentiation and basement membrane formation by HaCaT cells in surface transplants

European Journal of Cell Biology

Volumn 75, Issue 3, 1998, Pages 273-286

  Breitkreutz, Dirk ^a   Schoop, Veronika M ^a   Mirancea, Nicolae ^a,b   Baur, Markus ^a,c   Stark, Hans Jürgen ^a   Fusenig, Norbert E ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b INSTITUTE OF BIOLOGY   (Romania)

^c NESTLÉ RESEARCH CENTER   (Switzerland)

Author keywords

Basement membrane; Epidermal structure; HaCaT cells; Integrins; Surface transplants

Indexed keywords

FIBRONECTIN; FILAGGRIN; LORICRIN; TENASCIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL REGENERATION; CELL TRANSPLANTATION; CONTROLLED STUDY; EPIDERMIS CELL; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; KERATINOCYTE; MOUSE; NONHUMAN; PATHOLOGY; PHYSIOLOGY; PRIORITY JOURNAL;

ANIMALS; BASEMENT MEMBRANE; BIOLOGICAL MARKERS; CELL COMPARTMENTATION; CELL DIFFERENTIATION; CELL DIVISION; CELL LINE; CELL TRANSPLANTATION; EPIDERMIS; EPITHELIAL CELLS; EPITHELIUM; HUMANS; INTEGRINS; KERATINOCYTES; MICE; MICE, NUDE;

EID: 0031945960     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0171-9335(98)80123-4     Document Type: Article

References (74)

1. Aumailley, M., T. Krieg: Review: Structure and function of the cutaneous extracellular matrix. Eur. J. Dermatol. 4, 271-280 (1994).
2. Borradori, L., A. Sonnenberg: Hemidesmosomes: roles in adhesion, signaling and human diseases. Curr. Opin. Cell Biol. 8, 647-656 (1996).
3. Boukamp, P., D. Breitkreutz, H.-J. Stark, N. E. Fusenig: Mesenchyme-mediated and endogenenous regulation of growth and differentiation of human skin keratinocytes derived from different body sites. Differentiation 44, 150-161 (1990).
4. Boukamp, P., R. T. Dzarliewa-Petrusevska, D. Breitkreutz, J. Hornung, A. Markham, N. E. Fusenig: Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J. Cell Biol. 106, 761-771 (1988).
5. Boukamp, P., S. Popp, S. Altmeyer, A. Hülsen, C. Fasching, T. Cremer, N. E. Fusenig: Sustained nontumorigenic phenotype correlates with a largely stable chromosome content during longterm culture of the human keratinocyte line HaCaT. Genes, Chromosomes & Cancer 19, 201-214 (1997).
6. Boukamp, P., E. J. Stanbridge, D. Y. Foo, P. A. Cerutti, N. E. Fusenig: c-Ha-ras oncogene expression in immortalized human keratinocytes (HaCaT) alters growth potential in vivo but lacks correlation with malignancy. Cancer Res. 50, 2840-2847 (1990).
7. Breitkreutz, D., P. Boukamp, C. M. Ryle, H.-J. Stark, D. R. Roop, N. E. Fusenig: Epidermal morphogenesis and keratin expression in c-Ha-ras-transfected tumorigenic clones of the human HaCaT cell line. Cancer Res. 51, 4402-4409 (1991).
8. Breitkreutz, D., J. Hornung, J. Pöhlmann, L. Brown-Biermann, A. Bohnert, P. E. Bowden, N. E. Fusenig: Environmental induction of differentiation-specific keratins in malignant mouse keratinocyte lines. Eur. J. Cell Biol. 42, 255-267 (1986).
9. Breitkreutz, D., H.-J. Stark, N. Mirancea, P. Tomakidi, H. Steinbauer, N. E. Fusenig: Integrin and basement membrane normalization in mouse grafts of human keratinocytes - implications for epidermal homeostasis. Differentiation 61, 195-209 (1997).
10. 2+. Differentiation 54, 201-217 (1993).
11. Burgeson, R. E., M. Chiquet, R. Deutzmann, P. Ekblom, J. Engel, H. Kleinman, G. R. Martin, G. Meneguzzi, M. Paulsson, J. Sanes, R. Timpl, K. Tiyggvason, Y. Yamada, P. D. Yurchenco: A new nomenclature for the laminins. Matrix Biol. 14, 209-211 (1994).
12. Carter, W. G., P. Kaur, S. G. Gil, P. J. Gahr, E. A. Wayner: Distinct functions for integrins α3β1 in focal adhesions and α6β4/ bullous pemphigoid antigen in a new stable anchoring contact (SAC) of keratinocytes: relation to hemidesmosomes. J. Cell Biol. 111, 3141-3154 (1990).
13. Cavani, A., G. Zambruno, A. Marconi, V. Manca, M. Marchetti, A. Giannetti: Distinctive integrin expression in the newly forming epidermis during wound healing in humans. J. Investig. Dermatol. 101, 600-604 (1993).
14. Clark, E. A., J. S. Brugge: Integrins and signal transduction pathways: the road taken. Science 268, 233-239 (1995).
15. Dedhar, S., G. E. Hannigan: Integrin cytoplasmic interactions and bidirectional transmembrane signalling. Curr. Opin. Cell Biol. 8, 657-669 (1996).
16. Delcommenne, M., C. H. Streuli: Control of integrin expression by extracellular matrix. J. Biol. Chem. 270, 26794-26801 (1995).
17. DeLuca, M., G. Pellegrini, G. Zambruno, P. C. Marchisio: Role of integrins in cell adhesion and polarity in normal keratinocytes and human skin pathologies. J. Dermatol. 21, 821-828 (1994).
18. Ekblom, P.: Receptors for laminins during epithelial morphogenesis. Curr. Opin. Cell Biol. 8, 700-706 (1996).
19. Engvall, E., T. Earwicker, E. Haaparanta, E. Ruoslahti, J. R. Sanes: Distribution and isolation of four laminin variants: tissue restricted distribution of heterotrimers assembled from five different subunits. Cell Regul. 1, 731-740 (1990).
20. Falcioni, R., A. Sacchi, R. Resau, S. J. Kennel: Monoclonal antibody to human carcinoma-associated protein complex: quantitation in normal and tumor tissue. Cancer Res. 48, 816-821 (1988).
21. Foidart, J.-M., A. H. Reddi: Immunofluorescent localization of type IV collagen and laminin during endochondral bone differentiation and regulation by pituitary growth hormone. Dev. Biol. 75, 130-136 (1980).
22. Fox, J. W., U. Mayer, R. Nischt, M. Aumailley, D. Reinhardt, H. Wiedemann, K. Mann, R. Timpl, T. Krieg, J. Engel, M.-L. Chu: Recombinant nidogen consists of three globular domains and mediates binding of laminin to collagen IV. EMBO J. 10, 3137-3146 (1991).
23. Frisch, S. M., H. Francis: Disruption of epithelial cell-matrix interactions induces apoptosis. J. Cell Biol. 124, 619-626 (1994).
24. Fusenig, N. E.: Epithelial-mesenchymal interactions regulate keratinocyte growth and differentiation in vitro. In: I. Leigh, B. Lane, F. M. Watt (eds.): The Keratinocyte Handbook. pp. 71-94. Cambridge University Press. Cambridge 1994.
25. Fusenig, N. E.: Culture of keratinocytes on collagen gels and use of transplantation chambers for grafting onto mouse skin. In: I. Leigh, F. M. Watt (eds.): Keratinocyte Methods. pp. 57-61. Cambridge University Press. Cambridge 1994.
26. Gailit, J., M. P. Welch, R. A. F. Clark: TGF-βl stimulates expression of keratinocyte integrins during re-epithelialization of cutaneous wounds. J. Investig. Dermatol. 103, 221-227 (1994).
27. Game, S. M., A. Hülsen, V. Patel, M. Donnelly, W. A. Yeudall, A. Stone, N. E. Fusenig, S. S. Prime: Progressive abrogation of TGF-βl and EGF growth control is associated with tumour progression in ras-transfected human keratinocytes. Int. J. Cancer 52, 461-570 (1992).
28. Geiges, D., F. Marks, M. Gschwendt: Loss of protein kinase Cδ from human HaCaT keratinocytes upon ras transfection is mediated byTGFα. Exp. Cell Res. 219, 299-303 (1995).
29. Ghadially, R., B. E. Brown, K. Hanley, J. T. Reed, K. R. Feingold, P. M. Elias: Decreased epidermal lipid synthesis accounts for altered barrier function in aged mice. J. Investig. Dermatol. 106, 1064-1069 (1996).
30. Giancotti, F. G., E. Ruoslahti: Elevated levels of the α5β1 fibronectin receptor suppress the transformed phenotype of Chinese hamster ovary cells. Cell 60, 849-859 (1990).
31. Grinnell, F.: Commentary: wound repair, keratinocyte activation and integrin modulation. J. Cell Sci. 101, 1-5 (1992).
32. Hertle, M. D., M.-D. Kubler, I. M. Leigh, F. M. Watt: Aberrant integrin expression during epidermal wound healing and in psoriatic epidermis. J. Clin. Invest. 89, 1892-1901 (1992).
33. Hogervorst, F., I. Kuikman, A. G. Van Kessel, A. Sonnenberg: Molecular cloning of the human α6 integrin subunit. Eur. J. Biochem. 199, 425-433 (1991).
34. Hohl, D., T. Mehrel, U. Lichti, M. L. Turner, D. R. Roop, P. M. Steinert: Characterization of human loricrin. J. Biol. Chem. 266, 6626-6636 (1991).
35. Holbrook, K. A.: Ultrastructure of the epidermis. In: I. Leigh, B. Lane, F. M. Watt (eds.): The Keratinocyte Handbook. pp. 3-39. Cambridge University Press. Cambridge 1994.
36. Hormia, M., J. Falk-Marzillier, G. Plopper, R. N. Tamura, J. C. R. Jones, V. Quaranta: Rapid spreading and mature hemidesmosome formation in HaCaT keratinocytes induced by incubation with soluble laminin-5r. J. Investig. Dermatol. 105, 557-561 (1995).
37. Hotchin, N. A., A. Gandarillas, F. M. Watt: Regulation of cell surface β1 integrin levels during keratinocyte terminal differentiation. J. Cell Biol. 128, 1209-1219 (1995).
38. Illic, D., C. H. Damsky, T. Yamamoto: Focal adhesion kinase: at the crossroads of signal transduction, J. Cell Sci. 110, 401-407 (1997).
39. Keely, P. J., A. M. Fong, M. M. Zutter, S. A. Santoro: Alteration of collagen-dependent adhesion, motility and morphogenesis by the expression of antisense α2 integrin mRNA in mammary cells. J. Cell Sci. 108, 595-607 (1995).
40. Klein, E. C., T. Steinmayer, D. Kaufmann, L.Weber, E.-B. Bröcker: Identification of a melanoma progression antigen as integrins VLA-2. J. Investig. Dermatol. 96, 281-284 (1991).
41. Lang, E., B. M. Schaefer, U. Eickhoff, H.-P. Hohl, M. D. Kramer, K. Maier-Reif: Rapid normalization of epidermal integrin expression after allografting of human keratinocytes. J. Investig. Dermatol. 107, 423-427 (1996).
42. Latijnhouwers, M., M. Bergers, M. Ponec, H. Dijkman, M. Andriessen, J. Schalkwijk: Human epidermal keratinocytes are a source of tenascin-C during wound healing. J. Investig. Dermatol. 108, 776-783 (1997).
43. Lazarova, Z., N. Domloge-Hultsch, K. B. Yancey: Epiligrin is decreased in papulonodular basal cell carcinoma tumor nest basement membranes and the extracellular matrix of transformed human epithelial cells. Exp. Dermatol. 4, 121-129 (1995).
44. Leigh, I. M., P. E. Purkis, L. Bruckner-Tuderman: LH7.2 monoclonal antibody detects type VII collagen in the sublamina densa zone of ectodermally-derived epithelia, including skin. Epithelia 1, 17-29 (1987).
45. Limat, A., D. Breitkreutz, G. Thiekötter, E. C. Klein, L. R. Braathen, T. Hunziker, N. E. Fusenig: Formation of a regular neo-epidermis by cultured human outer root sheath cells grafted on nude mice. Transplantation 59, 1032-1038 (1995).
46. Limat, A., E. Stockhammer, D. Breitkreutz, T. Schaffner, T. Egelrud, D. Salomon, N. E. Fusenig, L. R. Braathen, T. Hunziker: Endogeneously regulated site-specific differentiation of human palmar skin keratinocytes in organotypic cocultures and in nude mouse transplants. Eur. J. Cell Biol. 69, 245-258 (1996).
47. Lynch, M. H., W. M. O'Guin, C. Hardy, L. Mak, T.-T. Sun: Acidic and basic hair/nail ("hard") keratins: their colocalization in upper cortical and cuticle cells of the human hair follicle and their relationship to "soft" keratins. J. Cell Biol. 103, 2593-2606 (1986).
48. Marinkovich, M. P., D. R. Keene, C. S. Rimberg, R. E. Burgeson: Cellular origin of the dermal-epidermal basement membrane. Dev. Dyn. 197, 255-267 (1993).
49. Miner, J. H., B. L. Patton, S. I. Lentz, D. J. Gilbert, W. D. Snider, N. A. Jenkins, N. G. Copeland, J. R. Sanes: The laminin α chains: expression, developmental transitions, and chromosomal locations of α1-5, identification of heterotrimeric laminins 8-11, and cloning of a novel α3 isoform. J. Cell Biol. 137, 685-701 (1997).
50. Purkis, P. E., J. B. Steel, I. C. Mackenzie, W. B. J. Nathrath, I. M. Leigh, E. B. Lane: Antibody markers of basal cells in complex epithelia. J. Cell Sci. 97, 39-50 (1990).
51. Reinartz, J., B. Schaefer, R. Batrla, E. C. Klein, M. D. Kramer: Plasmin abrogates αvβ5-mediated adhesion of a human keratinocyte cell line (HaCaT) to vitronectin. Exp. Cell Res. 220, 274-282 (1995).
52. Rijzewijk, J. J., P. E. J. van Erp, J. B. M. Boezeman, G. J. de Jongh, P. D. Mier, F. W. Bauer: The development of the bromo-deoxyuridine technique for kinetic studies in human epidermis. Epithelia 1, 323-333 (1987).
53. Roop, D. R., H. Huitfeld, A. Kilkenny, S. H. Yuspa: Regulated expression of differentiation-associated keratins in cultured epidermal cells detected by monospecific antibodies to unique peptides of mouse epidermal keratins. Differentiation 35, 143-150 (1987).
54. Roskelley, C. D., A. Srebrow, M. J. Bissell: A hierarchy of ECM-mediated signalling regulates tissue-specific gene expression, Curr. Opin. Cell Biol. 7, 736-747 (1995).
55. Rousselle, P., G. P. Lunstrum, D. R. Keene, R. E. Burgeson: Kalinin: an epithelium-specific basement membrane adhesion molecule that is a component of anchoring filaments. J. Cell Biol. 114, 567-576 (1991).
56. Ruoslahti, E., J. C. Reed: Anchorage dependence, integrins and apoptosis. Cell 77, 477-478 (1994).
57. Ryle, C. M., D. Breitkreutz, H.-J. Stark, I. M. Leigh, P. M. Steinert, D. R. Roop, N. E. Fusenig: Density-dependent modulation of synthesis of keratins 1 and 10 in the human keratinocyte line HaCaT and in ras-transfected tumorigenic clones. Differentiation 40, 42-54 (1989).
58. Sato, C., R. Tsuboi, C.-M. Shi, J. S. Rubin, H. Ogawa: Comparative study of hepatocyte growth factor/scatter factor and keratinocyte growth factor effects on human keratinocytes. J. Investig. Dermatol. 104, 958-963 (1995).
59. Scharffetter-Kochanek, K., C. E. Klein, G.Heinen, C. Mauch, T. Schaefer, B. C. Adelmann-Grill, G. Goerz, N. E. Fusenig, T. Krieg, G. Plewig: Migration of a human keratinocyte cell line (HaCaT) to interstitial collagen type I is mediated by the α2β1 integrin receptor. J. Investig. Dermatol. 98, 3-11 (1992).
60. Seltzer, J. L., A.-Y. Lee, K. T. Akers, B. Sudbeck, E. A. Southon, E. A. Wayner, A. Z. Eisen: Activation of 72-kDa type IV collagenase/gelatinase by normal fibroblasts in collagen lattices is mediated by integrin receptors but is not related to lattice contraction. Exp. Cell Res. 213, 365-374 (1994).
61. Slavin, J.: The role of cytokines in wound healing. J. Pathol. 178, 5-10 (1996).
62. Smola, H., G. Thiekötter, N. E. Fusenig: Mutual induction of growth factor gene expression by epidermal-dermal cell interaction. J. Cell Biol. 122, 417-429 (1993).
63. Sollberg, S., J. Ryynänen, D. R. Olsen, J. Uitto: Transforming growth factor-β up-regulates the expression of the genes for β4 integrin and bullous pemphigoid antigens (BPAG1 and BPAG2) in normal and transformed human keratinocytes. J. Investig. Dermatol. 99, 409-414 (1992).
64. Sonnenberg, A., J. Calafat, H. Janssen, H. Daams, L. M. H. Van der Raaij-Helmer, R. Falcioni, S. J. Kennel, J. D. Aplin, J. Baker, M. Loizidou, D. Garrod: Integrin α6β4 complex is located in hemidesmosomes, suggesting a major role in epidermal cellbasement membrane adhesion. J. Cell Biol. 113, 907-917 (1991).
65. Stanley, J. R., T. Tanaka, S. Mueller, V. Klaus-Kovtun, D. R. Roop: Isolation of complementary DNA for bullous pemphigoid antigen by use of patients' autoantibodies. J. Clin. Invest. 82, 1864-1870 (1988).
66. Stark, H.-J., D. Breitkreutz, A. Limat, P. E. Bowden, N. E. Fusenig: Keratins of the human hair follicle. "Hyperproliferative" keratins consistently expressed in outer root sheath cells in vivo and in vitro. Differentiation 35, 236-248 (1987).
67. Tennenbaum, T., L. Li, A. J. Belanger, L. M. DeLuca, S. H. Yuspa: Selective changes in laminin adhesion and α6β4 integrin regulation are associated with the initial steps in keratinocyte maturation. Cell Growth Differ. 7, 615-628 (1996).
68. Timpl, R.: Macromolecular organization of basement membranes. Curr. Opin. Cell Biol. 8, 618-624 (1996).
69. Watt, F. M.: Epidermal integrins. In: I. M. Leigh, E. B. Lane, F. M. Watt (eds.): The Keratinocyte Handbook, pp. 153-164. Cambridge University Press. Cambridge 1994.
70. Watt, F. M., P. Boukamp, J. Hornung, N. E. Fusenig: Effect of growth environment on spatial expression of involucrin by human epidermal keratinocytes. Arch. Dermatol. Res. 279, 335-340 (1987).
71. Werb, Z., P. M. Tremble, O. Behrendtsen, E. Crowley, C. H. Damsky: Signal transduction through the fibronectin receptor induces collagenase and stromelysin gene expression. J. Cell Biol. 109, 877-889 (1989).
72. Werner, S., H. Smola, X. Liao, M. T. Longaker, T. Krieg, P. H. Hofschneider, L. T. Williams: The role of KGF in morphogenesis of epithelium and re-epithelialization of wounds. Science 266, 819-822 (1994).
73. Yamada, K. M., B. Geiger: Molecular interactions in cell adhesion complexes. Curr. Opin. Cell Biol. 9, 76-85 (1997).
74. Zambruno, G., P. C. Marchisio, A. Marconi, C. Vaschierei, A. Melchiori, A. Giannetti, M. DeLuca: Transforming growth factorβ1 modulates β1 and β5 integrin receptors and induces the de novo expression of the αvβ6 heterodimer in normal human keratinocytes: implications for wound healing. J. Cell Biol. 129, 853-865 (1995).