Epidermal organization and differentiation of HaCat keratinocytes in organotypic coculture with human dermal fibroblasts

Journal of Investigative Dermatology

Volumn 112, Issue 3, 1999, Pages 343-353

  Schoop, Veronika M ^a   Mirancea, Nicolae ^b   Fusenig, Norbert E ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b INSTITUTE OF BIOLOGY   (Romania)

Author keywords

Collagen gel; Epidermal morphogenesis; Epithelial mesenchymal interaction; Skin equivalent

Indexed keywords

COLLAGEN GEL; DNA; FILAGGRIN; INVOLUCRIN; KERATIN; LORICRIN;

ARTICLE; CELL DIFFERENTIATION; DERMIS; EPIDERMIS; FIBROBLAST CULTURE; GENE EXPRESSION; HUMAN; HUMAN CELL; KERATINOCYTE; MESENCHYME CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION;

BASEMENT MEMBRANE; BIOLOGICAL MARKERS; CELL COMMUNICATION; CELL DEATH; CELL DIFFERENTIATION; CELL DIVISION; CELL LINE; COCULTURE TECHNIQUES; EPIDERMIS; FIBROBLASTS; HUMANS; KERATINOCYTES; ORGAN CULTURE TECHNIQUES; SKIN;

EID: 0033017076     PISSN: 0022202X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1523-1747.1999.00524.x     Document Type: Article

References (69)

1. Aaronson SA: Growth factors and cancer. Science 254:1146-1153, 1991
2. Asselineau D, Bernard BA, Bailly C, Darmon M: Retinoic acid improves epidermal morphogenesis. Dev Biol 133:322-335, 1989
3. Bell E, Ehrlich HP, Buttle DJ, Nakatsuji T: Living tissue formed in vitro and accepted as skin-equivalent tissue of full thickness. Science 211:1052-1054, 1981
4. Bernerd F, Asselineau D: Successive alteration and recovery of epidermal differentiation and morphogenesis after specific UVB-damages in skin reconstructed in vitro. Dev Biol 183:123-138, 1997
5. Bikle DD, Gee E, Pillai S: Regulation of keratinocyte growth, differentiation and vitamin D metabolism by analogs of 1,25-dihydroxyvitamin D. J Invest Dermatol 101:713-718, 1993
6. Bilbo PR, Nolte CJM, Oleson MA, Mason VS, Parenteau NL: Skin in complex culture: The transition from "culture" phenotype to organotypic phenotype. J Toxicol Cutan Ocular Toxicol 12:183-196, 1993
7. Blanton RA, Perez-Reyes N, Merrick DT, McDougall JK: Epithelial cells immortalized by human papillomaviruses have premalignant characteristics in organotypic culture. Am J Pathol 138:673-685, 1991
8. Boukamp P, Dzarliewa-Petrusevska RT, Breitkreutz D, Hornung J, Markham A, Fusenig NE: Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J Cell Biol 106:761-771, 1988
9. Boukamp P, Breitkreutz D, Hülsen A, Tomakidi P, Fusenig NE. In vitro transformation and tumor progression: A multistep model for skin carcinogenesis. In: Leigh IM, Lane EB, Watt FM (eds). The Keratinocyte Handbook Cambridge University Press, 1994, pp. 485-499
10. Boukamp P, Popp S, Altmeyer S, Hülsen A, Fasching C, Cremer T, Fusenig NE: Sustained nontumorigenic phenotype correlates with a largely stable chromosome content during long term culture of the human keratinocyte line HaCaT. Genes Chromosomes Cancer 19:201-214, 1997
11. Boyce ST: Cultured skin substitutes: a review. Tissue Eng 2:225-266, 1996
12. Boyce ST, Williams ML: Lipid supplemented medium induces lamellar bodies and precursors of barrier lipids in cultured analogues of human skin. J Invest Dermatol 101:180-184, 1993
13. 2+. Differentiation 54:201-217, 1993
14. Breitkreutz D, Stark HJ, Mirancea N, Tomakidi P, Steinbauer H, Fusenig NE: Integrin and basement membrane normalization in mouse grafts of human keratinocytes-implications for epidermal homeostasis. Differentiation 61:195-209, 1997
15. Breitkreutz D, Schoop VM, Mirancea N, Baur M, Stark HJ, Fusenig NE: Epidermal differentiation and basement membrane formation by HaCaT cells in surface transplants. Eur J Cell Biol 75:273-286, 1998
16. Contard P, Bartel RL, Jacobs L, et al: Culturing keratinocytes and fibroblasts in a three-dimensional mesh results in epidermal differentiation and formation of a basal lamina-anchoring zone. J Invest Dermatol 100:35-39, 1993
17. Coulomb B, Dubertret L: Production and use of skin cell cultures for the in vitro testing of chemicals and pharmaceuticals. Anim Cell Biotechnol 5:123-149, 1992
18. Coussens LM, Hanahan D, Arbeit JM: Genetic predisposition and parameters of malignant progression in K14-HPV 16 transgenic mice. Am J Pathol 149:1899-1917, 1996
19. Cross M, Dexter TM: Growth factors in development, transformation, and tumorigenesis. Cell 64:271-280, 1991
20. Fartasch M, Ponec M: Improved barrier structure formation in air-exposed human culture systems. J Invest Dermatol 102:366-374, 1994
21. Fleischmajer R, MacDonald ED, Contard P, Perlish JS: Immunochemistry of a keratinocyte-fibroblast co-culture model for reconstruction of human skin. J Histochem Cytochem 41:1359-1366, 1993
22. Fuchs E: Epidermal differentiation and keratin gene expression. J Cell Sci 17:197-208, 1993
23. Fusenig NE: Epithelial-mesenchymal interactions regulate keratinocyte growth and differentiation in vitro. In: Leigh I, Lane B, Watt F (eds). The Keratinocyte Handbook. Cambridge University Press, 1994a, pp. 71-94
24. Fusenig NE: Cell culture models: Reliable tools in pharmacology? In: Fusenig NE, Graf H (eds). Cell Culture in Pharmaceutical Research. Berlin: Springer-Verlag, 1994b, pp. 1-7
25. Fusenig NE, Worst PKM: Mouse epidermal cell cultures: II. Isolation, characterization, and cultivation of epidermal cells from perinatal mouse skin. Exp Cell Res 93:443-457, 1975
26. Fusenig NE, Boukamp P, Breitkreutz D, Hülsen A. Altered regulation of growth and differentiation at different stages of transformation of human skin keratinocytes. In: Rhim JS, Dritschilo A (eds). Neoplastic Transformation in Human Cell Culture. Totowa, NJ: Humana Press, 1991, pp. 235-250
27. Game SM, Hülsen A, Patel V, et al: Progressive abrogation of TGF-β1 and EGF growth control is associated with tumor progression in ras-transfected human keratinocytes. Int J Cancer 52:461-470, 1992
28. Garlick JA, Taichman LB: Fate of human keratinocytes during reepithelialization in an organotypic culture model. Lab Invest 70:916-924, 1994
29. Gavrieli Y, Sherman Y, Ben-Sasson SA: Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 199:493-501, 1992
30. Gay R, Swiderek M, Nelson D, Ernesti A: The living skin equivalent as a model in vitro for ranking the toxic potential of dermal irritants. Toxic In Vitro 6:303-315, 1992
31. 3. Arch Dermatol Res 288:729-738, 1996
32. Gibbs S, Vicanova J, Bouwstra J, Valstar D, Kempenaar J, Ponec M: Culture of reconstructed epidermis in a defined medium at 33°C shows a delayed epidermal maturation, prolonged lifespan and improved stratum corneum. Arch Dermatol Res 289:585-595, 1997
33. Gniadecki R, Hansen M, Wulf HC: Two pathways for induction of apoptosis by ultraviolet radiation in cultured human keratinocytes. J Invest Dermatol 109:163-169, 1997
34. Grabbe J, Welker P, Rosenbach T, et al: Release of stem cell factor from a human keratinocyte line, HaCaT, is increased in differentiating versus proliferating cells. J Invest Dermatol 107:219-224, 1996
35. Haake AR, Polakowska RR: UV-induced apoptosis in skin equivalents: inhibition by phorbol ester and Bcl-2 overexpression. Cell Death Diff 2:183-193, 1995
36. Lechner MS, Laimins LA: Human epithelial cells immortalized by SV40 retain differentiation capabilities in an in vitro raft system and maintain viral DNA extrachromosomally. Virology 185:563-571, 1991
37. 3 metabolism in human skin. J Invest Dermatol 108:78-82, 1997
38. Lehmann TA, Modali R, Boukamp P, et al: P53 mutations in immortalized epithelial cell lines. Carcinogenesis 14:833-839, 1993
39. Leigh I, Purkis PE, Bruckner-Tuderman E: LH7.2 monoclonal antibody detects type VII collagen in the sublamina densa zone of ectodermally-derived epithelia, including skin. Epithelia 1:17-29, 1987
40. Leigh IM, Navsaria H, Purkis PE, McKay IA, Bowden PE, Riddle PN: Keratins (K16 and K17) as markers of keratinocyte hyperproliferation in psoriasis in vivo and in vitro. Br J Dermatol 133:501-511, 1995
41. 3 and calcipotriol on organotypic cultures of outer root sheath cells: a potential model to evaluate antipsoriatic drugs. Arch Dermatol Res 285:402-409, 1993
42. Limat A, Mauri D, Hunziker T: Successful treatment of chronic leg ulcers with epidermal equivalents generated from cultured autologous outer root sheath cells. J Invest Dermatol 107:128-135, 1996
43. Mansbridge JN, Knapp AM: Changes in keratinocyte maturation during wound healing. J Invest Dermatol 89:253-263, 1987
44. Marinkovich MP, Keene DR, Rimberg CS, Burgeson RE: Cellular origin of the dermal-epidermal basement membrane. Dev Dyn 197:255-267, 1993
45. McCall CA, Cohen JJ: Programmed cell death in terminally differentiating keratinocytes: role of endogenous endonuclease. J Invest Dermatol 97:111-114, 1991
46. Moll R, Franke WW, Schiller DL: The catalog of human cytokeratins: Patterns of expression in normal epithelia, tumors and cultures cells. Cell 31:11-24, 1982
47. Nolte CJ, Oleson MA, Bilbo PR, Parenteau NL: Development of a stratum corneum and barrier function in an organotypic skin culture. Arch Dermatol Res 285:466-74, 1993
48. Oda D, Bigler L, Lee P, Blanton R: HPV immortalization of human oral epithelial cells: a model for carcinogenesis. Exp Cell Res 226:164-169, 1996
49. Parenteau NL, Nolte CM, Bilbo P, et al: Epidermis generated in vitro: Practical considerations and applications. J Cell Biochem 45:245-251, 1991
50. Polakowska RR, Haake AR: Apoptosis: the skin from a new perspective. Cell Death Diff 1:19-31, 1994
51. Ponec M: Reconstruction of human epidermis on de-epidermized dermis: expression of differentiation specific protein markers and lipid composition. Toxic In Vitro 5:597-606, 1991
52. Ponec M, Gibbs S, Weerheim A, Kempenaar J, Mulder A, Mommaas AM: Epidermal growth factor and temperature regulate keratinocyte differentiation. Arch Dermatol Res 289:317-326, 1997a
53. Ponec M, Weerheim A, Kempenaar J, Mulder A, Gooris GS, Bouwstra J, Mommaas AM: The formation of competent barrier lipids in reconstructed human epidermis requires the presence of vitamin C. J Invest Dermatol 109:348-355, 1997b
54. Regnier M, Darmon M: 1,25-dihydroxyvitamin D3 stimulates specifically the last steps of epidermal differentiation of cultured human keratinocytes. Differentiation 47:173-188, 1991
55. Reichert U, Michel S, Schmidt R. The cornified envelope: a key structure of terminally differentiating keratinocytes. In: Darmon M, Blumberg M (eds). The Keratinocyte Molecular Biology of the Skin. New York: Academic Press, 1994, pp. 71-94
56. Rheinwald JG, Green H: Serial cultivation of strains of human epidermal keratinocytes: The formation of keratinizing colonies from single cells. Cell 6:331-344, 1975
57. Rosdy M, Clauss LC: Terminal epidermal differentiation of human keratinocytes grown in chemically defined medium on inert filter substrates at the air-liquid interface. J Invest Dermatol 95:409-414, 1990
58. Ryle CM, Breitkreutz D, Stark HJ, Leigh IM, Steinert PM, Roop DR, Fusemg NE: Density dependent modulation of sysnthesis of keratin 1 and 10 in the human keratinocyte line HaCaT and in ras-transfected tumorigenic clones. Differentiation 40:42-54, 1989
59. Sarber R, Hull B, Merrill C, Soranno T, Bell E: Regulation of proliferation of fibroblasts of low and high population doubling levels grown in collagen lattices. Mech Ageing Dev 17:107-117, 1981
60. Scharffetter-Kochanek K, Klein CE, Keinen G, et al: Migration of a human keratinocyte cell line (HaCaT) to interstitial collagen type I is mediated by the alpha 2 beta 1-integrin receptor. J Invest Dermatol 98:3-11, 1992
61. Smola H, Thiekötter G, Fusenig NE: Mutual induction of growth factor gene expression by epidermal-dermal cell interaction. J Cell Biol 122:417-429, 1993
62. Smola H, Stark HJ, Thiekötter G, Mirancea N, Krieg T, Fusenig NE: Dynamics of basement membrane formation by keratinocyte-fibroblast interactions in organotypic skin culture. Exp Cell Res 239:399-410, 1998
63. Stark HJ, Baur M, Breitkreutz D, Mirancea N, Fusenig NE: Organotypic cultures with regular epidermal morphogenesis and differentiation in defined medium. J Invest Dermatol 1999, in press
64. Steinsträsser I, Koopmann K, Merkle HP: Epidermal aminopeptidase activity and metabolism as observed in an organized HaCaT cell sheet model. J Pharm Sci 86:378-383, 1997
65. Syrjänen S, Mikola H, Nykänen M, Hukkanen V: In vitro establishment of lytic and nonproductive infection by herpes simplex virus type 1 in three-dimensional keratinocyte culture. J Virol 70:6524-6528, 1996
66. Timpl R: Macro molecular organization of basement membranes. Curr Opin Cell Biol 8:618-624, 1996
67. 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 85:238-244, 1994
68. Werner S, Peters KG, Longaker MT, Fuller-Pace F, Banda MJ, Williams LT: Large induction of keratinocyte growth factor expression in the dermis during wound healing. Proc Natl Acad Sci USA 98:6896-6900, 1992
69. Wilson JL, Dollard SC, Chow LT, Broker TR: Epithelial-specific gene expression during differentiation of stratified primary human keratinocyte cultures. Cell Growth Differ 3:471-483, 1992