The spatial relationship between stem cells and their progeny in the basal layer of human epidermis: A new view based on whole-mount labelling and lineage analysis

Development

Volumn 126, Issue 11, 1999, Pages 2409-2418

  Jensen, Uffe B ^a   Lowell, Sally ^a   Watt, Fiona M ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

Epidermis; GFP; Human; Integrin; Lineage analysis; p53; Stem cell

Indexed keywords

BROXURIDINE; GREEN FLUORESCENT PROTEIN; INTEGRIN; KERATIN; KI 67 ANTIGEN; MONOCLONAL ANTIBODY; PROTEIN P53;

ARTICLE; BASEMENT MEMBRANE; CELL CULTURE; CELL DIFFERENTIATION; CELL LINEAGE; CELL MIGRATION; CELL MOTILITY; CELL SIZE; CYTOARCHITECTURE; DERMIS; EPIDERMIS; GENE CLUSTER; GENETIC MARKER; HUMAN; HUMAN TISSUE; IMMUNOFLUORESCENCE; KERATINOCYTE; MOLECULAR CLONING; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; STEM CELL; SUN EXPOSURE;

ANTIGENS, CD29; BIOLOGICAL MARKERS; BROMODEOXYURIDINE; CELL DIFFERENTIATION; CELL DIVISION; CELL LINEAGE; CELL MOVEMENT; CELLS, CULTURED; CLONE CELLS; COLLAGEN; EPIDERMIS; FLUORESCENT ANTIBODY TECHNIQUE; GREEN FLUORESCENT PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; KERATIN-10; KERATINOCYTES; KERATINS; KI-67 ANTIGEN; LUMINESCENT PROTEINS; MICROSCOPY, CONFOCAL; POLYPYRIMIDINE TRACT-BINDING PROTEIN; RIBONUCLEOPROTEINS; RNA-BINDING PROTEINS; STEM CELLS;

EID: 0032998902     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (52)

1. 1 integrin loss from the cell surface. Cell 63, 425-435.
2. Akiyama, S. K., Yamada, S. S., Chen, W.-T. and Yamada, K. M. (1989). Analysis of fibronectin receptor function with monoclonal antibodies: roles in cell adhesion, migration, matrix assembly and cyloskeletal organisation. J. Cell. Biol. 109, 863-875.
3. Anbazhagan, R., Bartkova, J., Stamp, G., Pignatelli, M., Gusterson, B. and Bartkova, J. (1995). Expression of integrin subunits in the human infant breast correlates with morphogenesis and differentiation. J. Pathol. 176, 227-232.
4. Banks, L., Matlashewski, G. and Crawford, L. (1986). Isolation of human - p53 - specific monoclonal antibodies and their use in the studies of human p53 expression. Eur. J. Biochem. 159, 529-534.
5. Briggaman, R. A., Yoshiike, T., Cronce, D. J. (1991). The epidermal-dermal junction and genetic disorders of this area. In Physiology, Biochemistry, and Molecular Biology of the Skin. (ed. L. A. Goldsmith). 2nd Ed, vol.2, pp. 1243-1266. Oxford University Press
6. Carayon P, and Bord A (1992). Identification of DNA-replicating lymphocyte subsets using a new method to label the bromo-deoxyuridine incorporated into the DNA. Immunol Methods 147, 225-30
7. Cotsarelis, G., Sun, T.-T. and Lavker, R. M. (1990). Label-retaining cells reside in the bulge area of pilosebaceous unit: implications for follicular stem cells, hair cycle, and skin carcinogenesis. Cell 61, 1329-1337.
8. Dittel, B. N., McCarthy, J. B., Wayner, E. A. and LeBien, T. W. (1993). Regulation of human B-cell precursor adhesion to bone marrow stromal cells by cytokines that exert opposing effects on the expression of vascular cell adhesion molecule -1 (VCAM-1). Blood 81, 2272-2282.
9. Dover, R. and Watt, F. M. (1987). Measurement of the rate of epidermal terminal differentiation: expression of involucrin by S-phase keratinocytes in culture and in psoriatic plaques. J. Invest. Dermatol. 89, 349-352.
10. Foellmer, H. G., Madri, J. A., Furthmayr, H. (1983). Monoclonal antibodies to type IV collagen: probes for the study of structure and function of basement membranes. Lab. Invest. 48, 639-649
11. Gandarillas, A. and Watt, F. M. (1997). c-Myc promotes differentiation of human epidermal stem cells. Genes Dev. 11, 2869-2882.
12. Godt, D. and Tepass, U. (1998). Drosophila oocyte localization is mediated by differential cadherin-based adhesion. Nature 395, 387-391.
13. Greenblatt, M. A., Bennett, W. P., Hollstein, M., Harris, C. C. (1994). Mutations in the p53 tumor suppressor gene: clues to cancer etiology and molecular pathogenesis. Cancer Res. 54, 4855-4879.
14. Hall, P. A. and Watt, F. M. (1989). Stem cells: the generation and maintenance of cellular diversity. Development 106, 619-633.
15. Heyworth, C. M., Testa, N. G., Buckle, A.-M. and Whetton, A. D. (1997). Growth factors and the regulation of haemopnietic stem cells. In Stem Cells. Ed CS Potten, Pub Academic Press, London pp. 423-445.
16. Hodivala, K. J. and Watt, F. M. (1994). Evidence that cadherins play a role in the downregulation of integrin expression that occurs during keratinocyte terminal differentiation. J. Cell Biol. 124, 589-600.
17. Hotchin, N. A., Gandarillas, A. and Watt, F. M. (1995). Regulation of cell surface β1 integrin levels during keratinocyte terminal differentiation. J. Cell Biol. 128, 1209-1219.
18. Huttenlocher, A., Sandborg, R. R. and Horwitz, A. F. (1995). Adhesion in cell migration. Curr. Opin. Cell Biol. 7, 697-706.
19. Huttenlocher, A., Lakonishok, M., Kinder, M., Wu, S., Truong, T., Knudsen, K. A. and Horwitz, A. F. (1998). Integrin and cadherin synergy regulates contact inhibition of migration and motile activity. J. Cell Biol. 141, 515-526.
20. Iizuka, H., Ishida-Yamamoto, A. and Honda, H. (1996). Epidermal remodelling in psoriasis. Br. J. Dermatol. 135, 433-438.
21. Iizuka, H. and Ishida-Yamamoto, A. (1997). Another support for the location of epidermal stem cells residing adjacent to the tips of dermal papillae in the interfollicular epidermis (letter). J. Invest. Dermatol. 109, 697.
22. Iizuka, H., Honda, H. and Ishida-Yamamoto, A. (1997). Epidermal remodelling in psoriasis (II): a quantitative analysis of the epidermal architecture. J. Invest. Dermatol. 109, 806-810.
23. Iversen, O. H., Bjerknes, R. and Devik, F. (1968). Kinetics of cell renewal, cell migration and cell loss in the hairless mouse dorsal epidermis. Cell Tissue Kinet. 1, 351-367.
24. Jonason, A. S., Kunala, S., Price, G. J., Restifo, R., Spinelli, H. M., Persing, J. A., Leffell, D.J., Tarone, R. E., Brash, D. E. (1996). Frequent clones of p53-mutated keratinocytes in normal human skin. Proc. Natl. Acad. Sci. USA 93, 14025-14029.
25. Jones, P. H., Watt, F. M. (1993). Separation of human epidermal stem cells from transit amplifying cells on the basis of differences in integrin function and expression. Cell 73, 713-724.
26. Jones, P. H., Harper, S., Watt, F. M. (1995). Stem cell patterning and fate in human epidermis. Cell 80, 83-93.
27. Jones, P. H. (1997). Epithelial stem cells. BioEssays 19, 683-690.
28. Kolodka, T. M., Garlick, J. A. and Taichman, L. B. (1998). Evidence for keratinocyte stem cells in vitro: long term engraftment and persistence of transgene expression from retrovirus-transduced keratinocytes. Proc. Natl. Acad. Sci. USA 95, 4356-4361.
29. Lajtha, L. G. (1979). Stem cell concepts. Differentiation 14, 23-34.
30. Lavker, R. M. and Sun, T.-T. (1983). Epidermal stem cells. J. Invest. Dermatol. (Suppl.) 81, 121S-127S.
31. Leigh, I. M., Purkis, P. E., Whitehead, P. and Lane, E. B. (1993). Monospecific monoclonal antibodies to keratin 1 carboxy terminal (synthetic peptide) and to keratin 10 as markers of epidermal differentiation. Br. J. Dermatol. 129, 110-119.
32. Markowitz, D., Goff, S. and Bank, A. (1988). Construction and use of a safe and efficient amphotropic packaging cell line. Virology 167, 400-406.
33. Mehregan, A. H. and Hashimoto, K. (1991). Epidermal architecture. In Pinkus' Guide to Dermatohistopathology, 5th Ed. pp 13-15. London: Prentice-Hall.
34. Molès, J.-P. and Watt, F. M. (1997). The epidermal stem cell compartment: variation in expression levels of E-cadherin and catenins within the basal layer of human epidermis. J. Histochem. Cytochem. 45, 867-874.
35. Morgenstern, J. P. and Land, H. (1990). Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper - free packaging cell line. Nucl. Acids Res. 18, 3587-3596.
36. Morrison, S. J., Shah, N. M. and Anderson, D. J. (1997). Regulatory mechanisms in stem cell biology. Cell 88, 287-298
37. Ng, R. L. H., Woodward, B., Bevan, S., Green, C. and Martin, R. (1997). Retroviral marking identifies grafted autologous keratinocytes in porcine wounds receiving cultured epithelium. J. Invest Dermatol. 108, 457-462.
38. Potten, C. S. (1981). Cell replacement in epidermis (keratopoiesis) via discrete units of proliferation. Int. Rev. Cytol. 69, 271-318.
39. Potten, C. S. and Morris, R. J. (1988). Epithelial stem cells in vivo. J. Cell Sci. Suppl. 10, 45-62.
40. Régnier, M., Vaigot, P., Darmon, M., Pruniéras, M. (1986). Onset of epidermal differentiation in rapidly proliferating basal keratinocytes. J. Invest. Dermatol. 87, 472-476.
41. Ren, Z.-P., Ahmadian, A., Pontén, F., Nistér, M., Berg, C., Lundeberg, J., Uhlén, M. and Pontén, J. (1997). Benign clonal keratinocyte patches with p53 mutations show no genetic link to synchronous squamous cell precancer or cancer in human skin. Am. J. Pathol. 150, 1791-1803.
42. Rheinwald, J. G. (1989). Methods for clonal growth and serial cultivation of normal human epidermal keratinocytes and mesothelial cells. In Cell Growth and Division. A Practical Approach. (ed. R. Baserga). pp. 81-94. Oxford: IRL Press.
43. Schliiter, C., Duchrow, M., Wohlenberg, C., Becker, M. H. G., Key, G., Flad, H.-D. and Gerdes, J. (1993). The cell proliferation - associated antigen of antibody Ki-67: a very large, ubiquitous nuclear protein with numerous repeated elements, representing a new kind of cell cycle -maintaining proteins. J. Cell Biol. 123, 513-522.
44. Schmidt, G. H., Winton, D. J. and Ponder, B. A. J. (1988). Development of the pattern of cell renewal in the crypt-villus unit of chimaeric mouse small intestine. Development 103, 785-790.
45. Schweizer, J., Kinjo, M., Fürstenberger, G. and Winter, H. (1984). Sequential expression of mRNA-encoded keratin sets in neonatal mouse epidermis: basal cells with properties of terminally differentiating cells. Cell 37, 159-170.
46. Sonnenberg, A., Calafat, J., Janssen, H., Daams, H., van der Raaij-Helmer, L. M. H., Falcioni, R., Kennel, S. J., Aplin, J. D., Baker, J., Loizidou, M. and Garrod, D. (1991). Integrin α6/β4 complex is located in hemidesmosomes, suggesting a major role in epidermal cell-basement membrane adhesion. J. Cell. Biol. 113, 907-917.
47. Stepp, M. A., Spurr-Michaud, S., Tisdale, A., Elwell, J. and Gipson, I. K. (1990). α6β4 integrin heterodimer is a component of hemidesmosomes. Proc. Natl. Acad. Sci. USA 87, 8970-8974.
48. Watt, F. M. and Green, H. (1981). Involucrin synthesis is correlated with cell size in human epidermal cells. J. Cell Biol. 90, 738-742.
49. Watt, F. M. (1998). Epidermal stem cells: markers, patterning and the control of stem cell fate. Phil. Trans. R. Soc. Land. B 353, 831-837.
50. Zhu, A. J. and Watt, F. M. (1996). Expression of a dominant negative cadherin mutant inhibits proliferation and stimulates terminal differentiation of human epidermal keratinocytes. J. Cell Sci. 109, 3013-3023.
51. Zhu, A. J. and Watt, F. M. (1999). ß-Catenin signalling modulates human epidermal stem cell fate independently of intercellular adhesion. Development (in press).
52. Ziegler, A., Jonason, A. S., Leffell, D. J., Simon, J. A., Sharma, H. W., Kimmelman, J., Remington, L., Jacks, T. and Brash, D. E. (1994). Sunburn and p53 in the onset of skin cancer. Nature 372, 773-776.