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Development, Vol 120, Issue 9 2369-2383, Copyright © 1994 by Company of Biologists

JOURNAL ARTICLES

Programming gene expression in developing epidermis

C Byrne, M Tainsky and E Fuchs
Howard Hughes Medical Institute, Department of Molecular Genetics and Cell Biology, University of Chicago, IL 60637.

As the major proteins of adult keratinocytes, keratins provide biochemical markers for exploring mouse epidermal embryogenesis. Here, we used a modified method of whole-mount in situ hybridization to track skin-specific expression of endogenous keratin mRNAs throughout embryogenesis. To monitor transcriptional regulation, we coupled this with beta-galactosidase expression of a human epidermal keratin promoter-driven transgene. These studies have radically changed our perception of how the program of gene expression becomes established during epidermal development. Specifically, we have discovered that (1) basal keratin (K5 and K14) genes are first detected at E9.5 in a highly regional fashion, and surprisingly as early as the single layered ectodermal stage; (2) the early patterns do not correlate with morphogenesis per se, but rather with regional variations in the embryonic origin of underlying mesenchyme, supporting morphogenetic criteria that early inductive cues are mesenchymal; (3) epidermal keratin genes are expressed in periderm, supporting the notion that this layer arises from ectodermal stratification, even though it is simple epithelial-like in morphology and is subsequently sloughed during development; (4) later embryonic patterns of K5 and K14 gene expression parallel proliferative capacity and not stratification; and (5) K1 and K10 mRNAs are first detected as early as E13.5, and their patterns correlate with differentiation and not stratification. These patterns of epidermal gene expression led us to explore whether potential transcriptional regulators of these genes are expressed similarly. We show that AP2 (but not Sp1) cRNAs hybridize in a pattern similar to, but preceding that of basal keratin cRNAs. Finally, using gene expression in cultured cells, we demonstrate that AP2 has a strong inductive effect on basal keratin expression in a cellular environment that does not normally possess AP2 activity.
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Directed Expression of Keratin 16 to the Progenitor Basal Cells of Transgenic Mouse Skin Delays Skin Maturation
J. Cell Biol., August 24, 1998; 142(4): 1035 - 1051.
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 Proc. Natl. Acad. Sci. USAHome page
C. S. Seitz, Q. Lin, H. Deng, and P. A. Khavari
Alterations in NF-kappa B function in transgenic epithelial tissue demonstrate a growth inhibitory role for NF-kappa B
PNAS, March 3, 1998; 95(5): 2307 - 2312.
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 Proc. Natl. Acad. Sci. USAHome page
M. Matsuki, F. Yamashita, A. Ishida-Yamamoto, K. Yamada, C. Kinoshita, S. Fushiki, E. Ueda, Y. Morishima, K. Tabata, H. Yasuno, et al.
Defective stratum corneum and early neonatal death in mice lacking the gene for transglutaminase 1 (keratinocyte transglutaminase)
PNAS, February 3, 1998; 95(3): 1044 - 1049.
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 DevelopmentHome page
M. Hardman, P Sisi, D. Banbury, and C Byrne
Patterned acquisition of skin barrier function during development
Development, January 4, 1998; 125(8): 1541 - 1552.
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 J. Biol. Chem.Home page
B. Andersen, A. Hariri, M. R. Pittelkow, and M. G. Rosenfeld
Characterization of Skn-1a/i POU Domain Factors and Linkage to Papillomavirus Gene Expression
J. Biol. Chem., June 20, 1997; 272(25): 15905 - 15913.
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 J. Biol. Chem.Home page
W. Johnson, C. Albanese, S. Handwerger, T. Williams, R. G. Pestell, and J. L. Jameson
Regulation of the Human Chorionic Gonadotropin alpha - and beta -Subunit Promoters by AP-2
J. Biol. Chem., June 13, 1997; 272(24): 15405 - 15412.
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 Proc. Natl. Acad. Sci. USAHome page
X. Wang, S. Zinkel, K. Polonsky, and E. Fuchs
Transgenic studies with a keratin promoter-driven growth hormone transgene: Prospects for gene therapy
PNAS, January 7, 1997; 94(1): 219 - 226.
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J. J. LaPres and L. G. Hudson
Identification of a Functional Determinant of Differentiation-dependent Expression in the Involucrin Gene
J. Biol. Chem., September 20, 1996; 271(38): 23154 - 23160.
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 J. Biol. Chem.Home page
G. N. Sando, E. J. Howard, and K. C. Madison
Induction of Ceramide Glucosyltransferase Activity in Cultured Human Keratinocytes. CORRELATION WITH CULTURE DIFFERENTIATION
J. Biol. Chem., September 6, 1996; 271(36): 22044 - 22051.
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 DevelopmentHome page
H Yoshida, T Kunisada, M Kusakabe, S Nishikawa, and S. Nishikawa
Distinct stages of melanocyte differentiation revealed by anlaysis of nonuniform pigmentation patterns
Development, January 4, 1996; 122(4): 1207 - 1214.
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J. M. Navarro, J. Casatorres, and J. L. Jorcano
Elements Controlling the Expression and Induction of the Skin Hyperproliferation-associated Keratin K6
J. Biol. Chem., September 8, 1995; 270(36): 21362 - 21367.
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K. Takahashi, R. D. Paladini, and P. A. Coulombe
Cloning and Characterization of Multiple Human Genes and cDNAs Encoding Highly Related Type II Keratin 6 Isoforms
J. Biol. Chem., August 4, 1995; 270(31): 18581 - 18592.
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 Genes Dev.Home page
P Zhou, C Byrne, J Jacobs, and E Fuchs
Lymphoid enhancer factor 1 directs hair follicle patterning and epithelial cell fate.
Genes & Dev., March 15, 1995; 9(6): 700 - 713.
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 DevelopmentHome page
M Moser, A Imhof, A Pscherer, R Bauer, W Amselgruber, F Sinowatz, F Hofstadter, R Schule, and R Buettner
Cloning and characterization of a second AP-2 transcription factor: AP-2 beta
Development, January 9, 1995; 121(9): 2779 - 2788.
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 Genes Dev.Home page
Y Chan, I Anton-Lamprecht, Q C Yu, A Jackel, B Zabel, J P Ernst, and E Fuchs
A human keratin 14 "knockout": the absence of K14 leads to severe epidermolysis bullosa simplex and a function for an intermediate filament protein.
Genes & Dev., November 1, 1994; 8(21): 2574 - 2587.
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F. H. Brembeck and A. K. Rustgi
The Tissue-dependent Keratin 19 Gene Transcription Is Regulated by GKLF/KLF4 and Sp1
J. Biol. Chem., September 1, 2000; 275(36): 28230 - 28239.
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C. H. Liu, S.-H. Chang, K. Narko, O. C. Trifan, M.-T. Wu, E. Smith, C. Haudenschild, T. F. Lane, and T. Hla
Overexpression of Cyclooxygenase-2 Is Sufficient to Induce Tumorigenesis in Transgenic Mice
J. Biol. Chem., May 18, 2001; 276(21): 18563 - 18569.
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M. Schuierer, K. Hilger-Eversheim, T. Dobner, A.-K. Bosserhoff, M. Moser, J. Turner, M. Crossley, and R. Buettner
Induction of AP-2alpha Expression by Adenoviral Infection Involves Inactivation of the AP-2rep Transcriptional Corepressor CtBP1
J. Biol. Chem., July 20, 2001; 276(30): 27944 - 27949.
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P. Pfisterer, J. Ehlermann, M. Hegen, and H. Schorle
A Subtractive Gene Expression Screen Suggests a Role of Transcription Factor AP-2alpha in Control of Proliferation and Differentiation
J. Biol. Chem., February 15, 2002; 277(8): 6637 - 6644.
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 Proc. Natl. Acad. Sci. USAHome page
M. J. Karkkainen, A. Saaristo, L. Jussila, K. A. Karila, E. C. Lawrence, K. Pajusola, H. Bueler, A. Eichmann, R. Kauppinen, M. I. Kettunen, et al.
A model for gene therapy of human hereditary lymphedema
PNAS, October 23, 2001; 98(22): 12677 - 12682.
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