Cross-talk between epidermal growth factor receptor and protein kinase C during calcium-induced differentiation of keratinocytes

Experimental Dermatology

Volumn 9, Issue 3, 2000, Pages 192-199

  Denning, M F ^a,b   Dlugosz, A A ^a,c   Cheng, C ^a   Dempsey, P J ^d   Coffey Jr , R J ^d   Threadgill, D W ^e   Magnuson, T ^f   Yuspa, Stuart H ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b LOYOLA UNIVERSITY MEDICAL CENTER   (United States)

^c UNIVERSITY OF MICHIGAN COMPREHENSIVE CANCER CENTER   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

^e VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Differentiation; Epidermal growth factor receptor; Keratinocyte; Protein kinase C; Transforming growth factor alpha; Tyrosine kinase

Indexed keywords

CALCIUM; EPIDERMAL GROWTH FACTOR RECEPTOR; PROTEIN KINASE C; PROTEIN TYROSINE KINASE; TRANSFORMING GROWTH FACTOR ALPHA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CELL DIFFERENTIATION; ENZYME ACTIVATION; EXTRACELLULAR CALCIUM; KERATINOCYTE; MOUSE; NEWBORN; NONHUMAN; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION;

ANIMALS; CALCIUM; CELL DIFFERENTIATION; CELLS, CULTURED; EPIDERMIS; ISOENZYMES; KERATINOCYTES; MICE; MICE, KNOCKOUT; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN KINASE C-DELTA; RECEPTOR CROSS-TALK; RECEPTOR, EPIDERMAL GROWTH FACTOR; TRANSFORMING GROWTH FACTOR ALPHA; TYROSINE;

EID: 0034058769     PISSN: 09066705     EISSN: None     Source Type: Journal    
DOI: 10.1034/j.1600-0625.2000.009003192.x     Document Type: Article

References (52)

1. Punnonen K, Denning M, Lee E, Li L, Rhee S G, Yuspa S H. Keratinocyte differentiation is associated with changes in the expression and regulation of phospholipase C isoenzymes. J Invest Dermatol 1993: 101: 719-726.
2. Lee E, Yuspa S H. Changes in inositol phosphate metabolism are associated with terminal differentiation and neoplasia in mouse keratinocytes. Carcinogenesis 1991: 12: 1651-1658.
3. 2+-mediated inositol lipid metabolism in normal and neoplastic epidermal cells. Carcinogenesis 1988: 9: 1033-1038.
4. 2+-induced keratinocyte differentiation. Selective blockade of MARCKS phosphorylation by calmodulin. J Biol Chem 1995: 270: 1362-1368.
5. Matsui M S, Chew S L, DeLeo V A. Protin kinase C in normal human epidermal keratinocytes during proliferation and calcium-induced differentiation. J Invest Dermatol 1992: 99: 565-571.
6. Denning M F, Dlugosz A A, Williams E K, Szallasi Z, Blumberg P M, Yuspa S H. Specific protein kinase C isozymes mediate the induction of keratinocyte differentiation markers by calcium. Cell Growth Differ 1995: 6: 149-157.
7. Calautti E, Missero C, Stein P L, Ezzell R M, Dotto G P. fyn tyrosine kinase is involved in keratinocyte differentiation control. Genes Dev 1995: 9: 2279-2291.
8. Filvaroff E, Calautti E, McCormick F, Dotto G P. Specific changes of Ras GTPase-activating protein (GAP) and a GAP-associated p62 protein during calcium-induced keratinocyte differentiation. Mol Cell Biol 1992: 12: 5319-5328.
9. Filvaroff E, Calautti E, Reiss M, Dotto G P. Functional evidence for an extracellular calcium receptor mechanism triggering tyrosine kinase activation associated with mouse keratinocyte differentiation. J Biol Chem 1994: 269: 21735-21740.
10. Zhao Y, Sudol M, Hanafusa H, Krueger J. Increased tyrosine kinase activity of c-Src during calcium-induced keratinocyte differentiation. Proc Natl Acad Sci U S A 1992: 89: 8298-8302.
11. Vasioukhin V, Tyner A L. A role for the epithelial-cell-specific tyrosine kinase Sik during keratinocyte differentiation. Proc Natl Acad Sci U S A 1997: 94: 14477-14482.
12. Dlugosz A A, Yuspa S H. Coordinate changes in gene expression which mark the spinous to granular cell transition in epidermis are regulated by protein kinase C. J Cell Biol 1993: 120: 217-225.
13. Takahashi H, Asano K, Manabe A, Kinouchi M, Ishida-Yamamoto A, Iizuka H. The α and η isoforms of protein kinase C stimulate transcription of human involucrin gene. J Invest Dermatol 1998: 110: 218-223.
14. Ohba M, Ishino K, Kashiwagi M et al. Induction of differentiation in normal human keratinocytes by adenovirus-mediated introduction of the eta and delta isoforms of protein kinase C. Mol Cell Biol 1998: 18: 5199-5207.
15. Lee Y S, Yuspa S H, Dlugosz A A. Differentiation of cultured human epidermal keratinocytes at high cell densities is mediated by endogenous activation of the protein kinase C signaling pathway. J Invest Dermatol 1998: 111: 762-766.
16. Ueda E, Ohno S, Kuroki T et al. The eta isoform of protein kinase C mediates transcriptional activation of the human transglutaminase 1 gene. J Biol Chem 1996: 271: 9790-9794.
17. Denning M F, Kazanietz M G, Blumberg P M, Yuspa S H. Cholesterol sulfate activates multiple protein kinase C isoenzymes and induces granular cell differentiation in cultured murine keratinocytes. Cell Growth Differ 1995: 6: 1619-1626.
18. Dlugosz A A, Mischak H, Mushinski J F, Yuspa S H. Transcripts encoding protein kinase C-alpha, -delta, -epsilon, -zeta, and -eta are expressed in basal and differentiating mouse keratinocytes in vitro and exhibit quantitative changes in neoplastic cells. Mol Carcinog 1992: 5: 286-292.
19. Lee Y S, Dlugosz A A, McKay R, Dean N M, Yuspa S H. Definition by specific antisense oligonucleotides of a role for protein kinase C alpha in expression of differentiation markers in normal and neoplastic mouse epidermal keratinocytes. Mol Carcinog 1997: 18: 44-53.
20. Zhang J, Wang L, Petrin J, Bishop W R, Bond R W. Characterization of site-specific mutants altered at protein kinase C beta 1 isozyme autophosphorylation sites. Proc Natl Acad Sci U S A 1993: 90: 6130-6134.
21. Dutil E M, Keranen L M, De Paoli-Roach A A, Newton A C. In vivo regulation of protein kinase C by trans-phosphorylation followed by autophosphorylation. J Biol Chem 1994: 269: 29359-29362.
22. Ha gene in murine keratinocytes induces tyrosine phosphorylation and reduced activity of protein kinase C delta. J Biol Chem 1993: 268: 26079-26081.
23. Cazaubon S M, Parker P J. Identification of the phosphorylated region responsible for the permissive activation of protein kinase C. J Biol Chem 1993: 268: 17559-17563.
24. Denning M F, Dlugosz A A, Threadgill D W, Magnuson T, Yuspa S H. Activation of the epidermal growth factor receptor signal transduction pathway stimulates tyrosine phosphorylation of protein kinase C delta. J Biol Chem 1996: 271: 5325-5331.
25. 2. Proc Natl Acad Sci U S A 1997: 94: 11233-11237.
26. Li W, Yu J C, Michieli P et al. Stimulation of the platelet-derived growth factor beta receptor signaling pathway activates protein kinase C-delta. Mol Cell Biol 1994: 14: 6727-6735.
27. Threadgill D W, Dlugosz A A, Hansen L A et al. Targeted disruption of mouse EGF receptor: effect of genetic background on mutant phenotype. Science 1995: 269: 230-234.
28. Hennings H, Michael D, Cheng C, Steinert P, Holbrook K, Yuspa S H. Calcium regulation of growth and differentiation of mouse epidermal cells in culture. Cell 1980: 19: 245-254.
29. Yuspa S H, Kilkenny A E, Steinert P M, Roop D R. Expression of murine epidermal differentiation markers is tightly regulated by restricted extracellular calcium concentrations in vitro. J Cell Biol 1989: 109: 1207-1217.
30. Galcheva-Gargova Z, Theroux S J, Davis R J. The epidermal growth factor receptor is covalently linked to ubiquitin. Oncogene 1995: 11: 2649-2655.
31. Dlugosz A A, Cheng C, Denning M F, Dempsey P J, Coffey R J Jr, Yuspa S H. Keratinocyte growth factor receptor ligands induce transforming growth factor alpha expression and activate the epidermal growth factor receptor signaling pathway in cultured epidermal keratinocytes. Cell Growth Differ 1994: 5: 1283-1292.
32. Russell W E, Dempsey P J, Sitaric S, Peck A J, Coffey R J Jr. Transforming growth factor-alpha (TGF alpha) concentrations increase in regenerating rat liver: evidence for a delayed accumulation of mature TGF alpha. Endocrinology 1993: 133: 1731-1738.
33. Dlugosz A A, Yuspa S H. Protein kinase C regulates keratinocyte transglutaminase (TGK) gene expression in cultured primary mouse epidermal keratinocytes induced to terminally differentiate by calcium. J Invest Dermatol 1994: 102: 409-414.
34. Coffey R J Jr, Derynck R, Wilcox J N et al. Production and auto-induction of transforming growth factor-alpha in human keratinocytes. Nature 1987: 328: 817-820.
35. Strickland J E, Dlugosz A A, Hennings H, Yuspa S H. Inhibition of tumor formation from grafted murine papilloma cells by treatment of grafts with staurosporine, an inducer of squamous differentiation. Carcinogenesis 1993: 14: 205-209.
36. 2+ compartments. Cell Growth Differ 1995: 6: 1171-1184.
37. Glick A B, Sporn M B, Yuspa S H. Altered regulation of TGF-beta 1 and TGF-alpha in primary keratinocytes and papillomas expressing v-Ha-ras. Mol Carcinog 1991: 4: 210-219.
38. Pandiella A, Bosenberg M W, Huang E J, Besmer P, Massague J. Cleavage of membrane-anchored growth factors involves distinct protease activities regulated through common mechanisms. J Biol Chem 1992: 267: 24028-24033.
39. Wong S T, Winchell L F, McCune B K et al. The TGF-alpha precursor expressed on the cell surface binds to the EGF receptor on adjacent cells, leading to signal transduction. Cell 1989: 56: 495-506.
40. Gschwendt M, Kielbassa K, Kittstein W, Marks F. Tyrosine phosphorylation and stimulation of protein kinase C delta from porcine spleen by src in vitro. Dependence on the activated state of protein kinase C delta. FEBS Lett 1994: 347: 85-89.
41. Zhao Y, Uyttendaele H, Krueger J G, Sudol M, Hanafusa H. Inactivation of c-Yes tyrosine kinase by elevation of intracellular calcium levels. Mol Cell Biol 1993: 13: 7507-7514.
42. Calautti E, Cabodi S, Stein P L, Hatzfeld M, Kedersha N, Dotto G P. Tyrosine phosphorylation and src family kinases control keratinocyte cell-cell adhesion. J Cell Biol 1998: 141: 1449-1465.
43. Betz N A, Pelling J C. Ha-ras p21-GTP levels remain constant during primary keratinocyte differentiation. Mol Carcinog 1995: 12: 66-76.
44. Medema J P, Sark M W, Backendorf C, Bos J L. Calcium inhibits epidermal growth factor-induced activation of p21ras in human primary keratinocytes. Mol Cell Biol 1994: 14: 7078-7085.
45. Di Fiore P P, Falco J, Borrello I, Weissman B, Aaronson S A. The calcium signal for BALB/MK keratinocyte terminal differentiation counteracts epidermal growth factor (EGF) very early in the EGF-induced proliferative pathway. Mol Cell Biol 1988: 8: 557-563.
46. Hansen L A, Alexander N, Hogan M E et al. Genetically null mice reveal a central role for epidermal growth factor receptor in the differentiation of the hair follicle and normal hair development. Am J Pathol 1997: 150: 1959-1975.
47. Sibilia M, Wagner E F. Strain-dependent epithelial defects in mice lacking the EGF receptor. Science 1995: 269: 234-238.
48. Nanney L B, Stoscheck C M, King L E, Jr, Underwood R A, Holbrook K A. Immunolocalization of epidermal growth factor receptors in normal developing human skin. J Invest Dermatol 1990: 94: 742-748.
49. King L E J, Gates R E, Stoscheck C M, Nanney L B. The EGF/TGF alpha receptor in skin. J Invest Dermatol 1990: 94: 164S-170S.
50. Vassar R, Fuchs E. Transgenic mice provide new insights into the role of TGF-alpha during epidermal development and differentiation. Genes Dev 1991: 5: 714-727.
51. Strickland J E, Jetten A M, Kawamura H, Yuspa S H. Interaction of epidermal growth factor with basal and differentiating epidermal cells of mice resistant and sensitive to carcinogenesis. Carcinogenesis 1984: 5: 735-740.
52. Dominey A M, Wang X J, King L E J et al. Targeted overexpression of transforming growth factor alpha in the epidermis of transgenic mice elicits hyperplasia, hyperkeratosis, and spontaneous, squamous papillomas. Cell Growth Differ 1993: 4: 1071-1082.