The growth-promoting effect of KGF on limbal epithelial cells is mediated by upregulation of ΔNp63α through the p38 pathway

Journal of Cell Science

Volumn 122, Issue 24, 2009, Pages 4473-4480

  Cheng, Chien Chia ^a   Wang, Der Yuan ^b   Kao, Ming Hui ^b   Chen, Jan Kan ^a  

^a CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^b Executive Yuan   (Taiwan)

Author keywords

Np63 ; Cornea; Epithelium; KGF; Limbus; Stem cell

Indexed keywords

CYTOKERATIN 14; CYTOKERATIN 3; KERATINOCYTE GROWTH FACTOR; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN P63;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL GROWTH; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; EPITHELIUM CELL; EX VIVO STUDY; IMMUNOFLUORESCENCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; UPREGULATION;

ANIMALS; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; EPITHELIUM, CORNEAL; FIBROBLAST GROWTH FACTOR 7; HEPATOCYTE GROWTH FACTOR; HUMANS; KERATIN-14; KERATIN-3; LIMBUS CORNEAE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RABBITS; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TUMOR SUPPRESSOR PROTEINS; UP-REGULATION;

EID: 71449097087     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.054791     Document Type: Article

References (60)

1. Barbieri, C. E., Barton, C. E. and Pietenpol, J. A. (2003). Delta Np63 alpha expression is regulated by the phosphoinositide 3-kinase pathway. J. Biol. Chem. 278, 51408-51414.
2. Boldrup, L., Coates, P. J., Hedberg, Y., Sjostrom, B., Dahlqvist, A. and Nylander, K. (2005). Expression of p63, COX-2, EGFR and beta-catenin in smokers and patients with squamous cell carcinoma of the head and neck reveal variations in non-neoplastic tissue and no obvious changes in smokers. Int. J. Oncol. 27, 1661-1667.
3. Candi, E., Rufini, A., Terrinoni, A., Giamboi-Miraglia, A., Lena, A. M., Mantovani, R., Knight, R. and Melino, G. (2007). DeltaNp63 regulates thymic development through enhanced expression of FgfR2 and Jag2. Proc. Natl. Acad. Sci. USA 104, 11999-12004.
4. Capone, A., Visco, V., Belleudi, F., Marchese, C., Cardinali, G., Bellocci, M., Picardo, M., Frati, L. and Torrisi, M. R. (2000). Up-modulation of the expression of functional keratinocyte growth factor receptors induced by high cell density in the human keratinocyte HaCaT cell line. Cell Growth Differ. 11, 607-614.
5. Chandrasekher, G., Kakazu, A. H. and Bazan, H. E. (2001). HGF- and KGF-induced activation of PI-3K/p70 s6 kinase pathway in corneal epithelial cells: its relevance in wound healing. Exp. Eye Res. 73, 191-202.
6. Chen, J. J. and Tseng, S. C. (1990). Corneal epithelial wound healing in partial limbal deficiency. Invest. Ophthalmol. Vis. Sci. 31, 1301-1314.
7. Chu, W. K., Lee, K. C., Chow, S. E. and Chen, J. K. (2006). Dual regulation of the DeltaNp63 transcriptional activity by DeltaNp63 in human nasopharyngeal carcinoma cell. Biochem. Biophys. Res. Commun. 342, 1356-1360.
8. Cotsarelis, G., Cheng, S. Z., Dong, G., Sun, T. T. and Lavker, R. M. (1989). Existence of slow-cycling limbal epithelial basal cells that can be preferentially stimulated to proliferate: implications on epithelial stem cells. Cell 57, 201-209.
9. D'Addario, M., Arora, P. D. and McCulloch, C. A. (2006). Role of p38 in stress activation of Sp1. Gene 379, 51-61.
10. Davanger, M. and Evensen, A. (1971). Role of the pericorneal papillary structure in renewal of corneal epithelium. Nature 229, 560-561.
11. de Oliveira, L. R., Ribeiro-Silva, A. and Zucoloto, S. (2007). Prognostic impact of p53 and p63 immunoexpression in oral squamous cell carcinoma. J. Oral Pathol. Med. 36, 191-197.
12. Di Iorio, E., Barbaro, V., Ruzza, A., Ponzin, D., Pellegrini, G. and De Luca, M. (2005). Isoforms of DeltaNp63 and the migration of ocular limbal cells in human corneal regeneration. Proc. Natl. Acad. Sci. USA 102, 9523-9528.
13. Dunsmore, S. E., Rubin, J. S., Kovacs, S. O., Chedid, M., Parks, W. C. and Welgus, H. G. (1996). Mechanisms of hepatocyte growth factor stimulation of keratinocyte metalloproteinase production. J. Biol. Chem. 271, 24576-24582.
14. Forge, A., Li, L., Corwin, J. T. and Nevill, G. (1993). Ultrastructural evidence for hair cell regeneration in the mammalian inner ear. Science 259, 1616-1619.
15. Furlong, R. A., Takehara, T., Taylor, W. G., Nakamura, T. and Rubin, J. S. (1991). Comparison of biological and immunochemical properties indicates that scatter factor and hepatocyte growth factor are indistinguishable. J. Cell Sci. 100 (Pt 1), 173-177.
16. Gherardi, E., Sharpe, M., Lane, K., Sirulnik, A. and Stoker, M. (1993). Hepatocyte growth factor/scatter factor (HGF/SF), the c-met receptor and the behaviour of epithelial cells. Symp. Soc. Exp. Biol. 47, 163-181.
17. Hsueh, Y. J., Wang, D. Y., Cheng, C. C. and Chen, J. K. (2004). Age-related expressions of p63 and other keratinocyte stem cell markers in rat cornea. J. Biomed. Sci. 11, 641-651.
18. Huang, A. J. and Tseng, S. C. (1991). Corneal epithelial wound healing in the absence of limbal epithelium. Invest Ophthalmol Vis. Sci. 32, 96-105.
19. Johnson, M., Koukoulis, G., Matsumoto, K., Nakamura, T. and Iyer, A. (1993). Hepatocyte growth factor induces proliferation and morphogenesis in nonparenchymal epithelial liver cells. Hepatology 17, 1052-1061.
20. Kawasaki, S., Tanioka, H., Yamasaki, K., Connon, C. J. and Kinoshita, S. (2006). Expression and tissue distribution of p63 isoforms in human ocular surface epithelia. Exp. Eye Res. 82, 293-299.
21. Koizumi, N., Inatomi, T., Suzuki, T., Sotozono, C. and Kinoshita, S. (2001). Cultivated corneal epithelial stem cell transplantation in ocular surface disorders. Ophthalmology 108, 1569-1574.
22. Koster, M. I. and Roop, D. R. (2004). The role of p63 in development and differentiation of the epidermis. J. Dermatol. Sci. 34, 3-9.
23. Koster, M. I., Kim, S., Mills, A. A., DeMayo, F. J. and Roop, D. R. (2004). p63 is the molecular switch for initiation of an epithelial stratification program. Genes Dev. 18, 126-131.
24. Lee, H. O., Lee, J. H., Choi, E., Seol, J. Y., Yun, Y. and Lee, H. (2006). A dominant negative form of p63 inhibits apoptosis in a p53-independent manner. Biochem. Biophys. Res. Commun. 344, 166-172.
25. Li, D. Q. and Tseng, S. C. (1995). Three patterns of cytokine expression potentially involved in epithelial-fibroblast interactions of human ocular surface. J. Cell Physiol. 163, 61-79.
26. Liu, J. J., Shay, J. W. and Wilson, S. E. (1998). Characterization of a soluble KGF receptor cDNA from human corneal and breast epithelial cells. Invest Ophthalmol. Vis. Sci. 39, 2584-2593.
27. Marchese, C., Rubin, J., Ron, D., Faggioni, A., Torrisi, M. R., Messina, A., Frati, L. and Aaronson, S. A. (1990). Human keratinocyte growth factor activity on proliferation and differentiation of human keratinocytes: differentiation response distinguishes KGF from EGF family. J. Cell Physiol. 144, 326-332.
28. Marchese, C., Sorice, M., De Stefano, C., Frati, L. and Torrisi, M. R. (1997). Modulation of keratinocyte growth factor receptor expression in human cultured keratinocytes. Cell Growth Differ. 8, 989-997.
29. Matheny, K. E., Barbieri, C. E., Sniezek, J. C., Arteaga, C. L. and Pietenpol, J. A. (2003). Inhibition of epidermal growth factor receptor signaling decreases p63 expression in head and neck squamous carcinoma cells. Laryngoscope 113, 936-939.
30. McKeon, F. (2004). p63 and the epithelial stem cell: more than status quo? Genes Dev. 18, 465-469.
31. Meller, D. and Tseng, S. C. (2000). [Amniotic membrane transplantation with or without limbal allografts in corneal surface reconstruction in limbal deficiency]. Ophthalmologe 97, 100-107.
32. Mills, A. A., Zheng, B., Wang, X. J., Vogel, H., Roop, D. R. and Bradley, A. (1999). p63 is a p53 homologue required for limb and epidermal morphogenesis. Nature 398, 708-713.
33. Montesano, R., Matsumoto, K., Nakamura, T. and Orci, L. (1991). Identification of a fibroblast-derived epithelial morphogen as hepatocyte growth factor. Cell 67, 901-908.
34. Pellegrini, G., Golisano, O., Paterna, P., Lambiase, A., Bonini, S., Rama, P. and De Luca, M. (1999). Location and clonal analysis of stem cells and their differentiated progeny in the human ocular surface. J. Cell Biol. 145, 769-782.
35. Pellegrini, G., Dellambra, E., Golisano, O., Martinelli, E., Fantozzi, I., Bondanza, S., Ponzin, D., McKeon, F. and De Luca, M. (2001). p63 identifies keratinocyte stem cells. Proc. Natl. Acad. Sci. USA 98, 3156-3161.
36. Rocco, J. W. and Ellisen, L. W. (2006). p63 and p73: life and death in squamous cell carcinoma. Cell Cycle 5, 936-940.
37. Romano, R. A., Birkaya, B. and Sinha, S. (2006). Defining the regulatory elements in the proximal promoter of DeltaNp63 in keratinocytes: Potential roles for Sp1/Sp3, NF-Y, and p63. J. Invest. Dermatol. 126, 1469-1479.
38. Schermer, A., Galvin, S. and Sun, T. T. (1986). Differentiation-related expression of a major 64K corneal keratin in vivo and in culture suggests limbal location of corneal epithelial stem cells. J. Cell Biol. 103, 49-62.
39. Sotozono, C., Kinoshita, S., Kita, M. and Imanishi, J. (1994). Expression of keratinocyte growth factor mRNA in ex vivo and in vitro specimens of human cornea and conjunctiva. Jpn. J. Ophthalmol. 38, 353-359.
40. Tang, A. and Gilchrest, B. A. (1996). Regulation of keratinocyte growth factor gene expression in human skin fibroblasts. J. Dermatol. Sci. 11, 41-50.
41. Thoft, R. A. and Friend, J. (1983). The X, Y, Z hypothesis of corneal epithelial maintenance. Invest. Ophthalmol. Vis. Sci. 24, 1442-1443.
42. Ti, S. E., Grueterich, M., Espana, E. M., Touhami, A., Anderson, D. F. and Tseng, S. C. (2004). Correlation of long term phenotypic and clinical outcomes following limbal epithelial transplantation cultivated on amniotic membrane in rabbits. Br. J. Ophthalmol. 88, 422-427.
43. Truong, A. B., Kretz, M., Ridky, T. W., Kimmel, R. and Khavari, P. A. (2006). p63 regulates proliferation and differentiation of developmentally mature keratinocytes. Genes Dev. 20, 3185-3197.
44. Tsai, R. J., Li, L. M. and Chen, J. K. (2000). Reconstruction of damaged corneas by transplantation of autologous limbal epithelial cells. N. Engl. J. Med. 343, 86-93.
45. Tseng, S. C. (1989). Concept and application of limbal stem cells. Eye 3 (Pt 2), 141-157.
46. Tseng, S. C., Prabhasawat, P., Barton, K., Gray, T. and Meller, D. (1998). Amniotic membrane transplantation with or without limbal allografts for corneal surface reconstruction in patients with limbal stem cell deficiency. Arch. Ophthalmol. 116, 431-441.
47. Tseng, S. C., Meller, D., Anderson, D. F., Touhami, A., Pires, R. T., Gruterich, M., Solomon, A., Espana, E., Sandoval, H., Ti, S. E. et al. (2002). Ex vivo preservation and expansion of human limbal epithelial stem cells on amniotic membrane for treating corneal diseases with total limbal stem cell deficiency. Adv. Exp. Med. Biol. 506, 1323-1334.
48. Wang, D. Y., Hsueh, Y. J., Yang, V. C. and Chen, J. K. (2003). Propagation and phenotypic preservation of rabbit limbal epithelial cells on amniotic membrane. Invest. Ophthalmol. Vis. Sci. 44, 4698-4704.
49. Wang, D. Y., Cheng, C. C., Kao, M. H., Hsueh, Y. J., Ma, D. H. and Chen, J. K. (2005). Regulation of limbal keratinocyte proliferation and differentiation by TAp63 and DeltaNp63 transcription factors. Invest. Ophthalmol. Vis. Sci. 46, 3102-3108.
50. Weidner, K. M., Behrens, J., Vandekerckhove, J. and Birchmeier, W. (1990). Scatter factor: molecular characteristics and effect on the invasiveness of epithelial cells. J. Cell Biol. 111, 2097-2108.
51. Werner, S., Peters, K. G., Longaker, M. T., Fuller-Pace, F., Banda, M. J. and Williams, L. T. (1992). Large induction of keratinocyte growth factor expression in the dermis during wound healing. Proc. Natl. Acad. Sci. USA 89, 6896-6900.
52. Werner, S., Breeden, M., Hubner, G., Greenhalgh, D. G. and Longaker, M. T. (1994a). Induction of keratinocyte growth factor expression is reduced and delayed during wound healing in the genetically diabetic mouse. J. Invest. Dermatol. 103, 469-473.
53. Werner, S., Smola, H., Liao, X., Longaker, M. T., Krieg, T., Hofschneider, P. H. and Williams, L. T. (1994b). The function of KGF in morphogenesis of epithelium and reepithelialization of wounds. Science 266, 819-822.
54. Westfall, M. D., Mays, D. J., Sniezek, J. C. and Pietenpol, J. A. (2003). The Delta Np63 alpha phosphoprotein binds the p21 and 14-3-3 sigma promoters in vivo and has transcriptional repressor activity that is reduced by Hay-Wells syndrome-derived mutations. Mol. Cell. Biol. 23, 2264-2276.
55. Williams, E. D., Lowes, A. P., Williams, D. and Williams, G. T. (1992). A stem cell niche theory of intestinal crypt maintenance based on a study of somatic mutation in colonic mucosa. Am. J. Pathol. 141, 773-776.
56. Wilson, S. E., Walker, J. W., Chwang, E. L. and He, Y. G. (1993). Hepatocyte growth factor, keratinocyte growth factor, their receptors, fibroblast growth factor receptor-2, and the cells of the cornea. Invest. Ophthalmol. Vis. Sci. 34, 2544-2561.
57. Wilson, S. E., Schultz, G. S., Chegini, N., Weng, J. and He, Y. G. (1994a). Epidermal growth factor, transforming growth factor alpha, transforming growth factor beta, acidic fibroblast growth factor, basic fibroblast growth factor, and interleukin-1 proteins in the cornea. Exp. Eye. Res. 59, 63-71.
58. Wilson, S. E., He, Y. G., Weng, J., Zieske, J. D., Jester, J. V. and Schultz, G. S. (1994b). Effect of epidermal growth factor, hepatocyte growth factor, and keratinocyte growth factor, on proliferation, motility and differentiation of human corneal epithelial cells. Exp. Eye. Res. 59, 665-678.
59. Wilson, S. E., Chen, L., Mohan, R. R., Liang, Q. and Liu, J. (1999). Expression of HGF, KGF, EGF and receptor messenger RNAs following corneal epithelial wounding. Exp. Eye. Res. 68, 377-397.
60. Yang, A., Kaghad, M., Wang, Y., Gillett, E., Fleming, M. D., Dotsch, V., Andrews, N. C., Caput, D. and McKeon, F. (1998). p63, a p53 homolog at 3q27-29, encodes multiple products with transactivating, death-inducing, and dominant-negative activities. Mol. Cell 2, 305-316.