Accelerated re-epithelialization in Dpr2-deficient mice is associated with enhanced response to TGFβ signaling

Journal of Cell Science

Volumn 121, Issue 17, 2008, Pages 2904-2912

  Meng, Fanwei ^a,b   Cheng, Xuan ^b   Yang, Leilei ^b   Hou, Ning ^b   Yang, Xiao ^b   Meng, Anming ^a  

^a TSINGHUA UNIVERSITY   (China)

^b BEIJING INSTITUTE OF BIOTECHNOLOGY   (China)

Author keywords

Dapper2; Keratinocyte; Re epithelialization; TGF ; Wound healing

Indexed keywords

DAPPER 2 PROTEIN; DISHEVELLED PROTEIN; FIBRONECTIN; INTEGRIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL MIGRATION; CELL STIMULATION; CONTROLLED STUDY; EPITHELIZATION; GENE EXPRESSION REGULATION; HAIR FOLLICLE; HOMOZYGOTE; KERATINOCYTE; KNOCKOUT GENE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; WOUND HEALING;

ANIMALS; ANTIGENS, CD29; CARRIER PROTEINS; CELL MOVEMENT; EMBRYONIC DEVELOPMENT; EPITHELIUM; GENE EXPRESSION PROFILING; GENE TARGETING; INTEGRIN ALPHAV; KERATINOCYTES; MICE; MICE, KNOCKOUT; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA; UP-REGULATION; WOUND HEALING;

MUS;

EID: 53349116514     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.032417     Document Type: Article

References (56)

1. Amendt, C., Mann, A., Schirmacher, P. and Blessing, M. (2002). Resistance of keratinocytes to TGFbeta-mediated growth restriction and apoptosis induction accelerates re-epithelialization in skin wounds. J. Cell Sci. 115, 2189-2198.
2. Ashcroft, G. S., Yang, X., Glick, A. B., Weinstein, M., Letterio, J. L., Mizel, D. E., Anzano, M., Greenwell-Wild, T., Wahl, S. M., Deng, C. et al. (1999). Mice lacking Smad3 show accelerated wound healing and an impaired local inflammatory response. Nat. Cell Biol. 1, 260-266.
3. Brown, R. L., Ormsby, I., Doetschman, T. C. and Greenhalgh, D. G. (1995). Wound healing in the transforming growth factor-beta-deficient mouse. Wound Repair Regen. 3, 25-36.
4. Chen, Y. G. and Meng, A. M. (2004). Negative regulation of TGF-beta signaling in development. Cell Res. 14, 441-449.
5. Cheyette, B. N., Waxman, J. S., Miller, J. R., Takemaru, K., Sheldahl, L. C., Khlebtsova, N., Fox, E. F., Earnest, T. and Moon, R. T. (2002). Dapper, a Dishevelled-associated antagonist of beta-catenin and JNK signaling, is required for notochord formation. Dev. Cell 2, 449-461.
6. Crowe, M. J., Doetschman, T. and Greenhalgh, D. G. (2000). Delayed wound healing in immunodeficient TGF-beta 1 knockout mice. J. Invest. Dermatol. 115, 3-11.
7. Deng, C. X., Wynshaw-Boris, A., Shen, M. M., Daugherty, C., Ornitz, D. M. and Leder, P. (1994). Murine FGFR-1 is required for early postimplantation growth and axial organization. Genes Dev. 8, 3045-3057.
8. Fisher, D. A., Kivimae, S., Hoshino, J., Suriben, R., Martin, P. M., Baxter, N. and Cheyette, B. N. (2006). Three Dact gene family members are expressed during embryonic development and in the adult brains of mice. Dev. Dyn. 235, 2620-2630.
9. Gailit, J., Welch, M. P. and Clark, R. A. (1994). TGF-beta 1 stimulates expression of keratinocyte integrins during re-epithelialization of cutaneous wounds. J. Invest. Dermatol. 103, 221-227.
10. Garlick, J. A. and Taichman, L. B. (1994). Fate of human keratinocytes during reepithelialization in an organotypic culture model. Lab. Invest. 70, 916-924.
11. Gat, U., DasGupta, R., Degenstein, L. and Fuchs, E. (1998). De Novo hair follicle morphogenesis and hair tumors in mice expressing a truncated beta-catenin in skin. Cell 95, 605-614.
12. Grose, R. and Werner, S. (2004). Wound-healing studies in transgenic and knockout mice. Mol. Biotechnol. 28, 147-166.
13. Grose, R., Hutter, C., Bloch, W., Thorey, I., Watt, E. M., Fassler, R., Brakebusch, C. and Werner, S. (2002). A crucial role of beta 1 integrins for keratinocyte migration in vitro and during cutaneous wound repair. Development 129, 2303-2315.
14. Hebda, P. A. (1988). Stimulatory effects of transforming growth factor-beta and epidermal growth factor on epidermal cell outgrowth from porcine skin explant cultures. J. Invest. Dermatol. 91, 440-445.
15. Hosokawa, R., Urata, M. M., Ito, Y., Bringas, P., Jr and Chai, Y. (2005). Functional significance of Smad2 in regulating basal keratinocyte migration during wound healing. J. Invest. Dermatol. 125, 1302-1309.
16. Huang, X., Wu, J., Spong, S. and Sheppard, D. (1999). The integrin alphavbeta6 is critical for keratinocyte migration on both its known ligand, fibronectin, and on vitronectin. J. Cell Sci. 111, 2189-2195.
17. Hynes, R. O. (1992). Integirins: versatility, modulation, and signaling in cell adhesion. Cell 69, 11-25.
18. James, D., Levine, A. J., Besser, D. and Hemmati-Brivanlou, A. (2005). TGFbeta/activin/nodal signaling is necessary for the maintenance of pluripotency in human embryonic stem cells. Development 132, 1273-1282.
19. Juhasz, I., Murphy, G. F., Yan, H. C., Herlyn, M. and Albelda, S. M. (1993). Regulation of extracellular matrix proteins and integrin cell substratum adhesion receptors on epithelium during cutaneous human wound healing in vivo. Am. J. Pathol. 143, 1458-1469.
20. Katoh, M. and Katoh, M. (2003). Identification and characterization of human DAPPER1 and DAPPER2 genes in silico. Int. J. Oncol. 22, 907-913.
21. Lakso, M., Pichel, J. G., Gorman, J. R., Sauer, B., Okamoto, Y., Lee, E., Alt, F. W. and Westphal, H. (1996). Efficient in vivo manipulation of mouse genomic sequences at the zygote stage. Proc. Natl. Acad. Sci. USA 93, 5860-5865.
22. Laping, N. J., Grygielko, E., Mathur, A., Butter, S., Bomberger, J., Tweed, C., Martin, W., Fornwald, J., Lehr, R., Harling, J. et al. (2002). Inhibition of transforming growth factor (TGF)-beta1-induced extracellular matrix with a novel inhibitor ofthe TGF-beta type I receptor kinase activity: SB-431542. Mol. Pharmacol. 62, 58-64.
23. Larjava, H., Salo, T., Haapasalmi, K., Kramer, R. H. and Heino, J. (1993). Expression of integrins and basement membrane components by wound keratinocytes. J. Clin. Invest. 92, 1425-1435.
24. Martin, P. (1997). Wound healing-aiming for perfect skin regeneration. Science 276, 75-81.
25. Massague, J. and Chen, Y. G. (2000). Controlling TGF-beta signaling. Genes Dev. 14, 627-644.
26. Millan, F. A., Denhez, R, Kondaiah, P. and Akhurst, R. J. (1991). Embryonic gene expression patterns of TGF beta 1, beta 2 and beta 3 suggest different developmental functions in vivo. Development 111, 131-143.
27. Paria, B. C., Jones, K. L., Flanders, K. C. and Dey, S. K. (1992). Localization and binding of transforming growth factor-beta isoforms in mouse preimplantation embryos and in delayed and activated blastocysts. Dev. Biol. 151, 91-104.
28. Reynolds, L. E., Conti, F. J., Lucas, M., Grose, R., Robinson, S., Stone, M., Saunders, G., Dickson, C., Hynes, R. O., Lacy-Hulbert, A. et al. (2005). Accelerated reepithelialization in beta3-integrin-deficient-mice is associated with enhanced TGF-beta1 signaling. Nat. Med. 11, 167-174.
29. Reynolds, L. E., Conti, F. J., Silva, R., Robinson, S. D., Iyer, V., Rudling, R., Cross, B., Nye, E., Hart, I. R., Dipersio, C. M. et al. (2008). alpha3beta1 integrin-controlled Smad7 regulates reepithelialization during wound healing in mice. J. Clin. Invest. 118, 965-974.
30. Schafer, M. and Werner, S. (2007). Transcriptional control of wound repair. Annu. Rev. Cell Dev. Biol. 23, 69-92.
31. Sellheyer, K., Bickenbach, J. R., Rothnagel, J. A., Bundman, D., Longley, M. A., Krieg, T., Roche, N. S., Roberts, A. B. and Roop, D. R. (1993). Inhibition of skin development by overexpression of transtorming growth factor beta 1 in the epidermis of transgenic mice. Proc. Natl. Acad. Sci. USA 90, 5237-5241.
32. Shah, M., Revis, D., Herrick, S., Baillie, R., Thorgeirson, S., Ferguson, M. and Roberts, A. (1999). Role of elevated plasma transforming growth factor-beta1 levels in wound healing. Am. J. Pathol. 154, 1115-1124.
33. Shen, M. M. (2007). Nodal signaling: developmental roles and regulation. Development 134, 1023-1034.
34. Singer, A. J. and Clark, R. A. (1999). Cutaneous wound healing. N. Engl. J. Med. 341, 738-746.
35. Steffensen, B., Hakkinen, L. and Larjava, H. (2001). Proteolytic events of wound-healing-coordinated interactions among matrix metalloproteinases (MMPs), integrins, and extracellular matrix molecules. Crit. Rev. Oral Biol. Med. 12, 373-398.
36. Stepp, M. A., Gibson, H. E., Gala, P. H., Iglesia, D. D., Pajoohesh-Ganji, A., Pal-Ghosh, S., Brown, M., Aquino, C., Schwartz, A. M., Goldberger, O. et al. (2002). Defects in keratinocyte activation during wound healing in the syndecan-1-deficient mouse. J. Cell Sci. 115, 4517-4531.
37. Stepp, M. A., Liu, Y., Pal-Ghosh, S., Jurjus, R. A., Tadvalkar, G., Sekaran, A., Losicco, K., Jiang, L., Larsen, M., Li, L. et al. (2007). Reduced migration, altered matrix and enhanced TGFbeta 1 signaling are signatures of mouse keratinocytes lacking Sdc1. J. Cell Sci. 120, 2851-2863.
38. Su, Y., Zhang, L., Gao, X., Meng, F., Wen, J., Zhou, H., Meng, A. and Chen, Y. G. (2007). The evolutionally conserved activity of Dapper2 in antagonizing TGF-beta signaling. FASEB J. 21, 682-690.
39. Teng, Y., Sun, A. N., Pan, X. C., Yang, G., Yang, L. L., Wang, M. R. and Yang, X. (2006). Synergistic function of Smad4 and PTEN in suppressing forestomach squamous cell carcinoma in the mouse. Cancer Res. 66, 6972-6981.
40. Thomas, G. J., Poomsawat, S., Lewis, M. P., Hart, I. R., Speight, P. M. and Marshall, J. F. (2001). alpha v beta 6 Integrin upregulates matrix metalloproteinase 9 and promotes migration of normal oral keratinocytes. J. Invest. Dermatol. 116, 898-904.
41. Tian, T. and Meng, A. M. (2006). Nodal signals pattern vertebrate embryos. Cell. Mol. Life Sci. 63, 672-685.
42. Vassar, R., Rosenberg, M., Ross, S., Tyner, A. and Fuchs, E. (1989). Tissue-specific and differentiation-specific expression of a human K14 keratin gene in transgenic mice. Proc. Natl. Acad Sci. USA 86, 1563-1567.
43. Waxman, J. S., Hocking, A. M., Stoick, C. L. and Moon, R. T. (2004). Zebrafish Dapper1 and Dapper2 play distinct roles in Wnt-mediated developmental processes. Development 131, 5909-5921.
44. Weinacker, A., Chen, A., Agrez, M., Cone, R. L, Nishimura, S., Wayner, E., Pytela, R. and Sheppard, D. (1994). Role of the integrin alpha v beta 6 in cell attachment to fibronectin. Heterologous expression of intact and secreted forms of the receptor. J. Biol. Chem. 269, 6940-6948.
45. Werner, S. and Grose, R. (2003). Regulation of wound healing by growth factors and cytokines. Physiol. Rev. 83, 835-870.
46. Werner, S., Krieg, T. and Smola, H. (2007). Keratinocyte-fibroblast interactions in wound healing. J. Invest. Dermatol. 127, 998-1008.
47. Whitman, M. (1998). Smads and early developmental signaling by the TGFbeta superfamily. Genes Dev. 12, 2445-2462.
48. Xu, X., Qiao, W., Li, C. and Deng, C. X. (2002). Generation of Fgfr1 conditional knockout mice. Genesis 32, 85-86.
49. Yamaguchi, T., Kurisaki, A., Yamakawa, N., Minakuchi, K. and Sugino, H. (2006). FKBP12 functions as an adaptor of the Smad7-Smurf1 complex on activin type I receptor. J. Mol. Endocrinol. 36, 569-579.
50. Yang, L., Chan, T., Demare, J., Iwashina, T., Ghahary, A., Scott, P. G. and Tredget, E. E. (2001). Healing of burn wounds in transgenic mice overexpressing transforming growth factor-beta 1 in the epidermis. Am. J. Pathol. 159, 2147-2157.
51. Yang, X., Li, C., Xu, X. and Deng, C. (1998). The tumor suppressor SMAD4/DPC4 is essential for epiblast proliferation and mesoderm induction in mice. Proc. Natl. Acad. Sci. USA 95, 3667-3672.
52. Yau, T. O., Chan, C. Y., Chan, K. L., Lee, M. E., Wong, C. M., Fan, S. T. and Ng, I. O. (2005). HDPR1, a novel inhibitor of the WNT/ beta-catenin signaling, is frequently downregulated in hepatocellular carcinoma: involvement of methylation-mediated gene silencing. Oncogene 24, 1607-1614.
53. Zambruno, G., Marchisio, P. C., Marconi, A., Vaschieri, C., Melchiori, A., Giannetti, A. and De Luca, M. (1995). Transforming growth factor-beta 1 modulates beta I and beta 5 integrin receptors and induces the de novo expression of the alpha v beta 6 heterodimer in normal human keratinocytes: implications for wound healing. J. Cell Biol. 129, 853-865.
54. Zhang, C., Meng, F., Wang, C., Guo, H., Fan, M., Liu, S., Zhou, R. and He, F. (2004a). Identification of a novel alternative splicing form of human netrin-4 and analyzing the expression patterns in adult rat brain. Brain Res. Mol. Brain Res. 130, 68-80.
55. Zhang, L., Zhou, H., Su, Y., Sun, Z., Zhang, H., Zhang, L., Zhang, Y., Ning, Y., Chen, Y. G. and Meng, A. (2004b). Zebrafish Dpr2 inhibits mesoderm induction by promoting degradation of nodal receptors. Science 306, 114-117.
56. Zhang, L., Gao, X., Wen, J., Ning, Y. and Chen, Y. G. (2006). Dapper 1 antagonizes Writ signaling by promoting dishevelled degradation. J. Biol. Chem. 281, 8607-8612.