Mesenchymal-epithelial interactions in the skin: Increased expression of dickkopf1 by palmoplantar fibroblasts inhibits melanocyte growth and differentiation

Journal of Cell Biology

Volumn 165, Issue 2, 2004, Pages 275-285

  Yamaguchi, Yuji ^a   Itami, Satoshi ^b   Watabe, Hidenori ^a   Yasumoto, Ken Ichi ^a   Abdel Malek, Zalfa A ^c   Kubo, Tateki ^b   Rouzaud, François ^a   Tanemura, Atsushi ^b   Yoshikawa, Kunihiko ^b   Hearing, Vincent J ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

catenin; Dickkopf; MITF; Pigmentation; Regulation

Indexed keywords

BETA CATENIN; COMPLEMENTARY DNA; PROTEIN; PROTEIN DICKKOPF1; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; WNT1 PROTEIN;

ARTICLE; CELL DIFFERENTIATION; CELL INTERACTION; CELL MIGRATION; CONTROLLED STUDY; DNA MICROARRAY; EMBRYO DEVELOPMENT; EPITHELIUM CELL; FIBROBLAST; GENETIC TRANSFECTION; HAND PALM; HUMAN; HUMAN CELL; HYPOPIGMENTATION; MELANOCYTE; MESENCHYME CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN PIGMENTATION;

ADULT; ANIMALS; BETA CATENIN; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL DIVISION; CYTOSKELETAL PROTEINS; DNA-BINDING PROTEINS; EPITHELIAL CELLS; FIBROBLASTS; FOOT; GENE EXPRESSION PROFILING; HAND; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MELANINS; MELANOCYTES; MESODERM; MICROPHTHALMIA-ASSOCIATED TRANSCRIPTION FACTOR; MIDDLE AGED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEINS; SIGNAL TRANSDUCTION; SKIN; SKIN PIGMENTATION; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

SOLEIDAE;

EID: 11144354692     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200311122     Document Type: Article

References (66)

1. Andl, T., S. Reddy, T. Gaddapara, and S.E. Millar. 2002. WNT signals are required for the initiation of hair follicle development. Dev. Cell. 2:643-653.
2. Arias, A.M. 2001. Epithelial mesenchymal interactions in cancer and development. Cell. 105:425-431.
3. Arias, A.M., A.M. Brown, and K. Brennan. 1999. Wnt signalling: pathway or network? Curr. Opin. Genet. Dev. 9:447-454.
4. Bordin, S., R.C. Page, and A.S. Narayanan. 1984. Heterogeneity of normal human diploid fibroblasts: isolation and characterization of one phenotype. Science. 223:171-173.
5. Busca, R., and R. Ballotti. 2000. Cyclic AMP: a key messenger in the regulation of skin pigmentation. Pigment Cell Res. 13:60-69.
6. Chang, H.Y., J.T. Chi, S. Dudoit, C. Bondre, M. van de Rijn, D. Botstein, and P.O. Brown. 2002. Diversity, topographic differentiation, and positional memory in human fibroblasts. Proc. Natl. Acad. Sci. USA. 99:12877-12882.
7. Dorsky, R.I., R.T. Moon, and D.W. Raible. 2000a. Environmental signals and cell fate specification in premigratory neural crest. Bioessays. 22:708-716.
8. Dorsky, R.I., D.W. Raible, and R.T. Moon. 2000b. Direct regulation of nacre, a zebrafish MITF homolog required for pigment cell formation, by the Wnt pathway. Genes Dev. 14:158-162.
9. Du, J., A.J. Miller, H.R. Widlund, M.A. Horstmann, S. Ramaswamy, and D.E. Fisher. 2003. MLANA/MART1 and SILV/PMEL17/GP100 are transcriptionally regulated by MITF in melanocytes and melanoma. Am. J. Pathol. 163:333-343.
10. Eger, A., A. Stockinger, B. Schaffhauser, H. Beug, and R. Foisner. 2000. Epithelial mesenchymal transition by c-Fos estrogen receptor activation involves nuclear translocation of β-catenin and upregulation of β-catenin/lymphoid enhancer binding factor-1 transcriptional activity. J. Cell Biol. 148:173-188.
11. Erickson, C.A., and M.V. Reedy. 1998. Neural crest development: the interplay between morphogenesis and cell differentiation. Curr. Top. Dev. Biol. 40:177-209.
12. Fang, D., Y. Tsuji, and V. Setaluri. 2002. Selective down-regulation of tyrosinase family gene TYRP1 by inhibition of the activity of melanocyte transcription factor, MITF. Nucleic Acids Res. 30:3096-3106.
13. Fedi, P., A. Bafico, A.N. Soria, W.H. Burgess, T. Miki, D.P. Bottaro, M.H. Kraus, and S.A. Aaronson. 1999. Isolation and biochemical characterization of the human Dkk-1 homologue, a novel inhibitor of mammalian Wnt signaling. J. Biol. Chem. 274:19465-19472.
14. Garcia-Castro, M.I., C. Marcelle, and M. Bronner-Fraser. 2002. Ectodermal Wnt function as a neural crest inducer. Science. 297:848-851.
15. Glinka, A., W. Wu, H. Delius, A.P. Monaghan, C. Blumenstock, and C. Niehrs. 1998. Dickkopf-1 is a member of a new family of secreted proteins and functions in head induction. Nature. 391:357-362.
16. Gregory, C.A., H. Singh, A.S. Perry, and D.J. Prockop. 2003. The Wnt signaling inhibitor dickkopf-1 is required for reentry into the cell cycle of human adult stem cells from bone marrow. J. Biol. Chem. 278:28067-28078.
17. Grotewald, L., and U. Ruther. 2002a. Bmp, Fgf and Wnt signalling in programmed cell death and chondrogenesis during vertebrate limb development: the role of Dickkopf-1. Int. J. Dev. Biol. 46:943-947.
18. Grotewald, L., and U. Ruther. 2002b. The Wnt antagonist Dickkopf-1 is regulated by Bmp signaling and c-Jun and modulates programmed cell death. EMBO J. 21:966-975.
19. Grotewald, L., T. Theil, and U. Ruther. 1999. Expression pattern of DKK-1 during mouse limb development. Mech. Dev. 89:151-153.
20. Hemesath, T.J., E. Steingrimsson, G. McGill, M.J. Hansen, J. Vaught, C.A. Hodgkinson, H. Arnheiter, N.G. Copeland, N.A. Jenkins, and D.E. Fisher. 1994. Microphthalmia, a critical factor in melanocyte development, defines a discrete transcription factor family. Genes Dev. 8:2770-2780.
21. Hornyak, T.J., D.J. Hayes, L.-Y. Chiu, and E.B. Ziff. 2001. Transcription factors in melanocyte development: distinct roles for Pax-3 and Mitf. Mech. Dev. 101:47-59.
22. Kawano, Y., and R. Kypta. 2003. Secreted antagonists of the Wnt signalling pathway. J. Cell Sci. 116:2627-2634.
23. Knapp, A.C., W.W. Franke, H. Heid, M. Hatzfeld, J.L. Jorcano, and R. Moll. 1986. Cytokeratin No. 9, an epidermal type I keratin characteristic of a special program of keratinocyte differentiation displaying body site specificity. J. Cell Biol. 103:657-667.
24. - human female reproductive tract fibroblasts. Am. J. Pathol. 159:925-935.
25. Krupnik, V.E., J.D. Sharp, C. Jiang, K. Robison, T.W. Chickering, L. Amaravadi, D.E. Brown, D. Guyot, G. Mays, K. Leiby, et al. 1999. Functional and structural diversity of the human Dickkopf gene family. Gene. 238:301-313.
26. Kubo, T., T. Yamashita, A. Yamaguchi, K. Hosokawa, and M. Tohyama. 2002. Analysis of genes induced in peripheral nerves after axotomy using cDNA microarrays. J. Neurochem. 82:1129-1136.
27. Lei, T.C., V. Virador, K. Yasumoto, W.D. Vieira, K. Toyofuku, and V.J. Hearing. 2002. Stimulation of melanoblast pigmentation induced by 8-methoxypsoralen: the involvement of microphthalmia-associated transcription factor, the protein kinase A signal pathway and proteasome-mediated degradation. J. Invest. Dermatol. 119:1341-1349.
28. Leslie, M. 2004. DATABASE: Heads or Tails. Science. 303:1589.
29. Mao, B., W. Wu, Y. Li, D. Hoppe, P. Stannek, A. Glinka, and C. Niehrs. 2001. LDL-receptor-related protein 6 is a receptor for Dickkopf protein. Nature. 411:321-325.
30. Mao, B., W. Wu, G. Davidson, J. Marhold, M. Li, B.M. Mechler, H. Delius, D. Hoppe, P. Stannek, C. Walter, et al. 2002. Kremen proteins are Dickkopf receptors that regulate Wnt/beta-catenin signalling. Nature. 417:664-667.
31. McGill, G.G., M.A. Horstmann, H.R. Widlund, J. Du, G. Motyckova, E. Nishimura, Y.L. Lin, S. Ramaswamy, W. Avery, H.F. Ding, et al. 2002. Bcl2 regulation by the melanocyte master regulator Mitf modulates lineage survival and melanoma cell viability. Cell. 109:707-718.
32. Monaghan, A.P., P. Kioschis, W. Wu, A. Zuniga, D. Bock, A. Poustka, H. Delius, and C. Niehrs. 1999. Dickkopf genes are co-ordinately expressed in mesodermal lineages. Mech. Dev. 87:45-56.
33. Mukhopadhyay, M., S. Shtrom, C. Rodriguez-Esteban, L. Chen, T. Tsukui, L. Gomer, D.W. Dorwand, A. Glinka, A. Grinberg, S.P. Huang, et al. 2001. Dickkopf1 is required for embryonic head induction and limb morphogenesis in the mouse. Dev. Cell. 1:423-434.
34. Niehrs, C., O. Kazanskaya, W. Wu, and A. Glinka. 1999. Dickkopf1 and the Spemann-Mangold head organizer. Int. J. Dev. Biol. 45:237-240.
35. Nusse, R. 2001. Developmental biology. Making head or tail of Dickkopf. Nature. 411:255-256.
36. Opdecamp, K., A. Nakayama, M.T.T. Nguyen, C.A. Hodgkinson, W.J. Pavan, and H. Arnheiter. 1997. Melanocyte development in vivo and in neural crest cell cultures: crucial dependence on the Mitf basic-helix-loop-helix-zipper transcription factor. Development. 124:2377-2386.
37. Reddy, S., T. Andl, O. Bagasra, M.M. Lu, D.J. Epstein, E.E. Morrisey, and S.E. Millar. 2001. Characterization of Wnt gene expression in developing and postnatal hair follicles and identification of Wnt5a as a target of Sonic hedgehog in hair follicle morphogenesis. Mech. Dev. 107:69-82.
38. Rouzaud, F., J.P. Annereau, J.C. Valencia, E.G. Costin, and V.J. Hearing. 2003. Distinct regulation of melanocortin 1 receptor expression at the mRNA and protein levels by its natural agonist and antagonist. FASEB J. 17:2154-2156.
39. Saito, H., K. Yasumoto, K. Takeda, K. Takahashi, A. Fukuzaki, S. Orikasa, and S. Shibahara. 2002. Melanocyte-specific microphthalmia-associated transcription factor isoform activates its own gene promoter through physical interaction with lymphoid-enhancing factor 1. J. Biol. Chem. 277:28787-28794.
40. Saitoh, A., L.A. Hansen, J.C. Vogel, and M.C. Udey. 1998. Characterization of Wnt gene expression in murine skin: possible involvement of epidermis-derived Wnt-4 in cutaneous epithelial-mesenchymal interactions. Exp. Cell Res. 243:150-160.
41. 2+ flux, PKC, and CamKII in vertebrate embros. J. Cell Biol. 161:769-777.
42. Shou, J., F. Ali-Osman, A.S. Multani, S. Pathak, P. Fedi, and K.S. Srivenugopal. 2002. Human Dkk-1, a gene encoding a Wnt antagonist, responds to DNA damage and its overexpression sensitizes brain tumor cells to apoptosis following alkylation damage of DNA. Oncogene. 21:878-889.
43. Spritz, R.A. 1997. Piebaldism, Waardenburg syndrom, and related disorders of melanocyte development. Semin. Cutan. Med. Surg. 16:15-23.
44. Swope, V.B., E.E. Medrano, D. Smalara, and Z.A. Abdel-Malek. 1995. Long-term proliferation of human melanocytes is supported by the physiologic mitogens α-melanotropin, endothelin-1, and basic fibroblast growth factor. Exp. Cell Biol. 217:453-459.
45. Syrris, P., K. Heathcote, R. Carrozzo, K. Devriendt, N. Elcioglu, C. Garrett, M. McEntagart, and N.D. Carter. 2002. Human piebaldism: six novel mutations of the proto-oncogene KIT. Hum. Mutat. 20:234.
46. Szabo, G. 1954. The number of melanocytes in human epidermis. BMJ. 1:1016-1017.
47. Szabowski, A., N. Maas-Szabowski, S. Andrecht, A. Kolbus, M. Schorpp-Kistner, N.E. Fusenig, and P. Angel. 2000. c-Jun and JunB antagonistically control cytokine-regulated mesenchymal-epidermal interaction in skin. Cell. 103:745-755.
48. Tachibana, M. 2000. MITF: a stream flowing for pigment cells. Pigment Cell Res. 13:230-240.
49. Tadokoro, T., N. Kobayashi, B.Z. Zmudzka, S. Ito, K. Wakamatsu, Y. Yamaguchi, K.S. Korossy, J.Z. Beer, and V.J. Hearing. 2003. UV-induced DNA damage and melanin content in human skin differing in racial/ethnic origin and photosensitivity. FASEB J. 17:1177-1179.
50. Taipale, J., and P.A. Beachy. 2001. The Hedgehog and Wnt signalling pathways in cancer. Nature. 411:349-354.
51. Takeda, K., C. Takemoto, I. Kobayashi, A. Watanabe, Y. Nobukuni, D.E. Fisher, and M. Tachibana. 2000a. Ser298 of MITF, a mutation site in Waardenburg syndrome type 2, is a phosphorylation site with functional significance. Hum. Mol. Genet. 9:125-132.
52. Takeda, K., K. Yasumoto, R. Takada, S. Takada, K. Watanabe, T. Udono, H. Saito, K. Takahashi, and S. Shibahara. 2000b. Induction of melanocyte-specific microphthalmia-associated transcription factor by Wnt-3a. J. Biol. Chem. 275:14013-14016.
53. Tian, E., F. Zhan, R. Walker, E. Rasmussen, Y. Ma, B. Barlogie, and J.D. Shaughnessy. 2003. The role of the Wnt-signaling antagonist DKK1 in the development of osteolytic lesions in multiple myeloma. N. Engl. J. Med. 349:2483-2494.
54. Topol, L., X. Jiang, H. Choi, L. Garrett-Beal, P.J. Carolan, and Y. Yang. 2003. Wnt-5a inhibits the canonical Wnt pathway by promoting GSK-3-independent β-catenin degradation. J. Cell Biol. 162:899-908.
55. Trainor, P., L. Ariza-McNaugton, and R. Krumlauf. 2002. Role of the isthmus and FGF in resolving the paradox of neural crest plasticity and prepatterning. Science. 295:1288-1291.
56. Virador, V., N. Kobayashi, J. Matsunaga, and V.J. Hearing. 1999. A standardized protocol for assessing regulators of pigmentation. Anal. Biochem. 270:207-219.
57. Virador, V., N. Matsunaga, J. Matsunaga, J. Valencia, R.J. Oldham, K. Kameyama, G.L. Peck, V.J. Ferrans, W.D. Vieira, Z.A. Abdel-Malek, and V.J. Hearing. 2001. Production of melanocyte-specific antibodies to human melanosomal proteins: expression patterns in normal human skin and in cutaneous pigmented lesions. Pigment Cell Res. 14:289-297.
58. Widlund, H.R., M.A. Horstmann, E.R. Price, J. Cui, S.L. Lessnick, M. Wu, X. He, and D.E. Fisher. 2002. β-Catenin-induced melanoma growth requires the downstream target Microphthalmia-associated transcription factor. J. Cell Biol. 158:1079-1087.
59. Wilson, S.L., A. Rydstrom, T. Trimborn, K. Willert, R. Nusse, T.M. Jessell, and T. Edlund. 2001. The status of Wnt signalling regulates neural and epidermal fates in the chick embryo. Nature. 411:325-330.
60. Yamaguchi, Y., and K. Yoshikawa. 2001. Cutaneous wound healing: an update. J. Dermatol. 28:521-534.
61. Yamaguchi, Y., S. Itami, M. Tarutani, K. Hosokawa, H. Miura, and K. Yoshikawa. 1999. Regulation of keratin 9 in nonpalmoplantar keratinocytes by palmoplantar fibroblasts through epithelial-mesenchymal interactions. J. Invest. Dermatol. 112:483-488.
62. Yamaguchi, Y., S. Crane, L. Zhou, S.M. Ochoa, and V. Falanga. 2000. Lack of coordinate expression of the alpha1(I) and alpha1(III) procollagen genes in fibroblast donal cultures. Br. J. Dermatol. 143:1149-1153.
63. Yasumoto, K., K. Yokoyama, K. Shibata, Y. Tomita, and S. Shibahara. 1994. Microphthalmia-associated transcription factor as a regulator for melanocyte-specific transcription of the human tyrosinase gene. Mol. Cell. Biol. 14:8058-8070.
64. Yasumoto, K., S. Amae, T. Udono, N. Fuse, K. Takeda, and S. Shibahara. 1998. A big gene linked to small eyes encodes multiple Mitfisoforms: many promoters make light work. Pigment Cell Res. 11:329-336.
65. Yasumoto, K., K. Takeda, H. Saito, K. Watanabe, K. Takahashi, and S. Shibahara. 2002. Microphthalmia-associated transcription factor interacts with LEF-1, a mediator of Wnt signaling. EMBO J. 21:2703-2714.
66. Yoon, T.J., T.C. Lei, Y. Yamaguchi, J. Batzer, R. Wolber, and V.J. Hearing. 2003. Reconstituted 3-dimensional human skin as a novel in vitro model for studies of pigmentation. Anal. Biochem. 318:260-269.