Ectodysplasin A1 promotes placodal cell fate during early morphogenesis of ectodermal appendages

Development

Volumn 131, Issue 20, 2004, Pages 4907-4919

  Mustonen, Tuija ^a   Ilmonen, Maritta ^a   Pummila, Marja ^a   Kangas, Aapo T ^a   Laurikkala, Johanna ^a   Jaatinen, Risto ^a   Pispa, Johanna ^a   Gaide, Olivier ^b,c   Schneider, Pascal ^b   Thesleff, Irma ^a   Mikkola, Marja L ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

Author keywords

Ectodysplasin; Hair placode; Mammary placode; Mouse; Tooth placode

Indexed keywords

BROXURIDINE; ECTODYSPLASIN A1; ISOPROTEIN; RECOMBINANT PROTEIN; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST DEVELOPMENT; CELL FATE; CELL PROLIFERATION; CONTROLLED STUDY; ECTODERM; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; EXPERIMENTAL MODEL; EXPOSURE; FEMALE; GENE OVEREXPRESSION; HAIR FOLLICLE; HAIR GROWTH; IN VITRO STUDY; IN VIVO STUDY; MALE; MESENCHYME; MORPHOGENESIS; MORPHOLOGY; MOUSE; NONHUMAN; ORGANOGENESIS; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SKIN APPENDAGE; SKIN EPITHELIUM; TIME; TOOTH DEVELOPMENT; TRANSGENIC MOUSE;

ANIMALS; CELL DIVISION; ECTODERM; ECTODYSPLASINS; FEMALE; GENE DOSAGE; HAIR; MALE; MAMMARY GLANDS, ANIMAL; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; TOOTH;

ANIMALIA; MAMMALIA; MUS MUSCULUS;

EID: 8444240419     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01377     Document Type: Article

References (83)

1. Andl, T., Reddy, S. T., Gaddapara, T. and Millar, S. E. (2002). WNT signals are required for the initiation of hair follicle development. Dev. Cell 2, 643-653.
2. Balinsky, B. I. (1950). On the prenatal growth of the mammary gland rudiment in the mouse. J. Anat. 84, 227-235.
3. Barsh, G. (1999). Of ancient tales and hairless tails. Nat. Genet. 22, 315-316.
4. Blecher, S. R., Debertin, M. and Murphy, J. S. (1983). Pleiotropic effect of Tabby gene on epidermal growth factor-containing cells of mouse submandibular gland. Anat. Rec. 207, 25-29.
5. Botchkarev, V. A., Botchkareva, N. V., Roth, W., Nakamura, M., Chen, L. H., Herzog, W., Lindner, G., McMahon, J. A., Peters, C., Lauster, R. et al. (1999). Noggin is a mesenchymally derived stimulator of hair-follicle induction. Nat. Cell Biol. 1, 158-164.
6. Celli, G., Larochelle, W. J., Mackem, S., Sharp, R. and Merlino, G. (1998). Soluble dominant-negative receptor uncovers essential roles for fibroblast growth factors in multi-organ induction and patterning. EMBO J. 17, 1642-1655.
7. Chen, Y., Molloy, S. S., Thomas, L., Gambee, J., Bachinger, H. P., Ferguson, B., Zonana, J., Thomas, G. and Morris, N. P. (2001). Mutations within a furin consensus sequence block proteolytic release of ectodysplasin-A and cause X-linked hypohidrotic ectodermal dysplasia. Proc. Natl. Acad. Sci. USA 98, 7218-7223.
8. Chiang, C., Swan, R. Z., Grachtchouk, M., Bolinger, M., Litingtung, Y., Robertson, E. K., Cooper, M. K., Gaffield, W., Westphal, H., Beachy, P. A. et al. (1999). Essential role for Sonic hedgehog during hair follicle morphogenesis. Dev. Biol. 205, 1-9.
9. Clarke, A., Phillips, D. I., Brown, R. and Harper, P. S. (1987). Clinical aspects of X-linked hypohidrotic ectodermal dysplasia. Arch. Dis. Child. 62, 989-996.
10. Claxton, J. H. (1967). The initiation and development of the hair follicle population in tabby mice. Genet. Res. 10 161-171.
11. Courtois, G., Smahi, A., Reichenbach, J., Doffinger, R., Cancrini, C., Bonnet, M., Puel, A., Chable-Bessia, C., Yamaoka, S., Feinberg, J. et al. (2003). A hypermorphic IkappaBalpha mutation is associated with autosomal dominant anhidrotic ectodermal dysplasia and T cell immunodeficiency. J. Clin. Invest. 112, 1108-1115.
12. Cui, C. Y., Durmowicz, M., Tanaka, T. S., Hartung, A. J., Tezuka, T., Hashimoto, K., Ko, M. S., Srivastava, A. K. and Schlessinger, D. (2002). EDA targets revealed by skin gene expression profiles of wild-type, Tabby and Tabby EDA-A1 transgenic mice. Hum. Mol. Genet. 11, 1763-1773.
13. Dassule, H. R. and McMahon, A. P. (1998). Analysis of epithelial-mesenchymal interactions in the initial morphogenesis of the mammalian tooth. Dev. Biol. 202, 215-227.
14. Elomaa, O., Pulkkinen, K., Hannelius, U., Mikkola, M., Saarialho-Kere, U. and Kere, J. (2001). Ectodysplasin is released by proteolytic shedding and binds to the EDAR protein. Hum. Mol. Genet. 10, 953-961
15. Falconer, D. S., Fraser, A. S., King, J. W. B. and King, J. W. (1951). The genetics and development of 'crinkled', a new mutant in the house mouse. J. Genet. 50, 324-344.
16. Fraser, A. S. (1951). Growth of the mouse coat. J. Exp. Zool. 117, 15-29.
17. Gaide, O. and Schneider, P. (2003). Permanent correction of an inherited ectodermal dysplasia with recombinant EDA. Nat. Med. 9, 614-618.
18. 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.
19. Grüneberg, H. (1965). Genes and genotypes affecting the teeth of the mouse. J. Embryol. Exp. Morph. 14, 137-159.
20. Grüneberg, H. (1971). The glandular aspects of the tabby syndrome in the mouse. J. Embryol. Exp. Morph. 25, 1-19.
21. Hardy, M. H. (1992). The secret life of the hair follicle. Trends Genet. 8, 55-61.
22. Headon, D. J. and Overbeek, P. A. (1999). Involvement of a novel TNF receptor homologue in hair follicle induction. Nat. Genet. 22, 370-374.
23. Headon, D. J., Emmal, S. A., Ferguson, B. M., Tucker, A. S., Justice, M. J., Sharpe, P. T., Zonana, J. and Overbeek, P. A. (12001). Gene defect in ectodermal dysplasia implicates a death domain adapter in development. Nature 414, 913-916.
24. Ho, S. N., Hunt, H. D., Horton, R. M., Pullen, J. K. and Pease, L. R. (1989). Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77, 51-59.
25. Huelsken, J., Vogel, R., Erdmann, B., Cotsarelis, G. and Birchmeier, W. (2001). β-catenin controls hair follicle morphogenesis and stem cell differentiation in the skin. Cell 105, 533-545.
26. Jamora, C., DasGupta, R., Kocieniewski, P. and Fuchs, E. (2003). Links between signal transduction, transcription and adhesion in epithelial bud development. Nature 422, 317-322.
27. Jernvall, J. and Thesleff, I. (2000). Reiterative signaling and patterning during mammalian tooth morphogenesis. Mech. Dev. 92, 19-29.
28. Jiang, T. X., Jung, H. S., Widelitz, R. B. and Chuong, C. M. (1999). Self-organization of periodic patterns by dissociated feather mesenchymal cells and the regulation of size, number and spacing of primordia. Development 126, 4997-5009.
29. Jung, H. S. and Chuong, C.-M. (1998). Periodic pattern formation of the feathers, In Molecular basis of epithelial appendage morphogenesis (ed. C.-M. Chuong), pp. 359-369. Austin, TX: R. G. Landes Company.
30. Jung, H. S., Francis-West, P. H., Widelitz, R. B., Jiang, T. X., Ting-Berreth, S., Tickle, C., Wolpert, L. and Chuong, C. M. (1998). Local inhibitory action of BMPs and their relationships with activators in feather formation: implications for periodic patterning. Dev. Biol. 196, 11-23.
31. Kere, J. and Elomaa, O. (2002). Healing a natural knockout of epithelial organogenesis. Trends Mol. Med. 8, 197-200.
32. Kere, J., Srivastava, A. K., Montonen, O., Zonana, J., Thomas, N., Ferguson, B., Munoz, F., Morgan, D., Clarke, A., Baybayan, P. et al. (1996). X-linked anhidrotic (hypohidrotic) ectodermal dysplasia is caused by mutation in a novel transmembrane protein. Nat. Genet. 13, 409-416.
33. Keränen, S. V. E., Åberg, T., Kettunen, P., Thesleff, I. and Jernvall, J. (1998). Association of developmental regulatory genes with the development of different molar tooth shapes in two species of rodents. Dev. Genes Evol. 208, 477-486.
34. Kettunen, P. and Thesleff, I. (1998). Expression and function of FGFs-4, -8, and -9 suggest functional redundancy and repetitive use as epithelial signals during tooth morphogenesis. Dev. Dyn. 211, 256-268.
35. Kim, H. J., Rice, D. P., Kettunen, P. J. and Thesleff, I. (1998). FGF-, BMP-and Shh-mediated signalling pathways in the regulation of cranial suture morphogenesis and calvarial bone development. Development 125, 1241-1251.
36. Koch, A. J. and Meinhardt, H. (1994). Biological pattern formation: from basic mechanisms to complex structures. Rev. Mod. Phys. 66, 1481-1507.
37. Koppinen, P., Pispa, J., Laurikkala, J., Thesleff, I. and Mikkola, M. L. (2001). Signalling and subcellular localization of the TNF receptor Edar. Exp. Cell Res. 269, 180-192.
38. Kratochwil, K., Dull, M., Fariñas, I., Galceran, J. and Grosschedl, R. (1996). Lef1 expression is activated by BMP-4 and regulates inductive tissue interactions in tooth and hair development. Genes Dev. 10, 1382-1394.
39. Kumar, A., Eby, M. T., Sinha, S., Jasmin, A. and Chaudhary, P. M. (2001). The ectodermal dysplasia receptor activates the nuclear factor-kappaB NF-κB, JNK, and cell death pathways and binds to ectodysplasin. Am. J. Biol. Chem. 276, 2668-2677.
40. Laurikkala, J., Mikkola, M., Mustonen, T., Åberg, T., Koppinen, P., Pispa, J., Nieminen, P., Galceran, J., Grosschedl, R. and Thesleff, I. (2001). TNF signaling via the ligand-receptor pair ectodysplasin and edar controls the function of epithelial signaling centers and is regulated by Wnt and activin during tooth organogenesis. Dev. Biol. 229, 443-455.
41. Laurikkala, J., Pispa, J., Jung, H. S., Nieminen, P., Mikkola, M., Wang, X., Saarialho-Kere, U., Galceran, J., Grosschedl, R. and Thesleff, I. (2002). Regulation of hair follicle development by the TNF signal ectodysplasin and its receptor Edar. Development 129, 2541-2553.
42. Lin, C. R., Kioussi, C., O'Connell, S., Briata, P., Szeto, D., Liu, F., Izpisua-Belmonte, J. C. and Rosenfeld, M. G. (1999). Pitx2 regulates lung asymmetry, cardiac positioning and pituitary and tooth morphogenesis. Nature 401, 279-282.
43. Lu, M. F., Cheng, H. T., Kern, M. J., Potter, S. S., Tran, B., Diekwisch, T. G. H. and Martin, J. F. (1999). prx-1 functions cooperatively with another paired-related homeobox gene, prx-2, to maintain cell fates within the craniofacial mesenchyme. Development 126, 495-504.
44. Magerl, M., Tobin, D. J., Muller-Rover, S., Hagen, E., Lindner, G., McKay, I. A. and Paus, R. (2001). Patterns of proliferation and apoptosis during murine hair follicle morphogenesis. J. Invest. Dermatol. 116, 947-955.
45. Mailleux, A. A., Spencer-Dene, B., Dillon, C., Ndiaye, D., Savona-Baron, C., Itoh, N., Kato, S., Dickson, C., Thiery, J. P. and Bellusci, S. (2002). Role of FGF10/FGFR2b signaling during mammary gland development in the mouse embryo. Development 129, 53-60.
46. Mandler, M. and Neubüser, A. (2001). FGF signaling is necessary for the specification of the odontogenic mesenchyme. Dev. Biol. 240, 548-559.
47. Mann, S. J. (1962). Prenatal formation of hair follicle types. Anat. Rec. 144, 135-141.
48. Mikkola, M. L. and Thesleff, I. (2003). Ectodysplasin signaling in development. Cytokine Growth Factor Rev. 14, 211-224.
49. Mikkola, M. L., Pispa, J., Pekkanen, M., Paulin, L., Nieminen, P., Kere, J. and Thesleff, I. (1999). Ectodysplasin, a protein required for epithelial morphogenesis, is a novel TNF homologue and promotes cell-matrix adhesion. Mech. Dev. 88, 133-146.
50. Millar, S. E. (2002). Molecular mechanisms regulating hair follicle development. J. Invest. Dermatol. 118, 216-225.
51. Mina, M. and Kollar, E. J. (1987). The induction of odontogenesis in nondental mesenchyme combined with early murine mandibular arch epithelium. Arch. Oral. Biol. 32, 123-127.
52. Mitsiadis, T. A., Chéraud, Y., Sharpe, P, and Fontaine-Pérus, J. (2003). Development of teeth in chick embryos following mouse neural crest transplantations. Proc. Natl. Acad. Sci. USA 100, 6541-6545.
53. Monreal, A. W., Ferguson, B. M., Headon, D. J., Street, S. L., Overbeek, P. A. and Zonana, J. (1999). Mutations in the human homologue of mouse dl cause autosomal recessive and dominant hypohidrotic ectodermal dysplasia. Nat. Genet. 22, 366-369.
54. Mucchielli, M. L., Mitsiadis, T. A., Raffo, S., Brunet, J. F., Proust, J. P. and Goridis, C. (1997). Mouse Otlx2/RIEG expression in the odontogenic epithelium precedes tooth initiation and requires mesenchyme-derived signals for its maintenance. Dev. Biol. 189 275-284.
55. Mustonen, T., Pispa, J., Mikkola, M. L., Pummila, M., Kangas, A. T., Jaatinen, R. and Thesleff, I. (2003). Stimulation of ectodermal organ development by ectodysplasin-A1. Dev. Biol. 259 123-136.
56. Newton, K., French, D. M., Yan, M., Frantz, G. D. and Dixit, V. M. (2004). Myodegeneration in EDA-A2 transgenic mice is prevented by XEDAR deficiency. Mol. Cell. Biol. 24, 1608-1613.
57. Noramly, S. and Morgan, B. A. (1998). BMPs mediate lateral inhibition at successive stages in feather tract development. Development 125, 3775-3787.
58. Noramly, S., Freeman, A. and Morgan, B. A. (1999). β-catenin signaling can initiate feather bud development. Development 126, 3509-3521.
59. Pispa, J. and Thesleff, I. (2003). Mechanisms of ectodermal organogenesis. Dev. Biol. 262, 195-205.
60. Pispa, J., Jung, H. S., Jernvall, J., Kettunen, P., Mustonen, T., Tabata, M. J., Kere, J. and Thesleff, I. (1999). Cusp patterning defect in Tabby mouse teeth and its partial rescue by FGF. Dev. Biol. 216, 521-534.
61. Pispa, J., Mikkola, M. L., Mustonen, T. and Thesleff, I. (2003). Ectodysplasin, Edar and TNFRSF19 are expressed in complementary and overlapping patterns during mouse embryogenesis. Gene Expr. Patterns 3, 675-679.
62. Propper, A. Y. (1978). Wandering epithelial cells in the rabbit embryo milk line. A preliminary scanning electron microscope study. Dev. Biol. 67, 225-231.
63. Schneider, P., Street, S. L., Gaide, O., Hertig, S., Tardivel, A., Tschopp, J., Runkel, L., Alevizopoulos, K., Ferguson, B. M. and Zonana, J. (2001). Mutations leading to X-linked hypohidrotic ectodermal dysplasia affect three major functional domains in the tumor necrosis factor family member ectodysplasin-A. J. Biol. Chem. 276, 19819-18827.
64. Smahi, A., Courtois, G., Rabia, S. H., Doffinger, R., Bodemer, C., Munnich, A., Casanova, J. L. and Israel, A. (2002). The NF-kappa B signalling pathway in human disease: from incontinentia pigmenti to ectodermal dysplasias and immune-deficiency syndromes. Hum. Mol. Genet. 11, 2371-2375.
65. Sofaer, J. A. (1969). Aspects of the tabby-crinkled-downless syndrome. I. The development of tabby teeth. J. Embryol. Exp. Morph. 22, 181-205.
66. Song, H., Wang, Y. and Goetinck, P. F. (1996). Fibroblast growth factor 2 can replace ectodermal signaling for feather development. Proc. Natl. Acad. Sci. USA 93, 10246-10249.
67. Srivastava, A. K., Durmowicz, M. C., Hartung, A. J., Hudson, J., Ouzts, L. V., Donovan, D. M., Cui, C. Y. and Schlessinger, D. (2001). Ectodysplasin-A1 is sufficient to rescue both hair growth and sweat glands in Tabby mice. Hum. Mol. Genet. 10, 2973-2981.
68. St-Jacques, B., Dassule, H. R., Karavanova, I., Botchkarev, V. A., Li, J., Danielian, P. S., McMahon, J. A., Lewis, P. M., Paus, R. and McMahon, A. P. (1998). Sonic hedgehog signaling is essential for hair development. Curr. Biol. 8, 1058-1068.
69. Thesleff, I. and Mikkola, M. L. (2002a). The role of growth factors in tooth development. Int. Rev. Cytol. 217, 93-135.
70. Thesleff, I. and Mikkola, M. L. (2002b). Death receptor signaling giving life to ectodermal organs. Science's STKE (http://stke.sciencemag.org/cgi/content/full/OC_sigtrans;2002/131/pe22).
71. Travis, A., Amsterdam, A., Belanger, C. and Grosschedl, R. (1991). LEF-1, a gene encoding a lymphoid-specific protein with an HMG domain, regulates T-cell receptor alpha enhancer function. Genes Dev. 5, 880-894.
72. Trumpp, A., Depew, M. J., Rubenstein, J. L., Bishop, J. M. and Martin, G. R. (1999). Cre-mediated gene inactivation demonstrates that FGF8 is required for cell survival and patterning of the first branchial arch. Genes Dev. 13, 3136-3148.
73. Tucker, A. S., Headon, D. J., Schneider, Ferguson, B. M., Overbeek, P., Tschopp, J. and Sharpe, P. T. (2000). Edar/Eda interactions regulate enamel knot formation during tooth morphogenesis. Development 127, 4691-4700.
74. Turing, A. M. (1952). The chemical basis of morphogenesis. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 237 37-72.
75. Vaahtokari, A., Åberg, T., Jernvall, J., Keränen, S. and Thesleff, I. (1996). The enamel knot as a signaling center in the developing mouse tooth. Mech. Dev. 54, 39-43.
76. Vainio, S., Karavanova, I., Jowett, A. and Thesleff, I. (1993). Identification of BMP-4 as a signal mediating secondary induction between epithelial and mesenchymal tissues during early tooth development. Cell 75, 45-58.
77. van Genderen, C., Okamura, R. M., Farinas, I., Quo, R. G., Parslow, T. G., Bruhn, L. and Grosschedl, R. (1994). Development of several organs that require inductive epithelial-mesenchymal interactions is impaired in LEF-1-deficient mice. Genes Dev. 8, 2691-2703.
78. Veltmaat, J. M., Mailleux, A. A., Thiery, J. P. and Bellusci, S. (2003). Mouse embryonic mammogenesis as a model for the molecular regulation of pattern formation. Differentiation 71 1-17.
79. Wessels, N. K. and Roessner, K. D. (1965). Nonproliferation in dermal condensations of mouse vibrissae and pelage hairs. Dev. Biol. 12, 419-433.
80. Wilkinson, D. and Green, J. (1990). In situ hybridization and the three-dimensional reconstruction of serial sections. In Postimplantation Mammalian Embryos (ed. A. J. Copp and D. E. Cole), pp. 155-171. London, UK: Oxford University Press.
81. Yan, M. H., Zhang, Z. M., Brady, J. R., Schilbach, S., Fairbrother, W. J. and Dixit, V. M. (2002). Identification of a novel death domain-containing adaptor molecule for ectodysplasin-a receptor that is mutated in crinkled mice. Curr. Biol. 12, 409-413.
82. Zhang, M., Brancaccio, A., Weiner, L., Missero, C. and Brissette, J. L. (2003). Ectodysplasin regulates pattern formation in the mammalian hair coat. Genesis 37, 30-37.
83. Zonana, J., Elder, M. E., Schneider, L. C., Orlow, S. J., Moss, C., Golabi, M., Shapira, S. K., Farndon, P. A., Wara, D. W., Emmal, S. A. et al. (2000). A novel X-linked disorder of immune deficiency and hypohidrotic ectodermal dysplasia is allelic to incontinentia pigmenti and due to mutations in IKK-gamma (NEMO). Am. J. Hum. Genet. 67, 1555-1562.