Overexpression of Sonic Hedgehog suppresses embryonic hair follicle morphogenesis

Developmental Biology

Volumn 263, Issue 2, 2003, Pages 203-215

  Ellis, Tammy ^a,b   Smyth, Ian ^a,b,c   Riley, Emily ^a,b   Bowles, Josephine ^a   Adolphe, Christelle ^a,b   Rothnagel, Joseph A ^a   Wicking, Carol ^a,b   Wainwright, Brandon J ^a,b  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b Department of Civil and Environmental Engineering   (Australia)

^c WESTERN GENERAL HOSPITAL   (United Kingdom)

Author keywords

Epidermis; Human keratin 1; Shh; Skin; Sonic hedgehog; Transgenic

Indexed keywords

KERATIN; SONIC HEDGEHOG PROTEIN;

ALOPECIA; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASAL CELL; CANCER GENETICS; COMPARATIVE STUDY; CONTROLLED STUDY; EMBRYO DEVELOPMENT; GENE OVEREXPRESSION; GENE REPRESSION; HAIR FOLLICLE; HAIR GROWTH; HYPERPIGMENTATION; INGUINAL REGION; MORPHOGENESIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN; SKIN DISEASE; TRANSGENIC MOUSE; UNINDEXED SEQUENCE;

ERINACEIDAE; MUS MUSCULUS;

EID: 0242270684     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0012-1606(03)00394-4     Document Type: Article

References (55)

1. Aszterbaum M., Epstein J., Oro A., Douglas V., LeBoit P.E., Scott M.P., Epstein E.H. Jr. Ultraviolet and ionizing radiation enhance the growth of BCCs and trichoblastomas in patched heterozygous knockout mice. Nat. Med. 5:1999;1285-1291.
2. Bitgood M.J., McMahon A.P. Hedgehog and Bmp genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo. Dev. Biol. 172:1995;126-138.
3. Botchkarev V.A., Botchkareva N.V., Sharov A.A., Funa K., Huber O., Gilchrest B.A. Modulation of BMP signaling by noggin is required for induction of the secondary (nontylotrich) hair follicles. J. Invest. Dermatol. 118:2002;3-10.
4. Byrne C., Tainsky M., Fuchs E. Programming gene expression in developing epidermis. Development. 120:1994;2369-2383.
5. Chiang C., Swan R.Z., Grachtchouk M., Bolinger M., Litingtung Y., Robertson E.K., Cooper M.K., Gaffield W., Westphal H., Beachy P.A., Dlugosz A.A. Essential role for Sonic hedgehog during hair follicle morphogenesis. Dev. Biol. 205:1999;1-9.
6. Christiansen J.H., Dennis C.L., Wicking C.A., Monkley S.J., Wilkinson D.G., Wainwright B.J. Murine Wnt-11 and Wnt-12 have temporally and spatially restricted expression patterns during embryonic development. Mech. Dev. 51:1995;341-350.
7. Conacci-Sorrell M., Zhurinsky J., Ben-Ze'ev A. The cadherin-catenin adhesion system in signaling and cancer. J. Clin. Invest. 109:2002;987-991.
8. Dahmane N., Lee J., Robins P., Heller P., Ruiz i Altaba A. Activation of the transcription factor Gli1 and the Sonic hedgehog signalling pathway in skin tumours. Nature. 389:1997;876-881.
9. Falconer, D.S., Fraser, A.S., King, J.W.B. The genetics and development of "Crinkled" a new mutant in the house mouse. J. Genet. 50, 324-346.
10. Fan H., Khavari P.A. Sonic hedgehog opposes epithelial cell cycle arrest. J. Cell Biol. 147:1999;71-76.
11. Fowles L.F., Bennets J.S., Berkman J.L., Williams E., Koopman P., Teasdale R.D., Wicking C. Genomic screen for genes involved in mammalian craniofacial development. Genesis. 35:2003;73-87.
12. Fuchs E., Raghavan S. Getting under the skin of epidermal morphogenesis. Nat. Rev. Genet. 3:2002;199-209.
13. Goodrich L.V., Johnson R.L., Milenkovic L., McMahon J.A., Scott M.P. Conservation of the hedgehog/patched signaling pathway from flies to mice induction of a mouse patched gene by Hedgehog . Genes Dev. 10:1996;301-312.
14. Greenhalgh D.A., Rothnagel J.A., Quintanilla M.I., Orengo C.C., Gagne T.A., Bundman D.S., Longley M.A., Roop D.R. Induction of epidermal hyperplasia, hyperkeratosis, and papillomas in transgenic mice by a targeted v-Ha-ras oncogene. Mol. Carcinog. 7:1993;99-110.
15. Greenhalgh D.A., Rothnagel J.A., Wang X.J., Quintanilla M.I., Orengo C.C., Gagne T.A., Bundman D.S., Longley M.A., Fisher C., Roop D.R. Hyperplasia, hyperkeratosis and benign tumor production in transgenic mice by a targeted v-fos oncogene suggest a role for fos in epidermal differentiation and neoplasia. Oncogene. 8:1993;2145-2157.
16. Gritli-Linde A., Lewis P., McMahon A.P., Linde A. The whereabouts of a morphogen direct evidence for short- and graded long-range activity of hedgehog signaling peptides . Dev. Biol. 236:2001;364-386.
17. Hahn H., Wicking C., Zaphiropoulous P.G., Gailani M.R., Shanley S., Chidambaram A., Vorechovsky I., Holmberg E., Unden A.B., Gillies S., Negus K., Smyth I., Pressman C., Leffell D.J., Gerrard B., Goldstein A.M., Dean M., Toftgard R., Chenevix-Trench G., Wainwright B., Bale A.E. Mutations of the human homolog of Drosophila patched in the nevoid basal cell carcinoma syndrome. Cell. 85:1996;841-851.
18. Hardy M.H. The secret life of the hair follicle. Trends Genet. 8:1992;55-61.
19. Headon D.J., Overbeek P.A. Involvement of a novel Tnf receptor homologue in hair follicle induction. Nat. Genet. 22:1999;370-374.
20. Hogan B., Beddington R., Constantini F., Lacy E. Manipulating the Mouse Embryos. 1994;Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
21. Huelsken J., Birchmeier W. New aspects of Wnt signaling pathways in higher vertebrates. Curr. Opin. Genet. Dev. 11:2001;547-553.
22. Huelsken J., Vogel R., Erdmann B., Cotsarelis G., Birchmeier W. beta-Catenin controls hair follicle morphogenesis and stem cell differentiation in the skin. Cell. 105:2001;533-545.
23. Imakado S., Bickenbach J.R., Bundman D.S., Rothnagel J.A., Attar P.S., Wang X.J., Walczak V.R., Wisniewski S., Pote J., Gordon J.S., et al. Targeting expression of a dominant-negative retinoic acid receptor mutant in the epidermis of transgenic mice results in loss of barrier function. Genes Dev. 9:1995;317-329.
24. Ingham P.W. Transducing Hedgehog the story so far . EMBO J. 17:1998;3505-3511.
25. Ingram W.J., Wicking C.A., Grimmond S.M., Forrest A.R., Wainwright B.J. Novel genes regulated by Sonic Hedgehog in pluripotent mesenchymal cells. Oncogene. 21:2002;8196-8205.
26. Johnson R.L., Rothman A.L., Xie J., Goodrich L.V., Bare J.W., Bonifas J.M., Quinn A.G., Myers R.M., Cox D.R., Epstein E.H. Jr., Scott M.P. Human homolog of patched, a candidate gene for the basal cell nevus syndrome. Science. 272:1996;1668-1671.
27. Kojima T., Morikawa Y., Copeland N.G., Gilbert D.J., Jenkins N.A., Senba E., Kitamura T. TROY, a newly identified member of the tumor necrosis factor receptor superfamily, exhibits a homology with Edar and is expressed in embryonic skin and hair follicles. J. Biol. Chem. 275:2000;20742-20747.
28. Laurikkala J., Pispa J., Jung H.S., Nieminen P., Mikkola M., Wang X., Saarialho-Kere U., Galceran J., Grosschedl R., Thesleff I. Regulation of hair follicle development by the TNF signal ectodysplasin and its receptor Edar. Development. 129:2002;2541-2553.
29. Magerl M., Tobin D.J., Muller-Rover S., Hagen E., Lindner G., McKay I.A., Paus R. Patterns of proliferation and apoptosis during murine hair follicle morphogenesis. J. Invest. Dermatol. 116:2001;947-955.
30. Mahony D., Karunaratne S., Cam G., Rothnagel J.A. Analysis of mouse keratin 6a regulatory sequences in transgenic mice reveals constitutive, tissue-specific expression by a keratin 6a minigene. J. Invest. Dermatol. 115:2000;795-804.
31. Mill P., Mo R., Fu H., Grachtchouk M., Kim P.C., Dlugosz A.A., Hui C.C. Sonic hedgehog-dependent activation of Gli2 is essential for embryonic hair follicle development. Genes Dev. 17:2003;282-294.
32. Moon R.T., Bowerman B., Boutros M., Perrimon N. The promise and perils of Wnt signaling through beta-catenin. Science. 296:2002;1644-1646.
33. Morgan B.A., Orkin R.W., Noramly S., Perez A. Stage-specific effects of sonic hedgehog expression in the epidermis. Dev. Biol. 201:1998;1-12.
34. Murone M., Rosenthal A., de Sauvage F.J. Sonic hedgehog signaling by the patched-smoothened receptor complex. Curr. Biol. 9:1999;76-84.
35. Naito A., Hisahiro Y., Nishioka E., Satoh M., Azuma S., Yamamoto T., Nishikawa S.-I., Inoue J. TRAF6-deficient mice display hypohidrotic ectodermal dysplasia. Proc. Natl. Acad. Sci. USA. 99:2001;8766-8771.
36. Nicolas M., Wolfer A., Raj K., Kummer J.A., Mill P., van Noort M., Hui C., Clevers H., Dotto G.P., Radtke F. Notch1 functions as a tumour suppressor in mouse skin. Nat. Genet. 33:2003;416-421.
37. Nilsson M., Unden A.B., Krause D., Malmqwist U., Raza K., Zaphiropoulos P.G., Toftgard R. Induction of basal cell carcinomas and trichoepitheliomas in mice overexpressing GLI-1. Proc. Natl. Acad. Sci. USA. 97:2000;3438-3443.
38. Nishioka E., Tanaka T., Yoshida H., Matsumura K., Nishikawa S., Naito A., Inoue J., Funasaka Y., Ichihashi M., Miyasaka M. Mucosal addressin cell adhesion molecule 1 plays an unexpected role in the development of mouse guard hair. J. Invest. Dermatol. 119:2002;632-638.
39. Oro A.E., Higgins K.M., Hu Z., Bonifas J.M., Epstein E.H. Jr., Scott M.P. Basal cell carcinomas in mice overexpressing sonic hedgehog. Science. 276:1997;817-821.
40. Paus R., Muller-Rover S., Van Der Veen C., Maurer M., Eichmuller S., Ling G., Hofmann U., Foitzik K., Mecklenburg L., Handjiski B. A comprehensive guide for the recognition and classification of distinct stages of hair follicle morphogenesis. J. Invest. Dermatol. 113:1999;523-532.
41. Ping X.L., Ratner D., Zhang H., Wu X.L., Zhang M.J., Chen F.F., Silvers D.N., Peacocke M., Tsou H.C. PTCH mutations in squamous cell carcinoma of the skin. J. Invest. Dermatol. 116:2001;614-616.
42. Ridanpaa M., Fodde R., Kielman M. Dynamic expression and nuclear accumulation of beta-catenin during the development of hair follicle-derived structures. Mech. Dev. 109:2001;173-181.
43. Rosenthal D.S., Steinert P.M., Chung S., Huff C.A., Johnson J., Yuspa S.H., Roop D.R. A human epidermal differentiation-specific keratin gene is regulated by calcium but not negative modulators of differentiation in transgenic mouse keratinocytes. Cell Growth Differ. 2:1991;107-113.
44. Rothnagel J.A., Greenhalgh D.A., Wang X.J., Sellheyer K., Bickenbach J.R., Dominey A.M., Roop D.R. Transgenic models of skin diseases. Arch. Dermatol. 129:1993;1430-1436.
45. Sato N., Leopold P.L., Crystal R.G. Induction of the hair growth phase in postnatal mice by localized transient expression of Sonic hedgehog. J. Clin. Invest. 104:1999;855-864.
46. Sheng H., Goich S., Wang A., Grachtchouk M., Lowe L., Mo R., Lin K., de Sauvage F.J., Sasaki H., Hui C.C., Dlugosz A.A. Dissecting the oncogenic potential of Gli2 deletion of an NH(2)-terminal fragment alters skin tumor phenotype . Cancer Res. 62:2002;5308-5316.
47. St-Jacques B., Dassule H.R., Karavanova I., Botchkarev V.A., Li J., Danielian P.S., McMahon J.A., Lewis P.M., Paus R., McMahon A.P. Sonic hedgehog signaling is essential for hair development. Curr. Biol. 8:1998;1058-1068.
48. Taylor G., Lehrer M.S., Jensen P.J., Sun T.T., Lavker R.M. Involvement of follicular stem cells in forming not only the follicle but also the epidermis. Cell. 102:2000;451-461.
49. Wang L.C., Liu Z.Y., Gambardella L., Delacour A., Shapiro R., Yang J., Sizing I., Rayhorn P., Garber E.A., Benjamin C.D., Williams K.P., Taylor F.R., Barrandon Y., Ling L., Burkly L.C. Conditional disruption of hedgehog signaling pathway defines its critical role in hair development and regeneration. J. Invest. Dermatol. 114:2000;901-908.
50. Wicking C., Smyth I., Bale A. The hedgehog signalling pathway in tumorigenesis and development. Oncogene. 18:1999;7844-7851.
51. Xie J., Murone M., Luoh S.M., Ryan A., Gu Q., Zhang C., Bonifas J.M., Lam C.W., Hynes M., Goddard A., Rosenthal A., Epstein E.H. Jr., de Sauvage F.J. Activating Smoothened mutations in sporadic basal-cell carcinoma. Nature. 391:1998;90-92.
52. Xin H., Matt D., Qin J.Z., Burg G., Boni R. The sebaceous nevus a nevus with deletions of the PTCH gene . Cancer Res. 59:1999;1834-1836.
53. Yamago G., Takata Y., Furuta I., Urase K., Momoi T., Huh N. Suppression of hair follicle development inhibits induction of sonic hedgehog, patched, and patched-2 in hair germs in mice. Arch. Dermatol. Res. 293:2001;435-441.
54. Yan M., Zhang Z., Brady J.R., Schilbach S., Fairbrother W.J., Dixit V.M. Identification of a novel death domain-containing adaptor molecule for ectodysplasin-A receptor that is mutated in crinkled mice. Curr. Biol. 12:2002;409-413.
55. Zeng X., Goetz J.A., Suber L.M., Scott W.J. Jr., Schreiner C.M., Robbins D.J. A freely diffusible form of Sonic hedgehog mediates long-range signalling. Nature. 411:2001;716-720.