Conditional disruption of hedgehog signaling pathway defines its critical role in hair development and regeneration

Journal of Investigative Dermatology

Volumn 114, Issue 5, 2000, Pages 901-908

  Wang, Li Chun ^a   Liu, Zhong Ying ^a   Gambardella, Laure ^b   Delacour, Alexandra ^b   Shapiro, Renee ^a   Yang, Jianliang ^a   Sizing, Irene ^a   Rayhorn, Paul ^a   Garber, Ellen A ^a   Benjamin, Chris D ^a   Williams, Kevin P ^a   Taylor, Frederick R ^a   Barrandon, Yann ^b   Ling, Leona ^a   Burkly, Linda C ^a  

^a BIOGEN   (United States)

^b ECOLE NORMALE SUPÉRIEURE   (France)

Author keywords

Anti hedgehog antibody; Hair follicle; Hair morphogenesis; Maternal transfer

Indexed keywords

SONIC HEDGEHOG PROTEIN; DROSOPHILA PROTEIN; HEDGEHOG PROTEIN, DROSOPHILA; INSECT PROTEIN; MONOCLONAL ANTIBODY;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO DEVELOPMENT; FEMALE; HAIR GROWTH; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; NEWBORN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; HAIR; HUMAN; IMMUNOLOGY; MALE; MORPHOGENESIS; MOUSE; PHYSIOLOGY; PREGNANCY; PRENATAL DEVELOPMENT; REGENERATION;

ANIMALS; ANTIBODIES, MONOCLONAL; DROSOPHILA PROTEINS; FEMALE; HAIR; HUMANS; INSECT PROTEINS; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MORPHOGENESIS; PREGNANCY; REGENERATION;

EID: 0034183346     PISSN: 0022202X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1523-1747.2000.00951.x     Document Type: Article

References (53)

1. Akiyama H, Shigeno C, Hiraki YH, et al: Cloning of a mouse smoothened cDNA and expression patterns of hedgehog signalling molecules during chondrogenesis and cartilage differentiation in clonal mouse EC cells, ATDC5. Biochem Biophys Res Commun 235:142-147, 1997
2. Alcedo J, Von Ayzenzon M, Ohlen T, Noll M, Hooper JE. The Drosophila smoothened gene encodes a seven-pass membrane protein, a putative receptor for the hedgehog signal. Cell 86:221-232, 1996
3. Arnold HL, Odom RB, James WD: Disease of the skin, clinical dermatology. In: The Skin: Basic Structure and Function. Philadephia: WB Saunders, 1990, pp 1-13
4. Basler K, Struhl G: Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein [see comments]. Nature 368:208-214, 1994
5. Bitgood MJ, Shen L, McMahon AP: Sertoli cell signaling by Desert hedgehog regulates the male germline. Curr Biol 6:298-304, 1996
6. Blair SS, Ralston A: Smoothened-mediated Hedgehog signalling is required for the maintenance of the anterior-posterior lineage restriction in the developing wing of Drosophila. Development 124:4053-4063, 1997
7. Carpenter D, Stone DM, Brush J, et al: Characterization of two patched receptors for the vertebrate hedgehog protein family. Proc Natl Acad Sci USA 95:13630-13634, 1998
8. Chiang C, Litingtung Y, Lee E, et al: Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383:407-413, 1996
9. Chiang C, Swan RZ, Grachtchouk M, et al: Essential role for sonic hedgehog during hair follicle morphogenesis. Dev Biol 205:1-9, 1999
10. Cotsarelis G, Sun TT, Lavker RM: Label-retaining cells reside in the bulge area of pilosebaceons unit: implications for follicular stem cells, hair cycle, and skin carcinogenesis. Cell 61:1329-1337, 1990
11. Diaz-Benjumea FJ, Cohen B, Cohen SM: Cell interaction between compartments establishes the proximal-distal axis of Drosophila legs [see comments]. Nature 372:175-179, 1994
12. Ding Q, Motoyama J, Gasca S, et al: Diminished Sonic hedgehog signaling and lack of floor plate differentiation in Gli2 mutant mice. Development 125:2533-2543, 1998
13. Echelard Y, Epstein DJ, St-Jacques B, et al: Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75:1417-1430, 1993
14. Ericson J, Morton S, Kawakami A, Roelink H, Jessell TM: Two critical periods of Sonic hedgehog signaling required for the specification of motor neuron identity. Cell 87:661-673, 1996
15. Gambardella L, Schneider-Maunoury S, Voiculescu O, Charnay P, Barrandon Y: Dynamic pattern of expression of the transcription factor Krox-20 in mouse hair follicle: implications for hair growth. Mech Dev 2000, in press
16. Gat U, DasGupta R, Degenstein L, Fuchs E: De Novo hair follicle morphogenesis and hair tumors in mice expressing a truncated beta-catenin in skin. Cell 95:605-614, 1998
17. Godwin AR, Capecchi MR: Hoxc13 mutant mice lack external hair. Genes Dev 12:11-20, 1998
18. Goodrich LV, Milenkovic L, Higgins KM, Scott MP: Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 277:1109-1113, 1997
19. Hammerschmidt M, Brook A, McMahon AP: The world according to hedgehog. Trends Genet 13:14-21, 1997
20. Hardcastle Z, Mo R, Hui CC, Sharpe PT: The Shh signalling pathway in tooth development: defects in Gli2 and Gli3 mutants. Development 125:2803-2811, 1998
21. Hardy MH: Glandular metaplasia of hair follicles and other responses to vitamin A excess in cultures of rodent skin. J Embryol Exp Morphol 19:157-180, 1968
22. van den Heuvel M, Ingham PW: smoothened encodes a receptor-like serpentine protein required for hedgehog signalling. Nature 382:547-551, 1996
23. Hui CC, Slusarski D, Platt KA, Holmgren R, Joyner AL: Expression of three mouse homologs of the Drosophila segment polarity gene cubitus interruptus, Gli, Gli-2, and Gli-3, in ectoderm-and mesoderm-derived tissues suggests multiple roles during postimplantation development. Dev Biol 162:402-113, 1994
24. Ingham PW: Transducing Hedgehog: the story so far. EMBO J 17:3505-3511, 1998
25. Ingham PW, Taylor AM, Nakano Y: Role of the Drosophila patched gene in positional signalling. Nature 353:184-187, 1991
26. Iseki S, Araga A, Ohuchi H, et al: Sonic hedgehog is expressed in epithelial cells during development of whisker, hair, and tooth. Biochem Biophys Res Commun 218:688-693, 1996
27. Kinto N, Iwamoto M, Enomoto-Iwamoto M, et al: Fibroblasts expressing Sonic hedgehog induce osteoblast differentiation and ectopic bone formation. FEBS Lett 404:319-323, 1997
28. Kobayashi K, Rochat A, Barrandon Y: Segregation of keratinocyte colony-forming cells in the bulge of the rat vibrissa. Proc Natl Acad Sci USA 90:7391-7395, 1993
29. Le Novere N, Zoli M, Changeux JP: Neuronal nicotinic receptor α6 subunit mRNA is selectively concentrated in catecholaminergic nuclei of the rat brain. Eur J Neurosci 8:2428-2439, 1996
30. Lerner EA: How to make a hybridoma. Yale J Biol Med 54:387-402, 1981
31. Litingtung Y, Lei L, Westphal H, Chiang C: Sonic hedgehog is essential to foregut development. Nat Genet 20:58-61, 1998
32. Majeau GR, Meier W, Jimmo B, Kioussis D, Hochman PS: Mechanism of lymphocyte function-associated molecule 3-Ig fusion proteins inhibition of T cell responses. Structure/function analysis in vitro and in human CD2 transgenic mice. J Immunol 152:2753-2767, 1994
33. Marigo V, Davey RA, Zuo Y, Cunningham JM, Tabin CJ: Biochemical evidence that patched is the Hedgehog receptor. Nature 384:176-179, 1996
34. Miller SJ, Sun T-T, Lavker RM: Hair follicles, stem cells, and skin cancer. J Invest Dermatol 100:288S-294S, 1993
35. Ming JE, Roessler E, Muenke M: Human developmental disorders and the Sonic hedgehog pathway. Mol Med Today 4:343-349, 1998
36. Mo R, Freer AM, Zinyk DL, et al: Specific and redundant functions of Gli2 and Gli3 zinc finger genes in skeletal patterning and development. Development 124:113-123, 1997
37. Motoyama J, Takabatake T, Takeshima K, Hui C: Ptch2, a second mouse Patched gene is co-expressed with Sonic hedgehog. Nat Genet 18:104-106, 1998a
38. Motoyama J, Liu J, Mo R, et al: Essential function of Gli2 and Gli3 in the formation of lung, trachea and oesophagus. Nat Genet 20:54-57, 1998b
39. Nusslein-Volhard C, Lohs-Schardin M, Sander K, Cremer C: A dorso-ventral shift of embryonic primordia in a new maternal-effect mutant of Drosophila. Nature 283:474-476, 1980
40. O'Guin WM, Sun TT, Manabe M: Interaction of trichohyalin with intermediate filaments: three immunologically defined stages of trichohyalin maturation. J Invest Dermatol 98:24-32, 1992
41. Oro AE, Scott MP: Splitting hairs: dissecting roles of signaling systems in epidermal development. Cell 95:575-578, 1998
42. Pepinsky RB, Zeng C, Wen D, et al: Identification of a palmitic acid-modified form of human Sonic hedgehog. J Biol Chem 273:14037-14045, 1998
43. Rennert PD, Browning JL, Mebius R, Mackay F, Hochman PS: Surface lymphotoxin alpha/beta complex is required for the development of peripheral lymphoid organs. J Exp Med 184:1999-2006, 1996
44. Rochat A, Kobayashi K, Barrandon Y: Location of stem cells of human hair follicles by clonal analysis. Cell 76:1063-1073, 1994
45. Roelink H, Augsburger A, Heemskerk J, et al: Floor plate and motor neuron induction by vhh-1, a vertebrate homolog of hedgehog expressed by the notochord. Cell 76:761-775, 1994
46. Sato N, Leopold PL, Crystal RG: Induction of the hair growth phase in postnatal mice by localized transient expression of Sonic hedgehog. J Clin Invest 104:855-864, 1999
47. St-Jacques B, Dassule HR, Karavanova I, et al: Sonic hedgehog signaling is essential for hair development. Curr Biol 8:1058-1068, 1998
48. Stone DM, Hynes M, Armanini M, et al: The tumour-suppressor gene patched encodes a candidate receptor for Sonic hedgehog. Nature 384:129-134, 1996
49. Vortkamp A, Lee K, Lanske B, et al: Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science 273:613-622, 1996
50. Yang JT, Liu CZ, Villavicencio EH, et al: Expression of human GLI in mice results in failure to thrive, early death, and patchy Hirschsprung-like gastrointestinal dilatation. Mol Med 3:826-835, 1997
51. Zecca M, Basler K, Struhl G: Sequential organizing activities of engrailed, hedgehog and decapentaplegic in the Drosophila wing. Development 121:2265-2278, 1995
52. Zhou P, Byrne C, Jacobs J, Fuchs E: Lymphoid enhancer factor 1 directs hair follicle patterning and epithelial cell fate. Genes Dev 9:700-713, 1995
53. Zoller M, Herrmann K, Buchner S, et al: Transient absence of CD44 expression and delay in development by anti-CD44 treatment during ontogeny: a surrogate of an inducible knockout? Cell Growth Differ 8:1211-1223, 1997