Epimorphin acts to induce hair follicle anagen in C57BL/6 mice

FASEB Journal

Volumn 17, Issue 14, 2003, Pages 2037-2047

  Takebe, Kyoko ^a   Oka, Yumiko ^a   Radisky, Derek ^b   Tsuda, Hokari ^a   Tochigui, Keiko ^a   Koshida, Shogo ^a   Kogo, Katsuyuki ^a   Hirai, Yohei ^a  

^a SUMITOMO ELECTRIC INDUSTRIES LTD   (Japan)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

Anagen induction; Hair cycle; Molecular dynamics; Morphogenesis; Organ culture assay

Indexed keywords

RECOMBINANT PROTEIN; SYNTAXIN 2; SYNTHETIC PEPTIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; HAIR FOLLICLE; HAIR GROWTH; IMMUNOHISTOCHEMISTRY; MOLECULAR DYNAMICS; MOLECULAR MODEL; MORPHOGENESIS; MOUSE; NONHUMAN; ORGAN CULTURE; PRIORITY JOURNAL; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS; BASE SEQUENCE; FEMALE; HAIR FOLLICLE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; ORGAN CULTURE TECHNIQUES; PEPTIDES; PROTEIN STRUCTURE, TERTIARY; SKIN;

ANIMALIA;

EID: 0242695639     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.03-0386com     Document Type: Article

References (74)

1. Stenn, K. S., and Paus, R. (2001) Controls of hair follicle cycling. Physiol. Rev. 81, 449-494
2. Link, R. E., Paus, R., Stenn, K. S., Kuklinska, E., and Moellmann, G. (1990) Epithelial growth by rat vibrissae follicles in vitro requires mesenchymal contact via native extracellular matrix. J. Invest. Dermatol. 95, 202-207
3. Couchman, J. R. (1993) Hair follicle proteoglycans. J. Invest. Dermatol. 101, 60S-64S
4. Jahoda, C. A., and Reynolds, A. J. (1996) Dermal-epidermal interactions. Adult follicle-derived cell populations and hair growth. Dermatol. Clin. 14, 573-583
5. Peus, D., and Pittelkow, M. R. (1996) Growth factors in hair organ development and the hair growth cycle. Dermatol. Clin. 14, 559-572
6. Nuck, B. A., Fogelson, S. L., and Lucky, A. W. (1987) Topical minoxidil does not act as an antiandrogen in the flank organ of the golden Syrian hamster. Arch. Dermatol. 123, 59-61
7. Paus, R., Stenn, K. S., and Link, R. E. (1989) The induction of anagen hair growth in telogen mouse skin by cyclosporine A administration. Lab. Invest. 60, 365-369
8. Thivolet, J., and Kanitakis, J. (1991) Cyclosporine A in dermatology. Presse Med. 20, 2249-2255
9. Galbraith, H. (1998) Nutritional and hormonal regulation of hair follicle growth and development. Proc. Nutr. Soc. 57, 195-205
10. Hoffmann, R. (2001) Enzymology of the hair follicle. Eur. J. Dermatol. 11, 296-300
11. Yano, K., Brown, L. F., and Detmar, M. (2001) Control of hair growth and follicle size by VEGF-mediated angiogenesis. J. Clin. Invest. 107, 409-417
12. Jindo, T., Tsuboi, R., Takamori, K., and Ogawa, H. (1998) Local injection of hepatocyte growth factor/scatter factor (HGF/SF) alters cyclic growth of murine hair follicles. J. Invest. Dermatol. 110, 338-342
13. Guo, L., Degenstein, L., and Fuchs, E. (1996) Keratinocyte growth factor is required for hair development but not for wound healing. Genes Dev. 10, 165-175
14. Danilenko, D. M., Ring, B. D., Yanagihara, D., Benson, W., Wiemann, B., Starnes, C. O., and Pierce, G. F. (1995) Keratinocyte growth factor is an important endogenous mediator of hair follicle growth, development, and differentiation. Normalization of the nu/nu follicular differentiation defect and amelioration of chemotherapy-induced alopecia. Am. J. Pathol. 147, 145-154
15. Su, H. Y., Hickford, J. G., Bickerstaffe, R., and Paliner, B. R. (1999) Insulin-like growth factor 1 and hair growth. Dermatol. Online J. 5, 1
16. Philpott, M. P., Sanders, D. A., and Kealey, T. (1994) Effects of insulin and insulin-like growth factors on cultured human hair follicles: IGF-I at physiologic concentrations is an important regulator of hair follicle growth in vitro. J. Invest. Dermatol. 102, 857-861
17. du Cros, D. L. (1993) Fibroblast growth factor and epidermal growth factor in hair development. J. Invest. Dermatol. 101, 106S-113S
18. Harmon, C. S., and Nevins, T. D. (1993) IL-1 alpha inhibits human hair follicle growth and hair fiber production in whole-organ cultures. Lymphokine Cytokine Res. 12, 197-203
19. Kishimoto, J., Ehama, R., Wu, L., Jiang, S., Jiang, N., and Burgeson, R. E. (1999) Selective activation of the versican promoter by epithelial-mesenchymal interactions during hair follicle development. Proc. Natl. Acad. Sci. USA 96, 7336-7341
20. Taylor, M., Ashcroft, A. T., Westgate, G. E., Gibson, W. T., and Messenger, A. G. (1992) Glycosaminoglycan synthesis by cultured human hair follicle dermal papilla cells: comparison with non-follicular dermal fibroblasts. Br. J. Dermatol. 126, 479-484
21. Buffey, J. A., Messenger, A. G., Taylor, M., Ashcroft, A. T., Westgate, G. E., and MacNeil, S. (1994) Extracellular matrix derived from hair and skin fibroblasts stimulates human skin melanocyte tyrosinase activity. Br. J. Dermatol. 131, 836-842
22. Chanda, S., Robinette, C. L., Couse, J. F., and Smart, R. C. (2000) 17beta-estradiol and ICI-182780 regulate the hair follicle cycle in mice through an estrogen receptor-alpha pathway. Am. J. Physiol. 278, E202-E210
23. Oh, H. S., and Smart, R. C. (1996) An estrogen receptor pathway regulates the telogen-anagen hair follicle transition and influences epidermal cell proliferation. Proc. Natl. Acad. Sci. USA 93, 12525-12530
24. Jung, H. S., Francis-West, P. H., Widelitz, R. B., Jiang, T. X., Ting-Berreth, S., Tickle, C., Wolpert, L., and Choung, 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
25. Sato, N., Leopold, P. L., and Crystal, R. G. (1999) Induction of the hair growth phase in postnatal mice by localized transient expression of Sonic hedgehog. J. Clin. Invest. 104, 855-864
26. Kishimoto, J., Burgeson, R. E., and Morgan, B. A. (2000) Wnt signaling maintains the hair-inducing activity of the dermal papilla. Genes Dev. 14, 1181-1185
27. Liu, X., Alexander, V., Vijayachandra, K., Bhogte, E., Diamond, I., and Glick, A. (2001) Conditional epidermal expression of TGFbeta 1 blocks neonatal lethality but causes a reversible hyperplasia and alopecia. Proc. Natl. Acad. Sci. USA 98, 9139-9144
28. Hirai, Y. (1994) Sodium-dodecyl-sulfate-resistant complex formation of epimorphin monomers and interaction of the 150-kDa complex with the cell surface. Eur. J. Biochem. 225, 1133-1139
29. Hirai, Y., Takebe, K., Takashina, M., Kobayashi, S., and Takeichi, M. (1992) Epimorphin: a mesenchymal protein essential for epithelial morphogenesis. Cell 69, 471-481
30. Hirai, Y. (2001) Epimorphin as a morphogen: Does a protein for intracellular vesicular targeting act as an extracellular signaling molecule? Cell Biol. Int. 25, 193-195
31. Pelham, H. R. (1993) Is epimorphin involved in vesicular transport? Cell 73, 425-426
32. Bennett, M. K., Garcia-Arraras, J. E., Elferink, L. A., Peterson, K., Fleming, A. M., Hazuka, C. D., and Scheller, R. H. (1993) The syntaxin family of vesicular transport receptors. Cell 74, 863-873
33. Koshida, S., and Hirai, Y. (1997) Identification of cellular recognition sequence of epimorphin and critical role of cell/ epimorphin interaction in lung branching morphogenesis. Biochem. Biophys. Res. Commun. 234, 522-525
34. Hirose, M., Watanabe, S., Oide, H., Kitamura, T., Miyazaki, A., and Sato, N. (1996) A new function of Ito cells in liver morphogenesis: evidence using a novel morphogenic protein, epimorphin, in vitro. Biochem. Biophys. Res. Commun. 225, 155-160
35. Watanabe, S., Hirose, M., Wang, X. E., Ikejima, K., Oide, H., Kitamura, T., Takei, Y., Miyazaki, A., and Sato, N. (1998) A novel hepatic stellate (Ito) cell-derived protein, epimorphin, plays a key role in the late stages of liver regeneration. Biochem. Biophys. Res. Commun. 250, 486-490
36. Zhang, L., Ishikawa, O., Takeuchi, Y., Yokoyama, Y., and Miyachi, Y. (1999) Influences of keratinocyte-fibroblast interaction on the expression of epimorphin by fibroblasts in vitro. J. Dermatol. Sci. 20, 191-196
37. Mori, M., and Miyazaki, K. (2000) Factors affecting morphogenesis of rabbit gallbladder epithelial cells cultured in collagen gels. Cell Tissue Res. 300, 331-344
38. Lehnert, L., Lerch, M. M., Hirai, Y., Kruse, M. L. Schmiegel, W., and Kalthoff, H. (2001) Autocrine stimulation of human pancreatic duct-like development by soluble isoforms of epimorphin in vitro. J. Cell Biol. 152, 911-922
39. Fritsch, C., Swietlicki, E. A., Lefebvre, O., Kedinger, M., Iordanov, H., Levin, M. S., and Rubin, D. C. (2002) Epimorphin expression in intestinal myofibroblasts induces epithelial morphogenesis. J. Clin. Invest. 110, 1629-1641
40. Hirai, Y., Lochter, A., Galosy, S., Koshida, S., Niwa, S., and Bissell, M.J. (1998) Epimorphin functions as a key morphoregulator for mammary epithelial cells. J. Cell Biol. 140, 159-169
41. Hirai, Y., Radisky, D., Boudreau, R., Simian, M., Stevens, M. E., Oka, Y., Takebe, K., Niwa, S., and Bissell, M. J. (2001) Epimorphin mediates mammary luminal morphogenesis through control of C/EBPbeta. J. Cell Biol. 153, 785-794
42. Bull, J.J., Muller-Rover, S., Chronnell, C. M., Paus, R., Philpott, M. P., and McKay, I. A. (2002) Contrasting expression patterns of CCAAT/enhancer-binding protein transcription factors in the hair follicle and at different stages of the hair growth cycle. J. Invest. Dermatol. 118, 17-24
43. Akiyama, M., Amagai, M., Smith, L. T., Hashimoto, K., Shimizu, H., and Nishikawa, T. (1999) Epimorphin expression during human foetal hair follicle development. Br. J. Dermatol. 141, 447-452
44. Fang, K. C. (2000) Mesenchymal regulation of alveolar repair in pulmonary fibrosis. Am. J. Respir. Cell Mol. Biol. 23, 142-145
45. Simian, M., Hirai, Y., Navre, M., Werb, Z., Lochter, A., and Bissell, M. J. (2001) The interplay of matrix metalloproteinases, morphogens and growth factors is necessary for branching of mammary epithelial cells. Development 128, 3117-3131
46. Silver, A. F., and Chase, H. B. (1966) An in vivo method for studying the hair cycle. Nature (London) 210, 1051
47. Mori, O., and Uno, H. (1990) The effect of topical minoxidil on hair follicular cycles of rats. J. Dermatol. 17, 276-281
48. Hamada, K., and Suzuki, K. (1996) Evaluation of biochemical indices as a hair cycle marker in C3H mice. Exp. Anim. 45, 251-256
49. Chase, H. B. (1954) Growth of the hair. Physiol. Rev. 34, 113
50. Oka, Y., and Hirai, Y. (1996) Inductive influences of epimorphin on endothelial cells in vitro. Exp. Cell Res. 222, 189-198
51. Hirai, Y., Nose, A., Kobayashi, S., and Takeichi, M. (1989) Expression and role of E- and P-cadherin adhesion molecules in embryonic histogenesis. II. Skin morphogenesis. Development 105, 271-277
52. Stenn, K. S., Lawrence, L., Veis, D., Korsmeyer, S., and Seiberg, M. (1994) Expression of the bcl-2 protooncogene in the cycling adult mouse hair follicle. J. Invest. Dermatol. 103, 107-111
53. Slominski, A., and Paus, R. (1993) Melanogenesis is coupled to murine anagen: toward new concepts for the role of melanocytes and the regulation of melanogenesis in hair growth. J. Invest. Dermatol. 101, 90S-97S
54. Cornell, W. D., Cieplak, P., Bayly, C. I., Gould, I. R., Merz, K. M., Ferguson, D. M., Spellmeyer, D. C., Fox, T., Caldwell, J. W., and Kollman, P. A. (1995) A second generation force field for the simulation of proteins and nucleic acids. J. Am. Chem. Soc. 117, 5179-5197
55. Jorgensen, W. L., Chandrasekas, J., Madura, J. D., Impey, R. W., and Klein, M. L. (1983) Comparison of simple potential functions for simulation of liquid water. J. Chem. Phys. 79, 926-935
56. Lindner, G., Menrad, A., Gherardi, E., Merlino, G., Welker, P., Handjiski, B., Roloff, B., and Paus, R. (2000) Involvement of hepatocyte growth factor/scatter factor and met receptor signaling in hair follicle morphogenesis and cycling. FASEB J. 14, 319-332
57. Jahoda, C. A., and Reynolds, A. J. (2001) Hair follicle dermal sheath cells: unsung participants in wound healing. Lancet 358, 1445-1448
58. Panteleyev, A. A., Jahoda, C. A., and Christiano, A. M. (2001) Hair follicle predetermination. J. Cell Sci. 114, 3419-3431
59. Peters, E. M., Maurer, M., Botchkarev, V. A., Gordon, D. S., and Paus, R. (1999) Hair growth-modulation by adrenergic drugs. Exp. Dermatol. 8, 274-281
60. Bos, J. D., and Meinardi, M. M. (2000) The 500 Dalton rule for the skin penetration of chemical compounds and drugs. Exp. Dermatol. 9, 165-169
61. Kao, J., Hall, J., and Helman, G. (1988) In vitro percutaneous absorption in mouse skin: influence of skin appendages. Toxicol. Appl. Pharmacol. 94, 93-103
62. Fernandez, I., Ubach, J., Dulubova, I., Zhang, X., Sudhof, T. C., and Rizo, J. (1998) Three-dimensional structure of an evolutionarily conserved N-terminal domain of syntaxin 1A. Cell 94, 841-849
63. Sutton, R. B., Fasshauer, D., Jahn, R., and Brunger, A. T. (1998) Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature (London) 395, 347-353
64. Lerman, J. C., Robblee, J., Fairman, R., and Hughson, F. M. (2000) Structural analysis of the neuronal SNARE protein syntaxin-1A. Biochemistry 39, 8470-8479
65. Jarrousse, F., Boisnic, S., Branchet, M. C., Beranger, J. Y., Godeau, G., Breton, I., Bernard, B. A., and Mahe, Y. F. (2001) Identification of clustered cells in human hair follicle responsible for MMP-9 gelatinolytic activity: consequences for the regulation of hair growth. Int. J. Dermatol. 40, 385-392
66. Davey, H. W., Wilkins, R. J., and Waxman, D. J. (1999) STAT5 signaling in sexually dimorphic gene expression and growth patterns. Am. J. Hum. Genet. 65, 959-965
67. 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
68. Commo, S., and Bernard, B. A. (1997) Immunohistochemical analysis of tissue remodelling during the anagen-catagen transition of the human hair follicle. Br. J. Dermatol. 137, 31-38
69. Lee, S. C., Lee, J. B., Kook, J. P., Seo, J. J., Nato, K. I., Park, S. S., and Kim, Y. P. (1999) Expression of differentiation markers during fetal skin development in humans: immunohistochemical studies on the precursor proteins forming the cornified cell envelope. J. Invest. Dermatol. 112, 882-886
70. O'Keefe, E. J., Hamilton, E. H., Lee, S. C., and Steinert, P. (1993) Trichohyalin: a structural protein of hair, tongue, nail, and epidermis. J. Invest. Dermatol. 101, 65S-71S
71. Schmidt, T., Karsunky, H., Frass, B., Baum, W., Denzel, A., and Moroy, T. (2000) A novel protein (Fbf-1) that binds to CD95/ APO-1/FAS and shows sequence similarity to trichohyalin and plectin. Biochim. Biophys. Acta 1493, 249-254
72. Tobin, D. J., Alhaidari, Z., and Olivry, T. (1998) Equine alopecia areata autoantibodies target multiple hair follicle antigens and may alter hair growth. A preliminary study. Exp. Dermatol. 7, 289-297
73. McElwee, K. J., Boggess, D., Olivry, T., Oliver, R. F., Whiting, D., Tobin, D. J., Bystryn, J. C., King, L. E., Jr., and Sundberg, J. P. (1998) Comparison of alopecia arcata in human and nonhuman mammalian species. Pathobiology 66, 90-107
74. Kulessa, H., Turk, G., and Hogan, B. L. (2000) Inhibition of Bmp signaling affects growth and differentiation in the anagen hair follicle. EMBO J. 19, 6664-6674