Journal of Dermatological Science
Volume 58, Issue 1 , Pages 64-71 , April 2010

Keratinocyte-derived anosmin-1, an extracellular glycoprotein encoded by the X-linked Kallmann syndrome gene, is involved in modulation of epidermal nerve density in atopic dermatitis

  • Suhandy Tengara

      Affiliations

    • Institute for Environmental and Gender Specific Medicine, Juntendo University Graduate School of Medicine, 2-1-1 Tomioka, Urayasu, Chiba 279-0021, Japan
  • ,
  • Mitsutoshi Tominaga

      Affiliations

    • Institute for Environmental and Gender Specific Medicine, Juntendo University Graduate School of Medicine, 2-1-1 Tomioka, Urayasu, Chiba 279-0021, Japan
  • ,
  • Atsuko Kamo

      Affiliations

    • Institute for Environmental and Gender Specific Medicine, Juntendo University Graduate School of Medicine, 2-1-1 Tomioka, Urayasu, Chiba 279-0021, Japan
  • ,
  • Kenichi Taneda

      Affiliations

    • Department of Dermatology, Juntendo University Urayasu Hospital, 2-1-1 Tomioka, Urayasu, Chiba 279-0021, Japan
  • ,
  • Osamu Negi

      Affiliations

    • Institute for Environmental and Gender Specific Medicine, Juntendo University Graduate School of Medicine, 2-1-1 Tomioka, Urayasu, Chiba 279-0021, Japan
    • Department of Dermatology, Juntendo University Urayasu Hospital, 2-1-1 Tomioka, Urayasu, Chiba 279-0021, Japan
  • ,
  • Hideoki Ogawa

      Affiliations

    • Institute for Environmental and Gender Specific Medicine, Juntendo University Graduate School of Medicine, 2-1-1 Tomioka, Urayasu, Chiba 279-0021, Japan
  • ,
  • Kenji Takamori

      Affiliations

    • Institute for Environmental and Gender Specific Medicine, Juntendo University Graduate School of Medicine, 2-1-1 Tomioka, Urayasu, Chiba 279-0021, Japan
    • Department of Dermatology, Juntendo University Urayasu Hospital, 2-1-1 Tomioka, Urayasu, Chiba 279-0021, Japan
    • Corresponding Author InformationCorresponding author at: Department of Dermatology, Juntendo University Urayasu Hospital, 2-1-1 Tomioka, Urayasu, Chiba 279-0021, Japan. Tel.: +81 47 353 3171; fax: +81 47 353 3178.

Received 5 October 2009 ,Revised 10 February 2010 ,Accepted 10 February 2010.

References 

  1. Greaves MW. Itch in systemic disease: therapeutic options. Dermatol Ther. 2005;18:323–327
  2. Ikoma A, Steinhoff M, Ständer S, Yosipovitch G, Schmelz M. The neurobiology of itch. Nat Rev Neurosci. 2006;7:535–547
  3. Paus R, Schmelz M, Bíró T, Steinhoff M. Frontiers in pruritus research: scratching the brain for more effective itch therapy. J Clin Invest. 2006;116:1174–1186
  4. Steinhoff M, Ständer S, Seeliger S, Ansel JC, Schmelz M, Luger T. Modern aspects of cutaneous neurogenic inflammation. Arch Dermatol. 2003;139:1479–1488
  5. Tominaga M, Ozawa S, Ogawa H, Takamori K. A hypothetical mechanism of intraepidermal neurite formation in NC/Nga mice with atopic dermatitis. J Dermatol Sci. 2007;46:199–210
  6. Tominaga M, Ozawa S, Tengara S, Ogawa H, Takamori K. Intraepidermal nerve fibers increase in dry skin of acetone-treated mice. J Dermatol Sci. 2007;48:103–111
  7. Tominaga M, Ogawa H, Takamori K. Decreased production of semaphorin 3A in the lesional skin of atopic dermatitis. Br J Dermatol. 2008;158:842–844
  8. Kakurai M, Monteforte R, Suto H, Tsai M, Nakae S, Galli SJ. Mast cell-derived tumor necrosis factor can promote nerve fiber elongation in the skin during contact hypersensitivity in mice. Am J Pathol. 2006;169:1713–1721
  9. Kim SH, Hu Y, Cadman S, Bouloux P. Diversity in fibroblast growth factor receptor 1 regulation: learning from the investigation of Kallmann syndrome. J Neuroendocrinol. 2008;20:141–163
  10. Soussi-Yanicostas N, Hardelin JP, Arroyo-Jimenez MM, Ardouin O, Legouis R, Levilliers J, et al. Initial characterization of anosmin-1, a putative extracellular matrix protein synthesized by definite neuronal cell populations in the central nervous system. J Cell Sci. 1996;109:1749–1757
  11. Soussi-Yanicostas N, Faivre-Sarrailh C, Hardelin JP, Levilliers J, Rougon G, Petit C. Anosmin-1 underlying the X chromosome-linked Kallmann syndrome is an adhesion molecule that can modulate neurite growth in a cell-type specific manner. J Cell Sci. 1998;111:2953–2965
  12. Soussi-Yanicostas N, de Castro F, Julliard AK, Perfettini I, Chédotal A, Petit C. Anosmin-1, defective in the X-linked form of Kallmann syndrome, promotes axonal branch formation from olfactory bulb output neurons. Cell. 2002;109:217–228
  13. Cariboni A, Pimpinelli F, Colamarino S, Zaninetti R, Piccolella M, Rumio C, et al. The product of X-linked Kallmann's syndrome gene (KAL1) affects the migratory activity of gonadotropin-releasing hormone (GnRH)-producing neurons. Hum Mol Genet. 2004;13:2781–2791
  14. Gianola S, De Castro F, Rossi F. Anosmin-1 stimulates outgrowth and branching of developing purkinje axons. Neuroscience. 2009;158:570–584
  15. Raju R, Dalakas MC. Gene expression profile in the muscles of patients with inflammatory myopathies: effect of therapy with IVIg and biological validation of clinically relevant genes. Brain. 2005;128:1887–1896
  16. Hanafin JM, Rajka G. Diagnostic features of atopic dermatitis. Acta Derm Venereol. 1980;92:44–47
  17. Tominaga M, Kamo A, Tengara S, Ogawa H, Takamori K. In vitro model for penetration of sensory nerve fibres on a Matrigel basement membrane: implications for possible application to intractable pruritus. Br J Dermatol. 2009;161:1028–1037
  18. Bribian A, Esteban PF, Clemente D, Soussi-Yanicostas N, Thomas JL, Zalc B, et al. A novel role for Anosmin-1 in the adhesion and migration of oligodendrocyte precursors. Dev Neurobiol. 2008;16:1503–1516
  19. Hu Y, Guimond SE, Travers P, Cadman S, Hohenester E, Turnbull JE, et al. Novel mechanisms of fibroblast growth factor receptor 1 regulation by extracellular matrix protein anosmin-1. J Biol Chem. 2009;284:29905–29920
  20. Hausott B, Schlick B, Vallant N, Dorn R, Klimaschewski L. Promotion of neurite outgrowth by fibroblast growth factor receptor 1 overexpression and lysosomal inhibition of receptor degradation in pheochromocytoma cells and adult sensory neurons. Neuroscience. 2008;153:461–473
  21. Takano N, Sakurai T, Ohashi Y, Kurachi M. Effects of high-affinity nerve growth factor receptor inhibitors on symptoms in the NC/Nga mouse atopic dermatitis model. Br J Dermatol. 2007;156:241–246
  22. Yamaguchi J, Nakamura F, Aihara M, Yamashita N, Usui H, Hida T, et al. Semaphorin3A alleviates skin lesions and scratching behavior in NC/Nga mice, an atopic dermatitis model. J Invest Dermatol. 2008;128:2842–2849
  23. Sato N, Katsumata N, Kagami M, Hasegawa T, Hori N, Kawakita S, et al. Clinical assessment and mutation analysis of Kallmann syndrome 1 (KAL1) and fibroblast growth factor receptor 1 (FGFR1, or KAL2) in five families and 18 sporadic patients. J Clin Endocrinol Metab. 2004;89:1079–1088
  24. Imai T, Yamazaki T, Kobayakawa R, Kobayakawa K, Abe T, Suzuki M, et al. Pre-target axon sorting establishes the neural map topography. Science. 2009;325:585–590
  25. Menon GK, Grayson S, Elias PM. Ionic calcium reservoirs in mammalian epidermis: ultrastructural localization by ion-capture cytochemistry. J Invest Dermatol. 1985;84:508–512
  26. Hennings H, Michael D, Cheng C, Steinert P, Holbrook K, Yuspa SH. Calcium regulation of growth and differentiation of mouse epidermal cells in culture. Cell. 1980;19:245–254
  27. Hershey GK. IL-13 receptors and signaling pathways: an evolving web. J Allergy Clin Immunol. 2003;111:677–690
  28. Albanesi C, Fairchild HR, Madonna S, Scarponi C, De Pità O, Leung DY, et al. IL-4 and IL-13 negatively regulate TNF-alpha- and IFN-gamma-induced beta-defensin expression through STAT-6, suppressor of cytokine signaling (SOCS)-1, and SOCS-3. J Immunol. 2007;179:984–992
  29. Toda M, Leung DY, Molet S, Boguniewicz M, Taha R, Christodoulopoulos P, et al. Polarized in vivo expression of IL-11 and IL-17 between acute and chronic skin lesions. J Allergy Clin Immunol. 2003;111:875–881
  30. Purwar R, Werfel T, Wittmann M. Regulation of IL-13 receptors in human keratinocytes. J Invest Dermatol. 2007;127:1271–1274
  31. Massagu J. How cells read TGF-β signals. Nat Rev Mol Cell Biol. 2000;1:169–178
  32. Ford JG, Rennick D, Donaldson DD, Venkayya R, McArthur C, Hansell E, et al. IL-13 and IFN-gamma: interactions in lung inflammation. J Immunol. 2001;167:1769–1777
  33. Heller NM, Matsukura S, Georas SN, Boothby MR, Rothman PB, Stellato C, et al. Interferon-gamma inhibits STAT6 signal transduction and gene expression in human airway epithelial cells. Am J Respir Cell Mol Biol. 2004;31:573–582
  34. Leung DY, Boguniewicz M, Howell MD, Nomura I, Hamid QA. New insights into atopic dermatitis. J Clin Invest. 2004;113:651–657
  35. Ong PY, Leung DY. Immune dysregulation in atopic dermatitis. Curr Allergy Asthma Rep. 2006;6:384–389

PII: S0923-1811(10)00054-X

doi: 10.1016/j.jdermsci.2010.02.010

Journal of Dermatological Science
Volume 58, Issue 1 , Pages 64-71 , April 2010