Journal of Dermatological Science
Volume 59, Issue 2 , Pages 73-80 , August 2010

Regulation of epidermal keratinocytes by growth factors

Received 15 April 2010 ,Accepted 7 May 2010.

References 

  1. Nickoloff BJ, Xin H, Nestle FO, Qin JZ. The cytokine and chemokine network in psoriasis. Clin Dermatol. 2007;25:568–573
  2. Tokura Y. Extrinsic and intrinsic types of atopic dermatitis. J Dermatol Sci. 2010;58:1–7
  3. Werner S, Grose R. Regulation of wound healing by growth factors and cytokines. Physiol Rev. 2003;83:835–870
  4. Harris RC, Chung E, Coffey RJ. EGF receptor ligands. Exp Cell Res. 2003;284:2–13
  5. Higashiyama S, Iwabuki H, Morimoto C, Hieda M, Inoue H, Matsushita N. Membrane-anchored growth factors, the epidermal growth factor family: beyond receptor ligands. Cancer Sci. 2008;99:214–220
  6. Jorissen RN, Walker F, Pouliot N, Garrett TP, Ward CW, Burgess AW. Epidermal growth factor receptor: mechanisms of activation and signalling. Exp Cell Res. 2003;284:31–53
  7. Hashimoto K. Regulation of keratinocyte function by growth factors. J Dermatol Sci. 2000;24:S46–S50
  8. Coffey RJ, Derynck R, Wilcox JN, Bringman TS, Goustin AS, Moses HL, et al. Production and auto-induction of transforming growth factor-alpha in human keratinocytes. Nature. 1987;328:817–820
  9. Elder JT, Fisher GJ, Lindquist PB, Bennett GL, Pittelkow MR, Coffey RJ, et al. Overexpression of transforming growth factor alpha in psoriatic epidermis. Science. 1989;243:811–814
  10. Cook PW, Pittelkow MR, Keeble WW, Graves-Deal R, Coffey RJ, Shipley GD. Amphiregulin messenger RNA is elevated in psoriatic epidermis and gastrointestinal carcinomas. Cancer Res. 1992;52:3224–3227
  11. Higashiyama S, Abraham JA, Miller J, Fiddes JC, Klagsbrun M. A heparin-binding growth factor secreted by macrophage-like cells that is related to EGF. Science. 1991;251:936–939
  12. Hashimoto K, Higashiyama S, Asada H, Hashimura E, Kobayashi T, Sudo K, et al. Heparin-binding epidermal growth factor-like growth factor is an autocrine growth factor for human keratinocytes. J Biol Chem. 1994;269:20060–20066
  13. Zheng Y, Peng Z, Wang Y, Tan S, Xi Y, Wang G. Alteration and significance of heparin-binding epidermal-growth-factor-like growth factor in psoriatic epidermis. Dermatology. 2003;207:22–27
  14. Shirakata Y, Tokumaru S, Sayama K, Hashimoto K. Auto- and cross-induction by betacellulin in epidermal keratinocytes. J Dermatol Sci. 2010;58:162–164
  15. Piepkorn M, Predd H, Underwood R, Cook P. Proliferation-differentiation relationships in the expression of heparin-binding epidermal growth factor-related factors and erbB receptors by normal and psoriatic human keratinocytes. Arch Dermatol Res. 2003;295:93–101
  16. Shirakata Y, Kishimoto J, Tokumaru S, Yamasaki K, Hanakawa Y, Tohyama M, et al. Epiregulin, a member of the EGF family, is over-expressed in psoriatic epidermis. J Dermatol Sci. 2007;45:69–72
  17. Shirakata Y, Komurasaki T, Toyoda H, Hanakawa Y, Yamasaki K, Tokumaru S, et al. Epiregulin, a novel member of the epidermal growth factor family, is an autocrine growth factor in normal human keratinocytes. J Biol Chem. 2000;275:5748–5753
  18. Miettinen PJ, Berger JE, Meneses J, Phung Y, Pedersen RA, Werb Z, et al. Epithelial immaturity and multiorgan failure in mice lacking epidermal growth factor receptor. Nature. 1995;376:337–341
  19. Sibilia M, Wagner EF. Strain-dependent epithelial defects in mice lacking the EGF receptor. Science. 1995;269:234–238
  20. Threadgill DW, Dlugosz AA, Hansen LA, Tennenbaum T, Lichti U, Yee D, et al. Targeted disruption of mouse EGF receptor: effect of genetic background on mutant phenotype. Science. 1995;269:230–234
  21. Fowler KJ, Walker F, Alexander W, Hibbs ML, Nice EC, Bohmer RM, et al. A mutation in the epidermal growth factor receptor in waved-2 mice has a profound effect on receptor biochemistry that results in impaired lactation. Proc Natl Acad Sci USA. 1995;92:1465–1469
  22. Murillas R, Larcher F, Conti CJ, Santos M, Ullrich A, Jorcano JL. Expression of a dominant negative mutant of epidermal growth factor receptor in the epidermis of transgenic mice elicits striking alterations in hair follicle development and skin structure. Embo J. 1995;14:5216–5223
  23. Sugawara K, Schneider MR, Dahlhoff M, Kloepper JE, Paus R. Cutaneous consequences of inhibiting EGF receptor signaling in vivo: normal hair follicle development, but retarded hair cycle induction and inhibition of adipocyte growth in Egfr(Wa5) mice. J Dermatol Sci. 2010;57:155–161
  24. Luetteke NC, Qiu TH, Peiffer RL, Oliver P, Smithies O, Lee DC. TGF alpha deficiency results in hair follicle and eye abnormalities in targeted and waved-1 mice. Cell. 1993;73:263–278
  25. Kim I, Mogford JE, Chao JD, Mustoe TA. Wound epithelialization deficits in the transforming growth factor-alpha knockout mouse. Wound Repair Regen. 2001;9:386–390
  26. Luetteke NC, Qiu TH, Fenton SE, Troyer KL, Riedel RF, Chang A, et al. Targeted inactivation of the EGF and amphiregulin genes reveals distinct roles for EGF receptor ligands in mouse mammary gland development. Development. 1999;126:2739–2750
  27. Shirasawa S, Sugiyama S, Baba I, Inokuchi J, Sekine S, Ogino K, et al. Dermatitis due to epiregulin deficiency and a critical role of epiregulin in immune-related responses of keratinocyte and macrophage. Proc Natl Acad Sci USA. 2004;101:13921–13926
  28. Shirakata Y, Kimura R, Nanba D, Iwamoto R, Tokumaru S, Morimoto C, et al. Heparin-binding EGF-like growth factor accelerates keratinocyte migration and skin wound healing. J Cell Sci. 2005;118:2363–2370
  29. Dominey AM, Wang XJ, King LE, Nanney LB, Gagne TA, Sellheyer K, et al. Targeted overexpression of transforming growth factor alpha in the epidermis of transgenic mice elicits hyperplasia, hyperkeratosis, and spontaneous, squamous papillomas. Cell Growth Differ. 1993;4:1071–1082
  30. Cook PW, Piepkorn M, Clegg CH, Plowman GD, DeMay JM, Brown JR, et al. Transgenic expression of the human amphiregulin gene induces a psoriasis-like phenotype. J Clin Invest. 1997;100:2286–2294
  31. Mak KK, Chan SY. Epidermal growth factor as a biologic switch in hair growth cycle. J Biol Chem. 2003;278:26120–26126
  32. Schneider MR, Antsiferova M, Feldmeyer L, Dahlhoff M, Bugnon P, Hasse S, et al. Betacellulin regulates hair follicle development and hair cycle induction and enhances angiogenesis in wounded skin. J Invest Dermatol. 2008;128:1256–1265
  33. Eswarakumar VP, Lax I, Schlessinger J. Cellular signaling by fibroblast growth factor receptors. Cytokine Growth Factor Rev. 2005;16:139–149
  34. Sogabe Y, Abe M, Yokoyama Y, Ishikawa O. Basic fibroblast growth factor stimulates human keratinocyte motility by Rac activation. Wound Repair Regen. 2006;14:457–462
  35. Finch PW, Rubin JS, Miki T, Ron D, Aaronson SA. Human KGF is FGF-related with properties of a paracrine effector of epithelial cell growth. Science. 1989;245:752–755
  36. Werner S. Keratinocyte growth factor: a unique player in epithelial repair processes. Cytokine Growth Factor Rev. 1998;9:153–165
  37. Marchese C, Chedid M, Dirsch OR, Csaky KG, Santanelli F, Latini C, et al. Modulation of keratinocyte growth factor and its receptor in reepithelializing human skin. J Exp Med. 1995;182:1369–1376
  38. Guo L, Degenstein L, Fuchs E. Keratinocyte growth factor is required for hair development but not for wound healing. Genes Dev. 1996;10:165–175
  39. Sato C, Tsuboi R, Shi CM, Rubin JS, Ogawa H. Comparative study of hepatocyte growth factor/scatter factor and keratinocyte growth factor effects on human keratinocytes. J Invest Dermatol. 1995;104:958–963
  40. Gohda E, Tsubouchi H, Nakayama H, Hirono S, Sakiyama O, Takahashi K, et al. Purification and partial characterization of hepatocyte growth factor from plasma of a patient with fulminant hepatic failure. J Clin Invest. 1988;81:414–419
  41. Giordano S, Di Renzo MF, Narsimhan RP, Cooper CS, Rosa C, Comoglio PM. Biosynthesis of the protein encoded by the c-met proto-oncogene. Oncogene. 1989;4:1383–1388
  42. Matsumoto K, Hashimoto K, Yoshikawa K, Nakamura T. Marked stimulation of growth and motility of human keratinocytes by hepatocyte growth factor. Exp Cell Res. 1991;196:114–120
  43. Tokumaru S, Sayama K, Yamasaki K, Shirakata Y, Hanakawa Y, Yahata Y, et al. SOCS3/CIS3 negative regulation of STAT3 in HGF-induced keratinocyte migration. Biochem Biophys Res Commun. 2005;327:100–105
  44. Botchkarev VA, Yaar M, Peters EM, Raychaudhuri SP, Botchkareva NV, Marconi A, et al. Neurotrophins in skin biology and pathology. J Invest Dermatol. 2006;126:1719–1727
  45. Segal RA. Selectivity in neurotrophin signaling: theme and variations. Annu Rev Neurosci. 2003;26:299–330
  46. Marconi A, Terracina M, Fila C, Franchi J, Bonte F, Romagnoli G, et al. Expression and function of neurotrophins and their receptors in cultured human keratinocytes. J Invest Dermatol. 2003;121:1515–1521
  47. Di Marco E, Mathor M, Bondanza S, Cutuli N, Marchisio PC, Cancedda R, et al. Nerve growth factor binds to normal human keratinocytes through high and low affinity receptors and stimulates their growth by a novel autocrine loop. J Biol Chem. 1993;268:22838–22846
  48. Pincelli C, Marconi A. Autocrine nerve growth factor in human keratinocytes. J Dermatol Sci. 2000;22:71–79
  49. Tavakkol A, Elder JT, Griffiths CE, Cooper KD, Talwar H, Fisher GJ, et al. Expression of growth hormone receptor, insulin-like growth factor 1 (IGF-1) and IGF-1 receptor mRNA and proteins in human skin. J Invest Dermatol. 1992;99:343–349
  50. Sadagurski M, Yakar S, Weingarten G, Holzenberger M, Rhodes CJ, Breitkreutz D, et al. Insulin-like growth factor 1 receptor signaling regulates skin development and inhibits skin keratinocyte differentiation. Mol Cell Biol. 2006;26:2675–2687
  51. Imokawa G, Yada Y, Kimura M, Morisaki N. Granulocyte/macrophage colony-stimulating factor is an intrinsic keratinocyte-derived growth factor for human melanocytes in UVA-induced melanosis. Biochem J. 1996;313(Pt 2):625–631
  52. Kawada A, Hiruma M, Noguchi H, Ishibashi A, Motoyoshi K, Kawada I. Granulocyte and macrophage colony-stimulating factors stimulate proliferation of human keratinocytes. Arch Dermatol Res. 1997;289:600–602
  53. Mann A, Breuhahn K, Schirmacher P, Blessing M. Keratinocyte-derived granulocyte-macrophage colony stimulating factor accelerates wound healing: stimulation of keratinocyte proliferation, granulation tissue formation, and vascularization. J Invest Dermatol. 2001;117:1382–1390
  54. Fang Y, Gong SJ, Xu YH, Hambly BD, Bao S. Impaired cutaneous wound healing in granulocyte/macrophage colony-stimulating factor knockout mice. Br J Dermatol. 2007;157:458–465
  55. Bagnato A, Venuti A, Di Castro V, Marcante ML. Identification of the ETA receptor subtype that mediates endothelin induced autocrine proliferation of normal human keratinocytes. Biochem Biophys Res Commun. 1995;209:80–86
  56. Tsuboi R, Sato C, Shi CM, Nakamura T, Sakurai T, Ogawa H. Endothelin-1 acts as an autocrine growth factor for normal human keratinocytes. J Cell Physiol. 1994;159:213–220
  57. Yahata Y, Shirakata Y, Tokumaru S, Yang L, Dai X, Tohyama M, et al. A novel function of angiotensin II in skin wound healing, Induction of fibroblast and keratinocyte migration by angiotensin II via heparin-binding epidermal growth factor (EGF)-like growth factor-mediated EGF receptor transactivation. J Biol Chem. 2006;281:13209–13216
  58. Kataoka H. EGFR ligands and their signaling scissors, ADAMs, as new molecular targets for anticancer treatments. J Dermatol Sci. 2009;56:148–153
  59. Tokumaru S, Sayama K, Shirakata Y, Komatsuzawa H, Ouhara K, Hanakawa Y, et al. Induction of keratinocyte migration via transactivation of the epidermal growth factor receptor by the antimicrobial peptide LL-37. J Immunol. 2005;175:4662–4668
  60. Massague J. TGF-beta signal transduction. Annu Rev Biochem. 1998;67:753–791
  61. Ihn H. Autocrine TGF-beta signaling in the pathogenesis of systemic sclerosis. J Dermatol Sci. 2008;49:103–113
  62. Miyazono K, ten Dijke P, Heldin CH. TGF-beta signaling by Smad proteins. Adv Immunol. 2000;75:115–157
  63. Nakao A, Afrakhte M, Moren A, Nakayama T, Christian JL, Heuchel R, et al. Identification of Smad7, a TGFbeta-inducible antagonist of TGF-beta signalling. Nature. 1997;389:631–635
  64. Imamura T, Takase M, Nishihara A, Oeda E, Hanai J, Kawabata M, et al. Smad6 inhibits signalling by the TGF-beta superfamily. Nature. 1997;389:622–626
  65. Pietenpol JA, Holt JT, Stein RW, Moses HL. Transforming growth factor beta 1 suppression of c-myc gene transcription: role in inhibition of keratinocyte proliferation. Proc Natl Acad Sci USA. 1990;87:3758–3762
  66. Matsumoto K, Hashimoto K, Hashiro M, Yoshimasa H, Yoshikawa K. Modulation of growth and differentiation in normal human keratinocytes by transforming growth factor-beta. J Cell Physiol. 1990;145:95–101
  67. Midorikawa K, Sayama K, Shirakata Y, Hanakawa Y, Sun L, Hashimoto K. Expression of vitamin D receptor in cultured human keratinocytes and fibroblasts is not altered by corticosteroids. J Dermatol Sci. 1999;21:8–12
  68. Reichrath J, Munssinger T, Kerber A, Rochette-Egly C, Chambon P, Bahmer FA, et al. In situ detection of retinoid-X receptor expression in normal and psoriatic human skin. Br J Dermatol. 1995;133:168–175
  69. Matsumoto K, Hashimoto K, Nishida Y, Hashiro M, Yoshikawa K. Growth-inhibitory effects of 1, 25-dihydroxyvitamin D3 on normal human keratinocytes cultured in serum-free medium. Biochem Biophys Res Commun. 1990;166:916–923
  70. Shirakata Y, Ueno H, Hanakawa Y, Kameda K, Yamasaki K, Tokumaru S, et al. TGF-beta is not involved in early phase growth inhibition of keratinocytes by 1alpha, 25(OH)2vitamin D3. J Dermatol Sci. 2004;36:41–50
  71. Takahashi H, Ibe M, Kinouchi M, Ishida-Yamamoto A, Hashimoto Y, Iizuka H. Similarly potent action of 1,25-dihydroxyvitamin D3 and its analogues, tacalcitol, calcipotriol, and maxacalcitol on normal human keratinocyte proliferation and differentiation. J Dermatol Sci. 2003;31:21–28
  72. Nickoloff BJ, Mahrle G, Morhenn V. Ultrastructural effects of recombinant gamma-interferon on cultured human keratinocytes. Ultrastruct Pathol. 1986;10:17–21
  73. Karlsson T, Vahlquist A, Torma H. Keratinocyte differentiation induced by calcium, phorbol ester or interferon-gamma elicits distinct changes in the retinoid signalling pathways. J Dermatol Sci. 2010;57:207–213
  74. Saunders NA, Jetten AM. Control of growth regulatory and differentiation-specific genes in human epidermal keratinocytes by interferon gamma, Antagonism by retinoic acid and transforming growth factor beta 1. J Biol Chem. 1994;269:2016–2022
  75. Uchi H, Terao H, Koga T, Furue M. Cytokines and chemokines in the epidermis. J Dermatol Sci. 2000;24(Suppl. 1):S29–S38
  76. Ansel J, Perry P, Brown J, Damm D, Phan T, Hart C, et al. Cytokine modulation of keratinocyte cytokines. J Invest Dermatol. 1990;94:101S–107S
  77. Grabbe J, Welker P, Dippel E, Czarnetzki BM. Stem cell factor, a novel cutaneous growth factor for mast cells and melanocytes. Arch Dermatol Res. 1994;287:78–84
  78. Shirakata Y, Tokumaru S, Yamasaki K, Sayama K, Hashimoto K. So-called biological dressing effects of cultured epidermal sheets are mediated by the production of EGF family, TGF-beta and VEGF. J Dermatol Sci. 2003;32:209–215
  79. Detmar M. The role of VEGF and thrombospondins in skin angiogenesis. J Dermatol Sci. 2000;24(Suppl 1):S78–84
  80. Streit M, Riccardi L, Velasco P, Brown LF, Hawighorst T, Bornstein P, et al. Thrombospondin-2: a potent endogenous inhibitor of tumor growth and angiogenesis. Proc Natl Acad Sci USA. 1999;96:14888–14893
  81. Locksley RM, Killeen N, Lenardo MJ. The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell. 2001;104:487–501
  82. Kock A, Schwarz T, Kirnbauer R, Urbanski A, Perry P, Ansel JC, et al. Human keratinocytes are a source for tumor necrosis factor alpha: evidence for synthesis and release upon stimulation with endotoxin or ultraviolet light. J Exp Med. 1990;172:1609–1614
  83. Bashir MM, Sharma MR, Werth VP. TNF-alpha production in the skin. Arch Dermatol Res. 2009;301:87–91
  84. Trefzer U, Brockhaus M, Lotscher H, Parlow F, Budnik A, Grewe M, et al. The 55-kD tumor necrosis factor receptor on human keratinocytes is regulated by tumor necrosis factor-alpha and by ultraviolet B radiation. J Clin Invest. 1993;92:462–470
  85. Li H, Lin X. Positive and negative signaling components involved in TNFalpha-induced NF-kappaB activation. Cytokine. 2008;41:1–8
  86. Vanden Berghe W, Plaisance S, Boone E, De Bosscher K, Schmitz ML, Fiers W, et al. p38 and extracellular signal-regulated kinase mitogen-activated protein kinase pathways are required for nuclear factor-kappaB p65 transactivation mediated by tumor necrosis factor. J Biol Chem. 1998;273:3285–3290
  87. Koo J, Khera P. Update on the mechanisms and efficacy of biological therapies for psoriasis. J Dermatol Sci. 2005;38:75–87
  88. Grone A. Keratinocytes and cytokines. Vet Immunol Immunopathol. 2002;88:1–12
  89. Kunz S, Wolk K, Witte E, Witte K, Doecke WD, Volk HD, et al. Interleukin (IL)-19, IL-20 and IL-24 are produced by and act on keratinocytes and are distinct from classical ILs. Exp Dermatol. 2006;15:991–1004
  90. Tohyama M, Hanakawa Y, Shirakata Y, Dai X, Yang L, Hirakawa S, et al. IL-17 and IL-22 mediate IL-20 subfamily cytokine production in cultured keratinocytes via increased IL-22 receptor expression. Eur J Immunol. 2009;39:2779–2788
  91. Yawalkar N, Tscharner GG, Hunger RE, Hassan AS. Increased expression of IL-12p70 and IL-23 by multiple dendritic cell and macrophage subsets in plaque psoriasis. J Dermatol Sci. 2009;54:99–105
  92. Kanda N, Watanabe S. Suppressive effects of antimycotics on tumor necrosis factor-alpha-induced CCL27, CCL2, and CCL5 production in human keratinocytes. Biochem Pharmacol. 2006;72:463–473
  93. Lee BS, Shim SM, Heo J, Pae HO, Seo BY, Han SY, et al. Wogonin suppresses TARC expression induced by mite antigen via heme oxygenase 1 in human keratinocytes, Suppressive effect of wogonin on mite antigen-induced TARC expression. J Dermatol Sci. 2007;46:31–40
  94. Nishi N, Yamamoto S, Ou W, Muro E, Inada Y, Hamasaki Y. Enhanced CCL26 production by IL-4 through IFN-gamma-induced upregulation of type 1 IL-4 receptor in keratinocytes. Biochem Biophys Res Commun. 2008;376:234–240
  95. Ohara H, Saito R, Hirakawa S, Shimada M, Mano N, Okuyama R, et al. Gene expression profiling defines the role of ATP-exposed keratinocytes in skin inflammation. J Dermatol Sci. 2010;
  96. Sugaya M, Nakamura K, Mitsui H, Takekoshi T, Saeki H, Tamaki K. Human keratinocytes express fractalkine/CX3CL1. J Dermatol Sci. 2003;31:179–187
  97. Tarutani M, Imai Y, Yasuda K, Tsutsui H, Nakanishi K, Yamanishi K. Neutrophil-dominant psoriasis-like skin inflammation induced by epidermal-specific expression of Raf in mice. J Dermatol Sci. 2010;58:28–35
  98. Tohyama M, Sayama K, Komatsuzawa H, Hanakawa Y, Shirakata Y, Dai X, et al. CXCL16 is a novel mediator of the innate immunity of epidermal keratinocytes. Int Immunol. 2007;19:1095–1102
  99. Tohyama M, Shirakara Y, Yamasaki K, Sayama K, Hashimoto K. Differentiated keratinocytes are responsible for TNF-alpha regulated production of macrophage inflammatory protein 3alpha/CCL20, a potent chemokine for Langerhans cells. J Dermatol Sci. 2001;27:130–139
  100. Tsuda T, Tohyama M, Yamasaki K, Shirakata Y, Yahata Y, Tokumaru S, et al. Lack of evidence for TARC/CCL17 production by normal human keratinocytes in vitro. J Dermatol Sci. 2003;31:37–42

PII: S0923-1811(10)00163-5

doi: 10.1016/j.jdermsci.2010.05.002

Journal of Dermatological Science
Volume 59, Issue 2 , Pages 73-80 , August 2010