Impact of Stat3 activation upon skin biology: A dichotomy of its role between homeostasis and diseases

Journal of Dermatological Science

Volumn 50, Issue 1, 2008, Pages 1-14

  Sano, Shigetoshi ^a   Chan, Keith Syson ^b   DiGiovanni, John ^c  

^a KOCHI UNIVERSITY   (Japan)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TEXAS   (United States)

Author keywords

Carcinogenesis; Gene targeting; Hair cycle; Keratinocyte; Psoriasis; Stat3; Transgenic mouse; UVB induced apoptosis; Wound healing

Indexed keywords

PROTEIN TYROSINE KINASE; STAT3 PROTEIN;

APOPTOSIS; CARCINOGENESIS; CARCINOMA IN SITU; CELL ACTIVATION; CELL MIGRATION; CELL NUCLEUS; CELL PROLIFERATION; CELL SURVIVAL; CHEMICAL CARCINOGENESIS; CYTOPLASM; EXTRACELLULAR SPACE; GENE DISRUPTION; HAIR FOLLICLE; HAIR GROWTH; HOMEOSTASIS; HUMAN; KERATINOCYTE; KNOCKOUT MOUSE; MALIGNANT TRANSFORMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PSORIASIS; RADIATION CARCINOGENESIS; REVIEW; SKIN CARCINOGENESIS; SKIN DISEASE; SKIN FUNCTION; SKIN INJURY; SKIN TUMOR; SQUAMOUS CELL CARCINOMA; ULTRAVIOLET B RADIATION; ULTRAVIOLET RADIATION; WOUND HEALING;

ANIMALS; HAIR FOLLICLE; HOMEOSTASIS; HUMANS; PSORIASIS; SKIN; SKIN NEOPLASMS; SKIN PHYSIOLOGY; STAT3 TRANSCRIPTION FACTOR; ULTRAVIOLET RAYS; WOUND HEALING;

EID: 39149102509     PISSN: 09231811     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jdermsci.2007.05.016     Document Type: Review

References (73)

1. Fu X.Y., Schindler C., Improta T., et al. The proteins of ISGF-3, the interferon alpha-induced transcriptional activator, define a gene family involved in signal transduction. Proc Natl Acad Sci USA 89 (1992) 7840-7843
2. Schindler C., Fu X.Y., Improta T., et al. Proteins of transcription factor ISGF-3: one gene encodes the 91-and 84-kDa ISGF-3 proteins that are activated by interferon alpha. Proc Natl Acad Sci USA 89 (1992) 7836-7839
3. Schindler C., Shuai K., Prezioso V.R., et al. Interferon-dependent tyrosine phosphorylation of a latent cytoplasmic transcription factor. Science 257 (1992) 809-813
4. Darnell Jr. J.E. STATs and gene regulation. Science 277 (1997) 1630-1635
5. Levy D.E., and Darnell Jr. J.E. Stats: transcriptional control and biological impact. Nat Rev Mol Cell Biol 3 (2002) 651-662
6. Bowman T., Garcia R., Turkson J., et al. STATs in oncogenesis. Oncogene 19 (2000) 2474-2488
7. Bromberg J.F. Activation of STAT proteins and growth control. Bioessays 23 (2001) 161-169
8. Bromberg J. Stat proteins and oncogenesis. J Clin Invest 109 (2002) 1139-1142
9. Takeda K., Noguchi K., Shi W., et al. Targeted disruption of the mouse Stat3 gene leads to early embryonic lethality. Proc Natl Acad Sci USA 94 (1997) 3801-3804
10. Levy D.E., and Lee C.K. What does Stat3 do?. J Clin Invest 109 (2002) 1143-1148
11. Hirano T., Ishihara K., and Hibi M. Roles of STAT3 in mediating the cell growth, differentiation and survival signals relayed through the IL-6 family of cytokine receptors. Oncogene 19 (2000) 2548-2556
12. Bromberg J.F., Wrzeszczynska M.H., Devgan G., et al. Stat3 as an oncogene. Cell 98 (1999) 295-303
13. Grandis J.R., Drenning S.D., Zeng Q., et al. Constitutive activation of Stat3 signaling abrogates apoptosis in squamous cell carcinogenesis in vivo. Proc Natl Acad Sci USA 97 (2000) 4227-4232
14. Leong P.L., Andrews G.A., Johnson D.E., et al. Targeted inhibition of Stat3 with a decoy oligonucleotide abrogates head and neck cancer cell growth. Proc Natl Acad Sci USA 100 (2003) 4138-4143
15. Bennett N.T., and Schultz G.S. Growth factors and wound healing: biochemical properties of growth factors and their receptors. Am J Surg 165 (1993) 728-737
16. Martin P. Wound healing-aiming for perfect skin regeneration. Science 276 (1997) 75-81
17. Coffey Jr. R.J., Derynck R., Wilcox J.N., et al. Production and auto-induction of transforming growth factor-alpha in human keratinocytes. Nature 328 (1987) 817-820
18. Marikovsky M., Breuing K., Liu P.Y., et al. Appearance of heparin-binding EGF-like growth factor in wound fluid as a response to injury. Proc Natl Acad Sci USA 90 (1993) 3889-3893
19. Stoll S., Garner W., and Elder J. Heparin-binding ligands mediate autocrine epidermal growth factor receptor activation in skin organ culture. J Clin Invest 100 (1997) 1271-1281
20. Chen J.D., Kim J.P., Zhang K., et al. Epidermal growth factor (EGF) promotes human keratinocyte locomotion on collagen by increasing the alpha 2 integrin subunit. Exp Cell Res 209 (1993) 216-223
21. Pilcher B.K., Dumin J.A., Sudbeck B.D., et al. The activity of collagenase-1 is required for keratinocyte migration on a type I collagen matrix. J Cell Biol 137 (1997) 1445-1457
22. McCawley L.J., O'Brien P., and Hudson L.G. Epidermal growth factor (EGF)- and scatter factor/hepatocyte growth factor (SF/HGF)- mediated keratinocyte migration is coincident with induction of matrix metalloproteinase (MMP)-9. J Cell Physiol 176 (1998) 255-265
23. Boccaccio C., Ando M., Tamagnone L., et al. Induction of epithelial tubules by growth factor HGF depends on the STAT pathway. Nature 391 (1998) 285-288
24. Rajewsky K., Gu H., Kuhn R., et al. Conditional gene targeting. J Clin Invest 98 (1996) 600-603
25. Takeda J., Sano S., Tarutani M., et al. Conditional gene targeting and its application in the skin. J Dermatol Sci 23 (2000) 147-154
26. Takeda K., Kaisho T., Yoshida N., et al. Stat3 activation is responsible for IL-6-dependent T cell proliferation through preventing apoptosis: generation and characterization of T cell-specific Stat3-deficient mice. J Immunol 161 (1998) 4652-4660
27. Tarutani M., Itami S., Okabe M., et al. Tissue-specific knockout of the mouse Pig-a gene reveals important roles for GPI-anchored proteins in skin development. Proc Natl Acad Sci USA 94 (1997) 7400-7405
28. Sano S., Itami S., Takeda K., et al. Keratinocyte-specific ablation of Stat3 exhibits impaired skin remodeling, but does not affect skin morphogenesis. Embo J 18 (1999) 4657-4668
29. Lauffenburger D.A., and Horwitz A.F. Cell migration: a physically integrated molecular process. Cell 84 (1996) 359-369
30. Mitchison T.J., and Cramer L.P. Actin-based cell motility and cell locomotion. Cell 84 (1996) 371-379
31. Kira M., Sano S., Takagi S., et al. STAT3 deficiency in keratinocytes leads to compromised cell migration through hyperphosphorylation of p130(cas). J Biol Chem 277 (2002) 12931-12936
32. Hardy M.H. The secret life of the hair follicle. Trends Genet 8 (1992) 55-61
33. Jahoda C.A., and Reynolds A.J. Dermal-epidermal interactions. Adult follicle-derived cell populations and hair growth. Dermatol Clin 14 (1996) 573-583
34. Peus D., and Pittelkow M.R. Growth factors in hair organ development and the hair growth cycle. Dermatol Clin 14 (1996) 559-572
35. Wilson C., Cotsarelis G., Wei Z.G., et al. Cells within the bulge region of mouse hair follicle transiently proliferate during early anagen: heterogeneity and functional differences of various hair cycles. Differentiation 55 (1994) 127-136
36. Cotsarelis G., Sun T.T., and Lavker R.M. Label-retaining cells reside in the bulge area of pilosebaceous unit: implications for follicular stem cells, hair cycle, and skin carcinogenesis. Cell 61 (1990) 1329-1337
37. Lindner G., Menrad A., Gherardi E., et al. Involvement of hepatocyte growth factor/scatter factor and met receptor signaling in hair follicle morphogenesis and cycling. FASEB J 14 (2000) 319-332
38. Taylor G., Lehrer M.S., Jensen P.J., et al. Involvement of follicular stem cells in forming not only the follicle but also the epidermis. Cell 102 (2000) 451-461
39. Sano S., Takeda J., Yoshikawa K., et al. Tissue regeneration: hair follicle as a model. J Investig Dermatol Symp Proc 6 (2001) 43-48
40. Sano S., Kira M., Takagi S., et al. Two distinct signaling pathways in hair cycle induction: Stat3-dependent and -independent pathways. Proc Natl Acad Sci USA 97 (2000) 13824-13829
41. DiGiovanni J. Multistage carcinogenesis in mouse skin. Pharmacol Ther 54 (1992) 63-128
42. Chan K.S., Carbajal S., Kiguchi K., et al. Epidermal growth factor receptor-mediated activation of Stat3 during multistage skin carcinogenesis. Cancer Res 64 (2004) 2382-2389
43. Chan K.S., Sano S., Kiguchi K., et al. Disruption of Stat3 reveals a critical role in both the initiation and the promotion stages of epithelial carcinogenesis. J Clin Invest 114 (2004) 720-728
44. Brash D.E., Ziegler A., Jonason A.S., et al. Sunlight and sunburn in human skin cancer: p53, apoptosis, and tumor promotion. J Investig Dermatol Symp Proc 1 (1996) 136-142
45. Kraemer K.H. Sunlight and skin cancer: another link revealed. Proc Natl Acad Sci USA 94 (1997) 11-14
46. Brash D.E. Sunlight and the onset of skin cancer. Trends Genet 13 (1997) 410-414
47. de Gruijl F.R., van Kranen H.J., and Mullenders L.H. UV-induced DNA damage, repair, mutations and oncogenic pathways in skin cancer. J Photochem Photobiol B 63 (2001) 19-27
48. Kulms D., and Schwarz T. Molecular mechanisms of UV-induced apoptosis. Photodermatol Photoimmunol Photomed 16 (2000) 195-201
49. Ziegler A., Jonason A.S., Leffell D.J., et al. Sunburn and p53 in the onset of skin cancer. Nature 372 (1994) 773-776
50. Hill L.L., Ouhtit A., Loughlin S.M., et al. Fas ligand: a sensor for DNA damage critical in skin cancer etiology. Science 285 (1999) 898-900
51. Pena J.C., Fuchs E., and Thompson C.B. Bcl-x expression influences keratinocyte cell survival but not terminal differentiation. Cell Growth Differ 8 (1997) 619-629
52. Mahboubi K., Li F., Plescia J., et al. Interleukin-11 up-regulates survivin expression in endothelial cells through a signal transducer and activator of transcription-3 pathway. Lab Invest 81 (2001) 327-334
53. Sano S., Chan K.S., Kira M., et al. Signal transducer and activator of transcription 3 is a key regulator of keratinocyte survival and proliferation following UV irradiation. Cancer Res 65 (2005) 5720-5729
54. Lu Y.P., Lou Y.R., Yen P., et al. Time course for early adaptive responses to ultraviolet B light in the epidermis of SKH-1 mice. Cancer Res 59 (1999) 4591-4602
55. Krueger J.G. The immunologic basis for the treatment of psoriasis with new biologic agents. J Am Acad Dermatol 46 (2002) 1-23 [quiz-6]
56. Nickoloff B.J., and Nestle F.O. Recent insights into the immunopathogenesis of psoriasis provide new therapeutic opportunities. J Clin Invest 113 (2004) 1664-1675
57. Nickoloff B.J., and Stevens S.R. What have we learned in dermatology from the biologic therapies?. J Am Acad Dermatol 54 (2006) S143-S151
58. Barker J.N. The pathophysiology of psoriasis. Lancet 338 (1991) 227-230
59. Hertle M.D., Kubler M.D., Leigh I.M., et al. Aberrant integrin expression during epidermal wound healing and in psoriatic epidermis. J Clin Invest 89 (1992) 1892-1901
60. Ortonne J.P. Aetiology and pathogenesis of psoriasis. Br J Dermatol 135 Suppl. 49 (1996) 1-5
61. Piepkorn M., Pittelkow M.R., and Cook P.W. Autocrine regulation of keratinocytes: the emerging role of heparin-binding, epidermal growth factor-related growth factors. J Invest Dermatol 111 (1998) 715-721
62. McKenzie R.C., and Sabin E. Aberrant signalling and transcription factor activation as an explanation for the defective growth control and differentiation of keratinocytes in psoriasis: a hypothesis. Exp Dermatol 12 (2003) 337-345
63. Sano S., Chan K.S., Carbajal S., et al. Stat3 links activated keratinocytes and immunocytes required for development of psoriasis in a novel transgenic mouse model. Nat Med 11 (2005) 43-49
64. Wrone-Smith T., Johnson T., Nelson B., et al. Discordant expression of Bcl-x and Bcl-2 by keratinocytes in vitro and psoriatic keratinocytes in vivo. Am J Pathol 146 (1995) 1079-1088
65. Bhushan M., McLaughlin B., Weiss J.B., et al. Levels of endothelial cell stimulating angiogenesis factor and vascular endothelial growth factor are elevated in psoriasis. Br J Dermatol 141 (1999) 1054-1060
66. Pittelkow M.R. Psoriasis: more than skin deep. Nat Med 11 (2005) 17-18
67. Zheng Y., Danilenko D.M., Valdez P., et al. Interleukin-22, a T(H)17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis. Nature 445 (2007) 648-651
68. Sa S.M., Valdez P.A., Wu J., et al. The effects of IL-20 subfamily cytokines on reconstituted human epidermis suggest potential roles in cutaneous innate defense and pathogenic adaptive immunity in psoriasis. J Immunol 178 (2007) 2229-2240
69. Atsumi T., Ishihara K., Kamimura D., et al. A point mutation of Tyr-759 in interleukin 6 family cytokine receptor subunit gp130 causes autoimmune arthritis. J Exp Med 196 (2002) 979-990
70. Sawa S., Kamimura D., Jin G.H., et al. Autoimmune arthritis associated with mutated interleukin (IL)-6 receptor gp130 is driven by STAT3/IL-7-dependent homeostatic proliferation of CD4+ T cells. J Exp Med 203 (2006) 1459-1470
71. Nickoloff B.J. Creation of psoriatic plaques: the ultimate tumor suppressor pathway. A new model for an ancient T-cell-mediated skin disease. Viewpoint. J Cutan Pathol 28 (2001) 57-64
72. Nickoloff B.J. The skin cancer paradox of psoriasis: a matter of life and death decisions in the epidermis. Arch Dermatol 140 (2004) 873-875
73. Paltiel O., Adler B., Herschko K., et al. Are patients with psoriasis susceptible to the classic risk factors for actinic keratoses?. Arch Dermatol 140 (2004) 805-810