Two mechanisms regulate keratin K15 expression in keratinocytes: Role of PKC/AP-1 and FOXM1 mediated signalling

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Bose, Amrita ^a   Teh, Muy Teck ^a   Hutchison, Iain L ^a   Wan, Hong ^a   Leigh, Irene M ^b   Waseem, Ahmad ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINYLGLYCYLASPARTIC ACID; BETA1 INTEGRIN; CELL CYCLE PROTEIN; CYTOKERATIN 14; CYTOKERATIN 15; FIBRONECTIN; MESSENGER RNA; METHYLCELLULOSE; PHORBOL ESTER; PROTEIN C JUN; PROTEIN FOXM1; PROTEIN KINASE C; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR AP 1; UNCLASSIFIED DRUG;

ARTICLE; BASAL CELL; CELL DENSITY; CELL DIFFERENTIATION; CELL SPECIFICITY; CELL STIMULATION; CELL SUSPENSION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME INHIBITION; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; KERATINOCYTE; POLYMERASE CHAIN REACTION; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN MOTIF; REGULATORY MECHANISM; RNA INTERFERENCE; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

BLOTTING, WESTERN; CELL DIFFERENTIATION; CELLS, CULTURED; EPIDERMIS; FIBRONECTINS; FLUORESCENT ANTIBODY TECHNIQUE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION PROFILING; HUMANS; KERATIN-15; KERATINOCYTES; OLIGOPEPTIDES; PROTEIN KINASE C-DELTA; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SKIN; STEM CELLS; TRANSCRIPTION FACTOR AP-1;

EID: 84862996253     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0038599     Document Type: Article

References (88)

1. Barrandon Y, Green H, (1987) Three clonal types of keratinocyte with different capacities for multiplication. Proc Natl Acad Sci U S A 84: 2302-2306.
2. Cotsarelis G, Sun TT, Lavker RM, (1990) Label-retaining cells reside in the bulge area of pilosebaceous unit: implications for follicular stem cells, hair cycle, and skin carcinogenesis. Cell 61: 1329-1337.
3. Jones PH, Watt FM, (1993) Separation of human epidermal stem cells from transit amplifying cells on the basis of differences in integrin function and expression. Cell 73: 713-724.
4. Morris RJ, Potten CS, (1994) Slowly cycling (label-retaining) epidermal cells behave like clonogenic stem cells in vitro. Cell Prolif 27: 279-289.
5. Rochat A, Kobayashi K, Barrandon Y, (1994) Location of stem cells of human hair follicles by clonal analysis. Cell 76: 1063-1073.
6. Taylor G, Lehrer MS, Jensen PJ, Sun TT, Lavker RM, (2000) Involvement of follicular stem cells in forming not only the follicle but also the epidermis. Cell 102: 451-461.
7. Janes SM, Lowell S, Hutter C, (2002) Epidermal stem cells. J Pathol 197: 479-491.
8. Adams JC, Watt FM, (1990) Changes in keratinocyte adhesion during terminal differentiation: reduction in fibronectin binding precedes alpha 5 beta 1 integrin loss from the cell surface. Cell 63: 425-435.
9. Hesse M, Magin TM, Weber K, (2001) Genes for intermediate filament proteins and the draft sequence of the human genome: novel keratin genes and a surprisingly high number of pseudogenes related to keratin genes 8 and 18. J Cell Sci 114: 2569-2575.
10. Schweizer J, Bowden PE, Coulombe PA, Langbein L, Lane EB, et al. (2006) New consensus nomenclature for mammalian keratins. J Cell Biol 174: 169-174.
11. Moll R, Franke WW, Schiller DL, Geiger B, Krepler R, (1982) The catalog of human cytokeratins: patterns of expression in normal epithelia, tumors and cultured cells. Cell 31: 11-24.
12. Kirfel J, Magin TM, Reichelt J, (2003) Keratins: a structural scaffold with emerging functions. Cell Mol Life Sci 60: 56-71.
13. Bloor BK, Su L, Shirlaw PJ, Morgan PR, (1998) Gene expression of differentiation-specific keratins (4/13 and 1/10) in normal human buccal mucosa. Lab Invest 78: 787-795.
14. Swensson O, Langbein L, McMillan JR, Stevens HP, Leigh IM, et al. (1998) Specialized keratin expression pattern in human ridged skin as an adaptation to high physical stress. Brit J Dermatol 139: 767-775.
15. Machesney M, Tidman N, Waseem A, Kirby L, Leigh I, (1998) Activated keratinocytes in the epidermis of hypertrophic scars. Am J Pathol 152: 1133-1141.
16. Bloor BK, Tidman N, Leigh IM, Odell E, Dogan B, et al. (2003) Expression of keratin K2e in cutaneous and oral lesions: association with keratinocyte activation, proliferation, and keratinization. Am J Pathol 162: 963-975.
17. Fuchs E, Green H, (1980) Changes in keratin gene expression during terminal differentiation of the keratinocyte. Cell 19: 1033-1042.
18. Lloyd C, Yu QC, Cheng J, Turksen K, Degenstein L, et al. (1995) The basal keratin network of stratified squamous epithelia: defining K15 function in the absence of K14. J Cell Biol 129: 1329-1344.
19. Moll R, Levy R, Czernobilsky B, Hohlweg-Majert P, Dallenbach-Hellweg G, et al. (1983) Cytokeratins of normal epithelia and some neoplasms of the female genital tract. Lab Invest 49: 599-610.
20. Jonkman MF, Heeres K, Pas HH, van Luyn MJ, Elema JD, et al. (1996) Effects of keratin 14 ablation on the clinical and cellular phenotype in a kindred with recessive epidermolysis bullosa simplex. J Invest Dermatol 107: 764-769.
21. Waseem A, Dogan B, Tidman N, Alam Y, Purkis P, et al. (1999) Keratin 15 expression in stratified epithelia: downregulation in activated keratinocytes. J Invest Dermatol 112: 362-369.
22. Porter RM, Lunny DP, Ogden PH, Morley SM, McLean WH, et al. (2000) K15 expression implies lateral differentiation within stratified epithelial basal cells. Lab Invest 80: 1701-1710.
23. Lyle S, Christofidou-Solomidou M, Liu Y, Elder DE, Albelda S, et al. (1998) The C8/144B monoclonal antibody recognizes cytokeratin 15 and defines the location of human hair follicle stem cells. J Cell Sci 111 (Pt 21): 3179-3188.
24. Zhan Q, Signoretti S, Whitaker-Menezes D, Friedman TM, Korngold R, et al. (2007) Cytokeratin15-positive basal epithelial cells targeted in graft-versus-host disease express a constitutive antiapoptotic phenotype. J Invest Dermatol 127: 106-115.
25. Ohyama M, Terunuma A, Tock CL, Radonovich MF, Pise-Masison CA, et al. (2006) Characterization and isolation of stem cell-enriched human hair follicle bulge cells. J Clin Invest 116: 249-260.
26. Yoshida S, Shimmura S, Kawakita T, Miyashita H, Den S, et al. (2006) Cytokeratin 15 can be used to identify the limbal phenotype in normal and diseased ocular surfaces. Invest Ophthalmol Vis Sci 47: 4780-4786.
27. Liu Y, Lyle S, Yang Z, Cotsarelis G, (2003) Keratin 15 promoter targets putative epithelial stem cells in the hair follicle bulge. J Invest Dermatol 121: 963-968.
28. Morris RJ, Liu Y, Marles L, Yang Z, Trempus C, et al. (2004) Capturing and profiling adult hair follicle stem cells. Nat Biotechnol 22: 411-417.
29. Jaks V, Barker N, Kasper M, van Es JH, Snippert HJ, et al. (2008) Lgr5 marks cycling, yet long-lived, hair follicle stem cells. Nat Genet 40: 1291-1299.
30. Whitbread LA, Powell BC, (1998) Expression of the intermediate filament keratin gene, K15, in the basal cell layers of epithelia and the hair follicle. Exp Cell Res 244: 448-459.
31. Barker N, van Es JH, Jaks V, Kasper M, Snippert H, et al. (2008) Very Long-term Self-renewal of Small Intestine, Colon, and Hair Follicles from Cycling Lgr5+ve Stem Cells. Cold Spring Harb Symp Quant Biol 73: 351-356.
32. Jih DM, Lyle S, Elenitsas R, Elder DE, Cotsarelis G, (1999) Cytokeratin 15 expression in trichoepitheliomas and a subset of basal cell carcinomas suggests they originate from hair follicle stem cells. J Cutan Pathol 26: 113-118.
33. Troy TC, Arabzadeh A, Turksen K, (2011) Re-Assessing K15 as an Epidermal Stem Cell Marker. Stem Cell Rev 7: 1041-1045.
34. Sakamoto K, Aragaki T, Morita K, Kawachi H, Kayamori K, et al. (2011) Down-regulation of keratin 4 and keratin 13 expression in oral squamous cell carcinoma and epithelial dysplasia: a clue for histopathogenesis. Histopathology 58: 531-542.
35. Al-Refu K, Edward S, Ingham E, Goodfield M, (2009) Expression of hair follicle stem cells detected by cytokeratin 15 stain: implications for pathogenesis of the scarring process in cutaneous lupus erythematosus. Brit J Dermatol 160: 1188-1196.
36. Werner S, Munz B, (2000) Suppression of keratin 15 expression by transforming growth factor beta in vitro and by cutaneous injury in vivo. Exp Cell Res 254: 80-90.
37. Sperling LC, Hussey S, Wang JA, Darling T, (2011) Cytokeratin 15 expression in central, centrifugal, cicatricial alopecia: new observations in normal and diseased hair follicles. J Cut Pathol 38: 407-414.
38. Pontiggia L, Biedermann T, Meuli M, Widmer D, Bottcher-Haberzeth S, et al. (2009) Markers to evaluate the quality and self-renewing potential of engineered human skin substitutes in vitro and after transplantation. J Invest Dermatol 129: 480-490.
39. Leube RE, Bader BL, Bosch FX, Zimbelmann R, Achtstaetter T, et al. (1988) Molecular characterization and expression of the stratification-related cytokeratins 4 and 15. J Cell Biol 106: 1249-1261.
40. Bloor BK, Seddon SV, Morgan PR, (2000) Gene expression of differentiation-specific keratins (K4, K13, K1 and K10) in oral non-dysplastic keratoses and lichen planus. J Oral Pathol & Med 29: 376-384.
41. Ryle CM, Breitkreutz D, Stark HJ, Leigh IM, Steinert PM, et al. (1989) Density-dependent modulation of synthesis of keratins 1 and 10 in the human keratinocyte line HACAT and in ras-transfected tumorigenic clones. Differentiation 40: 42-54.
42. Radoja N, Stojadinovic O, Waseem A, Tomic-Canic M, Milisavljevic V, et al. (2004) Thyroid hormones and gamma interferon specifically increase K15 keratin gene transcription. Mol Cell Biol 24: 3168-3179.
43. Adams JC, Watt FM, (1989) Fibronectin inhibits the terminal differentiation of human keratinocytes. Nature 340: 307-309.
44. Gemenetzidis E, Elena-Costea D, Parkinson EK, Waseem A, Wan H, et al. (2010) Induction of human epithelial stem/progenitor expansion by FOXM1. Cancer Res 70: 9515-9526.
45. Lash JW, Linask KK, Yamada KM, (1987) Synthetic peptides that mimic the adhesive recognition signal of fibronectin: differential effects on cell-cell and cell-substratum adhesion in embryonic chick cells. Dev Biol 123: 411-420.
46. Matsui MS, Illarda I, Wang N, DeLeo VA, (1993) Protein kinase C agonist and antagonist effects in normal human epidermal keratinocytes. Exp Dermatol 2: 247-256.
47. Roberts NA, Marber MS, Avkiran M, (2004) Specificity of action of bisindolylmaleimide protein kinase C inhibitors: do they inhibit the 70 kDa ribosomal S6 kinase in cardiac myocytes? Biochem Pharmacol 68: 1923-1928.
48. Dlugosz AA, Mischak H, Mushinski JF, Yuspa SH, (1992) Transcripts encoding protein kinase C-alpha,-delta,-epsilon,-zeta, and-eta are expressed in basal and differentiating mouse keratinocytes in vitro and exhibit quantitative changes in neoplastic cells. Mol Carcinogen 5: 286-292.
49. Halazonetis TD, Georgopoulos K, Greenberg ME, Leder P, (1988) c-Jun dimerizes with itself and with c-Fos, forming complexes of different DNA binding affinities. Cell 55: 917-924.
50. Fanjul A, Dawson MI, Hobbs PD, Jong L, Cameron JF, et al. (1994) A new class of retinoids with selective inhibition of AP-1 inhibits proliferation. Nature 372: 107-111.
51. Ye H, Kelly TF, Samadani U, Lim L, Rubio S, et al. (1997) Hepatocyte nuclear factor 3/fork head homolog 11 is expressed in proliferating epithelial and mesenchymal cells of embryonic and adult tissues. Mol Cell Biol 17: 1626-1641.
52. Webb A, Li A, Kaur P, (2004) Location and phenotype of human adult keratinocyte stem cells of the skin. Differentiation 72: 387-395.
53. Green H, (1977) Terminal differentiation of cultured human epidermal cells. Cell 11: 405-416.
54. Poumay Y, Pittelkow MR, (1995) Cell density and culture factors regulate keratinocyte commitment to differentiation and expression of suprabasal K1/K10 keratins. J Invest Dermatol 104: 271-276.
55. Poumay Y, Herphelin F, Smits P, De Potter IY, Pittelkow MR, (1999) High-cell-density phorbol ester and retinoic acid upregulate involucrin and downregulate suprabasal keratin 10 in autocrine cultures of human epidermal keratinocytes. Mol Cell Biol Res Comm: MCBRC 2: 138-144.
56. Dlugosz AA, Yuspa SH, (1993) Coordinate changes in gene expression which mark the spinous to granular cell transition in epidermis are regulated by protein kinase C. J Cell Biol 120: 217-225.
57. Jensen UB, Lowell S, Watt FM, (1999) The spatial relationship between stem cells and their progeny in the basal layer of human epidermis: a new view based on whole-mount labelling and lineage analysis. Development 126: 2409-2418.
58. Lavker RM, Sun TT, (1982) Heterogeneity in epidermal basal keratinocytes: morphological and functional correlations. Science 215: 1239-1241.
59. Ghazizadeh S, Taichman LB, (2005) Organization of stem cells and their progeny in human epidermis. J Invest Dermatol 124: 367-372.
60. Kose O, Lalli A, Kutulola AO, Odell EW, Waseem A, (2007) Changes in the expression of stem cell markers in oral lichen planus and hyperkeratotic lesions. J Oral Sci 49: 133-139.
61. Kose O, Stewart J, Waseem A, Lalli A, Fortune F, (2008) Expression of cytokeratins, adhesion and activation molecules in oral ulcers of Behcet's disease. Clin Exp Dermatol 33: 62-69.
62. Klein CE, Steinmayer T, Mattes JM, Kaufmann R, Weber L, (1990) Integrins of normal human epidermis: differential expression, synthesis and molecular structure. Brit J Dermatol 123: 171-178.
63. Hong J, Lee J, Min KH, Walker JR, Peters EC, et al. (2007) Identification and characterization of small-molecule inducers of epidermal keratinocyte differentiation. ACS Chem Biol 2: 171-175.
64. Efimova T, Eckert RL, (2000) Regulation of human involucrin promoter activity by novel protein kinase C isoforms. J Biol Chem 275: 1601-1607.
65. Efimova T, Deucher A, Kuroki T, Ohba M, Eckert RL, (2002) Novel protein kinase C isoforms regulate human keratinocyte differentiation by activating a p38 delta mitogen-activated protein kinase cascade that targets CCAAT/enhancer-binding protein alpha. J Biol Chem 277: 31753-31760.
66. Kashiwagi M, Ohba M, Chida K, Kuroki T, (2002) Protein kinase C eta (PKC eta): its involvement in keratinocyte differentiation. J Biochem 132: 853-857.
67. Adhikary G, Chew YC, Reece EA, Eckert RL, (2010) PKC-delta and-eta, MEKK-1, MEK-6, MEK-3, and p38-delta are essential mediators of the response of normal human epidermal keratinocytes to differentiating agents. J Invest Dermatol 130: 2017-2030.
68. Kamioka N, Akahane T, Kohno Y, Kuroki T, Iijima M, et al. (2010) Protein kinase C delta and eta differently regulate the expression of loricrin and Jun family proteins in human keratinocytes. Biochem Biophys Res Comm 394: 106-111.
69. Eckert RL, Welter JF, (1996) Transcription factor regulation of epidermal keratinocyte gene expression. Mol Biol Rep 23: 59-70.
70. Ma S, Rao L, Freedberg IM, Blumenberg M, (1997) Transcriptional control of K5, K6, K14, and K17 keratin genes by AP-1 and NF-kappaB family members. Gene Expression 6: 361-370.
71. Kulesh DA, Cecena G, Darmon YM, Vasseur M, Oshima RG, (1989) Posttranslational regulation of keratins: degradation of mouse and human keratins 18 and 8. Mol Cell Biol 9: 1553-1565.
72. Crowe DL, (1993) Retinoic acid mediates post-transcriptional regulation of keratin 19 mRNA levels. J Cell Sci 106: 183-188.
73. Tyner AL, Fuchs E, (1986) Evidence for posttranscriptional regulation of the keratins expressed during hyperproliferation and malignant transformation in human epidermis. J Cell Biol 103: 1945-1955.
74. Papp H, Czifra G, Lazar J, Gonczi M, Csernoch L, et al. (2003) Protein kinase C isozymes regulate proliferation and high cell density-mediated differentiation in HaCaT keratinocytes. Exp Dermatol 12: 811-824.
75. Lee YS, Yuspa SH, Dlugosz AA, (1998) Differentiation of cultured human epidermal keratinocytes at high cell densities is mediated by endogenous activation of the protein kinase C signaling pathway. J Invest Dermatol 111: 762-766.
76. Rutberg SE, Saez E, Glick A, Dlugosz AA, Spiegelman BM, et al. (1996) Differentiation of mouse keratinocytes is accompanied by PKC-dependent changes in AP-1 proteins. Oncogene 13: 167-176.
77. Rutberg SE, Saez E, Lo S, Jang SI, Markova N, et al. (1997) Opposing activities of c-Fos and Fra-2 on AP-1 regulated transcriptional activity in mouse keratinocytes induced to differentiate by calcium and phorbol esters. Oncogene 15: 1337-1346.
78. Verma AK, Wheeler DL, Aziz MH, Manoharan H, (2006) Protein kinase Cepsilon and development of squamous cell carcinoma, the nonmelanoma human skin cancer. Mol Carcinogen 45: 381-388.
79. Teh MT, Wong ST, Neill GW, Ghali LR, Philpott MP, et al. (2002) FOXM1 is a downstream target of Gli1 in basal cell carcinomas. Cancer Res 62: 4773-4780.
80. Ghali L, Wong ST, Green J, Tidman N, Quinn AG, (1999) Gli1 protein is expressed in basal cell carcinomas, outer root sheath keratinocytes and a subpopulation of mesenchymal cells in normal human skin. J Invest Dermatol 113: 595-599.
81. Wierstra I, Alves J, (2007) FOXM1, a typical proliferation-associated transcription factor. Biol Chem 388: 1257-1274.
82. Huynh KM, Soh JW, Dash R, Sarkar D, Fisher PB, et al. (2011) FOXM1 expression mediates growth suppression during terminal differentiation of HO-1 human metastatic melanoma cells. J Cell Physiol 226: 194-204.
83. Myatt SS, Lam EW, (2007) The emerging roles of forkhead box (Fox) proteins in cancer. Nat Rev Cancer 7: 847-859.
84. Gemenetzidis E, Bose A, Riaz AM, Chaplin T, Young BD, et al. (2009) FOXM1 upregulation is an early event in human squamous cell carcinoma and it is enhanced by nicotine during malignant transformation. PLoS One 4: e4849.
85. Waseem A, Ali M, Odell EW, Fortune F, Teh MT, (2010) Downstream targets of FOXM1: CEP55 and HELLS are cancer progression markers of head and neck squamous cell carcinoma. Oral Oncol 46: 536-542.
86. Freedberg IM, Tomic-Canic M, Komine M, Blumenberg M, (2001) Keratins and the keratinocyte activation cycle. J Invest Dermatol 116: 633-640.
87. Dickson MA, Hahn WC, Ino Y, Ronfard V, Wu JY, et al. (2000) Human keratinocytes that express hTERT and also bypass a p16(INK4a)-enforced mechanism that limits life span become immortal yet retain normal growth and differentiation characteristics. Mol Cell Biol 20: 1436-1447.
88. Boukamp P, Petrussevska RT, Breitkreutz D, Hornung J, Markham A, et al. (1988) Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J Cell Biol 106: 761-771.