Repeated exposures to UVB induce differentiation rather than senescence of human keratinocytes lacking p16INK-4A

Biogerontology

Volumn 11, Issue 2, 2010, Pages 167-181

  Bertrand Vallery, Véronique ^a   Boilan, Emmanuelle ^a   Ninane, Noëlle ^a   Demazy, Catherine ^a   Friguet, Bertrand ^a   Toussaint, Bertrand ^a   Poumay, Yves ^b   Debacq Chainiaux, Florence ^a  

^a UNIVERSITY OF NAMUR   (Belgium)

^b UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Differentiation; DNA damage; Keratinocytes; UVB Senescence

Indexed keywords

BETA GALACTOSIDASE; CELL MARKER; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 2A; CYTOKERATIN 16; CYTOKERATIN 17; CYTOKERATIN 6; FILAGGRIN; INVOLUCRIN; PROTEIN P53; TELOMERASE REVERSE TRANSCRIPTASE;

ADULT; APOPTOSIS; ARTICLE; CELL AGING; CELL CYCLE ARREST; CELL DEATH; CELL DIFFERENTIATION; CELL LINE; CELL STRESS; CELL VIABILITY; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IN VIVO STUDY; KERATINOCYTE; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RADIATION DOSE; RADIATION EXPOSURE; REPEAT PROCEDURE; SENESCENCE; ULTRAVIOLET B RADIATION;

APOPTOSIS; BETA-GALACTOSIDASE; CELL AGING; CELL CYCLE; CELL DIFFERENTIATION; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE INHIBITOR P16; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DNA DAMAGE; DOSE-RESPONSE RELATIONSHIP, RADIATION; HUMANS; INTERMEDIATE FILAMENT PROTEINS; KERATINOCYTES; KERATINS; PROTEIN PRECURSORS; TUMOR SUPPRESSOR PROTEIN P53; ULTRAVIOLET RAYS;

EID: 77950857822     PISSN: 13895729     EISSN: 15736768     Source Type: Journal    
DOI: 10.1007/s10522-009-9238-y     Document Type: Article

References (49)

1. Beausejour CM, Krtolica A, Galimi F, Narita M, Lowe SW, Yaswen P, Campisi J (2003) Reversal of human cellular senescence: roles of the p53 and p16 pathways. EMBO J 22:4212-4222
2. Ben-Porath I, Weinberg RA (2005) The signals and pathways activating cellular senescence. Int J Biochem Cell Biol 37:961-976
3. Berge U, Kristensen P, Rattan SI (2008) Hormetic modulation of differentiation of normal human epidermal keratinocytes undergoing replicative senescence in vitro. Exp Gerontol 43:658-662
4. Blackburn EH (2005) Telomeres and telomerase: their mechanisms of action and the effects of altering their functions. FEBS Lett 579:859-862
5. Bousquet O, Coulombe PA (2002) Les kératines: un autre regard sur la biologie de la peau. Medecine/Sciences 18:45-54
6. Bulteau AL, Moreau M, Nizard C, Friguet B (2002) Impairment of proteasome function upon UVA- and UVB-irradiation of human keratinocytes. Free Radic Biol Med 32:1157-1170
7. Carlen LM, Sanchez F, Bergman AC, Becker S, Hirschberg D, Franzen B, Coffey J, Jornvall H, Auer G, Alaiya AA, Stahle M (2005) Proteome analysis of skin distinguishesacute guttate from chronic plaque psoriasis. J InvestDermatol 124:63-69
8. Cuddihy AR, Bristow RG (2004) The p53 protein family and radiation sensitivity: yes or no? Cancer Metastasis Rev 23:237-257
9. Davies KJ (2001) Degradation of oxidized proteins by the 20S proteasome. Biochimie 83:301-310
10. de Magalhaes JP, Chainiaux F, Remacle J, Toussaint O (2002) Stress-induced premature senescence in BJ and hTERTBJ1 human foreskin fibroblasts. FEBS Lett 523:157-162 (Pubitemid 34786078)
11. de Winter S, Vink AA, Roza L, Pavel S (2001) Solar-simulated skin adaptation and its effect on subsequent UV-induced epidermal DNA damage. J Invest Dermatol 117:678-682
12. Debacq-Chainiaux F, Pascal T, Boilan E, Bastin C, Bauwens E, Toussaint O (2008) Screening of senescence-associated genes with specific DNA array reveals the role of IGFBP-3 in premature senescence of human diploid fibroblasts. Free Radic Biol Med 44:1817-1832
13. Decraene D, Smaers K, Maes D, Matsui M, Declercq L, Garmyn M (2005) A low UVB dose, with the potential to trigger a protective p53-dependent gene program, increases the resilience of keratinocytes against future UVB insults. J Invest Dermatol 125:1026-1031
14. Del Bino S, Vioux C, Rossio-Pasquier P, Jomard A, Demarchez M, Asselineau D, Bernerd F (2004) Ultraviolet B induces hyperproliferation and modification of epidermal differentiation in normal human skin grafted on to nude mice. Br J Dermatol 150:658-667
15. Dickson MA, Hahn WC, Ino Y, Ronfard V, Wu JY, Weinberg RA, Louis DN, Li FP, Rheinwald JG (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
16. Dierick J-F, Frippiat Salmon, Chainiaux Toussaint (2003) Cells, stress and tissue ageing. In: Osiewacz HD (ed) Modulating aging and longevity. Kluwer, Amsterdam, pp 101-125
17. Dimri GP, Lee X, Basile G, Acosta M, Scott G, Roskelley C, Medrano EE, Linskens M, Rubelj I, Pereira-Smith O et al (1995) A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci U S A 92:9363-9367
18. Dumont P, Burton M, Chen QM, Gonos ES, Frippiat C, Mazarati JB, Eliaers F, Remacle J, Toussaint O (2000) Induction of replicative senescence biomarkers by sublethal oxidative stresses in normal human fibroblast. Free Radic Biol Med 28:361-373
19. Dumont P, Royer V, Pascal T, Dierick JF, Chainiaux F, Frippiat C, de Magalhaes JP, Eliaers F, Remacle J, Toussaint O (2001) Growth kinetics rather than stress accelerate telomere shortening in cultures of human diploid fibroblasts in oxidative stress-induced premature senescence. FEBS Lett 502:109-112
20. Eckert RL, Crish JF, Robinson NA (1997) The epidermal keratinocyte as a model for the study of gene regulation and cell differentiation. Physiol Rev 77:397-424
21. Freedberg IM, Tomic-Canic M, Komine M, Blumenberg M (2001) Keratins and the keratinocyte activation cycle. J Invest Dermatol 116:633-640
22. Friguet B (2006) Oxidized protein degradation and repair in ageing and oxidative stress. FEBS Lett 580:2910-2916
23. Gandarillas A (2000) Epidermal differentiation, apoptosis, and senescence: common pathways? Exp Gerontol 35:53-62
24. Gazel A, Ramphal P, Rosdy M, De Wever B, Tornier C, Hosein N, Lee B, Tomic-Canic M, Blumenberg M (2003) Transcriptional profiling of epidermal keratinocytes: comparison of genes expressed in skin, cultured keratinocytes, and reconstituted epidermis, using large DNA microarrays. J Invest Dermatol 121:1459-1468
25. Gorbunova V, Seluanov A, Pereira-Smith OM (2002) Expression of human telomerase (hTERT) does not prevent stress-induced senescence in normal human fibroblasts but protects the cells from stress-induced apoptosis and necrosis. J Biol Chem 277:38540-38549
26. Hayflick L, Moorhead PS (1961) The serial cultivation of human diploid cell strains. Exp Cell Res 25:585-621
27. Ichihashi M, Ueda M, Budiyanto A, Bito T, Oka M, Fukunaga M, Tsuru K, Horikawa T (2003) UV-induced skin damage. Toxicology 189:21-39
28. Jiang CK, Flanagan S, Ohtsuki M, Shuai K, Freedberg IM, Blumenberg M (1994) Disease-activated transcription factor: allergic reactions in human skin cause nuclear translocation of STAT-91 and induce synthesis of keratin K17. Mol Cell Biol 14:4759-4769
29. Komine M, Freedberg IM, Blumenberg M (1996) Regulation of epidermal expression of keratin K17 in inflammatory skin diseases. J Invest Dermatol 107:569-575
30. Lee JH, An HT, Chung JH, Kim KH, Eun HC, Cho KH (2002) Acute effects of UVB radiation on the proliferation and differentiation of keratinocytes. Photodermatol Photoimmunol Photomed 18:253-261
31. Lewis DA, Yi Q, Travers JB, Spandau DF (2008) UVBinduced senescence in human keratinocytes requires a functional insulin-like growth factor-1 receptor and p53. Mol Biol Cell 19:1346-1353
32. Li D, Turi TG, Schuck A, Freedberg IM, Khitrov G, Blumenberg M (2001) Rays and arrays: the transcriptional program in the response of human epidermal keratinocytes to UVB illumination. FASEB J 15:2533-2535
33. Matuoka K, Chen KY (2002) Telomerase positive human diploid fibroblasts are resistant to replicative senescence but not premature senescence induced by chemical reagents. Biogerontology 3:365-372
34. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55-63
35. Nakamura S, Nishioka K (2003) Enhanced expression of p16 in seborrhoeic keratosis; a lesion of accumulated senescent epidermal cells in G1 arrest. Br J Dermatol 149:560-565
36. Paladini RD, Takahashi K, Bravo NS, Coulombe PA (1996) Onset of re-epithelialization after skin injury correlates with a reorganization of keratin filaments in wound edge keratinocytes: defining a potential role for keratin 16. J Cell Biol 132:381-397
37. Petropoulos I, Conconi M, Wang X, Hoenel B, Bregegere F, Milner Y, Friguet B (2000) Increase of xidatively modified protein is associated with a decrease of proteasome activity and content in aging epidermal cells. J Gerontol A Biol Sci Med Sci 55:B220-B227
38. 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
39. Rabe JH, Mamelak AJ, McElgunn PJ, Morison WL, Sauder DN (2006) Photoaging: mechanisms and repair. J Am Acad Dermatol 55:1-19
40. Ramirez RD, Morales CP, Herbert BS, Rohde JM, Passons C, Shay JW, Wright WE (2001) Putative telomere-independent mechanisms of replicative aging reflect inadequate growth conditions. Genes Dev 15:398-403
41. Ressler S, Bartkova J, Niederegger H, Bartek J, Scharffetter- Kochanek K, Jansen-Durr P, Wlaschek M (2006) p16INK4A is a robust in vivo biomarker of cellular aging in human skin. Aging Cell 5:379-389
42. Rittie L, Fisher GJ (2002) UV-light-induced signal cascades and skin aging. Ageing Res Rev 1:705-720
43. Sano T, Kume T, Fujimura T, Kawada H, Higuchi K, Iwamura M, Hotta M, Kitahara T, Takema Y (2009) Long-term alteration in the expression of keratins 6 and 16 in the epidermis of mice after chronic UVB exposure. Arch Dermatol Res 301:227-237
44. Schmitt CA (2007) Cellular senescence and cancer treatment. Biochim Biophys Acta 1775:5-20
45. Stoler A, Kopan R, Duvic M, Fuchs E (1988) Use of monospecific antisera and cRNA probes to localize the major changes in keratin expression during normal and abnormal epidermal differentiation. J Cell Biol 107:427-446
46. Takahashi K, Folmer J, Coulombe PA (1994) Increased expression of keratin 16 causes anomalies in cytoarchitecture and keratinization in transgenic mouse skin. J Cell Biol 127:505-520
47. Toussaint O, Remacle J, Dierick JF, Pascal T, Frippiat C, Royer V, Magalhacs JP, Zdanov S, Chainiaux F (2002) Stress-induced premature senescence: from biomarkers to likeliness of in vivo occurrence. Biogerontology 3:13-17
48. Weiss RA, Eichner R, Sun TT (1984) Monoclonal antibody analysis of keratin expression in epidermal diseases: a 48-and 56-kdalton keratin as molecular markers for hyperproliferative keratinocytes. J Cell Biol 98:1397-1406
49. Wong P, Coulombe PA (2003) Loss of keratin 6 (K6) proteins reveals a function for intermediate filaments during wound repair. J Cell Biol 163:327-337