UVB upregulates the bax promoter in immortalized human keratinocytes via ROS induction of Id3

Experimental Dermatology

Volumn 18, Issue 4, 2009, Pages 387-395

  Trabosh, Valerie Anne ^a   Daher, Ahmad ^a   Divito, Kyle A ^a   Amin, Karishma ^a   Simbulan rosenthal, Cynthia M ^a   Rosenthal, Dean S ^a  

^a GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Bax promoter; Id proteins; Immortalization; Superoxide

Indexed keywords

INHIBITOR OF DIFFERENTIATION 3; MESSENGER RNA; PROTEIN BAX; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; XANTHINE OXIDASE;

ARTICLE; BINDING SITE; CELL IMMORTALIZATION; CONTROLLED STUDY; ENZYME RELEASE; GENE ACTIVITY; GENE CONSTRUCT; GENE DELETION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; KERATINOCYTE; POINT MUTATION; PROMOTER REGION; QUANTITATIVE ANALYSIS; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION INITIATION; ULTRAVIOLET B RADIATION; UPREGULATION;

APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CELLS, CULTURED; E-BOX ELEMENTS; HUMANS; INHIBITOR OF DIFFERENTIATION PROTEINS; KERATINOCYTES; NEOPLASM PROTEINS; PROMOTER REGIONS, GENETIC; REACTIVE OXYGEN SPECIES; RNA, MESSENGER; ULTRAVIOLET RAYS; UP-REGULATION;

EID: 63149172769     PISSN: 09066705     EISSN: 16000625     Source Type: Journal    
DOI: 10.1111/j.1600-0625.2008.00801.x     Document Type: Article

References (56)

1. Fears T R, Scotto J. Estimating increases in skin cancer morbidity due to increases in ultraviolet radiation exposure. Cancer Invest 1983: 1: 119-126.
2. Strickland P T, Vitasa B C, West S K, Rosenthal F S, Emmett E A, Taylor H R. Quantitative carcinogenesis in man: Solar ultraviolet B dose dependence of skin cancer in Maryland watermen. J Natl Cancer Inst 1989: 81: 1910-1913.
3. Nomura T, Nakajima H, Hongyo T et al. Induction of cancer, actinic keratosis, and specific p53 mutations by UVB light in human skin maintained in severe combined immunodeficient mice. Cancer Res 1997: 57: 2081-2084.
4. Griffiths H R, Mistry P, Herbert K E, Lunec J. Molecular and cellular effects of ultraviolet light-induced genotoxicity. Crit Rev Clin Lab Sci 1998: 35: 189-237.
5. de Gruijl F R. Photocarcinogenesis: UVA vs UVB. Methods Enzymol 2000: 319: 359-366.
6. Herrling T, Fuchs J, Rehberg J, Groth N. UV-induced free radicals in the skin detected by ESR spectroscopy and imaging using nitroxides. Free Radic Biol Med 2003: 35: 59-67.
7. Herrling T, Jung K, Fuchs J. Measurements of UV-generated free radicals/ reactive oxygen species (ROS) in skin. Spectrochim Acta A Mol Biomol Spectrosc 2006: 63: 840-845.
8. Zhang W, Hanks A N, Boucher K et al. UVB-induced apoptosis drives clonal expansion during skin tumor development. Carcinogenesis 2005: 26: 249-257.
9. Simbulan-Rosenthal C M, Trabosh V, Velarde A et al. Id2 protein is selectively upregulated by UVB in primary, but not in immortalized human keratinocytes and inhibits differentiation. Oncogene 2005: 4: 5443-5458.
10. Simbulan-Rosenthal C M, Velena A, Veldman T, Schlegel R, Rosenthal D S. HPV-16 E6/7 immortalization sensitizes human keratinocytes to ultraviolet B by altering the pathway from caspase-8 to caspase-9-dependent apoptosis. J Biol Chem 2002: 277: 24709-24716.
11. Daher A, Simbulan-Rosenthal C M, Rosenthal D S. Apoptosis induced by ultraviolet B in HPV-immortalized human keratinocytes requires caspase-9 and is death receptor independent. Exp Dermatol 2006: 15: 23-34.
12. Simbulan-Rosenthal C M, Daher A, Trabosh V et al. Id3 induces a caspase-3- and -9-dependent apoptosis and mediates UVB sensitization of HPV16 E6/7 immortalized human keratinocytes. Oncogene 2006: 25: 3649-3660. Epub 2006 Jan 3630.
13. Atchley W R, Fitch W M. A natural classification of the basic helix-loop-helix class of transcription factors. Proc Natl Acad Sci U S A 1997: 94: 5172-5176.
14. Murre C, McCaw P S, Vaessin H et al. Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence. Cell 1989: 58: 537-544.
15. Norton J D. ID helix-loop-helix proteins in cell growth, differentiation and tumorigenesis. J Cell Sci 2000: 113: 3897-3905.
16. Yates P R, Atherton G T, Deed R W, Norton J D, Sharrocks A D. Id helix-loop-helix proteins inhibit nucleoprotein complex formation by the TCF ETS-domain transcription factors. EMBO J 1999: 18: 968-976.
17. Rotzer D, Krampert M, Sulyok S et al. Id proteins: Novel targets of activin action, which regulate epidermal homeostasis. Oncogene 2006: 25: 2070-2081.
18. Benezra R, Rafii S, Lyden D. The Id proteins and angiogenesis. Oncogene 2001: 20: 8334-8341.
19. Hasskarl J, Munger K. Id proteins -tumor markers or oncogenes? Cancer Biol Ther 2002: 1: 91-96.
20. Kee B L, Rivera R R, Murre C. Id3 inhibits B lymphocyte progenitor growth and survival in response to TGF-beta. Nat Immunol 2001: 2: 242-247.
21. Chen B, Han B H, Sun X H, Lim R W. Inhibition of muscle-specific gene expression by Id3: Requirement of the C-terminal region of the protein for stable expression and function. Nucleic Acids Res 1997: 25: 423-430.
22. Deleu S, Savonet V, Behrends J, Dumont J E, Maenhaut C. Study of gene expression in thyrotropin-stimulated thyroid cells by cDNA expression array: ID3 transcription modulating factor as an early response protein and tumor marker in thyroid carcinomas. Exp Cell Res 2002: 279: 62-70.
23. Mueller C, Baudler S, Welzel H, Bohm M, Nickenig G. Identification of a novel redox-sensitive gene, Id3, which mediates angiotensin II-induced cell growth. Circulation 2002: 105: 2423-2428.
24. Ko M, Ahn J, Lee C et al. E2A/HEB and Id3 proteins control the sensitivity to glucocorticoid-induced apoptosis in thymocytes by regulating the SRG3 expression. J Biol Chem 2004: 279: 21916-21923.
25. Versnel M A. Id3 knockout mice as a new model for sjogren's syndrome: only a T cell defect or more? Immunity 2004: 21: 457-458.
26. Norton J D, Atherton G T. Coupling of cell growth control and apoptosis functions of Id proteins. Mol Cell Biol 1998: 18: 2371-2381.
27. Kee B L. Id3 induces growth arrest and caspase-2-dependent apoptosis in B lymphocyte progenitors. J Immunol 2005: 175: 4518-4527.
28. Koyama T, Suzuki H, Imakiire A, Yanase N, Hata K, Mizuguchi J. Id3-mediated enhancement of cisplatin-induced apoptosis in a sarcoma cell line MG-63. Anticancer Res 2004: 24: 1519-1524.
29. Kee Y, Bronner-Fraser M. To proliferate or to die: Role of Id3 in cell cycle progression and survival of neural crest progenitors. Genes Dev 2005: 19: 744-755.
30. Ravi R, Bedi A. Requirement of BAX for TRAIL/Apo2L-induced apoptosis of colorectal cancers: Synergism with sulindac-mediated inhibition of Bcl-x(L). Cancer Res 2002: 62: 1583-1587.
31. Theodorakis P, Lomonosova E, Chinnadurai G. Critical requirement of BAX for manifestation of apoptosis induced by multiple stimuli in human epithelial cancer cells. Cancer Res 2002: 62: 3373-3376.
32. Boukamp P, Petrussevska R T, Breitkreutz D, Hornung J, Markham A, Fusenig N E. Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J Cell Biol 1988: 106: 761-771.
33. Staal F J, Roederer M, Herzenberg L A, Herzenberg L A. Intracellular thiols regulate activation of nuclear factor kappa B and transcription of human immunodeficiency virus. Proc Natl Acad Sci U S A 1990: 87: 9943-9947.
34. Yeh K, Lim R W. Genomic organization and promoter analysis of the murine Id3 gene. Gene 2000: 254: 163-171.
35. Li X J, Hata K, Mizuguchi J. Engagement of membrane immunoglobulin enhances Id3 promoter activity in WEHI-231 B lymphoma cells. Acta Pharmacol Sin 2005: 26: 486-491.
36. Wu J, Lim R W. Regulation of inhibitor of differentiation gene 3 (Id3) expression by Sp2-motif binding factor in myogenic C2C12 cells: downregulation of DNA binding activity following skeletal muscle differentiation. Biochim Biophys Acta 2005: 1731: 13-22.
37. Petrocelli T, Poon R, Drucker D J, Slingerland J M, Rosen C F. UVB radiation induces p21Cip1/WAF1 and mediates G1 and S phase checkpoints. Oncogene 1996: 12: 1387-1396.
38. Venner T J, Sauder D N, Feliciani C, McKenzie R C. Interleukin-8 and melanoma growth-stimulating activity (GRO) are induced by ultraviolet B radiation in human keratinocyte cell lines. Exp Dermatol 1995: 4: 138-145.
39. Howell B G, Wang B, Freed I, Mamelak A J, Watanabe H, Sauder D N. Microarray analysis of UVB-regulated genes in keratinocytes: downregulation of angiogenesis inhibitor thrombospondin-1. J Dermatol Sci 2004: 34: 185-194.
40. Dazard J E, Gal H, Amariglio N, Rechavi G, Domany E, Givol D. Genome-wide comparison of human keratinocyte and squamous cell carcinoma responses to UVB irradiation: Implications for skin and epithelial cancer. Oncogene 2003: 22: 2993-3006.
41. de Vos S, Brach M, Budnik A, Grewe M, Herrmann F, Krutmann J. Post-transcriptional regulation of interleukin-6 gene expression in human keratinocytes by ultraviolet B radiation. J Invest Dermatol 1994: 103: 92-96.
42. Tong X, Van Dross R T, Abu-Yousif A, Morrison A R, Pelling J C. Apigenin prevents UVB-induced cyclooxygenase 2 expression: Coupled mRNA stabilization and translational inhibition. Mol Cell Biol 2007: 27: 283-296.
43. Tang Q, Chen W, Gonzales M S, Finch J, Inoue H, Bowden G T. Role of cyclic AMP responsive element in the UVB induction of cyclooxygenase-2 transcription in human keratinocytes. Oncogene 2001: 20: 5164-5172.
44. Matsumura M E, Li F, Berthoux L et al. Vascular injury induces posttranscriptional regulation of the Id3 gene: Cloning of a novel Id3 isoform expressed during vascular lesion formation in rat and human atherosclerosis. Arterioscler Thromb Vasc Biol 2001: 21: 752-758.
45. Rezvani H R, Mazurier F, Cario-Andre M et al. Protective effects of catalase overexpression on UVB-induced apoptosis in normal human keratinocytes. J Biol Chem 2006: 281: 17999-18007.
46. Nickenig G, Baudler S, Muller C et al. Redox-sensitive vascular smooth muscle cell proliferation is mediated by GKLF and Id3 in vitro and in vivo. FASEB J 2002: 16: 1077-1086.
47. Hakozaki T, Date A, Yoshii T, Toyokuni S, Yasui H, Sakurai H. Visualization and characterization of UVB-induced reactive oxygen species in a human skin equivalent model. Arch Dermatol Res 2008 Apr; 300 Suppl 1: S51-6.
48. Mitchell K O, Ricci M S, Miyashita T et al. Bax is a transcriptional target and mediator of c-myc-induced apoptosis. Cancer Res 2000: 60: 6318-6325.
49. Kim Y G, Kim H J, Kim D S et al. Up-Regulation and redistribution of Bax in ultraviolet B-irradiated melanocytes. Pigment Cell Res 2000: 13: 352-357.
50. Miyashita T, Reed J C. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 1995: 80: 293-299.
51. Gehring S, Rottmann S, Menkel A R, Mertsching J, Krippner-Heidenreich A, Luscher B. Inhibition of proliferation and apoptosis by the transcriptional repressor Mad1. Repression of Fas-induced caspase-8 activation. J Biol Chem 2000: 275: 10413-10420.
52. Chiaramello A, Neuman K, Palm K, Metsis M, Neuman T. Helix-loop-helix transcription factors mediate activation and repression of the p75LNGFR gene. Mol Cell Biol 1995: 15: 6036-6044.
53. Marks R, Foley P, Goodman G, Hage B H, Selwood T S. Spontaneous remission of solar keratoses: The case for conservative management. Br J Dermatol 1986: 115: 649-655.
54. Marks R, Rennie G, Selwood T S. Malignant transformation of solar keratoses to squamous cell carcinoma. Lancet 1988: 1: 795-797.
55. Frost C, Williams G, Green A. High incidence and regression rates of solar keratoses in a queensland community. J Invest Dermatol 2000: 115: 273-277.
56. Harvey I, Frankel S, Marks R, Shalom D, Nolan-Farrell M. Non-melanoma skin cancer and solar keratoses. I. Methods and descriptive results of the South Wales Skin Cancer Study. Br J Cancer 1996: 74: 1302-1307.