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PMID: 11581300 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Transgenic expression of survivin in keratinocytes counteracts UVB-induced apoptosis and cooperates with loss of p53.

The Journal of clinical investigation ·Vol. 108 ·No. 7 ·2001-10-00 ·Pages 991-9

Grossman D, Kim PJ, Blanc-Brude OP, Brash DE, Tognin S, Marchisio PC, Altieri DC

Abstract

The inhibitor of apoptosis protein survivin has been implicated in both cell cycle control and apoptosis resistance. To discriminate between these different roles, we used transgenic expression of survivin in the skin as a model for cell proliferation, differentiation, and apoptosis. Transgenic mice expressing survivin under the control of a keratin-14 promoter developed normally, without histologic abnormalities of the skin or hair, epidermal hyperplasia, or developmental abnormalities of basal or suprabasal epidermis. Keratinocyte proliferation assessed under basal conditions, or after ultraviolet-B (UVB) irradiation, or phorbol ester stimulation was unchanged in survivin transgenic mice. In contrast, survivin expression inhibited UVB-induced apoptosis in vitro and in vivo (i.e., sunburn cell formation), whereas it did not affect Fas-induced cell death. When crossed with p53 knockout mice, transgenic expression of survivin in a p53(+/-) background substituted for the loss of a second p53 allele and further inhibited UVB-induced apoptosis. These data provide the first in vivo evidence that survivin inhibits apoptosis and suggest that this pathway may oppose the elimination of cancerous cells by p53.

MeSH Terms
Animals Apoptosis Chromosomal Proteins, Non-Histone/genetics,metabolism Gene Expression Humans Inhibitor of Apoptosis Proteins Keratin-14 Keratinocytes/cytology Keratins/genetics Mice Mice, Knockout Mice, Transgenic Microtubule-Associated Proteins Neoplasm Proteins Phenotype Promoter Regions, Genetic Skin/cytology,metabolism Survivin Tumor Suppressor Protein p53/genetics,metabolism Ultraviolet Rays
Chemicals
BIRC5 protein, human Chromosomal Proteins, Non-Histone Inhibitor of Apoptosis Proteins KRT14 protein, human Keratin-14 Krt14 protein, mouse Microtubule-Associated Proteins Neoplasm Proteins Survivin Tumor Suppressor Protein p53 Keratins
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Grossman D
Department of Dermatology, Boyer Center for Molecular Medicine, Yale University School of Medicine, New Haven, Connecticut 06536, USA.
Kim P J
Blanc-Brude O P
Brash D E
Tognin S
Marchisio P C
Altieri D C
References (47)
47 references, click to expand
  1. Evaluation of apoptotic cells induced by ultraviolet light B radiation in epidermal sheets stained by the TUNEL technique.
    J Invest Dermatol. 1999 Nov;113(5):802-7 PMID: 10571737
  2. NMR structure and mutagenesis of the inhibitor-of-apoptosis protein XIAP.
    Nature. 1999 Oct 21;401(6755):818-22 PMID: 10548111
  3. Expression and targeting of the apoptosis inhibitor, survivin, in human melanoma.
    J Invest Dermatol. 1999 Dec;113(6):1076-81 PMID: 10594755
  4. p53 induces apoptosis by caspase activation through mitochondrial cytochrome c release.
    J Biol Chem. 2000 Mar 10;275(10):7337-42 PMID: 10702305
  5. Structure of the human anti-apoptotic protein survivin reveals a dimeric arrangement.
    Nat Struct Biol. 2000 Jul;7(7):602-8 PMID: 10876248
  6. T cell-mediated Fas-induced keratinocyte apoptosis plays a key pathogenetic role in eczematous dermatitis.
    J Clin Invest. 2000 Jul;106(1):25-35 PMID: 10880045
  7. Death receptors in cutaneous biology and disease.
    J Invest Dermatol. 2000 Aug;115(2):141-8 PMID: 10951228
  8. Involvement of follicular stem cells in forming not only the follicle but also the epidermis.
    Cell. 2000 Aug 18;102(4):451-61 PMID: 10966107
  9. The survivin-like C. elegans BIR-1 protein acts with the Aurora-like kinase AIR-2 to affect chromosomes and the spindle midzone.
    Mol Cell. 2000 Aug;6(2):211-23 PMID: 10983970
  10. BIRinging chromosomes through cell division--and survivin' the experience.
    Cell. 2000 Sep 1;102(5):545-8 PMID: 11007472
  11. MDM2 induces hyperplasia and premalignant lesions when expressed in the basal layer of the epidermis.
    EMBO J. 2000 Oct 2;19(19):5135-47 PMID: 11013216
  12. Survivin and the inner centromere protein INCENP show similar cell-cycle localization and gene knockout phenotype.
    Curr Biol. 2000 Nov 2;10(21):1319-28 PMID: 11084331
  13. Regulation of apoptosis at cell division by p34cdc2 phosphorylation of survivin.
    Proc Natl Acad Sci U S A. 2000 Nov 21;97(24):13103-7 PMID: 11069302
  14. Role of PTCH and p53 genes in early-onset basal cell carcinoma.
    Am J Pathol. 2001 Feb;158(2):381-5 PMID: 11159175
  15. An anti-apoptotic protein human survivin is a direct inhibitor of caspase-3 and -7.
    Biochemistry. 2001 Jan 30;40(4):1117-23 PMID: 11170436
  16. Inhibition of melanoma tumor growth in vivo by survivin targeting.
    Proc Natl Acad Sci U S A. 2001 Jan 16;98(2):635-40 PMID: 11149963
  17. DNA demethylase is expressed in ovarian cancers and the expression correlates with demethylation of CpG sites in the promoter region of c-erbB-2 and survivin genes.
    Cancer Lett. 2001 Aug 28;169(2):155-64 PMID: 11431104
  18. The recognition of early stages of catagen.
    Am J Dermatopathol. 1984 Dec;6(6):553-5 PMID: 6524637
  19. FACS purification of bone marrow-derived epidermal populations in mice: Langerhans cells and Thy-1+ dendritic cells.
    J Invest Dermatol. 1985 Jun;84(6):491-5 PMID: 3998496
  20. Transgenic mice provide new insights into the role of TGF-alpha during epidermal development and differentiation.
    Genes Dev. 1991 May;5(5):714-27 PMID: 1709129
  21. Programmed cell death in terminally differentiating keratinocytes: role of endogenous endonuclease.
    J Invest Dermatol. 1991 Jul;97(1):111-4 PMID: 1647418
  22. Reduction of p53 gene dosage does not increase initiation or promotion but enhances malignant progression of chemically induced skin tumors.
    Cell. 1993 Sep 10;74(5):813-22 PMID: 8374952
  23. Overexpression of parathyroid hormone-related protein in the skin of transgenic mice interferes with hair follicle development.
    Proc Natl Acad Sci U S A. 1994 Feb 1;91(3):1133-7 PMID: 7508121
  24. Apoptosis in human skin development: morphogenesis, periderm, and stem cells.
    Dev Dyn. 1994 Mar;199(3):176-88 PMID: 7517223
  25. Expression of Fas antigen on keratinocytes in vivo and induction of apoptosis in cultured keratinocytes.
    J Invest Dermatol. 1994 Sep;103(3):330-4 PMID: 7521376
  26. Sunburn and p53 in the onset of skin cancer.
    Nature. 1994 Dec 22-29;372(6508):773-6 PMID: 7997263
  27. Keratins and the skin.
    Annu Rev Cell Dev Biol. 1995;11:123-53 PMID: 8689554
  28. Apoptosis is the predominant form of epithelial target cell injury in acute experimental graft-versus-host disease.
    J Invest Dermatol. 1996 Sep;107(3):377-83 PMID: 8751974
  29. Bcl-x expression influences keratinocyte cell survival but not terminal differentiation.
    Cell Growth Differ. 1997 Jun;8(6):619-29 PMID: 9185996
  30. A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma.
    Nat Med. 1997 Aug;3(8):917-21 PMID: 9256286
  31. Developmentally regulated expression of the novel cancer anti-apoptosis gene survivin in human and mouse differentiation.
    Am J Pathol. 1998 Jan;152(1):43-9 PMID: 9422522
  32. Human keratin-1.bcl-2 transgenic mice aberrantly express keratin 6, exhibit reduced sensitivity to keratinocyte cell death induction, and are susceptible to skin tumor formation.
    Oncogene. 1998 Feb 19;16(7):853-63 PMID: 9484776
  33. Partial purification and characterization of two distinct types of caspases from human epidermis.
    J Invest Dermatol. 1998 Sep;111(3):367-72 PMID: 9740225
  34. Differential regulation of P53 and Bcl-2 expression by ultraviolet A and B.
    J Invest Dermatol. 1998 Sep;111(3):380-4 PMID: 9740227
  35. Inhibition of toxic epidermal necrolysis by blockade of CD95 with human intravenous immunoglobulin.
    Science. 1998 Oct 16;282(5388):490-3 PMID: 9774279
  36. Control of apoptosis and mitotic spindle checkpoint by survivin.
    Nature. 1998 Dec 10;396(6711):580-4 PMID: 9859993
  37. IAP family proteins--suppressors of apoptosis.
    Genes Dev. 1999 Feb 1;13(3):239-52 PMID: 9990849
  38. Apaf-1 and caspase-9 in p53-dependent apoptosis and tumor inhibition.
    Science. 1999 Apr 2;284(5411):156-9 PMID: 10102818
  39. Caspase activation in the terminal differentiation of human epidermal keratinocytes.
    Curr Biol. 1999 Apr 8;9(7):361-4 PMID: 10209121
  40. The cancer antiapoptosis mouse survivin gene: characterization of locus and transcriptional requirements of basal and cell cycle-dependent expression.
    Cancer Res. 1999 Jul 1;59(13):3143-51 PMID: 10397257
  41. p53 protects against skin cancer induction by UV-B radiation.
    Oncogene. 1999 Jul 22;18(29):4247-53 PMID: 10435637
  42. Fas ligand: a sensor for DNA damage critical in skin cancer etiology.
    Science. 1999 Aug 6;285(5429):898-900 PMID: 10436160
  43. Communication: expression of the novel inhibitor of apoptosis survivin in normal and neoplastic skin.
    J Invest Dermatol. 1999 Sep;113(3):415-8 PMID: 10469343
  44. Expression of the apoptosis inhibitor, survivin, in nonmelanoma skin cancer and gene targeting in a keratinocyte cell line.
    Lab Invest. 1999 Sep;79(9):1121-6 PMID: 10496530
  45. BCL2 protein is topographically restricted in tissues characterized by apoptotic cell death.
    Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):6961-5 PMID: 1871110
  46. Survivin apoptosis: an interloper between cell death and cell proliferation in cancer.
    Lab Invest. 1999 Nov;79(11):1327-33 PMID: 10576203
  47. Programmed cell death in normal epidermis and loricrin keratoderma. Multiple functions of profilaggrin in keratinization.
    J Investig Dermatol Symp Proc. 1999 Sep;4(2):145-9 PMID: 10536989
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
0021-9738
Published
2001-10-00
Pages
991-9
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC200956
Subset
IM
Grants
NCI NIH HHS · R01 CA078810 · United States
NCI NIH HHS · CA-78810 · United States
NIAMS NIH HHS · T32 AR007016 · United States
NCI NIH HHS · CA-90917 · United States
NCI NIH HHS · R01 CA090917 · United States
NIAMS NIH HHS · 5T32AR07016 · United States
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