Home LiteratureArticle Details
PMID: 22228303 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

p63-microRNA feedback in keratinocyte senescence.

Rivetti di Val Cervo P, Lena AM, Nicoloso M, Rossi S, Mancini M, Zhou H, Saintigny G, Dellambra E, Odorisio T, Mahé C, Calin GA, Candi E, Melino G

Abstract

We investigated the expression of microRNAs (miRNAs) associated with replicative senescence in human primary keratinocytes. A cohort of miRNAs up-regulated in senescence was identified by genome-wide miRNA profiling, and their change in expression was validated in proliferative versus senescent cells. Among these, miRNA (miR)-138, -181a, -181b, and -130b expression increased with serial passages. miR-138, -181a, and -181b, but not miR-130b, overexpression in proliferating cells was sufficient per se to induce senescence, as evaluated by inhibition of BrdU incorporation and quantification of senescence-activated β-galactosidase staining. We identified Sirt1 as a direct target of miR-138, -181a, and -181b, whereas ΔNp63 expression was inhibited by miR-130b. We also found that ΔNp63α inhibits miR-138, -181a, -181b, and -130b expression by binding directly to p63-responsive elements located in close proximity to the genomic loci of these miRNAs in primary keratinocytes. These findings suggest that changes in miRNA expression, by modulating the levels of regulatory proteins such as p63 and Sirt1, strongly contribute to induction of senescence in primary human keratinocytes, thus linking these two proteins. Our data also indicate that suppression of miR-138, -181a, -181b, and -130b expression is part of a growth-promoting strategy of ΔNp63α in epidermal proliferating cells.

MeSH Terms
Blotting, Western Bromodeoxyuridine Cell Cycle/physiology Cell Line Cell Proliferation Cellular Senescence/physiology Chromatin Immunoprecipitation Computational Biology Flow Cytometry Gene Expression Regulation/genetics,physiology Humans Keratinocytes/cytology,metabolism Luciferases MicroRNAs/metabolism Real-Time Polymerase Chain Reaction Sirtuin 1/metabolism Transcription Factors/metabolism Tumor Suppressor Proteins/metabolism beta-Galactosidase
Chemicals
MicroRNAs TP63 protein, human Transcription Factors Tumor Suppressor Proteins Luciferases beta-Galactosidase SIRT1 protein, human Sirtuin 1 Bromodeoxyuridine
Authors & Affiliations
13 authors, click to expand affiliations / ORCID
Rivetti di Val Cervo Pia
Istituto Dermopatico dell'Immacolata-Istituto di Ricovero e Cura a Carattere Scientifico, Laboratory of Biochemistry, Department of Experimental Medicine and Biochemical Sciences, and University of Rome Tor Vergata, 00133 Rome, Italy.
Lena Anna Maria
Nicoloso Milena
Rossi Simona
Mancini Mara
Zhou Huiqing
Saintigny Gaelle
Dellambra Elena
Odorisio Teresa
Mahé Christian
Calin George Adrian
Candi Eleonora
Melino Gerry
References (42)
42 references, click to expand
  1. Differential roles of p63 isoforms in epidermal development: selective genetic complementation in p63 null mice.
    Cell Death Differ. 2006 Jun;13(6):1037-47 PMID: 16601749
  2. TAp63 prevents premature aging by promoting adult stem cell maintenance.
    Cell Stem Cell. 2009 Jul 2;5(1):64-75 PMID: 19570515
  3. SIRT1 promotes differentiation of normal human keratinocytes.
    J Invest Dermatol. 2009 Jan;129(1):41-9 PMID: 18563176
  4. Mammalian sirtuins: biological insights and disease relevance.
    Annu Rev Pathol. 2010;5:253-95 PMID: 20078221
  5. Downregulation of miR-138 is associated with overexpression of human telomerase reverse transcriptase protein in human anaplastic thyroid carcinoma cell lines.
    Cancer Sci. 2008 Feb;99(2):280-6 PMID: 18201269
  6. miRNAs regulate SIRT1 expression during mouse embryonic stem cell differentiation and in adult mouse tissues.
    Aging (Albany NY). 2010 Jul;2(7):415-31 PMID: 20634564
  7. hsa-mir-181a and hsa-mir-181b function as tumor suppressors in human glioma cells.
    Brain Res. 2008 Oct 21;1236:185-93 PMID: 18710654
  8. p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development.
    Nature. 1999 Apr 22;398(6729):714-8 PMID: 10227294
  9. SIRT1 confers protection against UVB- and H2O2-induced cell death via modulation of p53 and JNK in cultured skin keratinocytes.
    J Cell Mol Med. 2009 Sep;13(9B):3632-43 PMID: 18681908
  10. The essence of senescence.
    Genes Dev. 2010 Nov 15;24(22):2463-79 PMID: 21078816
  11. ENCODE whole-genome data in the UCSC genome browser (2011 update).
    Nucleic Acids Res. 2011 Jan;39(Database issue):D871-5 PMID: 21037257
  12. p63 deficiency activates a program of cellular senescence and leads to accelerated aging.
    Genes Dev. 2005 Sep 1;19(17):1986-99 PMID: 16107615
  13. p63 is a p53 homologue required for limb and epidermal morphogenesis.
    Nature. 1999 Apr 22;398(6729):708-13 PMID: 10227293
  14. Morphogenesis in skin is governed by discrete sets of differentially expressed microRNAs.
    Nat Genet. 2006 Mar;38(3):356-62 PMID: 16462742
  15. Senescent cells, tumor suppression, and organismal aging: good citizens, bad neighbors.
    Cell. 2005 Feb 25;120(4):513-22 PMID: 15734683
  16. TAp63 suppresses metastasis through coordinate regulation of Dicer and miRNAs.
    Nature. 2010 Oct 21;467(7318):986-90 PMID: 20962848
  17. Senescence comes of age.
    Nat Med. 2005 Sep;11(9):920-2 PMID: 16145569
  18. Cell senescence: hypertrophic arrest beyond the restriction point.
    J Cell Physiol. 2006 Dec;209(3):592-7 PMID: 17001692
  19. Cellular senescence: when bad things happen to good cells.
    Nat Rev Mol Cell Biol. 2007 Sep;8(9):729-40 PMID: 17667954
  20. p63 Is essential for the proliferative potential of stem cells in stratified epithelia.
    Cell. 2007 May 4;129(3):523-36 PMID: 17482546
  21. Identification of senescence-inducing microRNAs in normal human keratinocytes.
    Int J Oncol. 2011 Nov;39(5):1205-11 PMID: 21725593
  22. A skin microRNA promotes differentiation by repressing 'stemness'.
    Nature. 2008 Mar 13;452(7184):225-9 PMID: 18311128
  23. Aging and disease: connections to sirtuins.
    Aging Cell. 2010 Apr;9(2):285-90 PMID: 20409078
  24. Nucleosome dynamics define transcriptional enhancers.
    Nat Genet. 2010 Apr;42(4):343-7 PMID: 20208536
  25. Single-nucleotide polymorphisms inside microRNA target sites influence tumor susceptibility.
    Cancer Res. 2010 Apr 1;70(7):2789-98 PMID: 20332227
  26. Differential altered stability and transcriptional activity of ΔNp63 mutants in distinct ectodermal dysplasias.
    J Cell Sci. 2011 Jul 1;124(Pt 13):2200-7 PMID: 21652629
  27. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome.
    Nat Genet. 2007 Mar;39(3):311-8 PMID: 17277777
  28. A biomarker that identifies senescent human cells in culture and in aging skin in vivo.
    Proc Natl Acad Sci U S A. 1995 Sep 26;92(20):9363-7 PMID: 7568133
  29. miR-203 represses 'stemness' by repressing DeltaNp63.
    Cell Death Differ. 2008 Jul;15(7):1187-95 PMID: 18483491
  30. Dissecting the unique role of the retinoblastoma tumor suppressor during cellular senescence.
    Cancer Cell. 2010 Apr 13;17(4):376-87 PMID: 20385362
  31. Replicative senescence: a critical review.
    Mech Ageing Dev. 2004 Oct-Nov;125(10-11):827-48 PMID: 15541776
  32. TAp63 induces senescence and suppresses tumorigenesis in vivo.
    Nat Cell Biol. 2009 Dec;11(12):1451-7 PMID: 19898465
  33. MicroRNA-138 suppresses invasion and promotes apoptosis in head and neck squamous cell carcinoma cell lines.
    Cancer Lett. 2009 Dec 28;286(2):217-22 PMID: 19540661
  34. MicroRNA-mediated control in the skin.
    Cell Death Differ. 2010 Feb;17(2):229-35 PMID: 19609273
  35. Genome-wide profiling of p63 DNA-binding sites identifies an element that regulates gene expression during limb development in the 7q21 SHFM1 locus.
    PLoS Genet. 2010 Aug 19;6(8):e1001065 PMID: 20808887
  36. DGCR8-dependent microRNA biogenesis is essential for skin development.
    Proc Natl Acad Sci U S A. 2009 Jan 13;106(2):498-502 PMID: 19114655
  37. Telomeres and telomerase in cancer.
    Carcinogenesis. 2010 Jan;31(1):9-18 PMID: 19887512
  38. MicroRNA 217 modulates endothelial cell senescence via silent information regulator 1.
    Circulation. 2009 Oct 13;120(15):1524-32 PMID: 19786632
  39. Healing and hurting: molecular mechanisms, functions, and pathologies of cellular senescence.
    Mol Cell. 2009 Oct 9;36(1):2-14 PMID: 19818705
  40. p63, a p53 homolog at 3q27-29, encodes multiple products with transactivating, death-inducing, and dominant-negative activities.
    Mol Cell. 1998 Sep;2(3):305-16 PMID: 9774969
  41. A Mutant-p53/Smad complex opposes p63 to empower TGFbeta-induced metastasis.
    Cell. 2009 Apr 3;137(1):87-98 PMID: 19345189
  42. Bmi-1 reduction plays a key role in physiological and premature aging of primary human keratinocytes.
    J Invest Dermatol. 2010 Apr;130(4):1048-62 PMID: 19907431
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2012-01-24
Epub
2012-00-06
Pages
1133-8
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC3268329
Subset
IM
Grants
Medical Research Council · MC_U132670600 · United Kingdom
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com