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PMID: 12446784 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Complex transcriptional effects of p63 isoforms: identification of novel activation and repression domains.

Molecular and cellular biology ·Vol. 22 ·No. 24 ·2002-12-00 ·Pages 8659-68

Ghioni P, Bolognese F, Duijf PH, Van Bokhoven H, Mantovani R, Guerrini L

Abstract

p63 is a transcription factor structurally related to the p53 tumor suppressor. The C-terminal region differs from p53's in that it contains a sterile alpha motif (SAM) domain and is subject to multiple alternative splicings. The N-terminal region is present in the transactivation (TA) and DeltaN configurations, with the latter lacking the transcriptional activation domain 1. Single amino acid substitutions and frameshift mutations of p63 cause the human ankyloblepharon ectodermal dysplasia clefting (AEC) or ectrodactyly ectodermal dysplasia and facial clefting (EEC) syndromes. We have systematically compared the activities of the wild-type p63 isoforms and of the natural mutants in activation and repression assays on three promoters modulated by p53. We found that p63 proteins with an altered SAM domain or no SAM domain-the beta isoforms, the EEC frameshift mutant, and the missense AEC mutations-all showed a distinctly higher level of activation of the MDM2 promoter and decreased repression on the HSP70 promoter. Fusion of SAM to the GAL4 DNA-binding domain repressed a heterologous promoter. A second activation domain, TA2, corresponding to exons 11 to 12, was uncovered by comparing the activation of DeltaN isoforms on natural promoters and in GAL4 fusion systems. In colony formation assays, the AEC mutants, but not the EEC frameshift, were consistently less efficient in suppressing growth, in both the TA version and the DeltaN version, with respect to their p63alpha counterparts. These data highlight the modularity of p63, identifying the SAM domain as a dominant transcriptional repression module and indicating that the AEC and EEC frameshift mutants are characterized by a subversion of the p63 transcriptional potential.

MeSH Terms
Alternative Splicing Animals Cell Line DNA-Binding Proteins Exons/genetics Gene Expression Regulation Genes, Tumor Suppressor Humans Membrane Proteins Mutation Phosphoproteins/genetics,metabolism Promoter Regions, Genetic Protein Isoforms/genetics,metabolism Protein Structure, Tertiary Recombinant Fusion Proteins/genetics,metabolism Repressor Proteins/genetics,metabolism Trans-Activators/genetics,metabolism Transcription Factors Transcription, Genetic Tumor Suppressor Proteins
Chemicals
CKAP4 protein, human DNA-Binding Proteins Membrane Proteins Phosphoproteins Protein Isoforms Recombinant Fusion Proteins Repressor Proteins TP63 protein, human Trans-Activators Transcription Factors Tumor Suppressor Proteins
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Ghioni Pamela
Dipartimento di Genetica e Biologia dei Microrganismi, Milan, Italy.
Bolognese Fabrizio
Duijf Pascal H G
Van Bokhoven Hans
Mantovani Roberto
Guerrini Luisa
References (50)
50 references, click to expand
  1. Lack of homozygously inactivated p73 in single-copy MYCN primary neuroblastomas and neuroblastoma cell lines.
    Neoplasia. 1999 Apr;1(1):80-9 PMID: 10935473
  2. Wild-type p53 can down-modulate the activity of various promoters.
    Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):9979-83 PMID: 1946467
  3. The tumour suppressor protein p53 can repress transcription of cyclin B.
    Nucleic Acids Res. 2000 Nov 15;28(22):4410-8 PMID: 11071927
  4. Hay-Wells syndrome is caused by heterozygous missense mutations in the SAM domain of p63.
    Hum Mol Genet. 2001 Feb 1;10(3):221-9 PMID: 11159940
  5. A subset of tumor-derived mutant forms of p53 down-regulate p63 and p73 through a direct interaction with the p53 core domain.
    Mol Cell Biol. 2001 Mar;21(5):1874-87 PMID: 11238924
  6. p63 identifies keratinocyte stem cells.
    Proc Natl Acad Sci U S A. 2001 Mar 13;98(6):3156-61 PMID: 11248048
  7. P63 and P73: P53 mimics, menaces and more.
    Nat Rev Mol Cell Biol. 2000 Dec;1(3):199-207 PMID: 11252895
  8. Physical interaction with Yes-associated protein enhances p73 transcriptional activity.
    J Biol Chem. 2001 May 4;276(18):15164-73 PMID: 11278685
  9. p63alpha and DeltaNp63alpha can induce cell cycle arrest and apoptosis and differentially regulate p53 target genes.
    Oncogene. 2001 May 31;20(25):3193-205 PMID: 11423969
  10. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours.
    Nature. 1992 Mar 19;356(6366):215-21 PMID: 1552940
  11. Regulation of the human hsp70 promoter by p53.
    Science. 1993 Jan 1;259(5091):84-7 PMID: 8418500
  12. Differential DNA sequence specificity and regulation of HIV-1 enhancer activity by cRel-RelA transcription factor.
    J Biol Chem. 1994 Sep 2;269(35):22230-7 PMID: 8071349
  13. Different members of the Sp1 multigene family exert opposite transcriptional regulation of the long terminal repeat of HIV-1.
    Nucleic Acids Res. 1994 Nov 25;22(23):4914-21 PMID: 7800480
  14. A functional p53-responsive intronic promoter is contained within the human mdm2 gene.
    Nucleic Acids Res. 1995 Jul 25;23(14):2584-92 PMID: 7651818
  15. Role of chromatin and Xenopus laevis heat shock transcription factor in regulation of transcription from the X. laevis hsp70 promoter in vivo.
    Mol Cell Biol. 1995 Nov;15(11):6013-24 PMID: 7565754
  16. Sp3 is a bifunctional transcription regulator with modular independent activation and repression domains.
    J Biol Chem. 1997 Feb 14;272(7):4021-6 PMID: 9020109
  17. Monoallelically expressed gene related to p53 at 1p36, a region frequently deleted in neuroblastoma and other human cancers.
    Cell. 1997 Aug 22;90(4):809-19 PMID: 9288759
  18. p53 tumor-suppressor gene: clues to molecular carcinogenesis.
    J Cell Physiol. 1997 Nov;173(2):247-55 PMID: 9365531
  19. Predicting functions from protein sequences--where are the bottlenecks?
    Nat Genet. 1998 Apr;18(4):313-8 PMID: 9537411
  20. Cloning and functional analysis of human p51, which structurally and functionally resembles p53.
    Nat Med. 1998 Jul;4(7):839-43 PMID: 9662378
  21. 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
  22. NF-Y binding to twin CCAAT boxes: role of Q-rich domains and histone fold helices.
    J Mol Biol. 1999 Jan 29;285(4):1441-55 PMID: 9917388
  23. p63 is a p53 homologue required for limb and epidermal morphogenesis.
    Nature. 1999 Apr 22;398(6729):708-13 PMID: 10227293
  24. p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development.
    Nature. 1999 Apr 22;398(6729):714-8 PMID: 10227294
  25. p73 and p63 are homotetramers capable of weak heterotypic interactions with each other but not with p53.
    J Biol Chem. 1999 Jun 25;274(26):18709-14 PMID: 10373484
  26. Identification of a transactivation activity in the COOH-terminal region of p73 which is impaired in the naturally occurring mutants found in human neuroblastomas.
    Cancer Res. 1999 Jun 15;59(12):2810-4 PMID: 10383137
  27. Promoter specificity and stability control of the p53-related protein p73.
    Oncogene. 1999 Jul 22;18(29):4171-81 PMID: 10435630
  28. p53 Family members p63 and p73 are SAM domain-containing proteins.
    Protein Sci. 1999 Aug;8(8):1708-10 PMID: 10452616
  29. Solution structure of a conserved C-terminal domain of p73 with structural homology to the SAM domain.
    EMBO J. 1999 Aug 16;18(16):4438-45 PMID: 10449409
  30. New p73 variants with altered C-terminal structures have varied transcriptional activities.
    Oncogene. 1999 Sep 2;18(35):4993-8 PMID: 10490834
  31. p53 family update: p73 and p63 develop their own identities.
    Cell Growth Differ. 2001 Jul;12(7):337-49 PMID: 11457731
  32. Identification and tissue distribution of novel KET/p63 splice variants.
    FEBS Lett. 2001 Jul 20;501(2-3):121-6 PMID: 11470269
  33. p63 Gene mutations in eec syndrome, limb-mammary syndrome, and isolated split hand-split foot malformation suggest a genotype-phenotype correlation.
    Am J Hum Genet. 2001 Sep;69(3):481-92 PMID: 11462173
  34. p53 Homologue p63 represses epidermal growth factor receptor expression.
    J Biol Chem. 2001 Nov 9;276(45):41717-24 PMID: 11546792
  35. The p53 and Mdm2 families in cancer.
    Curr Opin Genet Dev. 2002 Feb;12(1):53-9 PMID: 11790555
  36. Heterozygous germline mutations in the p53 homolog p63 are the cause of EEC syndrome.
    Cell. 1999 Oct 15;99(2):143-53 PMID: 10535733
  37. Deletion of the COOH-terminal region of p73alpha enhances both its transactivation function and DNA-binding activity but inhibits induction of apoptosis in mammalian cells.
    Cancer Res. 1999 Dec 1;59(23):5902-7 PMID: 10606232
  38. Twenty years of p53 research: structural and functional aspects of the p53 protein.
    Oncogene. 1999 Dec 13;18(53):7621-36 PMID: 10618702
  39. p73-deficient mice have neurological, pheromonal and inflammatory defects but lack spontaneous tumours.
    Nature. 2000 Mar 2;404(6773):99-103 PMID: 10716451
  40. Regulation and function of the p53-related proteins: same family, different rules.
    Trends Cell Biol. 2000 May;10(5):197-202 PMID: 10754563
  41. The p53/p63/p73 family of transcription factors: overlapping and distinct functions.
    J Cell Sci. 2000 May;113 ( Pt 10):1661-70 PMID: 10769197
  42. p63 and p73: old members of a new family.
    Biochim Biophys Acta. 2000 May 17;1470(3):M93-M100 PMID: 10799748
  43. How to activate p53.
    Curr Biol. 2000 Apr 20;10(8):R315-7 PMID: 10801407
  44. Split-hand/split-foot malformation is caused by mutations in the p63 gene on 3q27.
    Am J Hum Genet. 2000 Jul;67(1):59-66 PMID: 10839977
  45. p51A (TAp63gamma), a p53 homolog, accumulates in response to DNA damage for cell regulation.
    Oncogene. 2000 Jun 22;19(27):3126-30 PMID: 10871867
  46. p63 and p73 transactivate differentiation gene promoters in human keratinocytes.
    Biochem Biophys Res Commun. 2000 Jun 24;273(1):342-6 PMID: 10873608
  47. The human MDM2 oncoprotein increases the transcriptional activity and the protein level of the p53 homolog p63.
    J Biol Chem. 2002 Jan 25;277(4):2674-81 PMID: 11714701
  48. Post-transcriptional regulation of glyceraldehyde-3-phosphate-dehydrogenase gene expression in rat tissues.
    Nucleic Acids Res. 1984 Sep 25;12(18):6951-63 PMID: 6548307
  49. Analysis of p53 mutants for transcriptional activity.
    Mol Cell Biol. 1991 Dec;11(12):6067-74 PMID: 1944276
  50. Orchestrated response: a symphony of transcription factors for gene control.
    Genes Dev. 2000 Oct 15;14(20):2551-69 PMID: 11040209
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2002-12-00
Pages
8659-68
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC139859
Subset
IM
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