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PMID: 11805282 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Functional p53 chimeras containing the Epstein-Barr virus Gly-Ala repeat are protected from Mdm2- and HPV-E6-induced proteolysis.

Heessen S, Leonchiks A, Issaeva N, Sharipo A, Selivanova G, Masucci MG, Dantuma NP

Abstract

Functional inactivation of the tumor suppressor protein p53 by accelerated ubiquitin/proteasome-dependent proteolysis is a common event in tumor progression. Proteasomal degradation is inhibited by the Gly-Ala repeat (GAr) of the Epstein-Barr virus nuclear antigen-1, which acts as a transferable element on a variety of proteasomal substrates. We demonstrate that p53 chimeras containing GAr domains of different lengths and positions within the protein are protected from proteolysis induced by the ubiquitin ligases murine double minute 2 and E6-associated protein but are still ubiquitinated and retain the capacity to interact with the S5a ubiquitin-binding subunit of the proteasome. The GAr chimeras transactivate p53 target genes, induce cell cycle arrest and apoptosis, and exhibit improved growth inhibitory activity in tumor cells with impaired endogenous p53 activity.

MeSH Terms
Apoptosis/physiology Base Sequence Cell Cycle/physiology Cell Division Cysteine Endopeptidases/metabolism DNA Primers DNA-Binding Proteins Dipeptides/chemistry Genes, p53 Herpesvirus 4, Human/genetics Humans Molecular Sequence Data Multienzyme Complexes/metabolism Neoplasm Proteins/metabolism Nuclear Proteins Oligodeoxyribonucleotides, Antisense Oncogene Proteins, Viral/genetics,metabolism Open Reading Frames Osteosarcoma Proteasome Endopeptidase Complex Proto-Oncogene Proteins/genetics,metabolism Proto-Oncogene Proteins c-mdm2 Recombinant Fusion Proteins Repetitive Sequences, Amino Acid Tumor Cells, Cultured Tumor Suppressor Protein p53/genetics,metabolism Ubiquitin/metabolism
Chemicals
DNA Primers DNA-Binding Proteins Dipeptides E6 protein, Human papillomavirus type 18 Multienzyme Complexes Neoplasm Proteins Nuclear Proteins Oligodeoxyribonucleotides, Antisense Oncogene Proteins, Viral Proto-Oncogene Proteins Recombinant Fusion Proteins Tumor Suppressor Protein p53 Ubiquitin N-glycylalanine MDM2 protein, human Proto-Oncogene Proteins c-mdm2 Cysteine Endopeptidases Proteasome Endopeptidase Complex
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Heessen Stijn
Microbiology and Tumor Biology Center, and Cancer Center Karolinska, Karolinska Institute, S-17177 Stockholm, Sweden.
Leonchiks Ainars
Issaeva Natalia
Sharipo Anatoly
Selivanova Galina
Masucci Maria G
Dantuma Nico P
References (38)
38 references, click to expand
  1. Opposing effects of Ras on p53: transcriptional activation of mdm2 and induction of p19ARF.
    Cell. 2000 Oct 13;103(2):321-30 PMID: 11057904
  2. An intact HDM2 RING-finger domain is required for nuclear exclusion of p53.
    Nat Cell Biol. 2000 Sep;2(9):563-8 PMID: 10980695
  3. Mdm2 inhibits the apoptotic function of p53 mainly by targeting it for degradation.
    J Biol Chem. 2000 Nov 24;275(47):37296-302 PMID: 10980197
  4. Surfing the p53 network.
    Nature. 2000 Nov 16;408(6810):307-10 PMID: 11099028
  5. p53: death star.
    Cell. 2000 Nov 22;103(5):691-4 PMID: 11114324
  6. A TSG101/MDM2 regulatory loop modulates MDM2 degradation and MDM2/p53 feedback control.
    Proc Natl Acad Sci U S A. 2001 Feb 13;98(4):1619-24 PMID: 11172000
  7. DNA sequence and expression of the B95-8 Epstein-Barr virus genome.
    Nature. 1984 Jul 19-25;310(5974):207-11 PMID: 6087149
  8. Suppression of human colorectal carcinoma cell growth by wild-type p53.
    Science. 1990 Aug 24;249(4971):912-5 PMID: 2144057
  9. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53.
    Cell. 1990 Dec 21;63(6):1129-36 PMID: 2175676
  10. The state of the p53 and retinoblastoma genes in human cervical carcinoma cell lines.
    Proc Natl Acad Sci U S A. 1991 Jul 1;88(13):5523-7 PMID: 1648218
  11. Inactivation of p53 gene in human and murine osteosarcoma cells.
    Br J Cancer. 1992 Feb;65(2):208-14 PMID: 1739619
  12. The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation.
    Cell. 1992 Jun 26;69(7):1237-45 PMID: 1535557
  13. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53.
    Cell. 1993 Nov 5;75(3):495-505 PMID: 8221889
  14. A 26 S protease subunit that binds ubiquitin conjugates.
    J Biol Chem. 1994 Mar 11;269(10):7059-61 PMID: 8125911
  15. Crystal structure of a p53 tumor suppressor-DNA complex: understanding tumorigenic mutations.
    Science. 1994 Jul 15;265(5170):346-55 PMID: 8023157
  16. MDM2 gene amplification and transcript levels in human sarcomas: relationship to TP53 gene status.
    J Natl Cancer Inst. 1994 Sep 7;86(17):1297-302 PMID: 8064888
  17. Regulation of mdm2 expression by p53: alternative promoters produce transcripts with nonidentical translation potential.
    Genes Dev. 1994 Aug 1;8(15):1739-49 PMID: 7958853
  18. Inhibition of antigen processing by the internal repeat region of the Epstein-Barr virus nuclear antigen-1.
    Nature. 1995 Jun 22;375(6533):685-8 PMID: 7540727
  19. Sensitivity of p53 lysine mutants to ubiquitin-directed degradation targeted by human papillomavirus E6.
    Virology. 1996 Mar 1;217(1):285-92 PMID: 8599213
  20. p53 levels, functional domains, and DNA damage determine the extent of the apoptotic response of tumor cells.
    Genes Dev. 1996 Oct 1;10(19):2438-51 PMID: 8843196
  21. p53, the cellular gatekeeper for growth and division.
    Cell. 1997 Feb 7;88(3):323-31 PMID: 9039259
  22. Regulation of p53 stability by Mdm2.
    Nature. 1997 May 15;387(6630):299-303 PMID: 9153396
  23. Inhibition of ubiquitin/proteasome-dependent protein degradation by the Gly-Ala repeat domain of the Epstein-Barr virus nuclear antigen 1.
    Proc Natl Acad Sci U S A. 1997 Nov 11;94(23):12616-21 PMID: 9356498
  24. Human CD8+ T cell responses to EBV EBNA1: HLA class I presentation of the (Gly-Ala)-containing protein requires exogenous processing.
    Immunity. 1997 Dec;7(6):791-802 PMID: 9430224
  25. Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53.
    FEBS Lett. 1997 Dec 22;420(1):25-7 PMID: 9450543
  26. ARF promotes MDM2 degradation and stabilizes p53: ARF-INK4a locus deletion impairs both the Rb and p53 tumor suppression pathways.
    Cell. 1998 Mar 20;92(6):725-34 PMID: 9529249
  27. Lessons from an age-old war.
    Nat Med. 1998 Aug;4(8):887-8 PMID: 9701231
  28. A minimal glycine-alanine repeat prevents the interaction of ubiquitinated I kappaB alpha with the proteasome: a new mechanism for selective inhibition of proteolysis.
    Nat Med. 1998 Aug;4(8):939-44 PMID: 9701247
  29. The ubiquitin system.
    Annu Rev Biochem. 1998;67:425-79 PMID: 9759494
  30. Functions of the MDM2 oncoprotein.
    Cell Mol Life Sci. 1999 Jan;55(1):96-107 PMID: 10065155
  31. RB regulates the stability and the apoptotic function of p53 via MDM2.
    Mol Cell. 1999 Feb;3(2):181-93 PMID: 10078201
  32. Nucleotide sequences and further characterization of human papillomavirus DNA present in the CaSki, SiHa and HeLa cervical carcinoma cell lines.
    J Gen Virol. 1999 Jul;80 ( Pt 7):1725-33 PMID: 10423141
  33. The base of the proteasome regulatory particle exhibits chaperone-like activity.
    Nat Cell Biol. 1999 Aug;1(4):221-6 PMID: 10559920
  34. Recognition of misfolding proteins by PA700, the regulatory subcomplex of the 26 S proteasome.
    J Biol Chem. 2000 Feb 25;275(8):5565-72 PMID: 10681537
  35. Physical association of ubiquitin ligases and the 26S proteasome.
    Proc Natl Acad Sci U S A. 2000 Mar 14;97(6):2497-502 PMID: 10688918
  36. Mdm2 is a RING finger-dependent ubiquitin protein ligase for itself and p53.
    J Biol Chem. 2000 Mar 24;275(12):8945-51 PMID: 10722742
  37. Inhibition of proteasomal degradation by the gly-Ala repeat of Epstein-Barr virus is influenced by the length of the repeat and the strength of the degradation signal.
    Proc Natl Acad Sci U S A. 2000 Jul 18;97(15):8381-5 PMID: 10890896
  38. A modified p53 overcomes mdm2-mediated oncogenic transformation: a potential cancer therapeutic agent.
    Cancer Res. 2000 Oct 15;60(20):5895-901 PMID: 11059788
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
0027-8424
Published
2002-02-05
Epub
2002-00-22
Pages
1532-7
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC122225
Subset
IM
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