Home LiteratureArticle Details
PMID: 10970867 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Regulation of the 26S proteasome by adenovirus E1A.

The EMBO journal ·Vol. 19 ·No. 17 ·2000-09-01 ·Pages 4759-73

Turnell AS, Grand RJ, Gorbea C, Zhang X, Wang W, Mymryk JS, Gallimore PH

Abstract

We have identified the N-terminus of adenovirus early region 1A (AdE1A) as a region that can regulate the 26S proteasome. Specifically, in vitro and in vivo co-precipitation studies have revealed that the 19S regulatory components of the proteasome, Sug1 (S8) and S4, bind through amino acids (aa) 4-25 of Ad5 E1A. In vivo expression of wild-type (wt) AdE1A, in contrast to the N-terminal AdE1A mutant that does not bind the proteasome, reduces ATPase activity associated with anti-S4 immunoprecipitates relative to mock-infected cells. This reduction in ATPase activity correlates positively with the ability of wt AdE1A, but not the N-terminal deletion mutant, to significantly reduce the ability of HPV16 E6 to target p53 for ubiquitin-mediated proteasomal degradation. AdE1A/proteasomal complexes are present in both the cytoplasm and the nucleus, suggesting that AdE1A interferes with both nuclear and cytoplasmic proteasomal degradation. We have also demonstrated that wt AdE1A and the N-terminal AdE1A deletion mutant are substrates for proteasomal-mediated degradation. AdE1A degradation is not, however, mediated through ubiquitylation, but is regulated through phosphorylation of residues within a C-terminal PEST region (aa 224-238).

MeSH Terms
ATPases Associated with Diverse Cellular Activities Adaptor Proteins, Signal Transducing Adenosine Triphosphatases/metabolism Adenovirus E1A Proteins/metabolism Binding Sites Carrier Proteins/metabolism DNA Helicases/metabolism Humans Intracellular Signaling Peptides and Proteins LIM Domain Proteins Oncogene Proteins, Viral/metabolism Peptide Hydrolases/metabolism Phosphorylation Precipitin Tests Proteasome Endopeptidase Complex Repressor Proteins Substrate Specificity Transcription Factors Ubiquitins/metabolism
Chemicals
Adaptor Proteins, Signal Transducing Adenovirus E1A Proteins Carrier Proteins E6 protein, Human papillomavirus type 16 Intracellular Signaling Peptides and Proteins LIM Domain Proteins Oncogene Proteins, Viral PSMC5 protein, human Repressor Proteins SUG1 protein, mammalian Transcription Factors Ubiquitins Peptide Hydrolases Proteasome Endopeptidase Complex ATP dependent 26S protease Adenosine Triphosphatases ATPases Associated with Diverse Cellular Activities DNA Helicases
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Turnell A S
CRC Institute for Cancer Studies, The Medical School, The University of Birmingham, Edgbaston, Birmingham B15 2TT, UK. A.S.Turnell@bham.ac.uk
Grand R J
Gorbea C
Zhang X
Wang W
Mymryk J S
Gallimore P H
References (66)
66 references, click to expand
  1. Sequences in E1A proteins of human adenovirus 5 required for cell transformation, repression of a transcriptional enhancer, and induction of proliferating cell nuclear antigen.
    Virology. 1989 Jul;171(1):120-30 PMID: 2568030
  2. Phosphorylation-dependent degradation of the cyclin-dependent kinase inhibitor p27.
    EMBO J. 1997 Sep 1;16(17):5334-44 PMID: 9311993
  3. Histone acetyltransferase activity of CBP is controlled by cycle-dependent kinases and oncoprotein E1A.
    Nature. 1998 Nov 12;396(6707):184-6 PMID: 9823900
  4. The transcriptional coactivators p300 and CBP are histone acetyltransferases.
    Cell. 1996 Nov 29;87(5):953-9 PMID: 8945521
  5. Mapping subunit contacts in the regulatory complex of the 26 S proteasome. S2 and S5b form a tetramer with ATPase subunits S4 and S7.
    J Biol Chem. 2000 Jan 14;275(2):875-82 PMID: 10625621
  6. The large E1B protein together with the E4orf6 protein target p53 for active degradation in adenovirus infected cells.
    Oncogene. 1998 Jan 22;16(3):349-57 PMID: 9467960
  7. Structure of cDNAs encoding human eukaryotic initiation factor 3 subunits. Possible roles in RNA binding and macromolecular assembly.
    J Biol Chem. 1997 Oct 24;272(43):27042-52 PMID: 9341143
  8. A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3.
    Cell. 1998 Sep 4;94(5):615-23 PMID: 9741626
  9. A novel protein complex involved in signal transduction possessing similarities to 26S proteasome subunits.
    FASEB J. 1998 Apr;12(6):469-78 PMID: 9535219
  10. Mammalian Sug1 and c-Fos in the nuclear 26S proteasome.
    Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8236-40 PMID: 8710853
  11. The adenovirus E1A-associated kinase consists of cyclin E-p33cdk2 and cyclin A-p33cdk2.
    J Virol. 1993 May;67(5):2456-65 PMID: 8386263
  12. Accumulation of p53 induced by the adenovirus E1A protein requires regions involved in the stimulation of DNA synthesis.
    J Virol. 1997 May;71(5):3526-33 PMID: 9094624
  13. Ubiquitinylation is not an absolute requirement for degradation of c-Jun protein by the 26 S proteasome.
    J Biol Chem. 1995 May 12;270(19):11623-7 PMID: 7744802
  14. AAA-ATPases at the crossroads of protein life and death.
    Nat Cell Biol. 1999 Aug;1(4):E97-8 PMID: 10559933
  15. Essential role for p53-mediated transcription in E1A-induced apoptosis.
    Genes Dev. 1995 Sep 1;9(17):2184-92 PMID: 7657169
  16. Active site mutants in the six regulatory particle ATPases reveal multiple roles for ATP in the proteasome.
    EMBO J. 1998 Sep 1;17(17):4909-19 PMID: 9724628
  17. Rapid intracellular turnover of adenovirus 5 early region 1A proteins.
    J Virol. 1984 Nov;52(2):706-10 PMID: 6333516
  18. Mammalian Srb/Mediator complex is targeted by adenovirus E1A protein.
    Nature. 1999 May 20;399(6733):276-9 PMID: 10353252
  19. Chemical inhibitors of cyclin-dependent kinases.
    Prog Cell Cycle Res. 1995;1:351-63 PMID: 9552377
  20. Association of p19(ARF) with Mdm2 inhibits ubiquitin ligase activity of Mdm2 for tumor suppressor p53.
    EMBO J. 1999 Jan 4;18(1):22-7 PMID: 9878046
  21. The ubiquitin-proteasome pathway: on protein death and cell life.
    EMBO J. 1998 Dec 15;17(24):7151-60 PMID: 9857172
  22. E1A signaling to p53 involves the p19(ARF) tumor suppressor.
    Genes Dev. 1998 Aug 1;12(15):2434-42 PMID: 9694807
  23. Adenovirus E1A 12S protein induces DNA synthesis and proliferation in primary epithelial cells in both the presence and absence of serum.
    J Virol. 1987 Mar;61(3):673-82 PMID: 3027395
  24. Molecular cloning and functional analysis of the adenovirus E1A-associated 300-kD protein (p300) reveals a protein with properties of a transcriptional adaptor.
    Genes Dev. 1994 Apr 15;8(8):869-84 PMID: 7523245
  25. Promoter targeting by adenovirus E1a through interaction with different cellular DNA-binding domains.
    Nature. 1994 Apr 7;368(6471):520-5 PMID: 8139685
  26. Proteasomal turnover of p21Cip1 does not require p21Cip1 ubiquitination.
    Mol Cell. 2000 Feb;5(2):403-10 PMID: 10882081
  27. p53, the cellular gatekeeper for growth and division.
    Cell. 1997 Feb 7;88(3):323-31 PMID: 9039259
  28. The degradation sequence of adenovirus E1A consists of the amino-terminal tetrapeptide Met-Arg-His-Ile.
    Mol Cell Biol. 1990 Nov;10(11):5609-15 PMID: 2146491
  29. Identification of specific adenovirus E1A N-terminal residues critical to the binding of cellular proteins and to the control of cell growth.
    J Virol. 1993 Jan;67(1):476-88 PMID: 8416379
  30. Regulation of p53 stability by Mdm2.
    Nature. 1997 May 15;387(6630):299-303 PMID: 9153396
  31. Control of p53 expression by adenovirus 12 early region 1A and early region 1B 54K proteins.
    Virology. 1996 Apr 1;218(1):23-34 PMID: 8615026
  32. The AAA team: related ATPases with diverse functions.
    Trends Cell Biol. 1998 Feb;8(2):65-71 PMID: 9695811
  33. Degradation of p53 can be targeted by HPV E6 sequences distinct from those required for p53 binding and trans-activation.
    Cell. 1991 Nov 1;67(3):547-56 PMID: 1657399
  34. The adenovirus E1A-associated 130-kD protein is encoded by a member of the retinoblastoma gene family and physically interacts with cyclins A and E.
    Genes Dev. 1993 Dec;7(12A):2366-77 PMID: 8253383
  35. Transcriptional modulation by the adenovirus E1A gene.
    Curr Top Microbiol Immunol. 1995;199 ( Pt 3):59-80 PMID: 7555084
  36. Adenovirus e1a proteins and transformation (review).
    Int J Oncol. 1994 Sep;5(3):425-44 PMID: 21559595
  37. Inactivation of p53 but not p73 by adenovirus type 5 E1B 55-kilodalton and E4 34-kilodalton oncoproteins.
    J Virol. 1998 Nov;72(11):8510-6 PMID: 9765388
  38. Effects of Ad5 E1A mutant viruses on the cell cycle in relation to the binding of cellular proteins including the retinoblastoma protein and cyclin A.
    Virology. 1992 Jan;186(1):15-24 PMID: 1530776
  39. Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis.
    Science. 1986 Oct 17;234(4774):364-8 PMID: 2876518
  40. Mdm2 promotes the rapid degradation of p53.
    Nature. 1997 May 15;387(6630):296-9 PMID: 9153395
  41. Association between an oncogene and an anti-oncogene: the adenovirus E1A proteins bind to the retinoblastoma gene product.
    Nature. 1988 Jul 14;334(6178):124-9 PMID: 2968522
  42. Ubiquitin-dependent c-Jun degradation in vivo is mediated by the delta domain.
    Cell. 1994 Sep 9;78(5):787-98 PMID: 8087846
  43. The proteasome: paradigm of a self-compartmentalizing protease.
    Cell. 1998 Feb 6;92(3):367-80 PMID: 9476896
  44. The CBP co-activator is a histone acetyltransferase.
    Nature. 1996 Dec 19-26;384(6610):641-3 PMID: 8967953
  45. Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53.
    FEBS Lett. 1997 Dec 22;420(1):25-7 PMID: 9450543
  46. SUG1, a putative transcriptional mediator and subunit of the PA700 proteasome regulatory complex, is a DNA helicase.
    J Biol Chem. 1997 Mar 14;272(11):7122-6 PMID: 9054406
  47. The zinc finger region of the adenovirus E1A transactivating domain complexes with the TATA box binding protein.
    Proc Natl Acad Sci U S A. 1994 Mar 29;91(7):2488-92 PMID: 8146144
  48. Degradation of the tumor suppressor protein p53 by the ubiquitin-mediated proteolytic system requires a novel species of ubiquitin-carrier protein, E2.
    J Biol Chem. 1994 Apr 1;269(13):9582-9 PMID: 8144545
  49. Molecular cloning and characterization of a cellular phosphoprotein that interacts with a conserved C-terminal domain of adenovirus E1A involved in negative modulation of oncogenic transformation.
    Proc Natl Acad Sci U S A. 1995 Nov 7;92(23):10467-71 PMID: 7479821
  50. Differential ligand-dependent interactions between the AF-2 activating domain of nuclear receptors and the putative transcriptional intermediary factors mSUG1 and TIF1.
    EMBO J. 1996 Jan 2;15(1):110-24 PMID: 8598193
  51. Human cells arrest in S phase in response to adenovirus 12 E1A.
    Virology. 1998 May 10;244(2):330-42 PMID: 9601504
  52. Wild-type p53 mediates apoptosis by E1A, which is inhibited by E1B.
    Genes Dev. 1993 Apr;7(4):546-54 PMID: 8384580
  53. Identification of the gal4 suppressor Sug1 as a subunit of the yeast 26S proteasome.
    Nature. 1996 Feb 15;379(6566):655-7 PMID: 8628401
  54. The role of the E6-p53 interaction in the molecular pathogenesis of HPV.
    Oncogene. 1999 Dec 13;18(53):7690-700 PMID: 10618709
  55. Adenovirus early region 1A protein binds to mammalian SUG1-a regulatory component of the proteasome.
    Oncogene. 1999 Jan 14;18(2):449-58 PMID: 9927201
  56. A highly conserved ATPase protein as a mediator between acidic activation domains and the TATA-binding protein.
    Nature. 1995 Mar 2;374(6517):88-91 PMID: 7870180
  57. Defective mitosis due to a mutation in the gene for a fission yeast 26S protease subunit.
    Nature. 1993 Nov 25;366(6453):355-7 PMID: 8247131
  58. Enhanced expression of p53 in human cells infected with mutant adenoviruses.
    Virology. 1994 Sep;203(2):229-40 PMID: 8053147
  59. Specific interactions between ATPase subunits of the 26 S protease.
    J Biol Chem. 1997 May 16;272(20):13403-11 PMID: 9148964
  60. Organic extraction of Pi with isobutanol/toluene.
    Anal Biochem. 1984 May 1;138(2):416-20 PMID: 6742419
  61. Regeneration of the binding properties of adenovirus 12 early region 1A proteins after preparation under denaturing conditions.
    Virology. 1998 Apr 25;244(1):230-42 PMID: 9581794
  62. 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
  63. Interaction of thyroid-hormone receptor with a conserved transcriptional mediator.
    Nature. 1995 Mar 2;374(6517):91-4 PMID: 7870181
  64. Stabilization of the p53 tumor suppressor is induced by adenovirus 5 E1A and accompanies apoptosis.
    Genes Dev. 1993 Apr;7(4):535-45 PMID: 8384579
  65. Nucleo-cytoplasmic shuttling of the hdm2 oncoprotein regulates the levels of the p53 protein via a pathway used by the human immunodeficiency virus rev protein.
    EMBO J. 1998 Jan 15;17(2):554-64 PMID: 9430646
  66. p300 binding by E1A cosegregates with p53 induction but is dispensable for apoptosis.
    J Virol. 1997 May;71(5):3515-25 PMID: 9094623
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
2000-09-01
Pages
4759-73
Language
English
Region
England
NLM ID
8208664
PMCID
PMC302057
Subset
IM
Grants
NIGMS NIH HHS · GM37009 · United States
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