Home LiteratureArticle Details
PMID: 9405677 Published · ppublish English Journal Article

Hepatitis B virus X protein and p53 tumor suppressor interactions in the modulation of apoptosis.

Elmore LW, Hancock AR, Chang SF, Wang XW, Chang S, Callahan CP, Geller DA, Will H, Harris CC

Abstract

We have reported previously that the hepatitis B virus oncoprotein, HBx, can bind to the C terminus of p53 and inhibit several critical p53-mediated cellular processes, including DNA sequence-specific binding, transcriptional transactivation, and apoptosis. Recognizing the importance of p53-mediated apoptosis for maintaining homeostasis and preventing neoplastic transformation, here we further examine the physical interaction between HBx and p53 as well as the functional consequences of this association. In vitro binding studies indicate that the ayw and adr viral subtypes of HBx bind similar amounts of glutathione S-transferase-p53 with the distal C terminus of HBx (from residues 111 to 154) being critical for this interaction. Using a microinjection technique, we show that this same C-terminal region of HBx is necessary for sequestering p53 in the cytoplasm and abrogating p53-mediated apoptosis. The transcriptional transactivation domain of HBx also maps to its C terminus; however, a comparison of the ability of full-length and truncated HBx protein to abrogate p53-induced apoptosis versus transactivate simian virus 40- or human nitric oxide synthase-2 promoter-driven reporter constructs indicates that these two functional properties are distinct and thus may contribute to hepatocarcinogenesis differently. Collectively, our data indicate that the distal C-terminal domain of HBx, independent of its transactivation activity, complexes with p53 in the cytoplasm, partially preventing its nuclear entry and ability to induce apoptosis. These pathobiological effects of HBx may contribute to the early stages of hepatocellular carcinogenesis.

MeSH Terms
Adult Apoptosis Cells, Cultured Child, Preschool Fibroblasts/metabolism,pathology Gene Expression Regulation Genes, Tumor Suppressor Humans Liver/metabolism,pathology Male Protein Binding Trans-Activators/genetics,metabolism Tumor Suppressor Protein p53/genetics,metabolism Viral Regulatory and Accessory Proteins
Chemicals
Trans-Activators Tumor Suppressor Protein p53 Viral Regulatory and Accessory Proteins hepatitis B virus X protein
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Elmore L W
Laboratory of Human Carcinogenesis, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892, USA.
Hancock A R
Chang S F
Wang X W
Chang S
Callahan C P
Geller D A
Will H
Harris C C
References (58)
58 references, click to expand
  1. Induction of apoptosis in fibroblasts by IL-1 beta-converting enzyme, a mammalian homolog of the C. elegans cell death gene ced-3.
    Cell. 1993 Nov 19;75(4):653-60 PMID: 8242741
  2. p53 gene abnormalities are closely related to hepatoviral infections and occur at a late stage of hepatocarcinogenesis.
    Cancer Res. 1994 Jan 1;54(1):231-5 PMID: 8261444
  3. Induction of the DNA-binding activity of c-jun/c-fos heterodimers by the hepatitis B virus transactivator pX.
    Mol Cell Biol. 1994 Feb;14(2):989-98 PMID: 7507209
  4. Genetic heterogeneity of hepatocellular carcinoma.
    Proc Natl Acad Sci U S A. 1994 Jan 18;91(2):822-6 PMID: 8290606
  5. Hepatitis B virus X protein inhibits p53 sequence-specific DNA binding, transcriptional activity, and association with transcription factor ERCC3.
    Proc Natl Acad Sci U S A. 1994 Mar 15;91(6):2230-4 PMID: 8134379
  6. Molecular events in the pathogenesis of hepadnavirus-associated hepatocellular carcinoma.
    Annu Rev Med. 1994;45:297-323 PMID: 8198385
  7. Cancer therapy meets p53.
    N Engl J Med. 1994 Jul 7;331(1):49-50 PMID: 8202105
  8. p53-dependent apoptosis in the absence of transcriptional activation of p53-target genes.
    Nature. 1994 Jul 21;370(6486):220-3 PMID: 8028670
  9. Mutations in the p53 tumor suppressor gene: clues to cancer etiology and molecular pathogenesis.
    Cancer Res. 1994 Sep 15;54(18):4855-78 PMID: 8069852
  10. Nitric oxide synthases: roles, tolls, and controls.
    Cell. 1994 Sep 23;78(6):915-8 PMID: 7522969
  11. Biology of hepatitis B virus variants.
    Lab Invest. 1994 Sep;71(3):324-49 PMID: 7933984
  12. Woodchuck hepatitis virus surface antigen induces nitric oxide synthesis in hepatocytes: possible role in hepatocarcinogenesis.
    Carcinogenesis. 1994 Dec;15(12):2875-7 PMID: 8001249
  13. Hepatitis B and C viruses in the development of hepatocellular carcinoma.
    Crit Rev Oncol Hematol. 1994 Oct;17(2):71-91 PMID: 7818788
  14. Selective accumulation of the X transcript of hepatitis B virus in patients negative for hepatitis B surface antigen with hepatocellular carcinoma.
    Hepatology. 1995 Feb;21(2):313-21 PMID: 7843699
  15. Functional inactivation but not structural mutation of p53 causes liver cancer.
    Nat Genet. 1995 Jan;9(1):41-7 PMID: 7704023
  16. Hepadna virus integration generates virus-cell cotranscripts carrying 3' truncated X genes in human and woodchuck liver tumors.
    J Med Virol. 1995 Jan;45(1):82-90 PMID: 7714496
  17. Transactivation of cellular gene expression by hepatitis B viral proteins: a possible molecular mechanism of hepatocarcinogenesis.
    J Hepatol. 1995;22(1 Suppl):34-7 PMID: 7602073
  18. Induction of apoptosis in HeLa cells by trans-activation-deficient p53.
    Genes Dev. 1995 Sep 1;9(17):2170-83 PMID: 7657168
  19. Nitric oxide induces oxidative damage in addition to deamination in macrophage DNA.
    Chem Res Toxicol. 1995 Apr-May;8(3):473-7 PMID: 7578935
  20. Abrogation of p53-induced apoptosis by the hepatitis B virus X gene.
    Cancer Res. 1995 Dec 15;55(24):6012-6 PMID: 8521383
  21. p53 in malignant and benign liver lesions.
    Eur J Cancer. 1995 Oct;31A(11):1847-50 PMID: 8541111
  22. Specific loss of apoptotic but not cell-cycle arrest function in a human tumor derived p53 mutant.
    EMBO J. 1996 Feb 15;15(4):827-38 PMID: 8631304
  23. Trans-activation function of a 3' truncated X gene-cell fusion product from integrated hepatitis B virus DNA in chronic hepatitis tissues.
    Proc Natl Acad Sci U S A. 1990 Aug;87(15):5628-32 PMID: 2165598
  24. Integration of hepatitis B virus DNA and its implications for hepatocarcinogenesis.
    Mol Biol Med. 1990 Jun;7(3):243-60 PMID: 2170810
  25. Mutational hotspot in the p53 gene in human hepatocellular carcinomas.
    Nature. 1991 Apr 4;350(6317):427-8 PMID: 1849234
  26. Identification of three essential regions of hepatitis B virus X protein for trans-activation function.
    Oncogene. 1992 Mar;7(3):397-403 PMID: 1549357
  27. DNA damage and mutation in human cells exposed to nitric oxide in vitro.
    Proc Natl Acad Sci U S A. 1992 Apr 1;89(7):3030-4 PMID: 1557408
  28. Stimulation of the nitric oxide synthase pathway in human hepatocytes by cytokines and endotoxin.
    J Exp Med. 1992 Jul 1;176(1):261-4 PMID: 1377225
  29. Infrequent mutation of p53 gene in hepatitis B virus positive primary hepatocellular carcinomas.
    Oncogene. 1993 Feb;8(2):491-6 PMID: 8093978
  30. Hepatitis B x antigen and p53 are associated in vitro and in liver tissues from patients with primary hepatocellular carcinoma.
    Oncogene. 1993 May;8(5):1109-17 PMID: 8386823
  31. Tumor progression in hepatocellular carcinoma may be mediated by p53 mutation.
    Cancer Res. 1993 Jun 15;53(12):2884-7 PMID: 8389246
  32. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death.
    Cell. 1993 Aug 27;74(4):609-19 PMID: 8358790
  33. Selective G to T mutations of p53 gene in hepatocellular carcinoma from southern Africa.
    Nature. 1991 Apr 4;350(6317):429-31 PMID: 1672732
  34. HBV X protein alters the DNA binding specificity of CREB and ATF-2 by protein-protein interactions.
    Science. 1991 May 10;252(5007):842-4 PMID: 1827531
  35. HBx gene of hepatitis B virus induces liver cancer in transgenic mice.
    Nature. 1991 May 23;351(6324):317-20 PMID: 2034275
  36. The p53 tumour suppressor gene.
    Nature. 1991 Jun 6;351(6326):453-6 PMID: 2046748
  37. Detection of aberrations of the p53 alleles and the gene transcript in human tumor cell lines by single-strand conformation polymorphism analysis.
    Cancer Res. 1991 Jul 1;51(13):3356-61 PMID: 2054775
  38. DNA deaminating ability and genotoxicity of nitric oxide and its progenitors.
    Science. 1991 Nov 15;254(5034):1001-3 PMID: 1948068
  39. Hepatitis B virus X protein activates transcription factor NF-kappa B without a requirement for protein kinase C.
    J Virol. 1992 Feb;66(2):983-91 PMID: 1309924
  40. Nitric oxide-induced p53 accumulation and regulation of inducible nitric oxide synthase expression by wild-type p53.
    Proc Natl Acad Sci U S A. 1996 Mar 19;93(6):2442-7 PMID: 8637893
  41. Increased sensitivity to the hepatocarcinogen diethylnitrosamine in transgenic mice carrying the hepatitis B virus X gene.
    Mol Carcinog. 1996 Apr;15(4):261-9 PMID: 8634084
  42. An aflatoxin-associated mutational hotspot at codon 249 in the p53 tumor suppressor gene occurs in hepatocellular carcinomas from Mexico.
    Carcinogenesis. 1996 May;17(5):1007-12 PMID: 8640905
  43. The XPB and XPD DNA helicases are components of the p53-mediated apoptosis pathway.
    Genes Dev. 1996 May 15;10(10):1219-32 PMID: 8675009
  44. A truncated mutant (residues 58-140) of the hepatitis B virus X protein retains transactivation function.
    Proc Natl Acad Sci U S A. 1996 May 28;93(11):5647-52 PMID: 8643631
  45. A functionally inactive p53 protein in teratocarcinoma cells is activated by either DNA damage or cellular differentiation.
    Nat Med. 1996 Jul;2(7):804-10 PMID: 8673928
  46. The hepatitis B virus transactivator protein, HBx, interacts with single-stranded DNA (ssDNA). Biochemical characterizations of the HBx-ssDNA interactions.
    J Biol Chem. 1996 Jun 28;271(26):15443-50 PMID: 8663128
  47. Characteristic histologic features of human hepatocellular carcinoma with mutant p53 protein.
    World J Surg. 1996 Feb;20(2):215-20 PMID: 8661820
  48. Structure and function of the p53 tumor suppressor gene: clues for rational cancer therapeutic strategies.
    J Natl Cancer Inst. 1996 Oct 16;88(20):1442-55 PMID: 8841019
  49. 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
  50. Hepatitis B virus transactivator protein, HBx, associates with the components of TFIIH and stimulates the DNA helicase activity of TFIIH.
    Proc Natl Acad Sci U S A. 1996 Oct 1;93(20):10578-83 PMID: 8855220
  51. Integrity of p53 in hepatitis B x antigen-positive and -negative hepatocellular carcinomas.
    Cancer Res. 1997 Feb 1;57(3):426-32 PMID: 9012469
  52. The hepatitis B virus X gene induces p53-mediated programmed cell death.
    Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):8162-7 PMID: 9223332
  53. The transactivation and p53-interacting functions of hepatitis B virus X protein are mutually interfering but distinct.
    Cancer Res. 1997 Nov 15;57(22):5137-42 PMID: 9371515
  54. Nitric oxide synthase expression is induced in hepatocytes in vivo during hepatic inflammation.
    J Surg Res. 1993 Oct;55(4):427-32 PMID: 7692140
  55. Familial chronic lymphocytic leukemia.
    J Natl Cancer Inst. 1983 Dec;71(6):1143-50 PMID: 6418939
  56. The X gene of hepatitis B virus induced growth stimulation and tumorigenic transformation of mouse NIH3T3 cells.
    Jpn J Cancer Res. 1989 Jul;80(7):617-21 PMID: 2507484
  57. Malignant transformation of immortalized transgenic hepatocytes after transfection with hepatitis B virus DNA.
    EMBO J. 1990 Apr;9(4):1137-45 PMID: 2323335
  58. A transactivating function encoded in the hepatitis B virus X gene is conserved in the integrated state.
    Oncogene. 1988 Nov;3(5):545-52 PMID: 2856254
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
1997-12-23
Pages
14707-12
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC25100
Subset
IM
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