Home LiteratureArticle Details
PMID: 18604271 Published · epublish English Journal Article Research Support, N.I.H., Extramural

APOBEC3G and APOBEC3F require an endogenous cofactor to block HIV-1 replication.

PLoS pathogens ·Vol. 4 ·No. 7 ·2008-07-04 ·Pages e1000095

Han Y, Wang X, Dang Y, Zheng YH

Abstract

APOBEC3G (A3G)/APOBEC3F (A3F) are two members of APOBEC3 cytidine deaminase subfamily. Although they potently inhibit the replication of vif-deficient HIV-1, this mechanism is still poorly understood. Initially, A3G/A3F were thought to catalyze C-to-U transitions on the minus-strand viral cDNAs during reverse transcription to disrupt the viral life cycle. Recently, it was found more likely that A3G/A3F directly interrupts viral reverse transcription or integration. In addition, A3G/A3F are both found in the high-molecular-mass complex in immortalized cell lines, where they interact with a number of different cellular proteins. However, there has been no evidence to prove that these interactions are required for A3G/A3F function. Here, we studied A3G/A3F-restricted HIV-1 replication in six different human T cell lines by infecting them with wild-type or vif-deficient HIV-1. Interestingly, in a CEM-derived cell line CEM-T4, which expresses high levels of A3G/A3F proteins, the vif-deficient virus replicated as equally well as the wild-type virus, suggesting that these endogenous antiretroviral genes lost anti-HIV activities. It was confirmed that these A3G/A3F genes do not contain any mutation and are functionally normal. Consistently, overexpression of exogenous A3G/A3F in CEM-T4 cells still failed to restore their anti-HIV activities. However, this activity could be restored if CEM-T4 cells were fused to 293T cells to form heterokaryons. These results demonstrate that CEM-T4 cells lack a cellular cofactor, which is critical for A3G/A3F anti-HIV activity. We propose that a further study of this novel factor will provide another strategy for a complete understanding of the A3G/A3F antiretroviral mechanism.

MeSH Terms
APOBEC-3G Deaminase Animals Base Sequence Cell Line, Transformed Cell Nucleus/metabolism,virology Cytidine Deaminase/metabolism Cytosine Deaminase/metabolism Fluorescent Antibody Technique, Indirect HIV-1/physiology Humans Mice Molecular Sequence Data Rabbits Repressor Proteins/metabolism T-Lymphocytes/metabolism,virology Virus Replication/physiology vif Gene Products, Human Immunodeficiency Virus/metabolism
Chemicals
Repressor Proteins vif Gene Products, Human Immunodeficiency Virus APOBEC3F protein, human Cytosine Deaminase APOBEC-3G Deaminase APOBEC3G protein, human Cytidine Deaminase
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Han Yanxing
Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, Michigan, United States of America.
Wang Xiaojun
Dang Ying
Zheng Yong-Hui
References (72)
72 references, click to expand
  1. DNA deamination mediates innate immunity to retroviral infection.
    Cell. 2003 Jun 13;113(6):803-9 PMID: 12809610
  2. Population stratification of a common APOBEC gene deletion polymorphism.
    PLoS Genet. 2007 Apr 20;3(4):e63 PMID: 17447845
  3. Human immunodeficiency virus type 1 cDNAs produced in the presence of APOBEC3G exhibit defects in plus-strand DNA transfer and integration.
    J Virol. 2007 Jul;81(13):7099-110 PMID: 17428871
  4. Biochemical activities of highly purified, catalytically active human APOBEC3G: correlation with antiviral effect.
    J Virol. 2006 Jun;80(12):5992-6002 PMID: 16731938
  5. Cytidine deamination of retroviral DNA by diverse APOBEC proteins.
    Curr Biol. 2004 Aug 10;14(15):1392-6 PMID: 15296758
  6. Antiviral potency of APOBEC proteins does not correlate with cytidine deamination.
    J Virol. 2006 Sep;80(17):8450-8 PMID: 16912295
  7. Human immunodeficiency virus type 1 Vif inhibits packaging and antiviral activity of a degradation-resistant APOBEC3G variant.
    J Virol. 2007 Aug;81(15):8236-46 PMID: 17522211
  8. Deaminase-independent inhibition of HIV-1 reverse transcription by APOBEC3G.
    Nucleic Acids Res. 2007;35(21):7096-108 PMID: 17942420
  9. Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts.
    Nature. 2003 Jul 3;424(6944):99-103 PMID: 12808466
  10. Molecular cloning of an apolipoprotein B messenger RNA editing protein.
    Science. 1993 Jun 18;260(5115):1816-9 PMID: 8511591
  11. Inhibition of a yeast LTR retrotransposon by human APOBEC3 cytidine deaminases.
    Curr Biol. 2005 Apr 12;15(7):661-6 PMID: 15823539
  12. APOBEC3 proteins inhibit human LINE-1 retrotransposition.
    J Biol Chem. 2006 Aug 4;281(31):22161-22172 PMID: 16735504
  13. APOBEC-mediated viral restriction: not simply editing?
    Trends Biochem Sci. 2007 Mar;32(3):118-28 PMID: 17303427
  14. Single-strand specificity of APOBEC3G accounts for minus-strand deamination of the HIV genome.
    Nat Struct Mol Biol. 2004 May;11(5):435-42 PMID: 15098018
  15. The restriction of zoonotic PERV transmission by human APOBEC3G.
    PLoS One. 2007 Sep 12;2(9):e893 PMID: 17849022
  16. HIV accessory proteins: multifunctional components of a complex system.
    Adv Pharmacol. 2000;48:75-120 PMID: 10987089
  17. APOBEC3G inhibits DNA strand transfer during HIV-1 reverse transcription.
    J Biol Chem. 2007 Nov 2;282(44):32065-74 PMID: 17855362
  18. Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein.
    Nature. 2002 Aug 8;418(6898):646-50 PMID: 12167863
  19. Uracil DNA glycosylase is dispensable for human immunodeficiency virus type 1 replication and does not contribute to the antiviral effects of the cytidine deaminase Apobec3G.
    J Virol. 2006 Jan;80(2):875-82 PMID: 16378989
  20. HIV-1 Vif blocks the antiviral activity of APOBEC3G by impairing both its translation and intracellular stability.
    Mol Cell. 2003 Sep;12(3):591-601 PMID: 14527406
  21. Human APOBEC3B is a potent inhibitor of HIV-1 infectivity and is resistant to HIV-1 Vif.
    Virology. 2005 Sep 1;339(2):281-8 PMID: 15993456
  22. Human cytidine deaminase APOBEC3H restricts HIV-1 replication.
    J Biol Chem. 2008 Apr 25;283(17):11606-14 PMID: 18299330
  23. Inhibition of hepatitis B virus replication by APOBEC3G.
    Science. 2004 Mar 19;303(5665):1829 PMID: 15031497
  24. The antiretroviral enzyme APOBEC3G is degraded by the proteasome in response to HIV-1 Vif.
    Nat Med. 2003 Nov;9(11):1404-7 PMID: 14528300
  25. Cellular inhibitors of long interspersed element 1 and Alu retrotransposition.
    Proc Natl Acad Sci U S A. 2006 Jun 6;103(23):8780-5 PMID: 16728505
  26. Human apolipoprotein B mRNA-editing enzyme-catalytic polypeptide-like 3G (APOBEC3G) is incorporated into HIV-1 virions through interactions with viral and nonviral RNAs.
    J Biol Chem. 2004 Aug 20;279(34):35822-8 PMID: 15210704
  27. Specific expression of activation-induced cytidine deaminase (AID), a novel member of the RNA-editing deaminase family in germinal center B cells.
    J Biol Chem. 1999 Jun 25;274(26):18470-6 PMID: 10373455
  28. An endogenous inhibitor of human immunodeficiency virus in human lymphocytes is overcome by the viral Vif protein.
    J Virol. 1998 Dec;72(12):10251-5 PMID: 9811770
  29. APOBEC3B and APOBEC3F inhibit L1 retrotransposition by a DNA deamination-independent mechanism.
    J Biol Chem. 2006 Jun 23;281(25):16837-16841 PMID: 16648136
  30. A second human antiretroviral factor, APOBEC3F, is suppressed by the HIV-1 and HIV-2 Vif proteins.
    EMBO J. 2004 Jun 16;23(12):2451-8 PMID: 15152192
  31. Inhibition of tRNA₃(Lys)-primed reverse transcription by human APOBEC3G during human immunodeficiency virus type 1 replication.
    J Virol. 2006 Dec;80(23):11710-22 PMID: 16971427
  32. Species-specific restriction of apobec3-mediated hypermutation.
    J Virol. 2008 Feb;82(3):1305-13 PMID: 18032489
  33. Identification of novel argonaute-associated proteins.
    Curr Biol. 2005 Dec 6;15(23):2149-55 PMID: 16289642
  34. The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA.
    Nature. 2003 Jul 3;424(6944):94-8 PMID: 12808465
  35. The DNA deaminase activity of human APOBEC3G is required for Ty1, MusD, and human immunodeficiency virus type 1 restriction.
    J Virol. 2008 Mar;82(6):2652-60 PMID: 18184715
  36. Inhibition of initiation of reverse transcription in HIV-1 by human APOBEC3F.
    Virology. 2007 Aug 15;365(1):92-100 PMID: 17459442
  37. Identification of APOBEC3DE as another antiretroviral factor from the human APOBEC family.
    J Virol. 2006 Nov;80(21):10522-33 PMID: 16920826
  38. Human immunodeficiency virus type 1 Vpr induces the degradation of the UNG and SMUG uracil-DNA glycosylases.
    J Virol. 2005 Sep;79(17):10978-87 PMID: 16103149
  39. Purification and molecular cloning of a novel essential component of the apolipoprotein B mRNA editing enzyme-complex.
    J Biol Chem. 2000 Jun 30;275(26):19848-56 PMID: 10781591
  40. Reversed functional organization of mouse and human APOBEC3 cytidine deaminase domains.
    J Biol Chem. 2006 Dec 1;281(48):36624-31 PMID: 17020885
  41. Comparison of cellular ribonucleoprotein complexes associated with the APOBEC3F and APOBEC3G antiviral proteins.
    J Virol. 2008 Jun;82(11):5636-42 PMID: 18367521
  42. Adaptive evolution and antiviral activity of the conserved mammalian cytidine deaminase APOBEC3H.
    J Virol. 2006 Apr;80(8):3853-62 PMID: 16571802
  43. Enzymatically active APOBEC3G is required for efficient inhibition of human immunodeficiency virus type 1.
    J Virol. 2007 Dec;81(24):13346-53 PMID: 17928335
  44. APOBEC3G hypermutates genomic DNA and inhibits Ty1 retrotransposition in yeast.
    Proc Natl Acad Sci U S A. 2005 Jul 12;102(28):9854-9 PMID: 16000409
  45. Biochemical differentiation of APOBEC3F and APOBEC3G proteins associated with HIV-1 life cycle.
    J Biol Chem. 2007 Jan 19;282(3):1585-94 PMID: 17142455
  46. The retroviral hypermutation specificity of APOBEC3F and APOBEC3G is governed by the C-terminal DNA cytosine deaminase domain.
    J Biol Chem. 2005 Mar 25;280(12):10920-4 PMID: 15647250
  47. APOBEC3F properties and hypermutation preferences indicate activity against HIV-1 in vivo.
    Curr Biol. 2004 Aug 10;14(15):1385-91 PMID: 15296757
  48. The anti-HIV-1 editing enzyme APOBEC3G binds HIV-1 RNA and messenger RNAs that shuttle between polysomes and stress granules.
    J Biol Chem. 2006 Sep 29;281(39):29105-19 PMID: 16887808
  49. Mutational comparison of the single-domained APOBEC3C and double-domained APOBEC3F/G anti-retroviral cytidine deaminases provides insight into their DNA target site specificities.
    Nucleic Acids Res. 2005 Apr 04;33(6):1913-23 PMID: 15809227
  50. Hypermutation of HIV-1 DNA in the absence of the Vif protein.
    Science. 2003 May 16;300(5622):1112 PMID: 12750511
  51. Antiviral protein APOBEC3G localizes to ribonucleoprotein complexes found in P bodies and stress granules.
    J Virol. 2007 Mar;81(5):2165-78 PMID: 17166910
  52. APOBEC3G targets human T-cell leukemia virus type 1.
    Retrovirology. 2005 May 19;2:32 PMID: 15943885
  53. APOBEC3F can inhibit the accumulation of HIV-1 reverse transcription products in the absence of hypermutation. Comparisons with APOBEC3G.
    J Biol Chem. 2007 Jan 26;282(4):2587-95 PMID: 17121840
  54. Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex.
    Science. 2003 Nov 7;302(5647):1056-60 PMID: 14564014
  55. Complementary function of the two catalytic domains of APOBEC3G.
    Virology. 2005 Mar 15;333(2):374-86 PMID: 15721369
  56. APOBEC3A and APOBEC3B are potent inhibitors of LTR-retrotransposon function in human cells.
    Nucleic Acids Res. 2006 Jan 10;34(1):89-95 PMID: 16407327
  57. APOBEC3A is a potent inhibitor of adeno-associated virus and retrotransposons.
    Curr Biol. 2006 Mar 7;16(5):480-5 PMID: 16527742
  58. Antiviral function of APOBEC3G can be dissociated from cytidine deaminase activity.
    Curr Biol. 2005 Jan 26;15(2):166-70 PMID: 15668174
  59. Evidence for a newly discovered cellular anti-HIV-1 phenotype.
    Nat Med. 1998 Dec;4(12):1397-400 PMID: 9846577
  60. Regulation of Apobec3F and human immunodeficiency virus type 1 Vif by Vif-Cul5-ElonB/C E3 ubiquitin ligase.
    J Virol. 2005 Aug;79(15):9579-87 PMID: 16014920
  61. Molecular cloning of apobec-1 complementation factor, a novel RNA-binding protein involved in the editing of apolipoprotein B mRNA.
    Mol Cell Biol. 2000 Mar;20(5):1846-54 PMID: 10669759
  62. The intrinsic antiretroviral factor APOBEC3B contains two enzymatically active cytidine deaminase domains.
    Virology. 2007 Aug 1;364(2):486-93 PMID: 17434555
  63. Virion-associated uracil DNA glycosylase-2 and apurinic/apyrimidinic endonuclease are involved in the degradation of APOBEC3G-edited nascent HIV-1 DNA.
    J Biol Chem. 2007 Apr 20;282(16):11667-75 PMID: 17272283
  64. Cellular APOBEC3G restricts HIV-1 infection in resting CD4+ T cells.
    Nature. 2005 May 5;435(7038):108-14 PMID: 15829920
  65. Human APOBEC3F is another host factor that blocks human immunodeficiency virus type 1 replication.
    J Virol. 2004 Jun;78(11):6073-6 PMID: 15141007
  66. High-molecular-mass APOBEC3G complexes restrict Alu retrotransposition.
    Proc Natl Acad Sci U S A. 2006 Oct 17;103(42):15588-93 PMID: 17030807
  67. HIV-1 Vif protein binds the editing enzyme APOBEC3G and induces its degradation.
    Nat Med. 2003 Nov;9(11):1398-403 PMID: 14528301
  68. Cytidine deaminases APOBEC3G and APOBEC3F interact with human immunodeficiency virus type 1 integrase and inhibit proviral DNA formation.
    J Virol. 2007 Jul;81(13):7238-48 PMID: 17428847
  69. Human retroviral host restriction factors APOBEC3G and APOBEC3F localize to mRNA processing bodies.
    PLoS Pathog. 2006 May;2(5):e41 PMID: 16699599
  70. Production of infectious human immunodeficiency virus type 1 does not require depletion of APOBEC3G from virus-producing cells.
    Retrovirology. 2004 Sep 17;1:27 PMID: 15373943
  71. The interaction of APOBEC3G with human immunodeficiency virus type 1 nucleocapsid inhibits tRNA3Lys annealing to viral RNA.
    J Virol. 2007 Oct;81(20):11322-31 PMID: 17670826
  72. APOBEC3G cytidine deaminase inhibits retrotransposition of endogenous retroviruses.
    Nature. 2005 Jan 27;433(7024):430-3 PMID: 15674295
Article Info
Journal
PLoS pathogens
Abbr.
PLoS Pathog
ISSN
1553-7374
Published
2008-07-04
Epub
2008-00-04
Pages
e1000095
Language
English
Region
United States
NLM ID
101238921
PMCID
PMC2435275
Subset
IM
Grants
NIAID NIH HHS · K02 AI080225 · United States
NIAID NIH HHS · R01 AI063944 · United States
NIAID NIH HHS · R56 AI063944 · United States
NIAID NIH HHS · AI063944 · United States
Databases
GENBANK
BC024268, BC038808
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