Selected Publications

Human APOBEC3 Proteins

  • Byeon I-JL, Byeon C-H, Wu T, Mitra M, Singer D, Levin JG*, Gronenborn AM. Nuclear Magnetic Resonance structure of the APOBEC3B catalytic domain: Structural basis for substrate binding and DNA deaminase activity. Biochemistry 55:2944-2959, 2016. PMID: 27163633       *Co-corresponding Author
  • Mitra M, Singer D, Mano Y, Hritz J, Nam G, Gorelick RJ, Byeon I-JL, Gronenborn AM, Iwatani Y, Levin JG. Sequence and structural determinants of human APOBEC3H deaminase and anti-HIV-1 activities. Retrovirology 12:3, 2015. PMID: 25614027
  • Chaurasiya KR, McCauley MJ, Wang W, Qualley DF, Wu T, Kitamura S, Geertsema H, Chan DSB, Hertz A, Iwatani Y, Levin JG, Musier-Forsyth K, Rouzina I, Williams MC. Oligomerization transforms human APOBEC3G from an efficient enzyme to a slowly dissociating nucleic acid binding protein. Nat. Chem. 6:28-33, 2014. PMID: 24345943 News and Views Commentary. Nat. Chem. 6:13-14, 2014.
  • Mitra M, Hercík K, Byeon I-JL, Ahn J, Hill S, Hinchee-Rodriguez K, Singer D, Byeon C-H, Charlton LM, Nam G, Heidecker G, Gronenborn AM, Levin JG. Structural determinants of human APOBEC3A enzymatic and nucleic acid binding properties. Nucleic Acids Res. 42:1095-1110, 2014. PMID: 24163103
  • Byeon I-JL, Ahn J, Mitra M, Byeon C-H, Hercík K, Hritz J, Charlton LM, Levin JG*, Gronenborn AM. NMR structure of human restriction factor APOBEC3A reveals substrate binding and enzyme specificity. Nat. Commun. 4:1890, 2013. PMID: 23695684      *Co-corresponding Author
  • Iwatani Y, Chan, DSB, Liu L, Yoshii H, Shibata J, Yamamoto N, Levin JG, Gronenborn AM, Sugiura W. HIV-1 Vif-mediated ubiquitination/degradation of APOBEC3G involves four critical lysine residues in its C-terminal domain. Proc. Natl. Acad. Sci. USA 106:19539-19544, 2009. PMID: 19887642
  • Iwatani Y, Chan DSB, Wang F, Maynard-Stewart K, Sugiura W, Gronenborn AM, Rouzina I, Williams MC, Musier-Forsyth K, Levin JG. Deaminase-independent inhibition of HIV-1 reverse transcription by APOBEC3G. Nucleic Acids Res. 35:7096-7108, 2007. PMID: 17942420
  • Iwatani Y, Takeuchi H, Strebel K, Levin, JG. Biochemical activities of highly purified, catalytically active human APOBEC3G: Correlation with antiviral effect. J. Virol. 80:5992-6002, 2006. PMID: 16731938

Nucleic Acid Chaperone Activity of the Nucleocapsid and Gag Precursor Proteins

  • Post K, Olson ED, Naufer MN, Gorelick RJ, Rouzina I, Williams MC, Musier-Forsyth K, Levin JG. Mechanistic differences between HIV-1 and SIV nucleocapsid proteins and cross-species HIV-1 genomic RNA recognition. Retrovirology 13:89, 2016. PMID: 28034301
  • Wu T, Gorelick RJ, Levin JG. Selection of fully processed nucleocapsid protein is required for optimal nucleic acid chaperone activity in reverse transcription. Virus Res. 193:52-64, 2014. PMID: 24954787
  • Hergott CB, Mitra M, Guo J, Wu T, Miller JT, Iwatani Y, Gorelick RJ, Levin JG. Zinc finger function of HIV-1 nucleocapsid protein is required for removal of 5’-terminal genomic RNA fragments: A paradigm for RNA removal reactions in HIV-1 reverse transcription. Virus Res. 171:346-355, 2013. PMID: 23149014
  • Wu T, Datta SAK, Mitra M, Gorelick RJ, Rein A, Levin JG. Fundamental differences between the nucleic acid chaperone activities of HIV-1 nucleocapsid protein and Gag or Gag-derived proteins: Biological implications. Virology 405:556-567, 2010. PMID: 20655566
  • Post  K, Kankia  B, Gopalakrishnan S, Yang V, Cramer E, Saladores P, Gorelick RJ, Guo J, Musier-Forsyth K, Levin JG. Fidelity of plus-strand priming requires the nucleic acid chaperone activity of HIV-1 nucleocapsid protein. Nucleic Acids Res. 37:1755-1766, 2009. PMID: 19158189
  • Wu T, Heilman-Miller SL, Levin JG. Effects of nucleic acid local structure and magnesium ions on minus-strand transfer mediated by the nucleic acid chaperone activity of HIV-1 nucleocapsid protein. Nucleic Acids Res. 35:3974-3987, 2007. PMID: 17553835
  • Heilman-Miller SL, Wu T, Levin JG. Alteration of nucleic acid structure and stability modulates the efficiency of minus-strand transfer mediated by the HIV-1 nucleocapsid protein. J. Biol. Chem. 279:44154-44165, 2004. PMID: 15271979
  • Iwatani Y, Rosen AE, Guo J, Musier-Forsyth, K, Levin JG. Efficient initiation of HIV-1 reverse transcription in vitro: Requirement for RNA sequences downstream of the primer binding site abrogated by nucleocapsid protein-dependent primer-template interactions. J. Biol. Chem. 278:14185-14195, 2003. PMID: 12560327
  • Guo J, Wu T, Kane BF, Johnson DG, Henderson, LE, Gorelick RJ, Levin JG. Subtle alterations of the native zinc finger structures have dramatic effects on the nucleic acid chaperone activity of human immunodeficiency virus type 1 nucleocapsid protein. J. Virol. 76:4370-4378, 2002. PMID: 11932404
  • Guo  J, Wu T, Anderson J, Kane BF, Johnson DJ, Gorelick RJ, Henderson LE, Levin JG. Zinc finger structures in the human immunodeficiency virus type 1 nucleocapsid protein facilitate efficient minus- and plus-strand transfer.  J. Virol. 74:8980-8988, 2000. PMID: 10982342
  • Johnson PE, Turner RB, Wu ZR, Hairston L, Guo J, Levin JG, Summers MF. A mechanism for plus-strand transfer enhancement by the HIV-1 nucleocapsid protein during reverse transcription.  Biochemistry 39:9084-9091, 2000. PMID: 10924101  
  • Wu T, Guo J, Bess J, Henderson LE, Levin JG. Molecular requirements for  human immunodeficiency virus type 1 plus-strand transfer: Analysis in reconstituted and endogenous reverse transcription systems. J. Virol. 73:4794-4805, 1999. PMID: 10233940
  • Guo J, Wu T, Bess J, Henderson LE, Levin JG: Actinomycin D inhibits human immunodeficiency virus type 1 minus-strand transfer in in vitro and endogenous reverse transcriptase assays. J. Virol. 72:6716-6724, 1998. PMID: 9658119
  • Guo J, Henderson LE, Bess J, Kane B, Levin JG. Human immunodeficiency virus type 1 nucleocapsid protein promotes efficient strand transfer and specific viral DNA synthesis by inhibiting TAR-dependent self-priming from minus-strand strong-stop DNA. J. Virol. 71:5178-5188, 1997. PMID: 9188585

Reviews on Nucleic Acid Chaperone Activity

  • Levin JG, Mitra M, Mascarenhas A, Musier-Forsyth K. Role of HIV-1 nucleocapsid protein in HIV-1 reverse transcription. RNA Biol. 7:754-774, 2010. PMID: 21160280
  • Levin JG, Guo J, Rouzina I, Musier-Forsyth K. Nucleic acid chaperone activity of HIV-1 nucleocapsid protein: critical role in reverse transcription and molecular mechanism. Prog. Nucleic Acid Res. Mol. Biol. 80:217-286, 2005. PMID: 16164976
  • Rein A, Henderson L, Levin JG: Nucleic-acid-chaperone activity of retroviral nucleocapsid proteins: Significance for viral replication. Trends Biochem. Sci. 23:297-301, 1998. PMID: 9757830

HIV-1 Virus Assembly

  • Jiyang J, Ablan SD, Derebail S, Hercík K, Soheilian F, Thomas JA, Tang S, Hewlett I, Nagashima K, Gorelick RJ, Freed EO, Levin JG. The interdomain linker region of HIV-1 capsid protein is a critical determinant of proper core assembly and stability. Virology 421:253-265, 2011. PMID: 22036671
  • Tang S, Ablan S, Dueck  M, Ayala-López W, Soto B, Caplan M, Nagashima K, Hewlett IK, Freed EO, Levin JG. A second-site suppressor significantly improves the defective phenotype imposed by mutation of an aromatic residue in the N-terminal domain of the HIV-1 capsid protein. Virology 359:105-115, 2007. PMID: 17055023
  • Tang S, Murakami T, Cheng N, Steven AC, Freed EO, Levin, JG. Human immunodeficiency virus type 1 N-terminal capsid mutants containing cores with abnormally high levels of capsid protein and virtually no reverse transcriptase. J. Virol. 77:12592-12602, 2003. PMID: 14610182
  • Tang S, Murakami T, Agresta BE, Campbell S, Freed EO, Levin JG.  Human immunodeficiency virus type 1 N-terminal capsid mutants that exhibit aberrant core morphology and are blocked in initiation of reverse transcription in infected cells. J. Virol. 75:9357-9366, 2001. PMID: 11533199    

Replication of Murine Leukemia Virus (MLV)

Mechanism of Readthrough Suppression

  • Feng Y-X, Yuan H, Rein A, Levin JG. Bipartite signal for readthrough suppression in murine leukemia virus mRNA:  an eight-nucleotide purine-rich sequence immediately downstream of the gag termination codon followed by an RNA pseudoknot. J. Virol. 66:5127-5132, 1992. PMID: 1629968
  • Feng Y-X, Copeland TD, Oroszlan S, Rein A, Levin JG. Identification of amino acids inserted during suppression of UAA and UGA termination codons at the gag-pol junction of Moloney murine leukemia virus.  Proc. Natl. Acad. Sci. USA 87:8860-8863, 1990. PMID: 2247457
  • Feng Y-X, Levin JG, Hatfield DL, Schaefer TS, Gorelick, RJ, Rein A.  Suppression of UAA and UGA termination codons in mutant murine leukemia viruses.  J. Virol. 63:2870-2873,1989. PMID: 2542597
  • Feng YX, Hatfield DL, Rein A, Levin JG. Translational readthrough of the murine leukemia virus gag gene amber codon does not require virus-induced alteration of tRNA.  J. Virol. 63:2405-2410, 1989. PMID: 2784837
Reviews
  • Levin JG, Hatfield DL, Oroszlan S, Rein, A. Mechanisms of translational suppression used in the biosynthesis of reverse transcriptase. Reverse Transcriptase, eds. AM Skalka and S Goff, p.5-31. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, 1993.
  • Rein A, Levin JG. Readthrough suppression in the mammalian type C retroviruses and what it has taught us. New Biol. 4:283-289, 1992. PMID: 1320396

MLV Assembly

  • Levin JG, Seidman JG. Effect of polymerase mutations on packaging of primer tRNAPro during murine leukemia virus assembly.  J. Virol. 38:403-408, 1981. PMID: 6165833
  • Messer LI, Levin JG, Chattopadhyay SK. Metabolism of viral RNA in murine leukemia virus-infected cells: evidence for differential stability of viral message and virion precursor RNA. J. Virol. 40:683-690, 1981. PMID: 6172599.
  • Levin JG, Seidman JG. Selective packaging of host tRNA's by murine leukemia virus particles does not require genomic RNA.  J. Virol. 29:328-335, 1979. PMID: 219227
  • Levin JG, Rosenak MJ. Synthesis of murine leukemia virus proteins associated with virions assembled in actinomycin D-treated cells:  evidence for persistence of viral messenger RNA.  Proc.  Natl. Acad. Sci., 73:1154-1158, 1976. PMID: 57617
  • Levin JG, Grimley PM, Ramseur JM, Berezesky IK. Deficiency of 60-70S RNA in murine leukemia virus particles assembled in cells treated with actinomycin D.  J. Virol. 14:152-161, 1974. PMID: 4134468  
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