Projects

During the first five years of funding, the PCHPI worked in several areas of HIV-1 biology, primarily related to post-entry events and/or HIV-1 accessory factors and their interactions with host proteins. In years 1-5, research topics included interactions of capsid (CA) within the assembled core and with TRIM5α and Cyclophilin A, of Vpr with the gluccocorticoid receptor and with DCAF1-CRL4 complexes, of Vif with APOBEC proteins, and of Nef with Hck, PACS, or the MHCI intracellular domain. Other projects were focused on discovering new host protein interactors for reverse transcriptase or developing tools to image HIV-1 in real-time, at a molecular level. Collaborative efforts in these areas have been very productive, as demonstrated by the list of publications below.

Several of these projects will continue during years 6-10, including those focused on CA interactions, structure studies of Vpr and Vpx with DCAF1-CRL4, and APOBEC proteins.New projects include studies of Reverse Transcriptase dynamics by solution NMR, structural studies of CPSF6 and TNPO3, and biochemical and proteomic analyses of the HIV-1 Pre-Integration Complex.

Publications

*CryoEM structure refinement by integrating NMR chemical shifts with molecular dynamics simulations. Juan R. Perilla, Gongpu Zhao, Manman Lu, Jiying Ning, Guangjin Hou, In-Ja L Byeon, Angela M. Gronenborn, Tatyana Polenova, and Peijun Zhang. J Phys Chem B. 2017 Feb 22. doi: 10.1021/acs.jpcb.6b13105. [Epub ahead of print]
*Inhibition of HIV-1 maturation via small molecule targeting of the amino-terminal domain in the viral capsid protein. Wang W, Zhou J, Halambage UD, Jurado KA, Jamin AV, Wang Y, Engelman AN, Aiken C. J Virol. 2017 Feb 15. pii: JVI.02155-16. doi: 10.1128/JVI.02155-16. [Epub ahead of print]
*Structural biology of supramolecular assemblies by magic-angle spinning NMR spectroscopy. Quinn CM, Polenova T.Q Rev Biophys. 2017 Jan;50:e1. doi: 10.1017/S0033583516000159.
*A supramolecular assembly mediates lentiviral DNA integration. Ballandras-Colas A, Maskell DP, Serrao E, Locke J, Swuec P, Jónsson SR, Kotecha A, Cook NJ, Pye VE, Taylor IA, Andrésdóttir V, Engelman AN, Costa A, Cherepanov P. Science. 2017 Jan 6;355(6320):93-95. PMC5321526 Free Text
*Toward closing the gap: Quantum mechanical calculations and experimentally measured chemical shifts of a microcrystalline lectin. Fritz M, Quinn CM, Wang M, Hou G, Lu X, Koharudin LM, Polenova T, Gronenborn AM. J Phys Chem B. 2016 Dec 21. doi: 10.1021/acs.jpcb.6b09479. [Epub ahead of print]
*In vitro protease cleavage and computer simulations reveal the HIV-1 capsid maturation pathway. Ning J, Erdemci-Tandogan G, Yufenyuy EL, Wagner J, Himes BA, Zhao G, Aiken C, Zandi R, Zhang P. Nat Commun. 2016 Dec 13;7:13689. doi: 10.1038/ncomms13689. PMC5159922 Free Text
*NMR structure of the HIV-1 reverse transcriptase thumb subdomain. Sharaf NG, Brereton AE, Byeon IL, Andrew Karplus P, Gronenborn AM.J Biomol NMR. 2016 Dec;66(4):273-280. doi: 10.1007/s10858-016-0077-2. Epub 2016 Nov 17. PMC5218889 Free Text
*HIV-1 capsid function is regulated by dynamics: Quantitative atomic-resolution insights by integrating magic-angle-spinning NMR, QM/MM, and MD. Zhang H, Hou G, Lu M, Ahn J, Byeon IL, Langmead CJ, Perilla JR, Hung I, Gor'kov PL, Gan Z, Brey WW, Case DA, Schulten K, Gronenborn AM, Polenova T. J Am Chem Soc. 2016 Oct 5. [Epub ahead of print] NIHMSID:838019
*The DDB1-DCAF1-Vpr-UNG2 crystal structure reveals how HIV-1 Vpr steers human UNG2 toward destruction. Wu Y, Zhou X, Barnes CO, DeLucia M, Cohen AE, Gronenborn AM, Ahn J, Calero G. Nat Struct Mol Biol. 23,  933–940  (2016) doi:10.1038/nsmb.3284 NIHMSID:837369
*SLX4/SLX1 independent downregulation of MUS81/EME1 by HIV-1 Vpr. Zhou X, DeLucia M, Ahn J. (2016) J Biol Chem 291(33):16936-47. PMC5016100 Free Text
*Time-resolved imaging of single HIV-1 uncoating in vitro and in living cells. Francis AC, Marin M, Shi J, Aiken C, Melikyan GB. (2016) PLoS Pathog 12(6):e1005709. PMC4913920 Free Text
*HIV-1 and HIV-2 exhibit divergent interactions with HLTF and UNG2 DNA repair proteins. Hrecka K, Hao C, Shun MC, Kaur S, Swanson SK, Florens L, Washburn MP, Skowronski J. (2016) Proc Natl Acad Sci U S A 113(27):E3921-30. PMC4941427 Free Text
*Establishment and reversal of HIV-1 latency in naïve and central memory CD4+ T cells in vitro. Zerbato JM, Serrao E, Lenzi G, Kim B, Ambrose Z, Watkins SC, Engelman AN, Sluis-Cremer N. (2016) J Virol. 90(18):8059-73. PMC5008097 Free Text
*Conformational plasticity of the NNRTI-binding pocket in HIV-1 reverse transcriptase: A fluorine nuclear magnetic resonance study. Sharaf NG, Ishima R, Gronenborn AM. (2016) Biochemistry. 2016 Jul 19;55(28):3864-73. PMC4955860 Free Text
*Nuclear magnetic resonance structure of the APOBEC3B catalytic domain: Structural basis for substrate binding and DNA deaminase activity. Byeon IL, Byeon CH, Wu T, Mitra M, Singer D, Levin JG, Gronenborn AM. (2016) Biochemistry 55(21):2944-59.  PMC4943463 Free Text
*Transmission electron microscopy for the evaluation and optimization of crystal growth. Stevenson HP, Lin G, Barnes CO, Sutkeviciute I, Krzysiak T, Weiss SC, Reynolds S, Wu Y, Nagarajan V, Makhov AM, Lawrence R, Lamm E, Clark L, Gardella TJ, Hogue BG, Ogata CM, Ahn J, Gronenborn AM, Conway JF, Vilardaga JP, Cohen AE, Calero G. (2016) Acta Crystallogr D Struct Biol. 72(Pt 5):603-15. PMC4854312   Free Text
*Click labeling of unnatural sugars metabolically incorporated into viral envelope glycoproteins enables visualization of single particle fusion. Oum YH, Desai TM, Marin M, Melikyan GB.  (2016) J Virol Methods 233:62-71. PMC5161462 Free Text
*Roles of capsid-interacting host factors in multimodal inhibition of HIV-1 by PF74.  Saito A, Ferhadian D, Sowd GA, Serrao E, Shi J, Halambage UD, Teng S, Soto J, Siddiqui MA, Engelman AN, Aiken C, Yamashita M. (2016) J Virol 90(12):5808-23. PMC4886767 Free Text
*Molecular architecture of the retroviral capsid. Perilla JR, Gronenborn AM. (2016) Trends Biochem Sci 41(5):410-20. PMC4879823 Free Text
*The Cleavage and Polyadenylation Specific Factor 6 (CPSF6) subunit of the capsid-recruited pre-messenger RNA Cleavage Factor I (CFIm) complex mediates HIV-1 integration into genes.  Rasheedi S, Shun MC, Serrao E, Sowd GA, Qian J, Hao C, Dasgupta T, Engelman AN, Skowronski J. (2016) J Biol Chem 291(22):11809-19. PMC4882448 Free Text
*Analysis of the mechanical properties of wild type and hyperstable mutants of the HIV-1 capsid. Ramalho R, Rankovic S, Zhou J, Aiken C, Rousso I. (2016) Retrovirology 13(1):17.  PMC4793510 Free Text
*Cyclophilin A stabilizes the HIV-1 capsid through a novel non-canonical binding site. Liu C, Perilla JR, Ning J, Lu M, Hou G, Ramalho R, Himes BA, Zhao G, Bedwell GJ, Byeon IJ, Ahn J, Gronenborn AM, Prevelige PE, Rousso I, Aiken C, Polenova T, Schulten K, Zhang P. (2016) Nat Commun 7:10714. PMC4785225 Free Text
*Cryo-EM reveals a novel octameric integrase structure for betaretroviral intasome function. Ballandras-Colas A, Brown M, Cook NJ, Dewdney TG, Demeler B, Cherepanov P, Lyumkis D, Engelman AN. Nature 2016; 530:358-61. PMC4908968 Free Text
*Dynamic nuclear polarization enhanced MAS NMR for structural analysis of HIV-1 protein assemblies. Gupta R, Lu M, Hou G, Caporini MA, Rosay M, Maas WE, Struppe JO, Suiter CL, Ahn J, Byeon IL, Franks WT, Orwick-Rydmark M, Bertarello A, Oschkinat H, Lesage A, Pintacuda G, Gronenborn AM, Polenova TE. (2016) J Phys Chem B 120(2):329-39. PMC4890707 Free Text
*Dynamic allostery governs cyclophilin A-HIV capsid interplay. Lu M, Hou G, Zhang H, Suiter CL, Ahn J, Byeon IL, Perilla JR, Langmead CJ, Hung I, Gor'kov PL, Gan Z, Brey W, Aiken C, Zhang P, Schulten K, Gronenborn AM, Polenova T. (2015) Proc Natl Acad Sci U S A. 112(47):14617-22. PMC4664340  Free Text
*Fluorescent protein-tagged Vpr dissociates from HIV-1 core after viral fusion and rapidly enters the cell nucleus. Desai TM, Marin M, Sood C, Shi J, Nawaz F, Aiken C, Melikyan GB. (2015) Retrovirology 12(1):88. PMC4625717 Free Text
*Analysis of local molecular motions of aromatic sidechains in proteins by 2D and 3D fast MAS NMR spectroscopy and quantum mechanical calculations. Paluch P, Pawlak T, Jeziorna A, Trébosc J, Hou G, Vega AJ, Amoureux JP, Dracinsky M, Polenova T, Potrzebowski MJ. (2015) Phys Chem Chem Phys 17(43):28789-801. PMC4890705 Free Text
*RF inhomogeneity and how it controls CPMAS. Gupta R, Hou G, Polenova T, Vega AJ. (2015) Solid State Nuclear Magnetic Resonance. 72:17-26.  PMC4674349. Free Text
*Temporal transcriptional response to latency reversing agents identifies specific factors regulating HIV-1 viral transcriptional switch. Venkatachari NJ, Zerbato JM, Jain S, Mancini AE, Chattopadhyay A, Sluis-Cremer N, Bar-Joseph Z, Ayyavoo V. (2015) Retrovirology  12(1):85. PMC459464 Free Text
*Sensitivity of nonuniform sampling NMR. Palmer MR, Suiter CL, Henry GE, Rovnyak J, Hoch JC, Polenova T, Rovnyak D. (2015) J Physical Chem B 119(22):6502-15. PMC4857715 Free Text
*Combined zero-quantum and spin-diffusion mixing for efficient homonuclear correlation spectroscopy under fast MAS: broadband recoupling and detection of long-range correlations. Lu X, Guo C, Hou G, Polenova T. (2015) J Biomol NMR 61(1):7-20. PMC4485404 Free Text
*Structural integrity of the ribonuclease H domain in HIV-1 reverse transcriptase. Slack RL, Spiriti J, Ahn J, Parniak MA, Zuckerman DM, Ishima R. (2015) Proteins 83(8):1526-38. PMC4509971 Free Text
*Structural basis for retroviral integration into nucleosomes. Maskell DP, Renault L, Serrao E, Lesbats P, Matadeen R, Hare S, Lindemann D, Engelman AN, Costa A, Cherepanov P.  (2015) Nature 523(7560):366-9.  PMC4530500 Free Text
*Structural basis of clade-specific engagement of SAMHD1 restriction factors by lentiviral Vpx virulence factors. Wu Y, Koharudin LM, Mehrens J, DeLucia M, Byeon CH, Byeon IJ, Calero G, Ahn J, Gronenborn AM. (2015) J Biol Chem 290(29):17935-45. PMC4505041 Free Text
*Cyclin A2 - CDK regulates SAMHD1 phosphohydrolase domain. Yan J, Hao C, DeLucia M, Swanson S, Florens L, Washburn MP, Ahn J, Skowronski J. (2015) J Biol Chem 290(21):13279-92.  PMC4505580  Free Text
*MAS NMR of HIV-1 protein assemblies. Suiter CL, Quinn CM, Lu M, Hou G, Zhang H, Polenova T. (2015) J Magn Reson. 253:10-22. PMC4432874 Free Text
*Magic angle spinning NMR of viruses. Quinn CM, Lu M, Suiter CL, Hou G, Zhang H, Polenova T. (2015) Prog Nucl Magn Reson Spectrosc 86-87C: 21-40. PMC4413014 Free Text
*Sequence and structural determinants of human APOBEC3H deaminase and anti-HIV-1 activities. Mitra M, Singer D, Mano Y, Hritz J, Nam G, Gorelick RJ, Byeon IL, Gronenborn AM, Iwatani Y, Levin JG. (2015) Retrovirology 12:3. PMC4323217. Free Text
*Correlative fluorescence and electron microscopy. (2014) Schirra RT Jr, Zhang P. Curr Protoc Cytom 70:12. PMC4211606. Free Text

*Structural insight into HIV-1 restriction by MxB. Fribourgh JL, Nguyen HC, Matreyek KA, Alvarez FJ, Summers BJ, Dewdney TG, Aiken C, Zhang P, Engelman A, Xiong Y. (2014) Cell Host Microbe 16(5):627-38. PMC4252739 Free Text

*Structural basis of allosteric activation of Sterile Alpha Motif and Histidine-Aspartate Domain containing protein 1 (SAMHD1) by nucleoside triphosphates. (2014) Koharudin LM, Wu Y, DeLucia M, Mehrens J, Gronenborn AM, Ahn J. (2014) J Biol Chem 289(47):32617-27. PMC4239615 Free Text

*Accurate measurement of heteronuclear dipolar couplings by phase-alternating R-symmetry (PARS) sequences in magic angle spinning NMR spectroscopy. Hou G, Lu X, Vega AJ, Polenova T. (2014) J Chem Phys 141(10):104202. PMC4162908 Free Text

*Interaction with the SH3-SH2 region of the Src-family kinase Hck structures the HIV-1 Nef dimer for kinase activation and effector recruitment. Alvarado JJ, Tarafdar S, Yeh JI, Smithgall TE. (2014) J Biol Chem 289(41):28539-53. PMC4192505 Free Text

*Solid-state NMR structural and dynamics studies of HIV-1 protein assemblies. Hou G, Han Y, Suiter C, Zhang H, Polenova T, Gan Z, Brey WW, Hung I, Gor’kov P.  (2014) MagLab Reports 21 (1) 41-42. Free Text

*Solid-state NMR structural and dynamics studies of HIV-1 protein assemblies. Hou, G., Han, Y., Suiter, C., Zhang, H., Polenova, T., Gan, Z., Brey, W., Hung, I., Gor’kov, P. (2013) MagLab Reports 20 (2) 50-51.

 *The p66 immature precursor of HIV-1 reverse transcriptase. Sharaf NG, Poliner E, Slack RL, Christen MT, Byeon IJ, Parniak MA, Gronenborn AM, Ishima R. (2014) Proteins 82(10):2343-52. Free Text

*HIV-1 uncoating: connection to nuclear entry and regulation by host proteins. Ambrose Z, Aiken C. (2014) Virology 454-455:371-9. PMC3988234 Free Text

*A probe to monitor performance of ¹⁵N longitudinal relaxation experiments for proteins in solution. Ishima R. (2014) J Biomol NMR 58(2):113-22. PMC3951101 Free Text

*Magic angle spinning NMR studies of protein assemblies: recent advances in methodology and applications. Hou G, Suiter CL, Yan S, Zhang H, Polenova T. (2013) Annual Reports on NMR Spectroscopy, 80, pp. 293-357.

*A magic-angle spinning NMR method for the site-specific measurement of proton chemical-shift anisotropy in biological and organic solids. Hou G, Gupta R, Polenova T, Vega AJ. (2014) Israel Journal of Chemistry 54 (1-2), pp. 171-193. PMC4255364 Free Text

*Sensitivity gains, linearity, and spectral reproducibility in nonuniformly sampled multidimensional MAS NMR spectra of high dynamic range. Suiter CL, Paramasivam S, Hou G, Sun S, Rice D, Hoch JC, Rovnyak D, Polenova T. (2014) J Biomol NMR 59(2):57-73. PMC4142058 Free Text

*Structural basis for nuclear import of splicing factors by human Transportin 3. Maertens GN, Cook NJ, Wang W, Hare S, Gupta SS, Oztop I, Lee K, Pye VE, Cosnefroy O, Snijders AP, Kewalramani VN, Fassati A, Engelman A, Cherepanov P. (2014) Proc Natl Acad Sci USA 111(7):2728-33. PMC3932936 Free text

*In Vivo Functions of CPSF6 for HIV-1 as Revealed by HIV-1 Capsid Evolution in HLA-B27-Positive Subjects. Henning MS, Dubose BN, Burse MJ, Aiken C, Yamashita M. (2014) PLoS Pathogens 10(1):e1003868. PMC3887095 Free text

*Mechanisms of allosteric activation and inhibition of the deoxyribonucleoside triphosphate triphosphohydrolase from Enterococcus faecalis. Vorontsov II, Wu Y, Delucia M, Minasov G, Mehrens J, Shuvalova L, Anderson WF, Ahn J. (2014) J Biol Chem 289(5):2815-24.  PMC3908413 Free Text Cover Image and Paper of the Week

*Binding of HIV-1 Vpr protein to the human homolog of the yeast DNA repair protein RAD23 (hHR23A) requires its xeroderma pigmentosum complementation group C binding (XPCB) domain as well as the ubiquitin-associated 2 (UBA2) domain. Jung J, Byeon IJ, Delucia M, Koharudin LM, Ahn J, Gronenborn AM. (2014) J Biol Chem 289(5):2577-88.  PMC3908392 Free Text

*Magic angle spinning NMR reveals sequence-dependent structural plasticity, dynamics, and the spacer peptide 1 conformation in HIV-1 capsid protein assemblies. Han Y, Hou G, Suiter CL, Ahn J, Byeon IJ, Lipton AS, Burton SD, Hung I, Gor'kov PL, Gan Z, Brey WW, Rice D, Gronenborn AM, Polenova TE. (2013) J Am Chem Soc 135(47):17793-803. PMC3928671 Free Text

*Structural determinants of human APOBEC3A enzymatic and nucleic acid binding properties. Mitra M, Hercík K, Byeon IJ, Ahn J, Hill S, Hinchee-Rodriguez K, Singer D, Byeon CH, Charlton LM, Nam G, Heidecker G, Gronenborn AM, Levin JG. (2013) Nucleic Acids Res 42(2):1095-110. PMC3902935 Free Text

*Viral and cellular requirements for the nuclear entry of retroviral preintegration nucleoprotein complexes. Matreyek KA, Engelman A. (2013) Viruses 5(10):2483-511.  PMC3814599 Free Text

*Mechanism of allosteric activation of SAMHD1 by dGTP. Ji X, Wu Y, Yan J, Mehrens J, Yang H, Delucia M, Hao C, Gronenborn AM, Skowronski J, Ahn J, Xiong Y. (2013) Nat Struct Mol Biol 20(11):1304-9. PMC3833828 Free Text

*Evolutionary toggling of Vpx/Vpr specificity results in divergent recognition of the restriction factor SAMHD1. Fregoso OI, Ahn J, Wang C, Mehrens J, Skowronski J, Emerman M. (2013) PLoS Pathog 9(7):e1003496. PMC3715410 Free Text

*HIV-2 and SIVmac accessory virulence factor Vpx down-regulates SAMHD1 enzyme catalysis prior to proteasome-dependent degradation. DeLucia M, Mehrens J, Wu Y, Ahn J.  (2013) J Biol Chem 288(26):19116-26. PMC3696684 Free Text

*Correlative cryo-electron tomography and optical microscopy of cells.  Zhang P. Curr Opin Struct Biol 23(5):763-70. PMC3812453. Free Text

*Evidence for biphasic uncoating during HIV-1 infection from a novel imaging assay. Xu H, Franks T, Gibson G, Huber K, Rahm N, Strambio De Castillia C, Luban J, Aiken C, Watkins S, Sluis-Cremer N, Ambrose Z. (2013) Retrovirology 10(1):70. PMC3716918 Free Text

*Multitask learning for host-pathogen protein interactions. Kshirsagar M, Carbonell J, Klein-Seetharaman J. Bioinformatics 29(13):i217-i226. PMC3694681. Free Text

*NMR structure of human restriction factor APOBEC3A reveals substrate binding and enzyme specificity. Byeon I-JL, Ahn J, Mitra M, Byeon C-H, Hercík K, Hritz J, Charlton LM, Levin JG, Gronenborn AM. (2013) Nature Commun 4:1890. PMC3674325 Free Text

*Mature HIV-1 capsid structure by cryo-electron microscopy and all-atom molecular dynamics. Zhao G, Perilla JR, Yufenyuy EL, Meng X, Chen B, Ning J, Ahn J, Gronenborn AM, Schulten K, Aiken C, Zhang P. (2013) Nature 497(7451):643-6. PMC3729984 Free Text

*Broadband homonuclear correlation spectroscopy driven by combined R2n(v) sequences under fast magic angle spinning for NMR structural analysis of organic and biological solids. Hou G, Yan S, Trébosc J, Amoureux J-P, Polenova T. (2013) J Magn Reson 232:18-30. PMC3703537 Free Text

*Correlative microscopy for 3D structural analysis of dynamic interactions.  Jun S, Zhao G, Ning J, Gibson GA, Watkins SC, Zhang P (2013) J Vis Exp (76), e50386, doi:10.3791/50386. PMC3728906. Free Text

*Tubular crystals and helical arrays: structural determination of HIV-1 capsid assemblies using Iterative Helical Real-Space Reconstruction. Zhang P, Meng X,and Zhao G. (2013) Methods Mol Biol 955:381-99. Free Text

 *Tetramerization of SAMHD1 is required for biological activity and inhibition of HIV infection. Yan J,  Kaur S,  DeLucia M,  Hao C,  Mehrens J,  Wang C,  Golczak M,  Palczewski K,  Gronenborn AM,  Ahn J, and Skowronski J. (2013) J Biol Chem 288(15):10406-17. PMC3624423 Free Text

 *Probing structure and dynamics of protein assemblies by magic angle spinning NMR spectroscopy. Yan S, Suiter CL, Hou G, Zhang H, Polenova T.  (2013) Acc Chem Res 46(9):2047-58. PMC3748245 Free Text

 *Multidimensional magic angle spinning NMR spectroscopy for site-resolved measurement of proton chemical shift anisotropy in biological solids. Hou G, Paramasivam S, Yan S, Polenova T, Vega AJ. (2013) J Am Chem Soc. 135(4):1358-68. PMC3586542 Free Text

 *The host proteins transportin SR2/TNPO3 and Cyclophilin A exert opposing effects on HIV-1 uncoating. Shah VB, Shi J, Hout DR, Oztop I, Krishnan L, Ahn J, Shotwell MS, Engelman A, Aiken C. (2012) J Virol. 87(1):422-32. PMC3536424 Free Text

 *Structural insight into HIV-1 capsid recognition by rhesus TRIM5α. Yang H, Ji X, Zhao G, Ning J, Zhao Q, Aiken C, Gronenborn AM, Zhang P, Xiong Y. (2012) Proc Natl Acad Sci USA. 109(45):18372-7. PMC3494900 Free Text

 *Recoupling of chemical shift anisotropy by R-symmetry sequences in magic angle spinning NMR spectroscopy. Hou G, Byeon IJ, Ahn J, Gronenborn AM, Polenova T. (2012) J Chem Phys. 137(13):134201. PMC3477183 Free Text

 *Protease cleavage leads to formation of mature trimer interface in HIV-1 capsid. Meng X, Zhao G, Yufenyuy E, Ke D, Ning J, Delucia M, Ahn J, Gronenborn AM, Aiken C, Zhang P. (2012) PLoS Pathog. 2012 Aug;8(8):e1002886. PMC3426514 Free Text

 *Damaged DNA induced UV-damaged DNA-binding protein (UV-DDB) dimerization and its roles in chromatinized DNA repair. Yeh JI, Levine AS, Du S, Chinte U, Ghodke H, Wang H, Shi H, Hsieh CL, Conway JF, Van Houten B, Rapić-Otrin V. Proc Natl Acad Sci U S A. 2012 Oct 9;109(41):E2737-46. PMC3478663 Free Text

*Thinning of large mammalian cells for cryo-TEM characterization by cryo-FIB milling. Strunk KM, Wang K, Ke D, Gray JL, Zhang P. (2012) J Microsc. 247(3): 220. PMC3748363 Free Text

*Enhanced sensitivity by nonuniform sampling enables multidimensional MAS NMR spectroscopy of protein assemblies. Paramasivam S, Suiter CL, Hou G, Sun S, Palmer M, Hoch JC, Rovnyak D, Polenova T. (2012) J Phys Chem B. 116(25): 7416. PMC3386641 Free Text

*3D structure determination of native mammalian cells using cryo-FIB and cryo-electron tomography. Wang K, Strunk K, Zhao G, Gray JL, Zhang P. (2012) J Struct Biol 180(2):318-26. PMC3483467 Free Text

*Second-site suppressors of HIV-1 capsid mutations: restoration of intracellular activities without correction of intrinsic capsid stability defects. Yang R, Shi J, Byeon IL, Ahn J, Sheehan JH, Meiler J, Gronenborn AM, Aiken C. (2012) Retrovirology 9(1): 30.  PMC3351742 Free Text

*Motions on the millisecond timescale and multiple conformations of HIV-1 capsid protein: implications for structural polymorphism of CA assemblies. Byeon IL, Hou G, Han Y, Suiter CL, Ahn J, Jung J, Byeon CH, Gronenborn AM, Polenova TE. (2012) J Am Chem Soc, 134 (14) 6455-6466. PMC3325613 Free Text

*HIV-1 Nef interaction influences the ATP-binding site of the Src-family kinase, Hck. Pene-Dumitrescu T, Shu ST, Wales TE, Alvarado JJ, Shi H, Narute P, Moroco JA, Yeh JI, Engen JR, Smithgall TE. (2012) BMC Chem Biol, 12(1):1. PMC3328272 Free Text

*HIV/SIV accessory virulence factor Vpx loads the host cell restriction factor SAMHD1 onto the E3 ubiquitin ligase complex CRL4DCAF1. Ahn J, Hao C, Yan J, DeLucia M, Mehrens J, Wang C, Gronenborn AM, Skowronski J. (2012) J Biol Chem, 287:12550.  PMC3321004 Free Text

*APOBEC2 is a monomer in solution: implications for APOBEC3G models. Krzysiak TC, Jung J, Thompson J, Baker D, Gronenborn AM. (2012) Biochemistry 51(9) 2008-17. PMC3316327 Free Text

*Human immunodeficiency virus type 1 (HIV-1) capsid mutation N74D alters cyclophilin A dependence and impairs macrophage infection. Ambrose Z, Lee K, Ndjomou J, Xu H, Oztop I, Matous J, Takemura T, Unutmaz D, Engelman A, Hughes SH, Kewalramani VN. (2012) J Virol, 86(8):4708-14. PMC3318671 Free Text

*CryoEM analysis of capsid assembly and structural changes upon interactions with a host restriction factor, TRIM5α. Zhao G and Zhang P. (2014) Methods Mol Biol. 1087:13-28.PMC4506781 Free Text

*Determining confidence of predicted interactions between HIV-1 and human proteins using conformal method. Nouretdinov I, Gammerman A, Qi Y, Klein-Seetharaman J. (2012) Pac Symp Biocomput 2012: 311-22. PMC3249613 Free Text

*Solid-state NMR spectroscopy of protein complexes. Sun S, Han Y, Paramasivam S, Yan S, Siglin AE, Williams JC, Byeon IJ, Ahn J, Gronenborn AM, Polenova T. (2012) Methods Mol Biol 831:303-31. PubMed

*Direct visualization of HIV-1 with correlative live-cell microscopy and cryo-electron tomography. Jun S, Ke D, Debiec K, Zhao G, Meng X, Ambrose Z, Gibson GA, Watkins SC, and Zhang P. (2011) Structure 19 (11): 1573-1581. PMC3217200 Free Text

*Structure of HIV-1 capsid assemblies by cryo-electron microscopy and iterative helical real-space reconstruction. Meng X, Zhao G, and Zhang P. (2011) J Vis Exp (54) PMC3211131 Free Text

*Rhesus TRIM5α disrupts the HIV-1 capsid at the interhexamer interfaces. Zhao G, Ke D, Vu T, Ahn J, Shah VB, Yang R, Aiken C, Charlton LM, Gronenborn AM and Zhang P. (2011) PLoS Path 7(3): e1002009. PMC3063768 Free Text

*Structure, dynamics, and Hck interaction of full-length HIV-1 Nef proteins. Jung J, Byeon IJ, Ahn J, Gronenborn AM. (2011) Proteins 79 (5): 1609-1622. PMC3076547 Free Text

*Structure of the HIV-1 full-length capsid protein in a conformationally trapped unassembled state induced by small-molecule binding. Du S, Betts L, Yang R, Shi H, Concel J, Ahn J, Aiken C, Zhang P, Yeh JI. (2011) J Mol Biol. 406, 371-386. PMC3194004 Free Text

*Spin diffusion driven by R-symmetry sequences: Applications to homonuclear correlation spectroscopy in MAS NMR of biological and organic solids. Hou G, Byeon IL, Ahn J, Concel J, Samoson A, Gronenborn AM, Polenova T. (2011) J Am Chem Soc 133, 3943-53. PMC3148607 Free Text

*The cullin-RING E3 ubiquitin ligase CRL4-DCAF1 complex dimerizes via a short helical region in DCAF1. Ahn J, Novince Z, Concel J, Byeon CH, Makhov AM, Byeon IJ, Zhang P, Gronenborn AM. (2011) Biochemistry. 50, 1359-1367. PMC3072279 Free Text

*1H-13C/1H-15N heteronuclear dipolar recoupling by R-symmetry sequences under fast magic angle spinning for dynamics analysis of biological and organic solids. Hou G, Byeon IL, Ahn J, Gronenborn AM, Polenova T. (2011) J Am Chem Soc 133 (46), 18646-18655. PMC3218250 Free Text

*Virus interactions with human signal transduction pathways. Zhao Z, Xia J, Tastan O, Singh I, Kshirsagar M, Carbonell J, Klein-Seetharaman J. (2011) Int J Comput Biol Drug Des 4 (1): 83-105. PMC3407688 Free Text

*Crystal structure of the Src-family kinase Hck SH3-SH2-linker regulatory region supports an SH3-dominant activation mechanism. Alvarado JJ, Betts L, Moroco JA, Smithgall TE, and Yeh JI. (2010) J Biol Chem 285, 35455-35461. PMC2975169 Free Text

*Determination of relative tensor orientations by γ-encoded chemical shift anisotropy/heteronuclear dipolar coupling 3D NMR spectroscopy in biological solids. Hou G, Paramasivam S, Byeon IL, Gronenborn AM, Polenova T. (2010) Phys Chem Chem Phys 12, 14873-14883. PMC3160241 Free Text

*HIV-1 Vpr loads uracil DNA glycosylase-2 onto DCAF1, a substrate recognition subunit of a cullin 4A-ring E3 ubiquitin ligase for proteasome-dependent degradation. Ahn J, Vu T, Novince Z, Guerrero-Santoro J, Rapic-Otrin V, Gronenborn AM. (2010) J Biol Chem. 285, 37333-37341. PMC2988339 Free Text

*Small molecule inhibition of HIV-1-induced MHC-I downregulation identifies a temporally regulated switch in Nef action. Dikeakos JD, Atkins KM, Thomas L, Emert-Sedlak L, Byeon, IL, Jung J, Ahn J, Wortmann WD, Kukull B, Saito M, Koizumi H, Williamson DM, Hiyoshi M, Barklis E, Takiguchi M, Suzu S, Gronenborn AM, Smithgall TE and Thomas G. (2010) Mol Biol Cell, 21, 3279-92. PMC2947465 Free Text

*The RNA binding protein HuR does not interact directly with HIV-1 reverse transcriptase and does not affect reverse transcription in vitro. Ahn J, Byeon IJ, Dharmasena S, Huber K, Concel J, Gronenborn AM, Sluis-Cremer N. (2010) Retrovirology 7:40. PMC2873509  Free Text

*Solid-State NMR studies of HIV-1 capsid protein assemblies. Han Y, Ahn J, Concel J, Byeon IL, Gronenborn AM, Yang J, Polenova T. (2010) J Am Chem Soc, 132,1976-1987. PMC2829833 Free Text

*1H, 15N and 13C assignments of the dimeric C-terminal domain of HIV-1 capsid protein. Jung J, Byeon IJ, Ahn J, Concel J, Gronenborn AM. (2010) Biomol NMR Assign 4:21-23. PMC3448961 Free Text

*Human immunodeficiency virus type 1 Vpr: oligomerization is an essential feature for its incorporation into virus particles. Venkatachari, N.J., Walker, L.A., Tastan, O., Le, T., Dempsey, T.M., Li, Y., Yanamala, N., Srinivasan, A., Klein-Seetharaman, J., Montelaro, R.C., and Ayyavoo, V. (2010) Virol J 7, 119. PMC2894018 Free Text

*Semi-supervised multi-task learning for predicting interactions between HIV-1 and human proteins. Qi Y, Tastan O, Carbonell JG, Klein-Seetharaman J, Weston J (2010) Bioinformatics 26 (18): i645-i652. PMC2935441 Free Text

*Structural convergence between Cryo-EM and NMR reveals intersubunit interactions critical for HIV-1 capsid function. Byeon IJ, Meng X, Jung J, Zhao G, Yang R, Ahn J, Shi J, Concel J, Aiken C, Zhang P, Gronenborn AM. (2009) Cell 139:780-790. PMC2782912  Free Text Also see commentary in Viruses.

*HIV-1 Vif-mediated ubiquitination/degradation of APOBEC3G involves four critical lysine residues in its C-terminal domain. Iwatani Y, Chan DS, Liu L, Yoshii H, Shibata J, Yamamoto N, Levin JG, Gronenborn AM, Sugiura W. (2009) Proc Natl Acad Sci USA 106:19539-19544. PMC2772817 Free Text

*Determination of multicomponent protein structures in solution using global orientation and shape restraints. Wang J, Zuo X, Yu P, Byeon IJ, Jung J, Wang X, Dyba M, Seifert S, Schwieters CD, Qin J, Gronenborn AM, Wang YX. (2009) J Am Chem Soc 131:10507-10515. PMC2873192 Free Text

*Prediction of interactions between HIV-1 and human proteins by information integration. Tastan O, Qi Y, Carbonell JG, Klein-Seetharaman J. (2009) Pac Symp Biocomput 2009:516-27. PMC3263379 Free Text

*Alternative paths in HIV-1 targeted human signal transduction pathways. Balakrishnan S, Tastan O, Carbonell J, Klein-Seetharaman J. (2009) BMC Genomics 10 Suppl 3:S30. PMC2788384 Free Text

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