Cited by 54HIV Research and TreatmentAdvanced Proteomics Techniques and ApplicationsHIV/AIDS drug development and treatment

Elucidating the in vivo interactome of HIV-1 RNA by hybridization capture and mass spectrometry

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Knoener, Rachel A., Becker, Jordan T., Scalf, Mark, Sherer, Nathan M., Smith, Lloyd M.·2017·Scientific Reports

Abstract

HIV-1 replication requires myriad interactions between cellular proteins and the viral unspliced RNA. These interactions are important in archetypal RNA processes such as transcription and translation as well as for more specialized functions including alternative splicing and packaging of unspliced genomic RNA into virions. We present here a hybridization capture strategy for purification of unspliced full-length HIV RNA-protein complexes preserved in vivo by formaldehyde crosslinking, and coupled with mass spectrometry to identify HIV RNA-protein interactors in HIV-1 infected cells. One hundred eighty-nine proteins were identified to interact with unspliced HIV RNA including Rev and Gag/Gag-Pol, 24 host proteins previously shown to bind segments of HIV RNA, and over 90 proteins previously shown to impact HIV replication. Further analysis using siRNA knockdown techniques against several of these proteins revealed significant changes to HIV expression. These results demonstrate the utility of the approach for the discovery of host proteins involved in HIV replication. Additionally, because this strategy only requires availability of 30 nucleotides of the HIV-RNA for hybridization with a capture oligonucleotide, it is readily applicable to any HIV system of interest regardless of cell type, HIV-1 virus strain, or experimental perturbation.

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  • Cellular factors interacting with HIV-1 proteins and RNAs have been identified using proteomic approaches.

    “In recent years, cellular factors interacting with HIV-1 proteins and RNAs have been identified using proteomic approaches (122-124).”
  • LeuRS is among the factors identified interacting with unspliced full-length HIV-1 RNA.

    “Interestingly, LeuRS is among the factors identified, and future studies are required to understand the significance of this finding (124).”

    From Role of host tRNAs and aminoacyl-tRNA synthetases in retroviral replication (2019) · cites this paper as [124]

    The Results and Discussion section ('HyPR-MS identifies proteins involved in cytoplasmic RNA processes'; page unavailable) reports identifying tRNA ligases among proteins associated with unspliced HIV RNA, but does not name LeuRS. Searches for LeuRS, LARS, and leucyl-tRNA synthetase found no passage identifying that specific factor. (LLM, conf=0.74)

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  1. [1]Purcell DFJ Martin MA Alternative splicing of human immunodeficiency virus type 1 mRNA modulates viral protein expression, replication, and infectivity Journal of virology 1993 67 6365 6378 8411338 PMC238071
  2. [2]Ocwieja KE Dynamic regulation of HIV-1 mRNA populations analyzed by single-molecule enrichment and long-read sequencing Nucleic Acids Research 2012 40 10345 10355 10.1093/nar/gks753 22923523 PMC3488221 · DOI
  3. [3]Kuzembayeva M Dilley K Sardo L Hu WS Life of psi: how full-length HIV-1 RNAs become packaged genomes in the viral particles Virology 2014 454 362 370 10.1016/j.virol.2014.01.019 24530126 PMC6258065 · DOI
  4. [4]Karn, J. & Stoltzfus, C. M. Transcriptional and posttranscriptional regulation of HIV-1 gene expression. Cold Spring Harbor Perspectives in Medicine2, 10.1101/Cshperspect.A006916 (2012). PMC3281586 22355797 · DOI · Paper page
  5. [5]LeBlanc J Weil J Beemon K Posttranscriptional regulation of retroviral gene expression: primary RNA transcripts play three roles as pre-mRNA, mRNA, and genomic RNA Wiley Interdisciplinary Reviews-Rna 2013 4 567 580 10.1002/wrna.1179 23754689 PMC3810403 · DOI
  6. [6]Felber BK Hadzopoulou-Cladaras M Cladaras C Copeland T Pavlakis GN Rev protein of human immunodeficiency virus type 1 affects the stability and transport of the viral mRNA Proc Natl Acad Sci USA 1989 86 1495 1499 10.1073/pnas.86.5.1495 2784208 PMC286723 · DOI
  7. [8]Kula, A. et al. Characterization of the HIV-1 RNA associated proteome identifies Matrin 3 as a nuclear cofactor of Rev function. Retrovirology8, 10.1186/1742-4690-8-60 (2011). PMC3160904 21771346 · DOI
  8. [9]Ajamian L Unexpected roles for UPF1 in HIV-1 RNA metabolism and translation Rna-a Publication of the Rna Society 2008 14 914 927 10.1261/rna.829208 PMC2327365 18369187 · DOI
  9. [10]Edgcomb SP DDX1 is an RNA-dependent ATPase involved in HIV-1 Rev function and virus replication Journal of Molecular Biology 2012 415 61 74 10.1016/j.jmb.2011.10.032 22051512 PMC3249508 · DOI
  10. [11]Huang F RNA helicase MOV10 functions as a co-factor of HIV-1 Rev to facilitate Rev/RRE-dependent nuclear export of viral mRNAs Virology 2015 486 15 26 10.1016/j.virol.2015.08.026 26379090 · DOI
  11. [12]Lai, M. C. et al. Human DDX3 interacts with the HIV-1 Tat protein to facilitate viral mRNA translation. Plos One8, 10.1371/journal.pone.0068665 (2013). PMC3698215 23840900 · DOI
  12. [13]Soto-Rifo R Rubilar PS Ohlmann T The DEAD-box helicase DDX3 substitutes for the cap-binding protein eIF4E to promote compartmentalized translation initiation of the HIV-1 genomic RNA Nucleic Acids Research 2013 41 6286 6299 10.1093/nar/gkt306 23630313 PMC3695493 · DOI
  13. [14]Abrahamyan LG Novel Staufen1 ribonucleoproteins prevent formation of stress granules but favour encapsidation of HIV-1 genomic RNA Journal of Cell Science 2010 123 369 383 10.1242/jcs.055897 20053637 · DOI
  14. [16]Zhou HL Genome-scale RNAi screen for host factors required for HIV replication Cell Host & Microbe 2008 4 495 504 10.1016/j.chom.2008.10.004 18976975 · DOI
  15. [17]Yeung ML Houzet L Yedavalli VSRK Jeang KT A genome-wide short hairpin RNA screening of Jurkat T-cells for human proteins contributing to productive HIV-1 replication Journal of Biological Chemistry 2009 284 19463 19473 10.1074/jbc.M109.010033 19460752 PMC2740572 · DOI
  16. [18]Konig R Global analysis of host-pathogen interactions that regulate early-stage HIV-1 replication Cell 2008 135 49 60 10.1016/j.cell.2008.07.032 18854154 PMC2628946 · DOI · Paper page
  17. [20]Bushman, F. D. et al. Host cell factors in HIV replication: meta-analysis of genome-wide studies. Plos Pathogens5, 10.1371/journal.ppat.1000437 (2009). PMC2682202 19478882 · DOI
  18. [21]Engeland CE Proteome analysis of the HIV-1 Gag interactome Virology 2014 460 194 206 10.1016/j.virol.2014.04.038 25010285 · DOI · Paper page
  19. [23]Marchand V Identification of protein partners of the human immunodeficiency virus 1 tat/rev exon 3 leads to the discovery of a new HIV-1 splicing regulator, protein hnRNP K RNA Biol 2011 8 325 342 10.4161/rna.8.2.13984 21368586 · DOI
  20. [24]Dejardin J Kingston RE Purification of proteins associated with specific genomic loci Cell 2009 136 175 186 10.1016/j.cell.2008.11.045 19135898 PMC3395431 · DOI
  21. [25]Kennedy-Darling J Discovery of chromatin-associated proteins via sequence-specific capture and mass spectrometric protein identification in Saccharomyces cerevisiae Journal of Proteome Research 2014 13 3810 3825 10.1021/pr5004938 24999558 PMC4123949 · DOI
  22. [26]Guillen-Ahlers H HyCCAPP as a tool to characterize promoter DNA-protein interactions in Saccharomyces cerevisiae Genomics 2016 107 267 273 10.1016/j.ygeno.2016.05.002 27184763 PMC5017017 · DOI
  23. [27]Chu C Systematic discovery of Xist RNA binding proteins Cell 2015 161 404 416 10.1016/j.cell.2015.03.025 25843628 PMC4425988 · DOI
  24. [28]McHugh, C. A. et al. The Xist lncRNA interacts directly with SHARP to silence transcription through HDAC3. Nature521, 232−+, 10.1038/nature14443 (2015). PMC4516396 25915022 · DOI
  25. [29]West JA The long noncoding RNAs NEAT1 and MALAT1 bind active chromatin sites Molecular Cell 2014 55 791 802 10.1016/j.molcel.2014.07.012 25155612 PMC4428586 · DOI
  26. [30]Dalgleish AG The CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus Nature 1984 312 763 767 10.1038/312763a0 6096719 · DOI
  27. [31]Page KA Landau NR Littman DR Construction and use of a human immunodeficiency virus vector for analysis of virus infectivity Journal of virology 1990 64 5270 5276 2214018 PMC248565
  28. [32]Moller K Rinke J Ross A Buddle G Brimacombe R The use of formaldehyde in RNA-protein cross-linking studies with ribosomal subunits from Escherichia coli Eur J Biochem 1977 76 175 187 10.1111/j.1432-1033.1977.tb11583.x 407080 · DOI
  29. [33]Solomon MJ Varshavsky A Formaldehyde-mediated DNA-protein crosslinking: a probe for in vivo chromatin structures Proc Natl Acad Sci USA 1985 82 6470 6474 10.1073/pnas.82.19.6470 2995966 PMC390738 · DOI
  30. [34]Kennedy-Darling J Holden MT Shortreed MR Smith LM Multiplexed programmable release of captured DNA Chembiochem 2014 15 2353 2356 10.1002/cbic.201402343 25157426 PMC4218743 · DOI
  31. [35]Barber RD Harmer DW Coleman RA Clark BJ GAPDH as a housekeeping gene: analysis of GAPDH mRNA expression in a panel of 72 human tissues Physiological Genomics 2005 21 389 395 10.1152/physiolgenomics.00025.2005 15769908 · DOI
  32. [36]Cox J Mann M MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification Nat Biotechnol 2008 26 1367 1372 10.1038/nbt.1511 19029910 · DOI · Paper page
  33. [37]Cox J Andromeda: a peptide search engine integrated into the MaxQuant environment J Proteome Res 2011 10 1794 1805 10.1021/pr101065j 21254760 · DOI
  34. [38]Cox J Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ Mol Cell Proteomics 2014 13 2513 2526 10.1074/mcp.M113.031591 24942700 PMC4159666 · DOI · Paper page
  35. [39]Tyanova S The Perseus computational platform for comprehensive analysis of (prote)omics data Nature methods 2016 13 731 740 10.1038/nmeth.3901 27348712 · DOI
  36. [40]Mu X Li W Wang X Gao G YB-1 stabilizes HIV-1 genomic RNA and enhances viral production Protein Cell 2013 4 591 597 10.1007/s13238-013-3011-3 23589019 PMC4875536 · DOI
  37. [41]Mu X HIV-1 exploits the host factor RuvB-like 2 to balance viral protein expression Cell Host Microbe 2015 18 233 242 10.1016/j.chom.2015.06.018 26211835 · DOI
  38. [42]Woolaway K Asai K Emili A Cochrane A hnRNP E1 and E2 have distinct roles in modulating HIV-1 gene expression Retrovirology 2007 4 28 10.1186/1742-4690-4-28 17451601 PMC1863430 · DOI
  39. [43]Dingwall C HIV-1 tat protein stimulates transcription by binding to a U-rich bulge in the stem of the TAR RNA structure EMBO J 1990 9 4145 4153 2249668 PMC552188
  40. [44]Heaphy S HIV-1 regulator of virion expression (Rev) protein binds to an RNA stem-loop structure located within the Rev response element region Cell 1990 60 685 693 10.1016/0092-8674(90)90671-Z 1689218 · DOI
  41. [45]Khorchid A Halwani R Wainberg MA Kleiman L Role of RNA in facilitating Gag/Gag-Pol interaction Journal of virology 2002 76 4131 4137 10.1128/JVI.76.8.4131-4137.2002 11907255 PMC136082 · DOI
  42. [47]Abbondanzieri EA Dynamic binding orientations direct activity of HIV reverse transcriptase Nature 2008 453 184 U182 10.1038/nature06941 18464735 PMC2655135 · DOI
  43. [48]Klein KC HIV Gag-leucine zipper chimeras form ABCE1-containing intermediates and RNase-resistant immature capsids similar to those formed by wild-type HIV-1 Gag Journal of virology 2011 85 7419 7435 10.1128/JVI.00288-11 21543480 PMC3126549 · DOI
  44. [49]Fu W Human immunodeficiency virus type 1, human protein interaction database at NCBI Nucleic Acids Research 2009 37 D417 D422 10.1093/nar/gkn708 18927109 PMC2686594 · DOI
  45. [51]Bateman A UniProt: a hub for protein information Nucleic Acids Research 2015 43 D204 D212 10.1093/nar/gku989 25348405 PMC4384041 · DOI · Paper page
  46. [52]Mi H PANTHER version 11: expanded annotation data from Gene Ontology and Reactome pathways, and data analysis tool enhancements Nucleic Acids Res 2017 45 D183 D189 10.1093/nar/gkw1138 27899595 PMC5210595 · DOI
  47. [53]Cullen BR HIV-1 auxiliary proteins: making connections in a dying cell Cell 1998 93 685 692 10.1016/S0092-8674(00)81431-2 9630214 · DOI
  48. [54]Naji, S. et al. Host cell interactome of HIV-1 Rev includes RNA helicases involved in multiple facets of virus production. Molecular & Cellular Proteomics11, 10.1074/Mcp.M111.015313 (2012). PMC3322577 22174317 · DOI
  49. [55]Yasuda-Inoue M Kuroki M Ariumi Y Distinct DDX DEAD-box RNA helicases cooperate to modulate the HIV-1 Rev function Biochemical and Biophysical Research Communications 2013 434 803 808 10.1016/j.bbrc.2013.04.016 23608157 PMC7092829 · DOI
  50. [56]Fang JH A DEAD box protein facilitates HIV-1 replication as a cellular co-factor of Rev Virology 2004 330 471 480 10.1016/j.virol.2004.09.039 15567440 · DOI
  51. [57]Huelga SC Integrative genome-wide analysis reveals cooperative regulation of alternative splicing by hnRNP proteins Cell Rep 2012 1 167 178 10.1016/j.celrep.2012.02.001 22574288 PMC3345519 · DOI · Paper page
  52. [58]Shetty S Regulation of urokinase receptor mRNA stability by hnRNP C in lung epithelial cells Mol Cell Biochem 2005 272 107 118 10.1007/s11010-005-7644-2 16010978 · DOI
  53. [59]Woo KC Circadian amplitude of cryptochrome 1 is modulated by mRNA stability regulation via cytoplasmic hnRNP D oscillation Mol Cell Biol 2010 30 197 205 10.1128/MCB.01154-09 19858287 PMC2798294 · DOI
  54. [60]Mili S Shu HJ Zhao Y Pinol-Roma S Distinct RNP complexes of shuttling hnRNP proteins with pre-mRNA and mRNA: candidate intermediates in formation and export of mRNA Mol Cell Biol 2001 21 7307 7319 10.1128/MCB.21.21.7307-7319.2001 11585913 PMC99905 · DOI
  55. [61]Damgaard CK Tange TO Kjems J hnRNP A1 controls HIV-1 mRNA splicing through cooperative binding to intron and exon splicing silencers in the context of a conserved secondary structure Rna-a Publication of the Rna Society 2002 8 1401 1415 10.1017/S1355838202023075 PMC1370347 12458794 · DOI
  56. [62]Najera I Krieg M Karn J Synergistic stimulation of HIV-1 Rev-dependent export of unspliced mRNA to the cytoplasm by hnRNP A1 Journal of Molecular Biology 1999 285 1951 1964 10.1006/jmbi.1998.2473 9925777 · DOI
  57. [63]Lund N Differential effects of hnRNP D/AUF1 isoforms on HIV-1 gene expression Nucleic Acids Research 2012 40 3663 3675 10.1093/nar/gkr1238 22187150 PMC3333888 · DOI
  58. [64]Vincendeau, M., Nagel, D., Brenke, J. K., Brack-Werner, R. & Hadian, K. Heterogenous nuclear ribonucleoprotein Q increases protein expression from HIV-1 Rev-dependent transcripts. Virology Journal10, 10.1186/1743-422x-10-151 (2013). PMC3673855 23679954 · DOI
  59. [65]Hadian K Identification of a heterogeneous nuclear ribonucleoprotein-recognition region in the HIV Rev protein Journal of Biological Chemistry 2009 284 33384 33391 10.1074/jbc.M109.021659 19808671 PMC2785182 · DOI
  60. [66]Liu N N(6)-methyladenosine-dependent RNA structural switches regulate RNA-protein interactions Nature 2015 518 560 564 10.1038/nature14234 25719671 PMC4355918 · DOI · Paper page
  61. [67]Kennedy EM Posttranscriptional m(6)A editing of HIV-1 mRNAs enhances viral gene expression Cell Host Microbe 2016 19 675 685 10.1016/j.chom.2016.04.002 27117054 PMC4867121 · DOI
  62. [68]Beckham CJ Parker R P bodies, stress granules, and viral life cycles Cell Host & Microbe 2008 3 206 212 10.1016/j.chom.2008.03.004 18407064 PMC2396818 · DOI
  63. [69]Hinman MN Lou H Diverse molecular functions of Hu proteins Cellular and Molecular Life Sciences 2008 65 3168 3181 10.1007/s00018-008-8252-6 18581050 PMC2580827 · DOI · Paper page
  64. [70]Rivas-Aravena A The Elav-like protein HuR exerts translational control of viral internal ribosome entry sites Virology 2009 392 178 185 10.1016/j.virol.2009.06.050 19647848 · DOI
  65. [71]Lemay, J. et al. HuR interacts with human immunodeficiency virus type 1 reverse transcriptase, and modulates reverse transcription in infected cells. Retrovirology5, 10.1186/1742-4690-5-47 (2008). PMC2441633 18544151 · DOI
  66. [72]Ahn, J. et al. The RNA binding protein HuR does not interact directly with HIV-1 reverse transcriptase and does not affect reverse transcription in vitro. Retrovirology7, 10.1186/1742-4690-7-40 (2010). PMC2873509 20459669 · DOI
  67. [73]Milev, M. P., Ravichandran, M., Khan, M. F., Schriemer, D. C. & Mouland, A. J. Characterization of Staufenl ribonucleoproteins by mass spectrometry and biochemical analyses reveal the presence of diverse host proteins associated with human immunodeficiency virus type 1. Frontiers in Microbiology3, 10.3389/Fmicb.2012.00367 (2012). PMC3486646 23125841 · DOI
  68. [74]Burdick R P body-associated protein Mov10 inhibits HIV-1 replication at multiple stages Journal of virology 2010 84 10241 10253 10.1128/JVI.00585-10 20668078 PMC2937795 · DOI
  69. [75]Furtak, V. et al. Perturbation of the P-body component Mov10 inhibits HIV-1infectivity. Plos One5, 10.1371/journal.pone.0009081 (2010). PMC2816699 20140200 · DOI
  70. [76]Abudu A Identification of molecular determinants from Moloney Leukemia Virus 10 homolog (MOV10) protein for virion packaging and anti-HIV-1 activity Journal of Biological Chemistry 2012 287 1220 1228 10.1074/jbc.M111.309831 22105071 PMC3256871 · DOI
  71. [77]Zimmerman C Identification of a host protein essential for assembly of immature HIV-1 capsids Nature 2002 415 88 92 10.1038/415088a 11780123 · DOI
  72. [78]Dooher JE Schneider BL Reed JC Lingappa JR Host ABCE1 is at plasma membrane HIV assembly sites and its dissociation from gag is linked to subsequent events of virus production Traffic 2007 8 195 211 10.1111/j.1600-0854.2006.00524.x 17233757 PMC1865004 · DOI
  73. [79]Ueno T Nucleolin and the packaging signal, psi, promote the budding of human immunodeficiency virus type 1 (HIV-1) Microbiology and Immunology 2004 48 111 118 10.1111/j.1348-0421.2004.tb03496.x 14978336 · DOI
  74. [80]Zhou YD Rong LW Lu JH Pan O Liang C Insulin-like growth factor II mRNA binding protein 1 associates with gag protein of human immunodeficiency virus type 1, and its overexpression affects virus assembly Journal of virology 2008 82 5683 5692 10.1128/JVI.00189-08 18385235 PMC2395162 · DOI
  75. [81]Engeland CE The cellular protein Lyric interacts with HIV-1 Gag Journal of virology 2011 85 13322 13332 10.1128/JVI.00174-11 21957284 PMC3233182 · DOI
  76. [82]Verreault A Kaufman PD Kobayashi R Stillman B Nucleosome assembly by a complex of CAF-1 and acetylated histones H3/H4 Cell 1996 87 95 104 10.1016/S0092-8674(00)81326-4 8858152 · DOI
  77. [83]Skowyra D Differential association of products of alternative transcripts of the candidate tumor suppressor ING1 with the mSin3/HDAC1 transcriptional corepressor complex The Journal of biological chemistry 2001 276 8734 8739 10.1074/jbc.M007664200 11118440 · DOI
  78. [84]Raghavendra, N. K. et al. Identification of host proteins associated with HIV-1 preintegration complexes isolated from infected CD4(+) cells. Retrovirology7, 10.1186/1742-4690-7-66 (2010). PMC2924840 20698996 · DOI · Paper page
  79. [85]Adachi A Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone Journal of virology 1986 59 284 291 3016298 PMC253077
  80. [86]Connor RI Chen BK Choe S Landau NR Vpr is required for efficient replication of human immunodeficiency virus type 1 in mononuclear phagocytes Virology 1995 206 935 944 10.1006/viro.1995.1016 7531918 · DOI · Paper page
  81. [87]Becker JT Sherer NM Subcellular localization of HIV-1 gag-pol mRNAs regulates sites of virion assembly Journal of virology 2017 PMC5331792 28053097
  82. [88]Erde J Loo RRO Loo JA Enhanced FASP (eFASP) to increase proteome coverage and sample recovery for quantitative proteomic experiments Journal of Proteome Research 2014 13 1885 1895 10.1021/pr4010019 24552128 PMC3993969 · DOI
  83. [89]Schindelin J Fiji: an open-source platform for biological-image analysis Nature methods 2012 9 676 682 10.1038/nmeth.2019 22743772 PMC3855844 · DOI · Paper page
  84. [91]Anderson I Heat shock protein 90 controls HIV-1 reactivation from latency Proceedings of the National Academy of Sciences of the United States of America 2014 111 E1528 E1537 10.1073/pnas.1320178111 24706778 PMC3992654 · DOI
  85. [92]Ansari SA Interaction of YB-1 with human immunodeficiency virus type 1 Tat and TAR RNA modulates viral promoter activity Journal of General Virology 1999 80 2629 2638 10.1099/0022-1317-80-10-2629 10573156 · DOI
  86. [93]Braaten D Luban J Cyclophilin A regulates HIV-1 infectivity, as demonstrated by gene targeting in human T cells Embo Journal 2001 20 1300 1309 10.1093/emboj/20.6.1300 11250896 PMC145517 · DOI
  87. [94]Caillet, M. et al. Rab7A is required for efficient production of infectious HIV-1. Plos Pathogens7, 10.1371/journal.ppat.1002347 (2011). PMC3207927 22072966 · DOI
  88. [95]Callahan MA Functional interaction of human immunodeficiency virus type 1 Vpu and Gag with a novel member of the tetratricopeptide repeat protein family Journal of virology 1998 72 5189 5197 9573291 PMC110095
  89. [96]De Iaco, A. & Luban, J. Cyclophilin A promotes HIV-1 reverse transcription but its effect on transduction correlates best with its effect on nuclear entry of viral cDNA. Retrovirology11, 10.1186/1742-4690-11-11 (2014). PMC3916700 24479545 · DOI
  90. [97]DeBoer J Alterations in the nuclear proteome of HIV-1 infected T-cells Virology 2014 468 409 420 10.1016/j.virol.2014.08.029 25240327 PMC4253593 · DOI
  91. [98]DeBoer J Madson CJ Belshan M Cyclophilin B enhances HIV-1 infection Virology 2016 489 282 291 10.1016/j.virol.2015.12.015 26774171 PMC4761315 · DOI
  92. [99]Dharan, A. et al. KIF5B and Nup358 cooperatively mediate the nuclear import of HIV-1 during infection. Plos Pathogens12, 10.1371/journal.ppat.1005700 (2016). PMC4915687 27327622 · DOI
  93. [100]du Chene I Suv39H1 and HP1 gamma are responsible for chromatin-mediated HIV-1 transcriptional silencing and post-integration latency Embo Journal 2007 26 424 435 10.1038/sj.emboj.7601517 17245432 PMC1783455 · DOI
  94. [101]Dunn SJ Identification of cell surface targets for HIV-1 therapeutics using genetic screens Virology 2004 321 260 273 10.1016/j.virol.2004.01.010 15051386 · DOI
  95. [102]Faure J ARF1 regulates Nef-induced CD4 degradation Curr Biol 2004 14 1056 1064 10.1016/j.cub.2004.06.021 15202998 · DOI
  96. [103]Gadad SS HIV-1 infection induces acetylation of NPM1 that facilitates Tat localization and enhances viral transactivation Journal of Molecular Biology 2011 410 997 1007 10.1016/j.jmb.2011.04.009 21763502 · DOI
  97. [104]Gallo DE Hope TJ Knockdown of MAP4 and DNAL1 produces a post-fusion and pre-nuclear translocation impairment in HIV-1 replication Virology 2012 422 13 21 10.1016/j.virol.2011.09.015 22018492 PMC3732191 · DOI
  98. [105]Gaudin R de Alencar BC Arhel N Benaroch P HIV trafficking in host cells: motors wanted! Trends in Cell Biology 2013 23 652 662 10.1016/j.tcb.2013.09.004 24119663 · DOI
  99. [106]Gautier, V. W. et al. In vitro nuclear interactome of the HIV-1 Tat protein. Retrovirology6, 10.1186/1742-4690-6-47 (2009). PMC2702331 19454010 · DOI
  100. [107]Gordon-Alonso M Actin-binding protein Drebrin regulates HIV-1-triggered actin polymerization and viral infection Journal of Biological Chemistry 2013 288 28382 28397 10.1074/jbc.M113.494906 23926103 PMC3784756 · DOI
  101. [108]Hearps AC Jans DA HIV-1 integrase is capable of targeting DNA to the nucleus via an importin alpha/beta-dependent mechanism Biochemical Journal 2006 398 475 484 10.1042/BJ20060466 16716146 PMC1559465 · DOI
  102. [109]Jarboui, M. A. et al. Nucleolar protein trafficking in response to HIV-1 Tat: rewiring the nucleolus. Plos One7, 10.1371/journal.pone.0048702 (2012). PMC3499507 23166591 · DOI
  103. [110]Le Sage, V., Cinti, A., Valiente-Echeverria, F. & Mouland, A. J. Proteomic analysis of HIV-1 Gag interacting partners using proximity-dependent biotinylation. Virology Journal12, 10.1186/S12985-015-0365-6 (2015). PMC4566291 26362536 · DOI
  104. [111]Li DS Wei T Abbott CM Harrich D The unexpected roles of eukaryotic translation elongation factors in RNA virus replication and pathogenesis Microbiology and Molecular Biology Reviews 2013 77 253 266 10.1128/MMBR.00059-12 23699257 PMC3668672 · DOI
  105. [112]Li, Y. & Belshan, M. NF45 and NF90 bind HIV-1 RNA and modulate HIV gene expression. Viruses-Basel8, 10.3390/V8020047 (2016). PMC4776202 26891316 · DOI
  106. [113]Lingappa JR Dooher JE Newman MA Kiser PK Klein KC Basic residues in the nucleocapsid domain of gag are required for interaction of HIV-1 Gag with ABCE1 (HP68), a cellular protein important for HIV-1 capsid assembly Journal of Biological Chemistry 2006 281 3773 3784 10.1074/jbc.M507255200 16275648 · DOI
  107. [114]Liu, Y., Belkina, N. V. & Shaw, S. HIV infection of T cells: actin-in and actin-out. Science Signaling2, 10.1126/scisignal.266pe23 (2009). 19366992 · DOI
  108. [115]Lukic Z Dharan A Fricke T Diaz-Griffero F Campbell EM HIV-1 uncoating is facilitated by dynein and kinesin 1 Journal of virology 2014 88 13613 13625 10.1128/JVI.02219-14 25231297 PMC4248982 · DOI
  109. [116]Marchand V A janus splicing regulatory element modulates HIV-1 tat and rev mRNA production by coordination of hnRNP A1 cooperative binding Journal of Molecular Biology 2002 323 629 652 10.1016/S0022-2836(02)00967-1 12419255 · DOI
  110. [117]Rojas-Araya B Ohlmann T Soto-Rifo R Translational control of the HIV unspliced genomic RNA Viruses-Basel 2015 7 4326 4351 10.3390/v7082822 PMC4576183 26247956 · DOI
  111. [118]Santos, S., Obukhov, Y., Nekhai, S., Bukrinsky, M. & Iordanskiy, S. Virus-producing cells determine the host protein profiles of HIV-1 virion cores. Retrovirology9, 10.1186/1742-4690-9-65 (2012). PMC3432596 22889230 · DOI
  112. [119]Schweitzer CJ Jagadish T Haverland N Ciborowski P Belshan M Proteomic analysis of early HIV-1 nucleoprotein complexes Journal of Proteome Research 2013 12 559 572 10.1021/pr300869h 23282062 PMC3564510 · DOI
  113. [120]Schweitzer, C. J. et al. Knockdown of the cellular protein LRPPRC attenuates HIV-1 infection. Plos One7, 10.1371/journal.pone.0040537 (2012). PMC3395635 22808186 · DOI
  114. [121]Thierry S High-mobility group box 1 protein induces HIV-1 expression from persistently infected cells Aids 2007 21 283 292 10.1097/QAD.0b013e3280115b50 17255735 · DOI
  115. [122]Warren K Eukaryotic elongation factor 1 complex subunits are critical HIV-1 reverse transcription cofactors Proceedings of the National Academy of Sciences of the United States of America 2012 109 9587 9592 10.1073/pnas.1204673109 22628567 PMC3386134 · DOI
  116. [123]Watanabe T The hematopoietic cell-specific Rho GTPase inhibitor ARHGDIB/D4GDI limits HIV Type 1 replication Aids Research and Human Retroviruses 2012 28 913 922 10.1089/aid.2011.0180 21936715 · DOI
  117. [124]Widera M An intronic G run within HIV-1 intron 2 is critical for splicing regulation of vif mRNA Journal of virology 2013 87 2707 2720 10.1128/JVI.02755-12 23255806 PMC3571361 · DOI
  118. [125]Yan, N., Cherepanov, P., Daigle, J. E., Engelman, A. & Lieberman, J. The SET complex acts as a barrier to autointegration of HIV-1. Plos Pathogens5, 10.1371/journal.ppat.1000327 (2009). PMC2644782 19266025 · DOI
  119. [126]Zhou, X. X. et al. DDX5 facilitates HIV-1 replication as a cellular co-factor of Rev. Plos One8, 10.1371/journal.pone.0065040 (2013). PMC3669200 23741449 · DOI
  120. [127]Allouch A The TRIM family protein KAP1 inhibits HIV-1 integration Cell Host & Microbe 2011 9 484 495 10.1016/j.chom.2011.05.004 21669397 · DOI
  121. [128]Lassot I The proteasome regulates HIV-1 transcription by both proteolytic and nonproteolytic mechanisms Molecular Cell 2007 25 369 383 10.1016/j.molcel.2006.12.020 17289585 · DOI

Cited by

Sorted by citations

Authors
Knoener, R. A., Becker, J. T., Scalf, M., Sherer, N. M., & Smith, L. M.
Affiliations
University of Wisconsin–Madison (US)
Corresponding author
Smith, Lloyd M.
Venue
Scientific Reports
Published
2017-12-05
Volume
7
Issue
1
Pages
16965-16965
ISSN
2045-2322 (ISSN-L)
OpenAlex
W2769941852
Cited by
54
References
6
Citations by year
2026: 6 · 2025: 3 · 2024: 7 · 2023: 7 · 2022: 2 · 2021: 10 · 2020: 7 · 2019: 6 · 2018: 6
FWCI
2.83
Type
journal article
Language
en
Open access
Locations
  • Scientific Reports (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
  • National Cancer Institute (R01CA193481)
  • National Institute of Allergy and Infectious Diseases (R01AI110221)
Topics
  • Life Sciences › Immunology and Microbiology › Virology › HIV Research and Treatment
  • Physical Sciences › Chemistry › Spectroscopy › Advanced Proteomics Techniques and Applications
  • Health Sciences › Medicine › Infectious Diseases › HIV/AIDS drug development and treatment
Keywords
HIV-1, RNA-protein interactions, unspliced viral RNA, hybridization capture, formaldehyde crosslinking, Rev, Gag-Pol, host factors, HIV replication, siRNA knockdown, viral RNA packaging, alternative splicing
MeSH terms
Cytoplasm, Humans, Microscopy, Fluorescence, Nucleic Acid Hybridization, Proteins, RNA Splicing, RNA, Viral, Mass Spectrometry, Viral Proteins, Reproducibility of Results, HIV-1, HIV Infections, RNA-Binding Proteins, RNA, Small Interfering, Gene Knockdown Techniques, HEK293 Cells

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