Random mutagenesis MAPPIT analysis identifies binding sites for Vif and Gag in both cytidine deaminase domains of Apobec3G

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Uyttendaele, Isabel ^a,b   Lavens, Delphine ^a,b   Catteeuw, Dominiek ^a,b   Lemmens, Irma ^a,b   Bovijn, Celia ^a,b   Tavernier, Jan ^a,b   Peelman, Frank ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3G; CYTIDINE DEAMINASE; GAG PROTEIN; VIF PROTEIN; APOBEC3G PROTEIN, HUMAN; MUTANT PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DIMERIZATION; HOMODIMERIZATION; HUMAN; MAPPIT; MUTAGENESIS; NUCLEOTIDE BINDING SITE; PROTEIN ANALYSIS; PROTEIN PROTEIN INTERACTION; TWO HYBRID SYSTEM; BINDING SITE; CELL STRAIN HEK293; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS 1; METABOLISM; MUTATION; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE;

BINDING SITES; CYTIDINE DEAMINASE; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HEK293 CELLS; HIV-1; HUMANS; MODELS, MOLECULAR; MUTAGENESIS; MUTANT PROTEINS; MUTATION; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; TWO-HYBRID SYSTEM TECHNIQUES; VIF GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

EID: 84874768704     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0044143     Document Type: Article

References (91)

1. Stein A, Mosca R, Aloy P (2011) Three-dimensional modeling of protein interactions and complexes is going 'omics. Curr Opin Struct Biol 21: 2002208.
2. Lensink MF, Wodak SJ (2010) Blind predictions of protein interfaces by docking calculations in CAPRI. Proteins 78: 308523095.
3. Janin J (2010) Protein-protein docking tested in blind predictions: the CAPRI experiment. Mol Biosyst 6: 235122362.
4. Kundrotas PJ, Lensink MF, Alexov E (2008) Homology-based modeling of 3D structures of protein-protein complexes using alignments of modified sequence profiles. Int J Biol Macromol 43: 1982208.
5. Mertens HD, Svergun DI (2010) Structural characterization of proteins and complexes using small-angle X-ray solution scattering. J Struct Biol 172: 1282141.
6. Spahn CM, Penczek PA (2009) Exploring conformational modes of macromolecular assemblies by multiparticle cryo-EM. Curr Opin Struct Biol 19: 6232631.
7. Yahav T, Maimon T, Grossman E, Dahan I, Medalia O (2011) Cryo-electron tomography: gaining insight into cellular processes by structural approaches. Curr Opin Struct Biol 21: 6702677.
8. de Vries SJ, Melquiond AS, Kastritis PL, Karaca E, Bordogna A, et al. (2010) Strengths and weaknesses of data-driven docking in critical assessment of prediction of interactions. Proteins 78: 324223249.
9. Eyckerman S, Verhee A, Van der Heyden J, Lemmens I, Van Ostade X, et al. (2001) Design and application of a cytokine-receptor-based interaction trap. Nat Cell Biol 3: 111421119.
10. Lavens D, Peelman F, Van der Heyden J, Uyttendaele I, Catteeuw D, et al. (2010) Definition of the interacting interfaces of Apobec3G and HIV-1 Vif using MAPPIT mutagenesis analysis. Nucleic Acids Res 38: 190221912.
11. Conticello SG (2008) The AID/APOBEC family of nucleic acid mutators. Genome Biol 9: 229.
12. Sheehy AM, Gaddis NC, Choi JD, Malim MH (2002) Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418: 6462650.
13. Mangeat B, Turelli P, Caron G, Friedli M, Perrin L, et al. (2003) Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts. Nature 424: 992103.
14. Zhang H, Yang B, Pomerantz RJ, Zhang C, Arunachalam SC, et al. (2003) The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA. Nature 424: 94298.
15. Harris RS, Bishop KN, Sheehy AM, Craig HM, Petersen-Mahrt SK, et al. (2003) DNA deamination mediates innate immunity to retroviral infection. Cell 113: 8032809.
16. Yu Q, Konig R, Pillai S, Chiles K, Kearney M, et al. (2004) Single-strand specificity of APOBEC3G accounts for minus-strand deamination of the HIV genome. Nat Struct Mol Biol 11: 4352442.
17. Shindo K, Takaori-Kondo A, Kobayashi M, Abudu A, Fukunaga K, et al. (2003) The enzymatic activity of CEM15/Apobec-3G is essential for the regulation of the infectivity of HIV-1 virion but not a sole determinant of its antiviral activity. J Biol Chem 278: 44412-44416.
18. Chiu YL, Soros VB, Kreisberg JF, Stopak K, Yonemoto W, et al. (2005) Cellular APOBEC3G restricts HIV-1 infection in resting CD4+ T cells. Nature 435: 108-114.
19. Newman EN, Holmes RK, Craig HM, Klein KC, Lingappa JR, et al. (2005) Antiviral function of APOBEC3G can be dissociated from cytidine deaminase activity. Curr Biol 15: 166-170.
20. Bishop KN, Holmes RK, Malim MH (2006) Antiviral potency of APOBEC proteins does not correlate with cytidine deamination. J Virol 80: 8450-8458.
21. Iwatani Y, Chan DS, Wang F, Maynard KS, Sugiura W, et al. (2007) Deaminase-independent inhibition of HIV-1 reverse transcription by APOBEC3G. Nucleic Acids Res 35: 7096-7108.
22. Guo F, Cen S, Niu M, Yang Y, Gorelick RJ, et al. (2007) The interaction of APOBEC3G with human immunodeficiency virus type 1 nucleocapsid inhibits tRNA3Lys annealing to viral RNA. J Virol 81: 11322-11331.
23. Li XY, Guo F, Zhang L, Kleiman L, Cen S (2007) APOBEC3G inhibits DNA strand transfer during HIV-1 reverse transcription. J Biol Chem 282: 32065-32074.
24. Luo K, Wang T, Liu B, Tian C, Xiao Z, et al. (2007) Cytidine deaminases APOBEC3G and APOBEC3F interact with human immunodeficiency virus type 1 integrase and inhibit proviral DNA formation. J Virol 81: 7238-7248.
25. Mbisa JL, Barr R, Thomas JA, Vandegraaff N, Dorweiler IJ, et al. (2007) Human immunodeficiency virus type 1 cDNAs produced in the presence of APOBEC3G exhibit defects in plus-strand DNA transfer and integration. J Virol 81: 7099-7110.
26. Bishop KN, Verma M, Kim EY, Wolinsky SM, Malim MH (2008) APOBEC3G inhibits elongation of HIV-1 reverse transcripts. PLoS Pathog 4: e1000231.
27. Marin M, Rose KM, Kozak SL, Kabat D (2003) HIV-1 Vif protein binds the editing enzyme APOBEC3G and induces its degradation. Nat Med 9: 1398-1403.
28. Sheehy AM, Gaddis NC, Malim MH (2003) The antiretroviral enzyme APOBEC3G is degraded by the proteasome in response to HIV-1 Vif. Nat Med 9: 1404-1407.
29. Stopak K, de Noronha C, Yonemoto W, Greene WC (2003) HIV-1 Vif blocks the antiviral activity of APOBEC3G by impairing both its translation and intracellular stability. Mol Cell 12: 591-601.
30. Mehle A, Strack B, Ancuta P, Zhang C, McPike M, et al. (2004) Vif overcomes the innate antiviral activity of APOBEC3G by promoting its degradation in the ubiquitin-proteasome pathway. J Biol Chem 279: 7792-7798.
31. Conticello SG, Harris RS, Neuberger MS (2003) The Vif protein of HIV triggers degradation of the human antiretroviral DNA deaminase APOBEC3G. Curr Biol 13: 2009-2013.
32. Yu X, Yu Y, Liu B, Luo K, Kong W, et al. (2003) Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex. Science 302: 1056-1060.
33. Yu Y, Xiao Z, Ehrlich ES, Yu X, Yu XF (2004) Selective assembly of HIV-1 Vif- Cul5-ElonginB-ElonginC E3 ubiquitin ligase complex through a novel SOCS box and upstream cysteines. Genes Dev 18: 2867-2872.
34. Jarmuz A, Chester A, Bayliss J, Gisbourne J, Dunham I, et al. (2002) An anthropoid-specific locus of orphan C to U RNA-editing enzymes on chromosome 22. Genomics 79: 285-296.
35. Hache G, Liddament MT, Harris RS (2005) The retroviral hypermutation specificity of APOBEC3F and APOBEC3G is governed by the C-terminal DNA cytosine deaminase domain. J Biol Chem 280: 10920-10924.
36. Navarro F, Bollman B, Chen H, Konig R, Yu Q, et al. (2005) Complementary function of the two catalytic domains of APOBEC3G. Virology 333: 374-386.
37. Gooch BD, Cullen BR (2008) Functional domain organization of human APOBEC3G. Virology 379: 118-124.
38. Luo K, Liu B, Xiao Z, Yu Y, Yu X, et al. (2004) Amino-terminal region of the human immunodeficiency virus type 1 nucleocapsid is required for human APOBEC3G packaging. J Virol 78: 11841-11852.
39. Cen S, Guo F, Niu M, Saadatmand J, Deflassieux J, et al. (2004) The interaction between HIV-1 Gag and APOBEC3G. J Biol Chem 279: 33177-33184.
40. Alce TM, Popik W (2004) APOBEC3G is incorporated into virus-like particles by a direct interaction with HIV-1 Gag nucleocapsid protein. J Biol Chem 279: 34083-34086.
41. Schafer A, Bogerd HP, Cullen BR (2004) Specific packaging of APOBEC3G into HIV-1 virions is mediated by the nucleocapsid domain of the gag polyprotein precursor. Virology 328: 163-168.
42. Zennou V, Perez-Caballero D, Gottlinger H, Bieniasz PD (2004) APOBEC3G incorporation into human immunodeficiency virus type 1 particles. J Virol 78: 12058-12061.
43. Svarovskaia ES, Xu H, Mbisa JL, Barr R, Gorelick RJ, et al. (2004) 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 279: 35822-35828.
44. Chen KM, Harjes E, Gross PJ, Fahmy A, Lu Y, et al. (2008) Structure of the DNA deaminase domain of the HIV-1 restriction factor APOBEC3G. Nature 452: 116-119.
45. Holden LG, Prochnow C, Chang YP, Bransteitter R, Chelico L, et al. (2008) Crystal structure of the anti-viral APOBEC3G catalytic domain and functional implications. Nature 456: 121-124.
46. Shandilya SM, Nalam MN, Nalivaika EA, Gross PJ, Valesano JC, et al. (2010) Crystal structure of the APOBEC3G catalytic domain reveals potential oligomerization interfaces. Structure 18: 28-38.
47. Harjes E, Gross PJ, Chen KM, Lu Y, Shindo K, et al. (2009) An extended structure of the APOBEC3G catalytic domain suggests a unique holoenzyme model. J Mol Biol 389: 819-832.
48. Furukawa A, Nagata T, Matsugami A, Habu Y, Sugiyama R, et al. (2009) Structure, interaction and real-time monitoring of the enzymatic reaction of wild-type APOBEC3G. EMBO J 28: 440-451.
49. Zhang KL, Mangeat B, Ortiz M, Zoete V, Trono D, et al. (2007) Model structure of human APOBEC3G. PLoS One 2: e378.
50. Wedekind JE, Gillilan R, Janda A, Krucinska J, Salter JD, et al. (2006) Nanostructures of APOBEC3G support a hierarchical assembly model of high molecular mass ribonucleoprotein particles from dimeric subunits. J Biol Chem 281: 38122-38126.
51. Huthoff H, Autore F, Gallois-Montbrun S, Fraternali F, Malim MH (2009) RNA-dependent oligomerization of APOBEC3G is required for restriction of HIV-1. PLoS Pathog 5: e1000330.
52. Bulliard Y, Turelli P, Rohrig UF, Zoete V, Mangeat B, et al. (2009) Functional analysis and structural modeling of human APOBEC3G reveal the role of evolutionarily conserved elements in the inhibition of human immunodeficiency virus type 1 infection and Alu transposition. J Virol 83: 12611-12621.
53. Prochnow C, Bransteitter R, Klein MG, Goodman MF, Chen XS (2007) The APOBEC-2 crystal structure and functional implications for the deaminase AID. Nature 445: 447-451.
54. Rui L, Mathews LS, Hotta K, Gustafson TA, Carter-Su C (1997) Identification of SH2-Bbeta as a substrate of the tyrosine kinase JAK2 involved in growth hormone signaling. Mol Cell Biol 17: 6633-6644.
55. Huthoff H, Malim MH (2007) Identification of amino acid residues in APOBEC3G required for regulation by human immunodeficiency virus type 1 Vif and Virion encapsidation. J Virol 81: 3807-3815.
56. Zhang L, Saadatmand J, Li X, Guo F, Niu M, et al. (2008) Function analysis of sequences in human APOBEC3G involved in Vif-mediated degradation. Virology 370: 113-121.
57. Boxem M, Maliga Z, Klitgord N, Li N, Lemmens I, et al. (2008) A protein domain-based interactome network for C. elegans early embryogenesis. Cell 134: 534-545.
58. Yu H, Braun P, Yildirim MA, Lemmens I, Venkatesan K, et al. (2008) Highquality binary protein interaction map of the yeast interactome network. Science 322: 104-110.
59. Braun P, Tasan M, Dreze M, Barrios-Rodiles M, Lemmens I, et al. (2009) An experimentally derived confidence score for binary protein-protein interactions. Nat Methods 6: 91-97.
60. Venkatesan K, Rual JF, Vazquez A, Stelzl U, Lemmens I, et al. (2009) An empirical framework for binary interactome mapping. Nat Methods 6: 83-90.
61. Simonis N, Rual JF, Carvunis AR, Tasan M, Lemmens I, et al. (2009) Empirically controlled mapping of the Caenorhabditis elegans protein-protein interactome network. Nat Methods 6: 47-54.
62. Lievens S, Vanderroost N, Van der Heyden J, Gesellchen V, Vidal M, et al. (2009) Array MAPPIT: High-throughput interactome analysis in mammalian cells. J Proteome Res 8: 877-886.
63. Dhayalan A, Jurkowski TP, Laser H, Reinhardt R, Jia D, et al. (2008) Mapping of protein-protein interaction sites by the 'absence of interference' approach. J Mol Biol 376: 1091-1099.
64. Fowler DM, Araya CL, Fleishman SJ, Kellogg EH, Stephany JJ, et al. (2010) High-resolution mapping of protein sequence-function relationships. Nat Methods 7: 741-746.
65. Stefan N, Martin-Killias P, Wyss-Stoeckle S, Honegger A, Zangemeister-Wittke U, et al. (2011) DARPins recognizing the tumor-associated antigen EpCAM selected by phage and ribosome display and engineered for multivalency. J Mol Biol 413: 826-843.
66. Lickfeld M, Schmitz HP (2011) Selection of STOP-free sequences from random mutagenesis for 'loss of interaction' two-hybrid studies. Yeast 28: 535-545.
67. Kim JY, Park OG, Lee YC (2012) One- plus two-hybrid system for the efficient selection of missense mutant alleles defective in protein-protein interactions. Methods Mol Biol 812: 209-223.
68. Lemmens I, Eyckerman S, Zabeau L, Catteeuw D, Vertenten E, et al. (2003) Heteromeric MAPPIT: a novel strategy to study modification-dependent protein-protein interactions in mammalian cells. Nucleic Acids Res 31: e75.
69. Rasila TS, Pajunen MI, Savilahti H (2009) Critical evaluation of random mutagenesis by error-prone polymerase chain reaction protocols, Escherichia coli mutator strain, and hydroxylamine treatment. Anal Biochem 388: 71-80.
70. Wong TS, Roccatano D, Zacharias M, Schwaneberg U (2006) A statistical analysis of random mutagenesis methods used for directed protein evolution. J Mol Biol 355: 858-871.
71. Yep A, Kenyon GL, McLeish MJ (2008) Saturation mutagenesis of putative catalytic residues of benzoylformate decarboxylase provides a challenge to the accepted mechanism. Proc Natl Acad Sci U S A 105: 5733-5738.
72. Liu J, Cropp TA (2012) A method for multi-codon scanning mutagenesis of proteins based on asymmetric transposons. Protein Eng Des Sel 25: 67-72.
73. Poussu E, Vihinen M, Paulin L, Savilahti H (2004) Probing the alphacomplementing domain of E. coli beta-galactosidase with use of an insertional pentapeptide mutagenesis strategy based on Mu in vitro DNA transposition. Proteins 54: 681-692.
74. Daggett KA, Layer M, Cropp TA (2009) A general method for scanning unnatural amino acid mutagenesis. ACS Chem Biol 4: 109-113.
75. Iwatani Y, Chan DS, Liu L, Yoshii H, Shibata J, et al. (2009) HIV-1 Vifmediated ubiquitination/degradation of APOBEC3G involves four critical lysine residues in its C-terminal domain. Proc Natl Acad Sci USA 106: 19539-19544.
76. Bogerd HP, Doehle BP, Wiegand HL, Cullen BR (2004) A single amino acid difference in the host APOBEC3G protein controls the primate species specificity of HIV type 1 virion infectivity factor. Proc Natl Acad Sci USA 101: 3770-3774.
77. Xu H, Svarovskaia ES, Barr R, Zhang Y, Khan MA, et al. (2004) A single amino acid substitution in human APOBEC3G antiretroviral enzyme confers resistance to HIV-1 virion infectivity factor-induced depletion. Proc Natl Acad Sci USA 101: 5652-5657.
78. Schrofelbauer B, Chen D, Landau NR (2004) A single amino acid of APOBEC3G controls its species-specific interaction with virion infectivity factor (Vif). Proc Natl Acad Sci USA 101: 3927-3932.
79. Mangeat B, Turelli P, Liao S, Trono D (2004) A single amino acid determinant governs the species-specific sensitivity of APOBEC3G to Vif action. J Biol Chem 279: 14481-14483.
80. Chelico L, Prochnow C, Erie DA, Chen XS, Goodman MF (2010) Structural model for deoxycytidine deamination mechanisms of the HIV-1 inactivation enzyme APOBEC3G. J Biol Chem 285: 16195-16205.
81. Shlyakhtenko LS, Lushnikov AY, Li M, Lackey L, Harris RS, et al. (2011) Atomic force microscopy studies provide direct evidence for dimerization of the HIV restriction factor APOBEC3G. J Biol Chem 286: 3387-3395.
82. Khan MA, Goila-Gaur R, Kao S, Miyagi E, Walker RC Jr, et al. (2009) Encapsidation of APOBEC3G into HIV-1 virions involves lipid raft association and does not correlate with APOBEC3G oligomerization. Retrovirology 6: 99.
83. Tavernier J, Eyckerman S, Lemmens I, Van der Heyden J, Vandekerckhove J, etal. (2002) MAPPIT: a cytokine receptor-based two-hybrid method in mammalian cells. Clin Exp Allergy 32: 1397-1404.
84. Uyttendaele I, Lemmens I, Verhee A, De Smet AS, Vandekerckhove J, et al. (2007) Mammalian protein-protein interaction trap (MAPPIT) analysis ofSTAT5, CIS, and SOCS2 interactions with the growth hormone receptor. Mol Endocrinol 21: 2821-2831.
85. Eyckerman S, Broekaert D, Verhee A, Vandekerckhove J, Tavernier J (2000) Identification of the Y985 and Y1077 motifs as SOCS3 recruitment sites in the murine leptin receptor. Febs Lett 486: 33-37.
86. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
87. Katoh K, Kuma K, Toh H, Miyata T (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33: 511-518.
88. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ (2009) Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189-1191.
89. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, et al. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25: 1605-1612.
90. Perez-Cano L, Fernandez-Recio J (2010) Optimal protein-RNA area, OPRA: a propensity-based method to identify RNA-binding sites on proteins. Proteins 78: 25-35.
91. Hubbard SJ, Campbell SF, Thornton JM (1991) Molecular recognition. Conformational analysis of limited proteolytic sites and serine proteinase protein inhibitors. J Mol Biol 220: 507-530.