Structure of a Conserved Retroviral RNA Packaging Element by NMR Spectroscopy and Cryo-Electron Tomography

Journal of Molecular Biology

Volumn 404, Issue 5, 2010, Pages 751-772

  Miyazaki, Yasuyuki ^a   Irobalieva, Rossitza N ^b   Tolbert, Blanton S ^a   Smalls Mantey, Adjoa ^a   Iyalla, Kilali ^a   Loeliger, Kelsey ^a   D'Souza, Victoria ^a   Khant, Htet ^b   Schmid, Michael F ^b   Garcia, Eric L ^c   Telesnitsky, Alice ^c   Chiu, Wah ^b   Summers, Michael F ^a  

^a UNIVERSITY OF MARYLAND BALTIMORE COUNTY   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Cryo electron tomography; Genome packaging; NMR spectroscopy; Retrovirus; RNA structure

Indexed keywords

DEUTERIUM; GAG PROTEIN; PROTON; SCAFFOLD PROTEIN; SHORT HAIRPIN RNA; VIRUS RNA;

5' UNTRANSLATED REGION; ARTICLE; BASE PAIRING; CARBON NUCLEAR MAGNETIC RESONANCE; CONTROLLED STUDY; DIMERIZATION; ELECTRON TOMOGRAPHY; MOLECULAR INTERACTION; MOLONEY LEUKEMIA ONCOVIRUS; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MOTIF; PROTON NUCLEAR MAGNETIC RESONANCE; RNA CONFORMATION; RNA PACKAGING ELEMENT; RNA STABILITY; RNA STRUCTURE; VIRUS ASSEMBLY; VIRUS GENOME;

MOLONEY MURINE LEUKEMIA VIRUS;

EID: 78649529383     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.09.009     Document Type: Article

References (120)

1. Rein A. Retroviral RNA packaging: a review. Arch. Virol. 1994, 9:513-522.
2. Berkowitz R., Fisher J., Goff S.P. RNA packaging. Curr. Top. Microbiol. Immunol. 1996, 214:177-218.
3. Jewell N.A., Mansky L.M. In the beginning: genome recognition, RNA encapsidation and the initiation of complex retrovirus assembly. J. Gen. Virol. 2000, 81:1889-1899.
4. Paillart J.C., Shehu-Xhilaga M., Marquet R., Mak J. Dimerization of retroviral RNA genomes: an inseparable pair. Nat. Rev. Microbiol. 2004, 2:461-472.
5. Russell R.S., Liang C., Wainberg M.A. Is HIV-1 RNA dimerization a prerequisite for packaging? Yes, no, probably?. Retrovirology 2004, 1:23.
6. Greatorex J. The retroviral RNA dimer linkage: different structures may reflect different roles. Retrovirology 2004, 1:22.
7. D'Souza V., Summers M.F. How retroviruses select their genomes. Nat. Rev. Microbiol. 2005, 3:643-655.
8. Mann R., Mulligan R.C., Baltimore D. Construction of a retrovirus packaging mutant and its use to produce helper-free defective retrovirus. Cell 1983, 33:153-159.
9. Coffin J.M., Hughes S.H., Varmus H.E. Retroviruses 1997, Cold Spring Harbor Laboratory Press, Plainview, NY.
10. Varmus H.E. Form and function of retroviral proviruses. Science 1982, 216:812-820.
11. Hu W.S., Temin H.M. Retroviral recombination and reverse transcription. Science 1990, 250:1227-1233.
12. Onafuwa A., An W., Robson N.D., Telesnitsky A. Human immunodeficiency virus type 1 genetic recombination is more frequent than that of Moloney murine leukemia virus despite similar template switching rates. J. Virol. 2003, 77:4577-4587.
13. Onafuwa-Nuga A., Telesnitsky A. The remarkable frequency of human immunodeficiency virus type 1 genetic recombination. Microbiol. Mol. Biol. Rev. 2009, 73:451-480.
14. Swanstrom R., Wills J.W. Synthesis, assembly and processing of viral proteins. Retroviruses 1997, 263-334. Cold Spring Harbor Press, Plainview, NY. J.M. Coffin, S.H. Hughes, H.E. Varmus (Eds.).
15. Berkhout B. Structure and function of the human immunodeficiency virus leader RNA. Prog. Nucleic Acid Res. Mol. Biol. 1996, 54:1-34.
16. Prats A.C., Roy C., Wang P., Erard M., Housset V., Gabus C., et al. cis elements and trans-acting factors involved in dimer formation of murine leukemia virus RNA. J. Virol. 1990, 64:774-783.
17. Song R., Kafaie J., Yang L., Laughrea M. HIV-1 viral RNA is selected in the form of monomers that dimerize in a three-step protease-dependent process; the DIS of stem-loop 1 initiates viral RNA dimerization. J. Mol. Biol. 2007, 371:1084-1096.
18. Levin J.G., Grimley P.M., Ramseur J.M., Berezesky I.K. Deficiency of 60 to 70S RNA in murine leukemia virus particles assembled in cells treated with actinomycin D. J. Virol. 1974, 14:152-161.
19. Fu W., Rein A. Maturation of dimeric viral RNA of Moloney murine leukemia virus. J. Virol. 1993, 67:5443-5449.
20. Housset V., De Rocquigny H., Roques B.P., Darlix J.L. Basic amino acids flanking the zinc finger of Moloney murine leukemia virus nucleocapsid protein NCp10 are critical for virus infectivity. J. Virol. 1993, 67:2537-2545.
21. Hibbert C.S., Mirro J., Rein A. mRNA molecules containing MLV packaging signals are encapsidated as dimers. J. Virol. 2004, 78:10927-10938.
22. Flynn J.A., King S.R., Telesnitsky A. Nonrandom dimerization of murine leukemia virus genomic RNAs. J. Virol. 2004, 78:12129-12139.
23. Flynn J.A., Telesnitsky A. Two distinct Moloney murine leukemia virus RNAs produced from a single locus dimerize at random. Virology 2006, 344:391-400.
24. Moore M.D., Fu W., Nikolaitchik O., Chen J., Ptak R.G., Hu W.S. Dimer initiation signal of human immunodeficiency virus type 1: its role in partner selection during RNA copackaging and its effects on recombination. J. Virol. 2007, 81:4002-4011.
25. Urisman A., Molinaro R.J., Fischer N., Plummer S.J., Casey G., Klein E.A., et al. Identification of a novel Gammaretrovirus in prostate tumors of patients homozygous for R462Q RNASEL variant. PLoS Pathog. 2006, 2:e25.
26. Schlaberg R., Choe D.J., Brown K.R., Thaker H.M., Singh I.R. XMRV is present in malignant prostatic epithelium and is associated with prostate cancer, especially high-grade tumors. Proc. Natl Acad. Sci. USA 2009, 106:16351-16356.
27. Lombardi V.C., Ruscetti F.W., Gupta J.D., Pfost M.A., Hagen K.S., Peterson D.L., et al. Detection of an infectious retrovirus, XMRV, in blood cells of patients with chronic fatigue syndrome. Science 2009, 326:585-589.
28. Hohn O., Krause H., Barbarotto P., Niederstadt L., Beimforde N., Denner J., et al. Lack of evidence for xenotropic murine leukemia virus-related virus (XMRV) in German prostate cancer patients. Retrovirology 2009, 6:92.
29. Erlwein O., Kaye S., McClure M.O., Weber J., Wills G., Collier D., et al. Failure to detect the novel retrovirus XMRV in chronic fatigue syndrome. PLoS ONE 2010, 5:e8519.
30. Lo S.C., Pripuzova N., Li B., Komaroff A.L., Hung G.C., Wang R., Alter H.J. Detection of MLV-related virus gene sequences in blood of patients with chronic fatigue syndrome and healthy blood donors. Proc. Natl Acad. Sci. USA 2010, 107:15874-15879.
31. De Tapia M., Metzler V., Mougel M., Ehresmann B., Ehresmann C. Dimerization of MoMuLV genomic RNA: redefinition of the role of the palindromic stem-loop H1 (278-303) and new roles for stem-loops H2 (310-352) and H3 (355-374). Biochemistry 1998, 37:6077-6085.
32. Mougel M., Tounekti N., Darlix J.L., Paoletti J., Ehresmann B., Ehresmann C. Conformational analysis of the 5' leader and the gag initiation site of Mo-MuLV RNA and allosteric transitions induced by dimerization. Nucleic Acids Res. 1993, 21:4677-4684.
33. Roy C., Tounekti N., Mougel M., Darlix J.L., Paoletti C., Ehresmann C., et al. An analytical study of the dimerization of in vitro generated RNA of Moloney murine leukemia virus MoMuLV. Nucleic Acids Res. 1990, 18:7287-7292.
34. Tounekti N., Mougel M., Roy C., Marquet R., Darlix J.L., Paoletti J., et al. Effect of dimerization on the conformation of the encapsidation psi domain of Moloney murine leukemia virus RNA. J. Mol. Biol. 1992, 223:205-220.
35. Girard P.M., Bonnet-Mathoniere B., Mauriaux D., Paoletti J. A short autocomplementary sequence in the 5' leader region is responsible for dimerization of MoMuLV genomic RNA. Biochemistry 1995, 34:9785-9794.
36. Ly H., Nierlich D.P., Olsen J.C., Kaplan A.H. Moloney murine sarcoma virus genomic RNAs dimerize via a two-step process: a concentration-dependent kissing-loop interaction is driven by initial contact between consecutive guanines. J. Virol. 1999, 73:7255-7261.
37. Oroudjev E.M., Kang P.C.E., Kohlstaedt L.A. An additional dimer linkage structure in Moloney murine leukemia virus RNA. J. Mol. Biol. 1999, 291:603-613.
38. Ly H., Parslow T.G. Bipartite signal for genomic RNA dimerization in the Moloney murine leukemia virus. J. Virol. 2002, 76:3135-3144.
39. Kim C.H., Tinoco I. A retroviral RNA kissing complex containing only two G-C base pairs. Proc. Natl Acad. Sci. USA 2000, 97:9396-9401.
40. Konings D.A.M., Nash M.A., Maizel J.V., Arlinghaus R.B. Novel GACG-hairpin pair motif in the 5' untranslated region of type C retrovirus related to murine leukemia virus. J. Virol. 1992, 66:632-640.
41. D'Souza V., Summers M.F. Structural basis for packaging the dimeric genome of Moloney murine leukaemia virus. Nature 2004, 431:586-590.
42. Mougel M., Barklis E. A role for two hairpin structures as a core RNA encapsidation signal in murine leukemia virus virions. J. Virol. 1997, 71:8061-8065.
43. D'Souza V., Melamed J., Habib D., Pullen K., Wallace K., Summers M.F. Identification of a high-affinity nucleocapsid protein binding site within the Moloney murine leukemia virus Ψ-RNA packaging signal. Implications for genome recognition. J. Mol. Biol. 2001, 314:217-232.
44. D'Souza V., Dey A., Habib D., Summers M.F. NMR structure of the 101 nucleotide core encapsidation signal of the Moloney murine leukemia virus. J. Mol. Biol. 2004, 337:427-442.
45. Badorrek C.S., Gherghe C.M., Weeks K.M. Structure of an RNA switch that enforces stringent retroviral genomic RNA dimerization. Proc. Natl Acad. Sci. USA 2006, 103:13640-13645.
46. Badorrek C.S., Weeks K.M. Architecture of a gamma retroviral genomic RNA dimer. Biochemistry 2006, 45:12664-12672.
47. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 2003, 31:3406-3415.
48. Robson N.D., Telesnitsky A. Effects of 3' untranslated region mutations on plus-strand priming during Moloney murine leukemia virus replication. J. Virol. 1999, 73:948-957.
49. Onafuwa-Nuga A.A., King S.R., Telesnitsky A. Nonrandom packaging of host RNAs in Moloney murine leukemia virus. J. Virol. 2005, 79:13528-13537.
50. Onafuwa-Nuga A.A., Telesnitsky A., King S.R. 7SL RNA, but not the 54-kd signal recognition particle protein, is an abundant component of both infectious HIV-1 and minimal virus-like particles. RNA 2006, 12:542-546.
51. Rulli S.J., Hibbert C.S., Mirro J., Pederson T., Biswal S., Rein A. Selective and nonselective packaging of cellular RNAs in retrovirus particles. J. Virol. 2007, 81:6623-6631.
52. Walker S.C., Avis J.M., Conn G.L. General plasmids for producing RNA in vitro transcripts with homogeneous ends. Nucleic Acids Res 2003, 31:e82.
53. 13C residual dipolar coupling on refinement. J. Biomol. NMR 2010, 47:205-219.
54. Lu K., Miyazaki Y., Summers M.F. Isotope labeling strategies for NMR studies of RNA. J. Biomol. NMR 2009, 46:113-125.
55. Clore G.M., Kuszewski J. Improving the accuracy of NMR structures of RNA by means of conformational database potentials of mean force as assessed by complete dipolar coupling cross-validation. J. Am. Chem. Soc. 2003, 125:1518-1525.
56. Rife J.P., Stallings S.C., Correll C.C., Dallas A., Steitz T.A., Moore P.B. Comparison of the crystal and solution structures of two RNA oligonucleotides. Biophys. J. 1999, 76:66-75.
57. Güntert P., Wüthrich K. Improved efficiency of protein structure calculations from NMR data using the program DIANA with redundant dihedral angle constraints. J. Biomol. NMR 1991, 1:447-456.
58. Trantirek L., Urbasek M., Stefl R., Feigon J., Sklenar V. A method for direct determination of helical parameters in nucleic acids using residual dipolar couplings. J. Am. Chem. Soc. 2000, 122:10454-10455.
59. Bayer P., Varani L., Varani G. Refinement of the structure of protein-RNA complexes by residual dipolar coupling analysis. J. Biomol. NMR 1999, 14:149-155.
60. Warren J.J., Moore P.B. Application of dipolar coupling data to the refinement of the solution structure of the sarcin-ricin loop RNA. J. Biomol. NMR 2001, 20:311-323.
61. Stefl R., Wu H., Ravindranathan S., Sklenar V., Feigon J. DNA A-tract bending in three dimensions: solving the dA4T4 vs. dT4A4 conundrum. Proc. Natl Acad. Sci. USA 2004, 101:1177-1182.
62. Tjandra N., Tate S., Ono A., Kainosho M., Bax A. The NMR structure of a DNA dodecamer in an aqueous dilute liquid crystalline phase. J. Am. Chem. Soc. 2000, 122:6190-6200.
63. Mollova E.T., Hansen M.R., Pardi A. Global structure of RNA determined with residual dipolar couplings. J. Am. Chem. Soc. 2000, 122:11561-11562.
64. Ying J., Grishaev A., Latham M.P., Pardi A., Bax A. Magnetic field induced residual dipolar couplings of imino groups in nucleic acids from measurements at a single magnetic field. J. Biomol. NMR 2007, 39:91-96.
65. Latham M.P., Hanson P., Brown D.J., Pardi A. Comparison of alignment tensors generated for native tRNAVal using magnetic fields and liquid crystalline media. J. Biomol. NMR 2008, 40:83-94.
66. Bax A., Grishaev A. Weak alignment NMR: a hawk-eyed view of biomolecular structure. Curr. Opin. Struct. Biol. 2005, 15:563-570.
67. Lukavsky P.J., Puglisi J.D. Structure determination of large biological RNAs. Methods Enzymol. 2005, 394:399-415.
68. Lukavsky P.J., Kim I., Otto G.A., Puglisi J.D. Structure of HCV IRES domain II determined by NMR. Nat. Struct. Biol. 2003, 10:1033-1038.
69. Al-Hashimi H.M., Walter N.G. RNA dynamics: it is about time. Curr. Opin. Struct. Biol. 2008, 18:321-329.
70. Al-Hashimi H.M., Tolman J.R., Majumdar A., Gorin A., Patel D.J. Determining stoichiometry in homomultimeric nucleic acid complexes using magnetic field induced residual dipolar couplings. J. Am. Chem. Soc. 2001, 123:5806-5807.
71. 2+-induced variations in the conformation and dynamics of HIV-1 TAR RNA probed using NMR residual dipolar couplings. J. Mol. Biol. 2003, 329:867-873.
72. Al-Hashimi H.M., Patel D.J. Residual dipolar couplings: synergy between NMR and structural genomics. J. Biomol. NMR 2002, 22:1-8.
73. Al-Hashimi H.M., Majumdar A., Gorin A., Kettani A., Skripkin E., Patel D.J. Field- and phage-induced dipolar couplings in a homodimeric DNA quadruplex: relative orientation of G.(C-A) triad and G-tetrad motifs and direct determination of C2 symmetry axis orientation. J. Am. Chem. Soc. 2001, 123:633-640.
74. Al-Hashimi H.M., Gosser Y., Gorin A., Hu W., Majumdar A., Patel D.J. Concerted motions in HIV-1 TAR RNA may allow access to bound state conformations: RNA dynamics from NMR residual dipolar couplings. J. Mol. Biol. 2002, 315:95-102.
75. Al-Hashimi H.M., Gorin A., Majumdar A., Patel D.J. Alignment of the HTLV-I Rex peptide bound to its target RNA aptamer from magnetic field-induced residual dipolar couplings and intermolecular hydrogen bonds. J. Am. Chem. Soc. 2001, 123:3179-3180.
76. Al-Hashimi H.M. Beyond static structures of RNA by NMR: folding, refolding, and dynamics at atomic resolution. Biopolymers 2007, 86:345-347.
77. Zhang Q., Al-Hashimi H.M. Extending the NMR spatial resolution limit for RNA by motional couplings. Nat. Methods 2008, 5:243-245.
78. Frank A.T., Stelzer A.C., Al-Hashimi H.M., Andricioaei I. Constructing RNA dynamical ensembles by combining MD and motionally decoupled NMR RDCs: new insights into RNA dynamics and adaptive ligand recognition. Nucleic Acids Res. 2009, 37:3670-3679.
79. Fisher C.K., Al-Hashimi H.M. Approximate reconstruction of continuous spatially complex domain motions by multialignment NMR residual dipolar couplings. J. Phys. Chem. B 2009, 113:6173-6176.
80. Lawrence D.C., Stover C.C., Noznitsky J., Wu Z.R., Summers M.F. Structure of the intact stem and bulge of HIV-1 Ψ-RNA stem loop SL1. J. Mol. Biol. 2003, 326:529-542.
81. Zuo X., Wang J., Foster T.R., Schwieters C.D., Tiede D.M., Butcher S.E., Wang Y.X. Global molecular structure and interfaces: refining an RNA:RNA complex structure using solution X-ray scattering data. J. Am. Chem. Soc. 2008, 130:3292-3293.
82. Walsh J.D., Wang Y.X. Periodicity, planarity, residual dipolar coupling, and structures. J. Magn. Reson. 2005, 174:152-162.
83. Walsh J.D., Cabello-Villegas J., Wang Y.X. Periodicity in residual dipolar couplings and nucleic acid structures. J. Am. Chem. Soc. 2004, 126:1938-1939.
84. Wang J., Walsh J.D., Kuszewski J., Wang Y.X. Periodicity, planarity, and pixel (3P): a program using the intrinsic residual dipolar coupling periodicity-to-peptide plane correlation and phi/psi angles to derive protein backbone structures. J. Magn. Reson. 2007, 189:90-103.
85. Grishaev A., Ying J., Bax A. Pseudo-CSA restraints for NMR refinement of nucleic acid structures. J. Am. Chem. Soc. 2006, 128:10010-10011.
86. Davis J.H., Tonelli M., Scott L.G., Jaeger L., Williamson J.R., Butcher S.E. RNA helical packing in solution: NMR structure of a 30 kDa GAAA tetraloop-receptor complex. J. Mol. Biol. 2005, 351:371-382.
87. Staple D.W., Butcher S.E. Solution structure and thermodynamic investigation of the HIV-1 frameshift inducing element. J. Mol. Biol. 2005, 349:1011-1023.
88. Kim N.K., Zhang Q., Zhou J., Theimer C.A., Peterson R.D., Feigon J. Solution structure and dynamics of the wild-type pseudoknot of human telomerase RNA. J. Mol. Biol. 2008, 384:1249-1261.
89. Skrisovska L., Bourgeois C.F., Stefl R., Grellscheid S.N., Kister L., Wenter P., et al. The testis-specific human protein RBMY recognizes RNA through a novel mode of interaction. EMBO Rep. 2007, 8:372-379.
90. Zhang Q., Sun X., Watt E.D., Al-Hashimi H.M. Resolving the motional modes that code for RNA adaptation. Science 2006, 311:653-656.
91. Zhang Q., Stelzer A.C., Fisher C.K., Al-Hashimi H.M. Visualizing spatially correlated dynamics that directs RNA conformational transitions. Nature 2007, 450:1263-1267.
92. Kato T., Goodman R.P., Erben C.M., Turberfield A.J., Namba K. High-resolution structural analysis of a DNA nanostructure by cryoEM. Nano Lett. 2009, 9:2747-2750.
93. Nissen P., Ippolito J.A., Ban N., Moore P.B., Steitz T.A. RNA tertiary interactions in the large ribosomal subunit: the A-minor motif. Proc. Natl Acad. Sci. USA 2001, 98:4899-4903.
94. Klein D.J., Schmeing T.M., Moore P.B., Steitz T.A. The kink-turn: a new RNA secondary structure motif. EMBO J. 2001, 20:4214-4221.
95. Wang J., Zuo X., Yu P., Xu H., Starich M.R., Tiede D.M., et al. A method for helical RNA global structure determination in solution using small-angle x-ray scattering and NMR measurements. J. Mol. Biol. 2009, 393:717-734.
96. Wang Y.X., Zuo X., Wang J., Yu P., Butcher S.E. Rapid global structure determination of large RNA and RNA complexes using NMR and small-angle X-ray scattering. Methods 2010, 52:180-191.
97. Yang S., Temin H.M. A double hairpin structure is necessary for the efficient encapsidation of spleen necrosis virus retroviral RNA. EMBO J. 1994, 13:713-726.
98. Mougel M., Zhang Y., Barklis E. cis-active structural motifs involved in specific encapsidation of Moloney murine leukemia virus RNA. J. Virol. 1996, 70:5043-5050.
99. Fisher J., Goff S.P. Mutational analysis of stem-loops in the RNA packaging signal of the Moloney murine leukemia virus. Virology 1998, 244:133-145.
100. Miyazaki Y., Garcia E., King S.R., Iyalla K., Loeliger K., Starck P., et al. An RNA structural switch regulates diploid genome packaging by Moloney murine leukemia virus. J. Mol. Biol. 2010, 396:141-152.
101. Jouvenet N., Simon S.M., Bieniasz P.D. Imaging the interaction of HIV-1 genomes and Gag during assembly of individual viral particles. Proc. Natl Acad. Sci. USA 2009, 106:19114-19119.
102. Dey A., York D., Smalls-Mantey A., Summers M.F. Composition and sequence dependent binding of RNA to the nucleocapsid protein of Moloney murine leukemia virus. Biochemistry 2005, 44:3735-3744.
103. Rabi J.A., Fox J.J. Nucleosides. LXXIX. Facile base-catalyzed hydrogen isotope labeling at position 6 of pyrimidine nucleosides. J. Am. Chem. Soc. 1973, 95:1628-1632.
104. Goodman L. Chemical synthesis and transformations of nucleosides. Basic Principles in Nucleic Acid Chemistry 1974, vol. 1:170-208. Academic Press, New York, NY. P.O.P. Ts'o (Ed.).
105. Milligan J.F., Uhlenbeck O.C. Synthesis of small RNAs using T7 RNA polymerase. Methods Enzymol. 1989, 180:51-62.
106. Pfeiffer J.K., Topping R.S., Shin N.H., Telesnitsky A. Altering the intracellular environment increases the frequency of tandem repeat deletion during Moloney murine leukemia virus reverse transcription. J. Virol. 1999, 73:8441-8447.
107. Yang S., Delgado R., King S.R., Woffendin C., Barker C.S., Yang Z.Y., et al. Generation of retroviral vector for clinical studies using transient transfection. Hum. Gene Ther. 1999, 10:123-132.
108. Ausubel F.M., Brent R., Kingston R.E., Moore D.D., Smith J.A., Struhl K. Current Protocols in Molecular Biology 1994, John Wiley and Sons, Inc., New York.
109. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., Bax A. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 1995, 6:277-293.
110. Johnson B.A., Blevins R.A. NMRView: a computer program for the visualization and analysis of NMR data. J. Biomol. NMR 1994, 4:603-614.
111. Jeener J., Meier B.H., Bachmann P., Ernst R.R. Investigation of exchange processes by two-dimensional NMR spectroscopy. J. Chem. Phys. 1979, 71:4546-4553.
112. Macura S., Ernst R.R. Elucidation of cross relaxation in liquids by two-dimensional NMR spectroscopy. Mol. Phys. 1980, 41:95-117.
113. Güntert P., Mumenthaler C., Wüthrich K. Torsion angle dynamics for protein structure calculations with a new program, DYANA. J. Mol. Biol. 1997, 273:283-298.
114. Case D.A. AMBER 7 User's Manual 2002, University of California, San Francisco, CA.
115. Saenger W. Principles of Nucleic Acid Structure 1984, Springer-Verlag, New York, NY.
116. Mastronarde D.N. Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 2005, 152:36-51.
117. Kremer J.R., Mastronarde D.N., McIntosh J.R. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 1996, 116:71-76.
118. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., Ferrin T.E. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 2004, 25:1605-1612.
119. Schmid M.F., Booth C.R. Methods for aligning and for averaging 3D volumes with missing data. J. Struct. Biol. 2008, 161:243-248.
120. Davis I.W., Leaver-Fay A., Chen V.B., Block J.N., Kapral G.J., Wang X., et al. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 2007, 35:W375-W383.