Structural modeling of sequence specificity by an autoantibody against single-stranded DNA

Biochemistry

Volumn 46, Issue 23, 2007, Pages 6753-6765

  Bobeck, Melissa J ^a   Rueda, David ^a,b   Walter, Nils G ^a   Glick, Gary D ^a,c  

^a UNIVERSITY OF MICHIGAN   (United States)

^b WAYNE STATE UNIVERSITY   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODIES; BINDING SITES; ENERGY TRANSFER; FLUORESCENCE; FREE ENERGY; MUTAGENESIS; NUCLEOTIDES;

DOMINANT SOMATIC MUTATION; FLUORESCENCE RESONANCE; INTERMOLECULAR DISTANCES; STRUCTURAL MODELING;

DNA SEQUENCES;

ARGININE; AUTOANTIBODY; HYDROGEN; NUCLEOTIDE; SINGLE STRANDED DNA; THYMINE;

ARTICLE; BINDING AFFINITY; BINDING SITE; COMPLEMENTARITY DETERMINING REGION; COMPLEX FORMATION; CRYSTAL STRUCTURE; CRYSTALLIZATION; DNA BINDING; DNA SEQUENCE; FLUORESCENCE RESONANCE ENERGY TRANSFER; HYDROGEN BOND; MOLECULAR MODEL; MOLECULAR RECOGNITION; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SOMATIC MUTATION;

ANIMALS; ANTIBODY SPECIFICITY; AUTOANTIBODIES; BASE SEQUENCE; DNA, SINGLE-STRANDED; HYDROGEN BONDING; LIGANDS; MICE; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; SPECTROMETRY, FLUORESCENCE; THERMODYNAMICS;

EID: 34250358312     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi700212s     Document Type: Article

References (89)

1. Bochkarev, A., and Bochkareva, E. (2004) From RPA to BR-CA2: Lessons from single-stranded DNA binding by the OB-fold, Curr. Opin. Struct. Biol. 14, 36-42.
2. Kur, J., Olszewski, M., Dlugolecka, A., and Filipkowski, P. (2005) Single-stranded DNA-binding proteins (SSBs): Sources and applications in molecular biology, Acta Biochim. Pol. 52, 569-574.
3. Desveaux, D., Allard, J., Brisson, N., and Sygusch, J. (2002) A new family of plant transcription factors displays a novel ssDNA-binding surface, Nat. Struct. Biol. 9, 512-517.
4. Kusakabe, T., Hine, A. V., Hyberts, S. G., and Richardson, C. C. (1999) The Cys4 zinc finger of bacteriophage T7 primase in sequence-specific single-stranded DNA recognition, Proc. Natl. Acad. Sci. U.S.A. 96, 4295-4300.
5. Stassen, A. P., Folmer, R. H., Hilbers, C. W., and Konings, R. N. (1994) Single-stranded DNA binding protein encoded by the filamentous bacteriophage M13: Structural and functional characteristics, Mol. Biol. Rep. 20, 109-127.
6. Myong, S., Rasnik, 1., Joo, C., Lohman, T. M., and Ha, T. (2005) Repetitive shuttling of a motor protein on DNA, Nature 437, 1321-1325.
7. Mitton-Fry, R. M., Anderson, E. M., Theobald, D. L., Glustrom, L. W., and Wuttke, D. S. (2004) Structural basis for telomeric single-stranded DNA recognition by yeast Cdc13, J. Mol. Biol. 338, 241-255.
8. Theobald, D. L., and Schultz, S. C. (2003) Nucleotide shuffling and ssDNA recognition in Oxytricha nova telomere end-bidning protein complexes, EMBO J. 22, 4314-4324.
9. Chothia, C., and Lesk, A. M. (1987) Canonical Structures for the Hypervariable Regions of Immunoglobulins, J. Mol. Biol. 196, 901-917.
10. Waldman, M., and Madaio, M. P. (2005) Pathogenic autoantibodies in lupus nephritis, Lupus 14, 19-24.
11. Tsao, B. P., Ebling, F. M., Roman, C., Panisian-Sahakian, N., Calame, K., and Hahn, B. H. (1990) Structural characterization of the variable regions of immunogloulin genes encoding a pathogenic autoantibody in murine lupus, J. Clin. Invest. 85, 530-540.
12. Ravirajan, C. T., Rahman, M. A., Papadaki, L., Griffiths, M. H., Kalsi, J. K., Martin, A. C. R., Ehrenstein, M. R., Latchman, D. S., and Isenberg, D. A. (1998) Genetic, structural and functional properties of an IgG DNA-binding monoclonal antibody from a lupus patient with nephritis, Eur. J. Immunol. 28, 339-350.
13. Foster, M. H., Cizman, B., and Madaio, M. P. (1993) Biology of Disease. Nephritogenic autoantibodies in systemic lupus erythematosus: Immunochemical properties, mechanisms of immune deposition, and genetic origins, Lab. Invest. 69, 494-507.
14. Koffler, D., Carr, D., Agnello, V., Thiburn, R., and Kunkel, H. G. (1971) Antibodies to polynucleotide in sera: Antigenic specificity and relation to disease, J. Exp. Med. 134, 294-312.
15. Katz, J. B., Limpanasithikul, W., and Diamond, B. (1994) Mutational analysis of an autoantibody: Differential binidng and pathogenicity, J. Exp. Med. 180, 925-932.
16. Swanson, P. C., Ackroyd, C., and Glick, G. D. (1996) Ligand recognition by anti-DNA autoantibodies. Affinity, specificity, and mode of binding, Biochemistry 35, 1624-1633.
17. Swanson, P. C., Yung, R. L., Blatt, N. B., Eagan, M. A., Norris, J. M., Richardson, B. C., Johnson, K. J., and Glick, G. D. (1996) Ligand recogition by murine anti-DNA antibodies. II. Genetic analysis and pathogenicity, J. Clin. Invest. 97, 1-13.
18. Stevens, S. Y., and Glick, G. D. (1999) Evidence for sequence-specific recognition of DNA by anti-single-stranded DNA autoantibodies, Biochemists 38, 560-568.
19. Cleary, J., and Glick, G. D. (2003) Mutational Analysis of a Sequence-Specific ssDNA Binding Lupus Autoantibody, Biochemistry 42, 30-41.
20. Bendich, A. J., and Bolton, E. T. (1968) The DNA-Agar Procedure, Methods Enzymol. 12B, 635-640.
21. Mach, H., Middaugh, C. R., and Lewis, R. V. (1992) Statistical determination of the average values of the extinction coefficients of trypotphan and tyrosine in native proteins, Anal. Biochem. 200, 74-80.
22. Haugland, R. P. (2005) Handbook of Fluorescent Probes and Research Products, 9th ed., Molecular Probes, Eugene, OR.
23. Ackroyd, P. C., Cleary, J., and Glick, G. D. (2001) Thermodynamic basis for sequence-specific recognition of ssDNA by an autoantibody, Biochemistry 40, 2911-2922.
24. Walter, N. G. (2002) Probing RNA structural dynamics and function by fluorescence resonance energy transfer (FRET), Curr. Protoc. Nucleic Acid Chem. 11.10, 11.10.11-11.10.23.
25. Haas, E., Katchalski-Katzir, E., and Steinberg, I. Z. (1978) Effect of the Orientation of Donor and Acceptor on the Probability of Energy Transfer Involving Electronic Transitions of Mixed Polarization, Biochemistry 17, 5064-5070.
26. Walter, N. G., Burke, J. M., and Millar, D. P. (1999) Stability of hairpin ribozyme tertiary structure is governed by the interdomain junction, Nat. Struct. Biol. 6, 544-549.
27. Pereira, M. J. B., Harris, D. A., Rueda, D., and Walter, N. G. (2002) Reaction Pathway of the Trans-Acting Hepatitis Delta Virus Ribozyme: A Conformational Change Accompanies Catalysis, Biochemists 41, 730-740.
28. 2+ ions slightly reoirent stems I and II of the hammerhead ribozyme to increase the probability of formation of the catalytic core, Biochemists 42, 9924-9936.
29. Walter, N. G., and Burke, J. M. (2000) Fluorescence assays to study structure, dynamics, and function of RNA and RNA-ligand interactions, Methods Enzymol. 317, 409-440.
30. Chothia, C., Lesk, A. M., Levitt, M., Amit, A. G., Mariuzza, R. A., Phillips, S. E. V., and Poljak, R. J. (1986) The predicted structure of immunoglobulin D1.3 and its comparison with the crystal structure, Science 233, 755-758.
31. Eagan, M. A., Norris, J. M., Cooper, B. C., and Glick, G. D. (1995) Structural patterns in anti-DNA autoantibodies: A molecular modeling study, Bioorg. Chem. 23, 482-498.
32. Mueller, F., Doring, T., Erdemir, T., Greuer, B., Junke, N., Osswald, M., Rinke-Appel, J., Stade, K., Thamm, S., and Brimacombe, R. (1995) Getting closer to an understanding of the three-dimensional structure of ribosomal RNA, Biochem. Cell Biol. 73, 767-773.
33. Mueller, F., and Brimacombe, R. (1997) A New Model for the Three-dimensional Folding of Escherichia coli 16S Ribosomal RNA. I. Fitting the RNA to a 3D Electron Microscopic Map at 20 Å, J. Mol. Biol. 271, 524-544.
34. Dominguez, C., Boelens, R., and Bonvin, A. M. J. J. (2003) HADDOCK: A Protien-Protein Docking Approach Based on Biochemical or Biophysical Information, J. Am. Chem. Soc. 125, 1731-1737.
35. Tanner, J. J., Komissarov, A. A., and Deutscher, S. L. (2001) Crystal structure of an antigen-binding fragment bound to single-stranded DNA, J. Mol. Biol. 314, 807-822.
36. Herron, J. N., He, X. M., Ballard, D. W., Blier, P. R., Pace, P. E., Blothwell, A. L. M., Voss, E. W. J., and Edmundson, A. B. (1991) An autoantibody to single-stranded DNA: A comparison of the three-dimentional structures of the unliganded Fab and a deoxynucleotide-Fab complex, Proteins 11, 159-175.
37. Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R., and Thornton, J. M. (1996) AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR, J. Biomol. NMR 8, 477-486.
38. Furey, W. S., Joyce, C. M., Osborne, M. A., Klenerman, D., Peliska, J. A., and Blasubramanian, S. (1998) Use of fluorescence resonance energy transfer to investigate the conformation of DNA substrates bound to the Klenow fragment, Biochemists 37, 2979-2990.
39. Kohler, J. J., and Schepartz, A. (2001) Kinetic Studies of Fos*Jun*DNA Complex Formation: DNA Binding Prior to Dimerization, Biochemistry 40, 130-142.
40. Stryer, L. (1978) Fluorescence Energy Transfer as a Spectroscopic Ruler, Annu. Rev. Biochem. 47, 819-846.
41. DiPilato, L. M., Cheng, X., and Zhang, J. (2004) Fluorescent indicators of cAMP and Epac activation reveal differential dynamics of cAMP signaling within discrete subcellular compartments, Proc. Natl. Acad. Sci. U.S.A. 101, 16513-16518.
42. Beckingham, J. A., and Glick, G. D. (2001) Sequence specific recognition of ssDNA by a lupus autoantibody: Kinetics and mechanism of binding, Bioorg. Med. Chem. 9, 2243-2252.
43. Beckingham, J. A., Cleary, J., Bobeck, M. J., and Glick, G. D. (2003) Kinetic Analysis of Sequence-Specific Recognition of ssDNA by an Autoantibody, Biochemistry 42, 4118-4126.
44. Ratner, V., Kahana, E., Eichler, M., and Haas, E. (2002) A General Strategy for Site-Specific Double Labeling of Globular Proteins for Kinetic FRET Studies, Bioconjugate Chem. 13, 1163-1170.
45. Bobeck, M. J., Cleary, J., Beckingham, J. A., Ackroyd, P. C., and Glick, G. D. (2007) Effect of Somatic Mutation on DNA Binding Properties of Anti-DNA Autoantibodies, Biopolymers (in press).
46. Paula, S., Monson, N., and Ball, W. J. J. (2005) Molecular Modeling of Cardiac Glycoside Binding by the Human Sequence Monoclonal Antibody 1B3, Proteins 60, 382-391.
47. Kim, Y.-R., Kim, J.-S., Lee, S.-H., Lee, W.-R., Sohn, J.-N., Chung, Y.-C., Shim, H.K., Lee, S.-C., Kwon, M.-H., and Kim, Y.-S. (2006) Heavy and Light Chain Variable Single Domains of an Anti-DNA Binding Antibody Hydrolyze Both Double- and Single-stranded DNAs without Sequence Specificity, J. Biol. Chem. 281, 15287-15295.
48. Pellequer, J.-L., Chen, S.-w. W., Keum, Y.-s., Karu, A. E., Li, Q. X., and Roberts, V. A. (2005) Structural basis for preferential binding of non-ortho-substituted polychlorinated biphenyls by the monoclonar antibody S2B1, J. Mol. Recognit. 18, 282-294.
49. Swanson, P. C. (1995) Anti-DNA autoantibodies from a lupusprone mouse: Ligand binding properties, structure and pathogenicity, Ph.D. Thesis, University of Michigan, Ann Arbor, MI.
50. Lopez, M. M., Yutani, K., and Makhatadze, G. I. (2001) Interactions of the Cold Shock Protein CspB from Bacillus subtilis with Single-Stranded DNA, J. Biol. Chem. 18, 15511-15518.
51. Theobald, D. L., Mitton-Fry, R. M., and Wuttke, D. S. (2003) Nucleic Acid Recognition by OB-Fold Proteins, Annu. Rev. Biophys. Biomol. Struct. 32, 115-133.
52. Horvath, M. P. S., Bevilacqua, J. M., Ruggles, J. A., and Schultz, S. C. (1998) Crystal Structure of the Oxytricha nova Telomere End Binding Protein Complexed with Single Stranded DNA, Cell 95, 963-974.
53. Larkin, C., Datta, S., Harley, M. J., Anderson, B. J., Ebie, A., Hargreaves, V., and Schildbach, J. F. (2005) Inter- and intramolecular determinants of the specificity of single-stranded DNA binding and cleavage by the F factor relaxase, Structure 10, 1533-1544.
54. Liu, Y., Yang, Z., Utzat, C. D., Liu, Y., Geacintov, N. E., Basu, A. K., and Zou, Y. (2005) Interactions of human replication protein A with single-stranded DNA adducts, Biochem. J. 385, 519-526.
55. Wojciechowski, M., Fogolari, F., and Baginski, M. (2005) Thermodynamic and electrostatic properties of ternary Oxytricha nova TEBP-DNA complex, J. Struct. Biol. 152, 169-184.
56. Rouzina, I., Pant, K., Karpel, R. L., and Williams, M. C. (2005) Theory of Electrostatically Regulated Binding of T4 Gene 32 Protein to Single- and Double-Stranded DNA, Biophys. J. 89, 1941-1956.
57. Bugreeva, I. P., Bugreev, D. V., and Nevinsky, G. A. (2005) Formation of nucleoprotein RecA filament on single-stranded DNA: Analysis by stepwise increase in ligand complexity, FEBS J. 272, 2734-2745.
58. Stern, J. C., Aderson, B. J., Owens, T. J., and Schildbach, J. F. (2004) Energetics of the Sequence-specific Binding of Single-stranded DNA by the F Factor Relaxase Domain, J. Biol. Chem. 279, 29155-29159.
59. Hoffman, M. M., Khrapov, M. A., Cox, J. C., Yao, J., Tong, L., and Ellington, A. D. (2004) AANT: The Amino Acid-Nucleotide Interaction Database, Nucleic Acids Res. 32, D174-D181.
60. Haley, J., Mason, L. J., Nagl, S., Giles, I., Latchman, D. S., Isenberg, D. A., and Rahman, A. (2004) Somatic mutations to arginine residues affect the binding of human monoclonal antibod-ies to DNA, histories, SmD and Ro antigen, Mol. Immunol. 40, 745-758.
61. Wilkinson, T. A., Botuyan, M. V., Kaplan, B. E., Rossi, J. J., and Chen, Y. (2000) Arginine side-chain dynamics in the HIV-1 Rev-RRE complex, J. Mol. Biol. 303, 515-529.
62. Wintjens, R., Lievin, J., Rooman, M., and Buisine, E. (2000) Contribution of cation-π interactions to the stability of protein-DNA complexes, J. Mol. Biol. 302, 395-410.
63. Allain, F. H.-T., Howe, P. W. A., Neuhaus, D., and Varani, G. (1997) Structural basis of the RNA-binding specificity of human U1A protein, EMBO J. 16, 5764-5774.
64. GuhaThakurta, D., and Draper, D. E. (2000) Contribution of basic residues to ribosomal protein L11 recognition of RNA, J. Mol. Biol. 295, 569-580.
65. Luscombe, N. M., Austin, S. E., Barman, H. M., and Thorton, J. M. (2001) An overview of the structures of protein-DNA complexes, Genome Biol. 1, 1-37.
66. Izatt, R. M., Bradshaw, J. S., Pawlak, K., Bruening, R. L., and Tarbet, B. J. (1992) Thermodynamic and kinetic data for macro-cycle interaction with neutral molecules, Chem. Rev. 92, 1261-1354.
67. Gallivan, J. P., and Dougherty, D. A. (1999) Cation-π interactions in structural biology, Proc. Natl. Acad. Sci. U.S.A. 96, 9459-9464.
68. Gromiha, M. M., Santhosh, C., and Ahmad, S. (2004) Structural analysis of cation-π interactions in DNA binding proteins, Int. J. Biol. Macromol. 24, 203-211.
69. Lamoureux, J. S., and Glover, J. N. (2006) Principles of protein-DNA recognition revealed in the structural analysis of Ndt80-MSE DNA complexes, Structure 14, 555-565.
70. Trotta, C. R., Paushkin, S. V., Patel, M., Li, H., and Peltz, S. W. (2006) Cleavage of pre-tRNAs by the splicing endonuclease requires a composite active site, Nature 441, 375-377.
71. Cheng, A. C., Chen, W. W., Fuhrmann, C. N., and Frankel, A. D. (2003) Recognition of Nucleic Acid Bases and Base-pairs by Hydrogen Bonding to Amino Acid Side Chains, J. Mol. Biol. 327, 781-796.
72. Xiaomei, Y., Ellington, G. A., and Patel, D. J. (1996) Deep penetration of an α-helix into a widened RNA major groove in the HIV-1 rev peptide-RNA aptamer complex, Nat. Struct. Biol. 3, 1026-1033.
73. Allain, F. H.-T., Bouvet, P., Dieckmann, T., and Feigon, J. (2000) Molecular basis of sequence-specific recognition of pre-ribosomal RNA by nucleolin, EMBO J. 19, 6870-6881.
74. Jamieson, A. C., Wang, H., and Kim, S.-H. (1996) A zinc finger directory for high-affinity DNA recognition, Proc. Natl. Acad. Sci. U.S.A. 93, 12834-12839.
75. Moulinier, L., Elier, S., Eriani, G., Gangloff, J., Thierry, J.-C., Gabriel, K., McClain, W. H., and Moras, D. (2001) The structure of an AspRS-tRNAASP complex reveals a tRNA-dependent control mechanism, EMBO J. 20, 5290-5301.
76. Oubridge, C., Ito, H., Evans, P. R., Teo, C. H., and Nagai, K. (1994) Crystal structure at 1.92 Angstrom resolution of the RNA-binding domain of the U1A spliceosomal protein complexed with an RNA hairpin, Nature 372, 432-438.
77. Sekine, S., Nureki, O., Shimada, A., Vassylyev, D. G., and Yoloyama, S. (2001) Structural basis for anticodon recognition by discriminating glutamyl-tRNA synthetase, Nat. Struct. Biol. 8, 203-206.
78. Schulze, J. O., Masoumi, A., Nickel, D., Jahn, M., Jahn, D., Schubert, W.-D., and Heinz, D. W. (2006) Crystal Structure of a Non-discriminating Glutamyl-tRNA Synthetase, J. Mol. Biol. 361, 888-897.
79. Hermann, T., and Patel, D. J. (2000) Adaptive Recognition by Nucleic Acid Aptamers, Science 287, 820-825.
80. Norman, D. P. G., Bruner, S. D., and Verdine, G. L. (2001) Coupling of Substrate Recognitino and Catalysis by a Human Base-Excision DNA Repair Protein, J. Am. Chem. Soc. 123, 359-360.
81. Agalarov, S. C., Prasad, S., Funke, P. M., Stout, C. D., and Williamson, J. R. (2000) Structure of the S15,S6,S18-rRNA Complex: Assembly of the 30S Ribosome Central Domain, Science 288, 107-112.
82. Radic, M. Z., and Weigert, M. (1994) Genetic and structural evidence for antigen selection of anti-DNA antibodies, Annu. Rev. Immunol. 12, 487-520.
83. Blatt, N. B., Bill, R. M., and Glick, G. D. (1998) Characterization of a unique anti-DNA hybridoma, Hybridoma 17, 33-39.
84. Eilat, D. (1990) The role of germline gene expresssion and somatic mutation in the generation of autoantibodies to DNA, Mol. Immunol. 27, 203-210.
85. Shlomchik, M., Mascelli, H., Shan, H., Radic, M. Z., Pisetsky, D., Rothstein-Marshak, A., and Weigert, M. (1990) Anti-DNA antibodies from autoimmune mice arise by clonal expansion and somatic mutation, J. Exp. Med. 171, 265-297.
86. Radic, M. Z., Mascelli, M. A., Erikson, J., Shan, H., Shlomchik, M., and Weigert, M. (1989) Structural patterns in anti-DNA antibodies from MRL/lpr mice, Cold Spring Harbor Symp. Quant. Biol. 54, 933-946.
87. Ramirez-Benitez, M. D. C., and Almagro, J. C. (2001) Analysis of Antibodies of Known Structure Suggests a Lack of Correspondence Between the Residues in Contact With the Antigen and Those Modified by Somatic Hypermutation, Proteins: Struct., Fund., Bioinf. 45, 199-206.
88. Li, Y., Hongmin, L., Yang, F., Smith-Gill, S. J., and Mariuzza, R. A. (2003) X-ray snapshots of the maturation of an antibody response to a protein antigen, Nat. Struct. Biol. 10, 482-488.
89. Aharoni, A., Gaidukov, L., Khersonsky, O., Gould, S. M., Roodveldt, C., and Tawfik, S. (2005) The 'evolvability' of promiscuous protein functions, Nat. Genet. 37, 73-76.