Estimation of interdomain flexibility of N-terminus of factor H using residual dipolar couplings

Biochemistry

Volumn 50, Issue 38, 2011, Pages 8138-8149

  MacIejewski, Mateusz ^a,b   Tjandra, Nico ^a   Barlow, Paul N ^b  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID RESIDUES; BICELLES; BIOLOGICAL MECHANISMS; DATA SETS; DISK-LIKE PARTICLE; DIVERSE PROTEINS; HUMAN FACTOR H; INTER-DOMAIN; LOCAL DYNAMICS; N-TERMINAL DOMAINS; NUCLEAR OVERHAUSER EFFECTS; PROTEIN FRAGMENTS; RESIDUAL DIPOLAR COUPLINGS; SOLVED CRYSTAL STRUCTURES; THREE-DIMENSIONAL SOLUTIONS;

AMINO ACIDS; CRYSTAL STRUCTURE; HUMAN ENGINEERING; NUCLEAR MAGNETIC RESONANCE; PHOSPHOLIPIDS; PROTEINS;

FLEXIBLE COUPLINGS;

COMPLEMENT FACTOR H; PEPTIDE FRAGMENT; PHOSPHOLIPID; PROTEIN C3B; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN STRUCTURE;

COMPLEMENT ACTIVATION; COMPLEMENT C3B; COMPLEMENT FACTOR H; HUMANS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECOMBINANT PROTEINS;

SUGARCANE RAMU STUNT DISEASE PHYTOPLASMA;

EID: 80053025476     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200575b     Document Type: Article

References (58)

1. Litman, G. W., Cannon, J. P., and Dishaw, L. J. (2005) Reconstructing immune phylogeny: new perspectives Nat. Rev. Immunol. 5, 866-879 (Pubitemid 41581668)
2. Hoebe, K., Janssen, E., and Beutler, B. (2004) The interface between innate and adaptive immunity Nature Immunol. 5, 971-974 (Pubitemid 41057712)
3. Apic, G., Gough, J., and Teichmann, S. A. (2001) Domain combinations in archaeal, eubacterial and eukaryotic proteomes J. Mol. Biol. 310, 311-325 (Pubitemid 32664871)
4. Bork, P., Downing, A. K., Kieffer, B., and Campbell, I. D. (1996) Structure and distribution of modules in extracellular proteins Q. Rev. Biophys. 29, 119-167 (Pubitemid 26280788)
5. Ekman, D., Björklund, A. K., Frey-Skött, J., and Elofsson, A. (2005) Multi-domain proteins in the three kingdoms of life: orphan domains and other unassigned regions J. Mol. Biol. 348, 231-243 (Pubitemid 40461853)
6. Walport, M. J. (2001) Complement N. Engl. J. Med. 344, 1058-1066
7. Ricklin, D., Hajishengallis, G., Yang, K., and Lambris, J. D. (2010) Complement: a key system for immune surveillance and homeostasis Nature Immunol. 11, 785-797
8. Lachmann, P. J. (2009) The Amplification Loop of the Complement Pathways Adv. Immunol. 104, 115-149
9. Kirkitadze, M. D. and Barlow, P. N. (2001) Structure and flexibility of the multiple domain proteins that regulate complement activation Immunol. Rev. 180, 146-161 (Pubitemid 32472859)
10. Hourcade, D., Holers, V. M., and Atkinson, J. P. (1989) The regulators of complement activation (RCA) gene cluster Adv. Immunol. 45, 381-416 (Pubitemid 19195511)
11. Reid, K. and Day, A. J. (1989) Structure-function relationships of the complement components Immunol. Today 10, 177-180 (Pubitemid 19133695)
12. Soares, D. C. and Barlow, P. N. (2005) Complement Control Protein Modules in the Regulators of Complement Activation, in Structural Biology of the Complement System, pp 19-62, CRC Press, Boca Raton, FL.
13. Soares, D. C., Gerloff, D. L., Syme, N. R., Coulson, A. F. W., Parkinson, J., and Barlow, P. N. (2005) Large-scale modelling as a route to multiple surface comparisons of the CCP module family Protein Eng., Des. Sel. 18, 379-388 (Pubitemid 41187254)
14. Barlow, P. N., Baron, M., Norman, D. G., Day, A. J., Willis, A. C., Sim, R. B., and Campbell, I. D. (1991) Secondary structure of a complement control protein module by two-dimensional 1H NMR Biochemistry 30, 997-1004
15. Norman, D. G., Barlow, P. N., Baron, M., Day, A. J., Sim, R. B., and Campbell, I. D. (1991) Three-dimensional structure of a complement control protein module in solution J. Mol. Biol. 219, 717-725 (Pubitemid 121003544)
16. Barlow, P. N., Stainkasserer, A., Norman, D. G., Kieffer, B., Wiles, A. P., Sim, R. B., and Campbell, I. D. (1993) Solution Structure of a Pair of Complement Modules by Nuclear Magnetic Resonance J. Mol. Biol. 232, 268-284 (Pubitemid 23245413)
17. Weisman, H. F., Bartow, T., Leppo, M. K., Marsh, H. C., Carson, G. R., Concino, M. F., Boyle, M. P., Roux, K. H., Weisfeldt, M. L., and Fearon, D. T. (1990) Soluble Human Complement Receptor Type 1: In Vivo Inhibitor of Complement Suppressing Post- Ischemic Myocardial Inflammation and Necrosis Science 249, 146-151
18. DiScipio, R. G. (1992) Ultrastructures and Interactions of Complement Factors H and I J. Immunol. 149, 2592-2599
19. Kirkitadze, M. D., Krych, M., Uhrín, D., Dryden, D. T. F., Smith, B. O., Cooper, A., Wang, X., Hauhart, R., Atkinson, J. P., and Barlow, P. N. (1999) Independently Melting Modules and Highly Structured Intermodular Junctions within Complement Receptor Type 1 Biochemistry 38, 7019-7031
20. Kirkitadze, M. D., Dryden, D. T. F., Kelly, S. M., Price, N. C., Wang, X., Krych, M., Atkinson, J. P., and Barlow, P. N. (1999) Co-operativity between modules within a C3b-binding site of complement receptor type 1 FEBS Lett. 459, 133-138 (Pubitemid 29447670)
21. Henderson, C. E., Bromek, K., Mullin, N. P., Smith, B. O., Uhrín, D., and Barlow, P. N. (2001) Solution structure and dynamics of the central CCP module pair of a poxvirus complement control protein J. Mol. Biol. 307, 323-339 (Pubitemid 33029985)
22. Kirkitadze, M. D., Henderson, C., Price, N. C., Kelly, S. M., Mullin, N. P., Parkinson, J., Dryden, D. T., and Barlow, P. N. (1999) Central modules of the vaccinia virus complement control protein are not in extensive contact Biochem. J. 344, 167-175
23. Okemefuna, A. I., Nan, R., Gor, J., and Perkins, S. J. (2009) Electrostatic interactions contribute to the folded-back conformation of wild type human factor H J. Mol. Biol. 391, 98-118
24. Furtado, P. B., Huang, C. Y., Ihyembe, D., Hammond, R. A., Marsh, H. C., and Perkins, S. J. (2008) The partly folded back solution structure arrangement of the 30 SCR domains in human complement receptor type 1 (CR1) permits access to its C3b and C4b ligands J. Mol. Biol. 375, 102-118 (Pubitemid 350160686)
25. Fernando, A. N., Furtado, P. B., Clark, S. J., Gilbert, H. E., Day, A. J., Sim, R. B., and Perkins, S. J. (2007) Associative and structural properties of the region of complement factor H encompassing the Tyr402His disease-related polymorphism and its interactions with heparin J. Mol. Biol. 368, 564-581 (Pubitemid 46483491)
26. Okemefuna, A. I., Gilbert, H. E., Griggs, K. M., Ormsby, R. J., Gordon, D. L., and Perkins, S. J. (2008) The regulatory SCR-1/5 and cell surface-binding SCR-16/20 fragments of factor H reveal partially folded-back solution structures and different self-associative properties J. Mol. Biol. 375, 80-101 (Pubitemid 350161888)
27. Janssen, B. J. C., Christodoulidou, A., McCarthy, A., Lambris, J. D., and Gros, P. (2006) Structure of C3b reveals conformational changes that underlie complement activity Nature 444, 213-216 (Pubitemid 44722062)
28. Ferreira, V. P., Herbert, A. P., Hocking, H. G., Barlow, P. N., and Pangburn, M. K. (2006) Critical role of the C-terminal domains of factor H in regulating complement activation at cell surfaces J. Immunol. 177, 6308-6316 (Pubitemid 44628849)
29. Wu, J., Wu, Y.-Q., Ricklin, D., Janssen, B. J. C., Lambris, J. D., and Gros, P. (2009) Structure of complement fragment C3b-factor H and implications for host protection by complement regulators Nature Immunol. 10, 728-733
30. Gordon, D. L., Kaufman, R. M., Blackmore, T. K., Kwong, J., and Lublin, D. M. (1995) Identification of complement regulatory domains in human factor H J. Immunol. 155, 348-356
31. Hocking, H. G., Herbert, A. P., Kavanagh, D., Soares, D. C., Ferreira, V. P., Pangburn, M. K., Uhrín, D., and Barlow, P. N. (2008) Structure of the N-terminal Region of Complement Factor H and Conformational Implications of Disease-linked Sequence Variations J. Biol. Chem. 283, 9475-9487
32. Schmidt, C. Q., Herbert, A. P., Kavanagh, D., Gandy, C., Fenton, C. J., Blaum, B. S., Lyon, M., Uhrín, D., and Barlow, P. N. (2008) A New Map of Glycosaminoglycan and C3b Binding Sites on Factor H J. Immunol. 181, 2610-2619
33. Tjandra, N. and Bax, A. (1997) Direct Measurement of Distances and Angles in Biomolecules by NMR in a Dilute Liquid Crystalline Medium Science 278, 1111-1114 (Pubitemid 27517889)
34. Chen, K. and Tjandra, N. (2008) Extended Model Free Approach To Analyze Correlation Functions of Multidomain Proteins in the Presence of Motional Coupling J. Am. Chem. Soc. 130, 12745-12751
35. Meiler, J., Prompers, J. J., Peti, W., Griesinger, C., and Brüschweiler, R. (2001) Model-Free Approach to the Dynamic Interpretation of Residual Dipolar Couplings in Globular Proteins J. Am. Chem. Soc. 123, 6098-6107 (Pubitemid 32888479)
36. Lipari, G. and Szabo, A. (1982) Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity J. Am. Chem. Soc. 104, 4546-4559
37. Tolman, J. R. (2002) A Novel Approach to the Retrieval of Structural and Dynamic Information from Residual Dipolar Couplings Using Several Oriented Media in Biomolecular NMR Spectroscopy J. Am. Chem. Soc. 124, 12020-12030
38. Lakomek, N.-A., Walter, K. F. A., Farès, C., Lange, O. F., Groot, B. L., Grubmüller, H., Brüschweiler, R., Munk, A., Becker, S., Meiler, J., and Griesinger, C. (2008) Self-consistent residual dipolar coupling based model-free analysis for the robust determination of nanosecond to microsecond protein dynamics J. Biomol. NMR 41, 139-155
39. Bertini, I., Bianco, C. D., Gelis, I., Katsaros, N., Luchinat, C., Parigi, G., Peana, M., Provenzani, A., Zoroddu, M. A., and Gray, H. B. (2004) Experimentally Exploring the Conformational Space Sampled by Domain Reorientation in Calmodulin Proc. Natl. Acad. Sci. U.S.A. 101, 6841-6846 (Pubitemid 38596405)
40. Bertini, I., Gupta, Y. K., Luchinat, C., Parigi, G., Peana, M., Sgheri, L., and Yuan, J. (2007) Paramagnetism-based NMR restraints provide maximum allowed probabilities for the different conformations of partially independent protein domains J. Am. Chem. Soc. 129, 12786-12794 (Pubitemid 350004491)
41. Bertini, I., Giachetti, A., Luchinat, C., Parigi, G., Petoukhov, M. V., Pierattelli, R., Ravera, E., and Svergun, D. I. (2010) Conformational Space of Flexible Biological Macromolecules from Average Data J. Am. Chem. Soc. 132, 13553-13558
42. Ottiger, M., Delaglio, F., and Bax, A. (1998) Measurement of J and Dipolar Couplings from Simplified Two-Dimensional NMR Spectra J. Magn. Reson. 131, 373-378 (Pubitemid 128450579)
43. Losonczi, J. and Prestegard, J. (1998) Improved dilute bicelle solutions for high-resolution NMR of biological macromolecules J. Biomol. NMR 12, 447-451 (Pubitemid 128511311)
44. Delaglio, F., Grzesiek, S., Vuister, G., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6, 277-293
45. Vranken, W. F., Boucher, W., Stevens, T. J., Fogh, R. H., Pajon, A., Llinas, M., Ulrich, E. L., Markley, J. L., Ionides, J., and Laue, E. D. (2005) The CCPN data model for NMR spectroscopy: Development of a software pipeline Proteins 59, 687-696 (Pubitemid 40695845)
46. Ulrich, E. L., Akutsu, H., Doreleijers, J. F., Harano, Y., Ioannidis, Y. E., Lin, J., Livny, M., Mading, S., Maziuk, D., Miller, Z., Nakatani, E., Schulte, C. F., Tolmie, D. E., Kent Wenger, R., Yao, H., and Markley, J. L. (2007) BioMagResBank Nucleic Acids Res. 36, D402-D408
47. Garrett, D. S., Powers, R., Gronenborn, A. M., and Clore, G. M. (1991) A common sense approach to peak picking in two-, three-, and four-dimensional spectra using automatic computer analysis of contour diagrams J. Magn. Reson. 95, 214-220
48. Schwieters, C. D., Kuszewski, J. J., Tjandra, N., and Marius Clore, G. (2003) The Xplor-NIH NMR molecular structure determination package J. Magn. Reson. 160, 65-73
49. Schwieters, C. D., Kuszewski, J. J., and Marius Clore, G. (2006) Using Xplo NIH for NMR molecular structure determination Prog. Nucl. Magn. Reson. Spectrosc. 48, 47-62
50. McRee, D. E. (1999) XtalView/Xfit-A Versatile Program for Manipulating Atomic Coordinates and Electron Denisty J. Struct. Biol. 125, 156-165 (Pubitemid 29402600)
51. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 26, 283-291
52. Clore, G. M., Gronenborn, A. M., and Bax, A. (1998) A Robust Method for Determining the Magnitude of the Fully Asymmetric Alignment Tensor of Oriented Macromolecules in the Absence of Structural Information J. Magn. Reson. 133, 216-221 (Pubitemid 128450633)
53. Cornilescu, G., Marquardt, J. L., Ottiger, M., and Bax, A. (1998) Validation of protein structure from anisotropic carbonyl chemical shifts in a dilute liquid crystalline phase J. Am. Chem. Soc. 120, 6836-6837 (Pubitemid 28347351)
54. Clore, G. M. and Schwieters, C. D. (2004) How Much Backbone Motion in Ubiquitin Is Required To Account for Dipolar Coupling Data Measured in Multiple Alignment Media as Assessed by Independent Cross-Validation? J. Am. Chem. Soc. 126, 2923-2938 (Pubitemid 38314298)
55. Clore, G. M., Szabo, A., Bax, A., Kay, L. E., Driscoll, P. C., and Gronenborn, A. M. (1990) Deviations from the simple two-parameter model-free approach to the interpretation of nitrogen-15 nuclear magnetic relaxation of proteins J. Am. Chem. Soc. 112, 4989-4991 (Pubitemid 20285925)
56. Bernadó, P., Mylonas, E., Petoukhov, M. V., Blackledge, M., and Svergun, D. I. (2007) Structural Characterization of Flexible Proteins Using Small-Angle X-ray Scattering J. Am. Chem. Soc. 129, 5656-5664 (Pubitemid 46697655)
57. Longinetti, M., Luchinat, C., Parigi, G., and Sgheri, L. (2006) Efficient determination of the most favoured orientations of protein domains from paramagnetic NMR data Inverse Probl. 22, 1485
58. Morgan, H. P., Schmidt, C. Q., Guariento, M., Blaum, B. S., Gillespie, D., Herbert, A. P., Kavanagh, D., Mertens, H. D. T., Svergun, D. I., Johansson, C. M., Uhrín, D., Barlow, P. N., and Hannan, J. P. (2011) Structural basis for engagement by complement factor H of C3b on a self surface Nat. Struct. Mol. Biol. 18, 463-470