Multimerization of solution-state proteins by tetrakis(4-sulfonatophenyl) porphyrin

Biochemistry

Volumn 53, Issue 31, 2014, Pages 5070-5079

  Kokhan, Oleksandr ^a   Ponomarenko, Nina ^a   Pokkuluri, P Raj ^a   Schiffer, Marianne ^a   Tiede, David M ^a  

^a ARGONNE NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINITY; BINDING ENERGY; LIGANDS; MOLECULAR DYNAMICS; PORPHYRINS; STAINLESS STEEL; X RAY SCATTERING; ZINC COMPOUNDS;

ALKALINE CONDITIONS; GEOBACTER SULFURREDUCENS; HIGH SALT CONCENTRATION; HYDROPHOBIC INTERACTIONS; INTERPRETATION OF DATA; MOLECULAR DYNAMICS SIMULATIONS; PROTEIN AGGREGATION; SMALL ANGLE X-RAY SCATTERING;

PROTEINS;

ARGININE; ASPARTIC ACID; CYTOCHROME; CYTOCHROME C; CYTOCHROME C7; GLUTAMIC ACID; HISTIDINE; HYDROGEN; LYSOZYME; PORPHYRIN DERIVATIVE; PROPIONIC ACID; TETRAKIS(4 SULFONATOPHENYL)PORPHYRIN; UNCLASSIFIED DRUG; ZINC;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; COMPARATIVE STUDY; CONTROLLED STUDY; ELECTRON TRANSPORT; FOLLOW UP; GEOBACTER SULFURREDUCENS; HEART; HEN; HORSE; HYDROGEN BOND; HYDROPHOBICITY; IONIC STRENGTH; IONIZATION; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; MOLECULAR WEIGHT; NONHUMAN; PHOTOCHEMICAL QUENCHING; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN MULTIMERIZATION; PROTON TRANSPORT; SOLUTION AND SOLUBILITY; STATIC ELECTRICITY; STOICHIOMETRY; SURFACE PROPERTY; X RAY CRYSTALLOGRAPHY;

ANIMALS; BINDING SITES; CATIONS; CYTOCHROMES C; LIGANDS; METALLOPORPHYRINS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MURAMIDASE; PORPHYRINS; PROTEIN MULTIMERIZATION; SCATTERING, SMALL ANGLE; SOLUTIONS; STATIC ELECTRICITY; X-RAY DIFFRACTION;

EID: 84905983840     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi500278g     Document Type: Article

References (65)

1. Lin, Q., Park, H. S., Hamuro, Y., Lee, C. S., and Hamilton, A. D. (1998) Protein Surface Recognition by Synthetic Agents: Design and Structural Requirements of a Family of Artificial Receptors that Bind to Cytochrome c Biopolymers 47, 285-297
2. Oshima, T. and Baba, Y. (2012) Recognition of Exterior Protein Surfaces Using Artificial Ligands Based on Calixarenes, Crown Ethers, and Tetraphenylporphyrins J. Inclusion Phenom. Macrocyclic Chem. 73, 17-32
3. Shinoda, S. and Tsukube, H. (2011) Molecular Recognition of Cytochrome c by Designed Receptors for Generation of in vi vo and in vitro Functions Chem. Sci. 2, 2301-2305
4. Wilson, A. J. (2009) Inhibition of Protein-protein Interactions Using Designed Molecules Chem. Soc. Rev. 38, 3289-3300
5. Clark-Ferris, K. K. and Fisher, J. (1985) Topographical Mimicry of the Enzyme Binding Domain of Cytochrome c J. Am. Chem. Soc. 107, 5007-5008
6. Cho, K. C., Che, C. M., Ng, K. M., and Choy, C. L. (1986) Electron Transfer between Cytochrome c and Porphyrins J. Am. Chem. Soc. 108, 2814-2818
7. Zhou, J. S., Granada, E. S. V., Leontis, N. B., and Rodgers, M. A. J. (1990) Photoinduced Electron Transfer in Self-associated Complexes of Several Uroporphyrins and Cytochrome c J. Am. Chem. Soc. 112, 5074-5080
8. Zhou, J. S. and Rodgers, M. A. J. (1991) Driving Force Dependence of Rate Constants of Electron Transfer within Cytochrome c and Uroporphyrin Complexes J. Am. Chem. Soc. 113, 7728-7734
9. Larsen, R. W., Omdal, D. H., Jasuja, R., Niu, S. L., and Jameson, D. M. (1997) Conformational Modulation of Electron Transfer within Electrostatic Porphyrin:cytochrome c Complexes J. Phys. Chem. B 101, 8012-8020
10. Croney, J. C., Helms, M. K., Jameson, D. M., and Larsen, R. W. (2000) Temperature Dependence of Photoinduced Electron Transfer within Self-assembled Uroporphyrin-cytochrome c Complexes J. Phys. Chem. B 104, 973-977
11. Jain, R. K. and Hamilton, A. D. (2000) Protein Surface Recognition by Synthetic Receptors Based on a Tetraphenylporphyrin Scaffold Org. Lett. 2, 1721-1723
12. Yin, H. and Hamilton, A. D. (2005) Strategies for Targeting Protein-protein Interactions with Synthetic Agents Angew. Chem., Int. Ed. 44, 4130-4163
13. Jain, R. K. and Hamilton, A. D. (2002) Designing Protein Denaturants: Synthetic Agents Induce Cytochrome c Unfolding at Low Concentrations and Stoichiometries Angew. Chem., Int. Ed. 41, 641-643
14. Wilson, A. J., Groves, K., Jain, R. K., Park, H. S., and Hamilton, A. D. (2003) Directed Denaturation: Room Temperature and Stoichiometric Unfolding of Cytochrome c by a Metalloporphyrin Dimer J. Am. Chem. Soc. 125, 4420-4421
15. Crowley, P. B., Ganji, P., and Ibrahim, H. (2008) Protein Surface Recognition: Structural Characterization of Cytochrome c-Porphyrin Complexes ChemBioChem 9, 1029-1033
16. Anula, H. M., Myshkin, E., Guliaev, A., Luman, C., Danilov, E. O., Castellano, F. N., Bullerjahn, G. S., and Rodgers, M. A. (2006) Photo Process on Self-associated Cationic Porphyrins and Plastocyanin Complexes 1. Ligation of Plastocyanin Tyrosine 83 onto Metalloproteins and Electron-transfer Fluorescence Quenching J. Phys. Chem. A 110, 2545-2559
17. Goel, M., Jain, D., Kaur, K. J., Kenoth, R., Maiya, B. G., Swamy, M. J., and Salunke, D. M. (2001) Functional Equality in the Absence of Structural Similarity. An Added Dimension to Molecular Mimicry J. Biol. Chem. 276, 39277-39281
18. Goel, M., Anuradha, P., Kaur, K. J., Maiya, B. G., Swamy, M. J., and Salunke, D. M. (2004) Porphyrin binding to Jacalin is Facilitated by the Inherent Plasticity of the Carbohydrate-binding Site: Novel Mode of Lectin-ligand Interaction Acta Crystallogr. D60, 281-288
19. Goel, M., Damai, R. S., Sethi, D. K., Kaur, K. J., Maiya, B. G., Swamy, M. J., and Salunke, D. M. (2005) Crystal Structures of the PNA-Porphyrin Complex in the Presence and Absence of Lactose: Mapping the Conformational Changes on Lactose Binding, Interacting Surfaces, and Supramolecular Aggregations Biochemistry 44, 5588-5596
20. Purrello, R., Bellacchio, E., Gurrieri, S., Lauceri, R., Raudino, A., Scolaro, L. M., and Santoro, A. M. (1998) pH Modulation of Porphyrin Self-Assembly onto Polylysine J. Phys. Chem. B 102, 8852-8857
21. Jankowska, K. I., Pagba, C. V., Piatnitski Chekler, E. L., Deshayes, K., and Piotrowiak, P. (2010) Electrostatic Docking of a Supramolecular Host-Guest Assembly to Cytochrome c Probed by Bidirectional Photoinduced Electron Transfer J. Am. Chem. Soc. 132, 16423-16431
22. Martos, V., Bell, S. C., Santos, E., Isacoff, E. Y., Trauner, D., and de Mendoza, J. (2009) Calix[4]arene-based Conical-shaped Ligands for Voltage-dependent Potassium Channels Proc. Natl. Acad. Sci. U.S.A. 106, 10482-10486
23. McGovern, R. E., Fernandes, H., Khan, A. R., Power, N. P., and Crowley, P. B. (2012) Protein Camouflage in Cytochrome c-calixarene Complexes Nat. Chem. 4, 527-533
24. Chinai, J. M., Taylor, A. B., Ryno, L. M., Hargreaves, N. D., Morris, C. A., Hart, J. P., and Urbach, A. R. (2011) Molecular Recognition of Insulin by a Synthetic Receptor J. Am. Chem. Soc. 133, 8810-8813
25. Dang, D. T., Schill, J., and Brunsveld, L. (2012) Cucurbit[8]uril- mediated Protein Homotetramerization Chem. Sci. 3, 2679-2684
26. Aachmann, F. L., Otzen, D. E., Larsen, K. L., and Wimmer, R. (2003) Structural Background of Cyclodextrin-protein Interactions Protein Eng. 16, 905-912
27. Kano, K., Watanabe, K., and Ishida, Y. (2008) Porphyrin J-aggregates Stabilized by Ferric Myoglobin in Neutral Aqueous Solution J. Phys. Chem. B 112, 14402-14408
28. Forster, F., Webb, B., Krukenberg, K. A., Tsuruta, H., Agard, D. A., and Sali, A. (2008) Integration of Small-angle X-ray Scattering Data into Structural Modeling of Proteins and their Assemblies J. Mol. Biol. 382, 1089-1106
29. Hammel, M. (2012) Validation of Macromolecular Flexibility in Solution by Small-angle X-ray Scattering (SAXS) Eur. Biophys. J. 41, 789-799
30. Madl, T., Gabel, F., and Sattler, M. (2011) NMR and Small-angle Scattering-based Structural Analysis of Protein Complexes in Solution J. Struct. Biol. 173, 472-482
31. Putnam, C. D., Hammel, M., Hura, G. L., and Tainer, J. A. (2007) X-ray Solution Scattering (SAXS) Combined with Crystallography and Computation: Defining Accurate Macromolecular Structures, Conformations and Assemblies in Solution Q. Rev. Biophys. 40, 191-285
32. Tiede, D. M., Mardis, K., and Zuo, X. (2009) X-ray Scattering Combined with Coordinate-based Analyses for Applications in Natural and Artificial Photosynthesis Photosynth. Res. 102, 267-279
33. Guinier, A. and Fournet, G. (1955) Small Angle Scattering of X-rays, Wiley, New York.
34. Lipfert, J. and Doniach, S. (2007) Small-angle X-ray Scattering from RNA, Proteins, and Protein Complexes Annu. Rev. Biophys. Biomol. Struct. 36, 307-327
35. Svensson, B., Tiede, D. M., and Barry, B. A. (2002) Small-angle X-ray Scattering Studies of the Manganese-stabilizing Subunit in Photosystem II J. Phys. Chem. B 106, 8485-8488
36. Svensson, B., Tiede, D. M., Nelson, D. R., and Barry, B. A. (2004) Structural Studies of the Manganese-stabilizing Subunit in Photosystem II Biophys. J. 86, 1807-1812
37. Londer, Y. Y., Pokkuluri, P. R., Tiede, D. M., and Schiffer, M. (2002) Production and Preliminary Characterization of a Recombinant Triheme Cytochrome c7 from Geobacter sulfurreducens in Escherichia coli Biochim. Biophys. Acta 1554, 202-211
38. Rambo, R. P. and Tainer, J. A. (2013) Super-Resolution in Solution X-ray Scattering and Its Applications to Structural Systems Biology Annu. Rev. Biophys. 42, 415-441
39. Tiede, D. M., Zhang, R., and Seifert, S. (2002) Protein conformations explored by difference high-angle solution X-ray scattering: Oxidation state and temperature dependent changes in cytochrome c Biochemistry 41, 6605-6614
40. Pokkuluri, P. R., Londer, Y. Y., Duke, N. E., Erickson, J., Pessanha, M., Salgueiro, C. A., and Schiffer, M. (2004) Structure of a novel c7-type three-heme cytochrome domain from a multidomain cytochrome c polymer Protein Sci. 13, 1684-1692
41. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD: Visual Molecular Dynamics J. Mol. Graphics 14, 33-38
42. MacKerell, A. D., Bashford, D., Bellot, M., Dunbrack, R. L., Jr., Evansec, J. D., Field, M. J., Fisher, S., Gao, J., Guo, H., Ha, S., Joseph, D., Kuchnir, L., Kuczera, K., Lau, F. T. K., Mattos, C., Michnick, S., Ngo, T., Nguyen, D. T., Prodhom, B., Reiher, I. W. E., Roux, B., Schlenkrich, M., Smith, J., Stote, R., Straub, J., Watanabe, M., Wiorkiewicz-Kuczera, J., Yin, D., and Karplus, M. (1998) All-atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins J. Phys. Chem. B 102, 3586-3616
43. Autenrieth, F., Tajkhorshid, E., Baudry, J., and Luthey-Schulten, Z. (2004) Classical Force Field Parameters for the Heme Prosthetic Group of Cytochrome c J. Comput. Chem. 25, 1613-1622
44. Phillips, J. C., Braun, R., Wang, W., Gumbart, J. C., Tajkhorshid, E., Villa, E., Chipot, C., Skeel, R. D., Kale, L., and Schulten, K. (2005) Scalable Molecular Dynamics with NAMD J. Comput. Chem. 26, 1781-1802
45. Zuo, X. and Tiede, D. M. (2005) Resolving Conflicting Crystallographic and NMR Models for Solution-State DNA with Solution X-ray Diffraction J. Am. Chem. Soc. 127, 16-17
46. 1 Complex Mediated by the Conformation of the Rieske Iron-sulfur Protein Biochemistry 46, 7138-7145
47. Rosen, D., Okamura, M. Y., and Feher, G. (1980) Interaction of Cytochrome c with Reaction Centers of Rhodopseudomonas sphaerodies R-26: Determination of Number of Binding Sites and Dissociation Constants by Equilibrium Dialysis Biochemistry 19, 5687-5692
48. Mauk, M. R., Ferrer, J. C., and Mauk, A. G. (1994) Proton Linkage in Formation of the Cytochrome c-cytochrome c Peroxidase Complex: Electrostatic Properties of the High- and Low-affinity Cytochrome Binding Sites on the Peroxidase Biochemistry 33, 12609-12614
49. 2 docking J. Phys. Chem. B 108, 20376-20387
50. Solmaz, S. R. and Hunte, C. (2008) Structure of Complex III with Bound Cytochrome c in Reduced State and Definition of a Minimal Core Interface for Electron Transfer J. Biol. Chem. 283, 17542-17549
51. Ahmed, A. J., Smith, H. T., Smith, M. B., and Millett, F. S. (1978) Effect of Specific Lysine Modification on the Reduction of Cytochrome c by Succinate-cytochrome c Reductase Biochemistry 17, 2479-2483
52. 1. Differential Acetylation of Lysyl Residues in Free and Compelxed Cytochrome c J. Biol. Chem. 255, 4732-4739
53. 1 and Cytochrome c Oxidase J. Biol. Chem. 256, 4984-4990
54. Speck, S. H., Ferguson-Miller, S., Osheroff, N., and Margoliash, E. (1979) Definition of Cytochrome c Binding Domains by Chemical Modification: Kinetics of Reaction with Beef Mitochondrial Reductase and Functional Organization of the Respiratory Chain Proc. Natl. Acad. Sci. U.S.A. 76, 155-159
55. Pelletier, H. and Kraut, J. (1992) Crystal Structure of a Complex between Electron Transfer Partners, Cytochrome c Peroxidase and Cytochrome c Science 258, 1748-1755
56. Volkov, A. N., Worrall, A. J., Holtzmann, E., and Ubbink, M. (2006) Solution Structure and Dynamics of the Complex between Cytochrome c and Cytochrome c Peroxidase Determined by Paramagnetic NMR Proc. Natl. Acad. Sci. U.S.A. 103, 18945-18950
57. 1 Complex and Cytochrome c: A Structural Analysis Biochim. Biophys. Acta 1555, 21-28
58. 1 Complex with its Bound Substrate Cytochrome c Proc. Natl. Acad. Sci. U.S.A. 99, 2800-2805
59. 2 Complex from Rhodobacter sphaeroides Biochemistry 35, 2535-2547
60. Axelrod, H. L., Abresch, E. C., Okamura, M. Y., Yeh, A. P., Rees, D. C., and Feher, G. (2002) X-ray Structure Determination of the Cytochrome c2:reaction Center Electron Transfer Complex from Rhodobacter sphaeroides J. Mol. Biol. 319, 501-515
61. 2) Exit Strategy: Dissociation Studies and Evolutionary Implications J. Phys. Chem. B 111, 618-634
62. 1 Complex: Rationalizing the Role of Key Residues Biophys. J. 99, 2647-2656
63. Dantas, J. M., Morgado, L., Catarino, T., Kokhan, O., Pokkuluri, P. R., and Salgueiro, C. A. (2014) Evidence for Interaction between the Triheme Cytochrome PpcA from Geobacter sulfurreducens and Anthrahydroquinone-2,6- sulfonate, an Analog of the Redox Active Components of Humic Substances Biochim. Biophys. Acta 1837, 750-760
64. Rosell, F. I., Ferrer, J. C., and Mauk, A. G. (1998) Proton Linked Protein Conformational Switching: Definition of the Alkaline Conformational Transition of Yeast iso-1-Ferricytochrome c J. Am. Chem. Soc. 120, 11234-11245
65. Dumortier, C., Meyer, T. E., and Cusanovich, M. A. (1999) Protein Dynamics: Imidazole Binding to Class I c-type Cytochromes Arch. Biochem. Biophys. 371, 142-148