A joint x-ray and neutron study on amicyanin reveals the role of protein dynamics in electron transfer

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 15, 2010, Pages 6817-6822

  Sukumar, N ^a   Mathews, F S ^b   Langan, P ^c   Davidson, V L ^d  

^a Department of Obstetrics Gynecology   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c LOS ALAMOS NATIONAL LABORATORY   (United States)

^d UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

Author keywords

Copper protein; Hydrogen bonding; Hydrogen deuterium exchange; Oxidation reduction; Redox potential

Indexed keywords

AMICYANIN; AMIDE; CARBON; COPPER; DEUTERIUM; HYDROGEN; REAGENT; WATER;

ARTICLE; ATOM; BINDING SITE; CHEMICAL BOND; CRYSTALLIZATION; ELECTRON TRANSPORT; HYDROGEN BOND; NEUTRON; NEUTRON DIFFRACTION; NONHUMAN; OXIDATION REDUCTION REACTION; PARACOCCUS DENITRIFICANS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; X RAY;

BACTERIAL PROTEINS; BINDING SITES; COPPER; CRYSTALLIZATION; ELECTRON TRANSPORT; HYDROGEN; HYDROGEN BONDING; MODELS, MOLECULAR; MOLECULAR CONFORMATION; OXIDATION-REDUCTION; PARACOCCUS DENITRIFICANS; PROTEIN CONFORMATION; PROTEINS; PROTONS; X-RAYS;

PARACOCCUS DENITRIFICANS;

EID: 77951062013     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0912672107     Document Type: Article

References (45)

1. Adman ET (1991) Copper protein structures. Adv Protein Chem 42:145-197.
2. Gray HB, Ellis WR, Jr (1994) Electron Transfers in Biology, in Bioinorganic Chemistry, eds I Bertini, HB Gary, SJ Lippard, and JS Valentine (University Science Books, Mill Valley, CA), pp 315-364.
3. Cunane LM, Chen ZW, Durley RC, Mathews FS (1996) X-ray structure of the cupredoxin amicyanin, from Paracoccus denitrificans, refined at 1.31 Å resolution. Acta Crystallogr D52:676-686. (Pubitemid 27064292)
4. Husain M, Davidson VL, Smith AJ (1986) Properties of Paracoccus denitrificans amicyanin. Biochem 25:2431-2436.
5. Husain M, Davidson VL (1985) An inducible periplasmic blue copper protein from Paracoccus denitrificans Purification, properties, and physiological role. J Biol Chem 260:14626-14629.
6. Carrell CJ, Sun D, Jiang S, Davidson VL, Mathews FS (2004) Structural studies of two mutants of amicyanin from Paracoccus denitrificans that stabilize the reduced state of the copper. Biochem 43:9372-9380. (Pubitemid 38955470)
7. Chen L, et al. (1992) Crystal structure of an electron-transfer complex between methylamine dehydrogenase and amicyanin. Biochem 31:4959-4964.
8. Chen L, Durley RC, Mathews FS, Davidson VL (1994) Structure of an electron transfer complex: Methylamine dehydrogenase, amicyanin, and cytochrome c551i. Science 264:86-90. (Pubitemid 24987849)
9. Durley R, Chen L, Lim LW, Mathews FS, Davidson VL (1993) Crystal structure analysis of amicyanin and apoamicyanin from Paracoccus denitrificans at 2.0 Å and 1.8 Å resolution. Protein Sci 2:739-752. (Pubitemid 23121089)
10. Lim LW, Mathews FS, Husain M, Davidson VL (1986) Preliminary x-ray crystallographic study of amicyanin from Paracoccus denitrificans. J Mol Biol 189:257-258.
11. Sukumar N, et al. (2005) A preliminary time-of-flight neutron diffraction study on amicyanin from Paracoccus denitrificans. Acta Crystallogr D61:640-642. (Pubitemid 44336737)
12. Davidson VL (2008) Protein control of true, gated, and coupled electron transfer reactions. Acc Chem Res 41:730-738.
13. Adams PD, Mustyakimov M, Afonine PV, Langan P (2009) Generalized x-ray and neutron crystallographic analysis: More accurate and complete structures for biological macromolecules. Acta Crystallogr D65:567-573.
14. Schoenborn BP (1969) Neutron diffraction analysis of myoglobin. Nature 224:143-146.
15. Blakeley MP (2009) Neutron macromolecular crystallography. Crystallogr Rev 15:157-218.
16. Blakeley MP, Langan P, Niimura N, Podjarny A (2008) Neutron Crystallography: Opportunities, challenges, and limitation. Curr Opin Struc Biol 18:593-600.
17. Kossiakoff AA (1982) Protein dynamics investigated by the neutron diffraction-hydrogen exchange technique. Nature 296:713-721.
18. Bennett B, et al. (2006) Neutron diffraction studies of Escherichia coli dihydrofolate reductase complexed with methotrexate. Proc Natl Acad Sci USA 103:18493-18498. (Pubitemid 44913438)
19. Bennett BC, Gardberg AS, Blair MD, Dealwis CG (2008) On the determinants of amide backbone exchange in proteins: A neutron crystallographic comparative study. Acta Crystallogr D64:764-783.
20. Davidson VL, Jones LH (1996) Electron transfer from copper to heme within the methylamine dehydrogenase-amicyanin-cytochrome c-551i complex. Biochem 35:8120-8125.
21. Chakravarty S, Varadarajan R (1999) Residue depth: A novel parameter for the analysis of protein structure and stability. Structure 7:723-732. (Pubitemid 29329844)
22. Sharma KD, Loehr TM, Sanders-Loehr J, Husain M, Davidson VL (1988) Resonance Raman spectroscopy of amicyanin, a blue copper protein from Paracoccus denitrificans. J Biol Chem 263:3303-3306. (Pubitemid 18072787)
23. Zhu Z, et al. (1998) Molecular basis for interprotein complex-dependent effects on the redox properties of amicyanin. Biochem 37:17128-17136. (Pubitemid 29013769)
24. Davidson VL, Jones LH, Graichen ME, Zhu Z (2000) Tyr(30) of amicyanin is not critical for electron transfer to cytochrome c-551i: Implications for predicting electron transfer pathways. Biochim Biophys Acta 1457:27-35.
25. Regan JJ, Risser SM, Beratan DN, Onuchic JN (1993) Protein electron transport: Single versus multiple pathways. J Phys Chem 97:13083-13088.
26. Page CC, Moser CC, Chen X, Dutton PL (1999) Natural engineering principles of electron tunnelling in biological oxidation-reduction. Nature 402:47-52. (Pubitemid 29533508)
27. Ferrari D, et al. (2003) Catalysis and electron transfer in protein crystals: The binary and ternary complexes of methylamine dehydrogenase with electron acceptors. Biochim Biophys Acta 1647:337-342. (Pubitemid 38234677)
28. Wahl MC, Sundaralingam M (1997) C-H...O hydrogen bonding in biology. Trends Biochem Sci 22:97-102.
29. Desiraju GR, Steiner T (1999) The weak hydrogen bond in structural chemistry and biology (Oxford Univ Press, Oxford).
30. Domagala M, Grabowski SJ, Urbaniak K, Mloston G (2003) Role of C-H...S and C-H...N hydrogen bonds in organic crystal structures - The crystal and molecular structure of 3-Methyl-2,4-diphenyl-(1,3)-thiazolidine-5-spiro-20- adamantane and 3-Methyl-2,4,5, 5-tetraphenyl-(1,3)-thiazolidine. J Phys Chem A 107:2730-2736.
31. Guo H, Beahm RF, Guo H (2004) Stabilization and destabilization of the C-H...O = C hydrogen bonds involving proline residues in helices. J Phys Chem 108:18065-18072.
32. Otwinowski Z, Minor W (1997) Processing of x-ray diffraction data collected by oscillation methods. Methods Enzymol 276:307-326. (Pubitemid 27085611)
33. Langan P, Greene G (2004) Protein crystallography with spallation neutrons: Collecting and processing wavelength-resolved Laue protein data. J Appl Crystallogr 37:253-257.
34. Helliwell JR, et al. (1989) The recording and analysis of synchrotron x-radiation Laue diffraction photographs. J Appl Crystallogr 22:483-497.
35. Kissinger CR, Gehlhaar DK, Smith BA, Bouzida D (2001) Molecular replacement by evolutionary search. Acta Crystallogr D57:1474-1479.
36. Brunger AT (1992) Free R value: A novel statistical quantity for assessing the accuracy of crystal structures. Nature 355:472-475.
37. Brünger AT, et al. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr D54:905-921. (Pubitemid 28443603)
38. Adams PD, et al. (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D58:1948-1954.
39. Tiwari A, Panigrahi SK, Desiraju GR Hydrogen Bond Analysis Tool (HBAT) School of Chemistry (University of Hyderabad, Hyderabad, India).
40. CCP4 (1994) Collaborative Computational Project Number 4. Acta Crystallogr D50:760-763.
41. Panigrahi SK, Desiraju GR (2007) Strong and weak hydrogen bonds in the protein-ligand interface. Proteins 67:128-141. (Pubitemid 46340133)
42. Pintar A, Carugo O, Pongor S (2003) DPX: for the analysis of the protein core. Bioinformatics 19:313-314.
43. Lee B, Richards FM (1971) The interpretation of protein structures: Estimation of static accessibility. J Mol Biol 55:379-400.
44. Potterton L, et al. (2004) Developments in the CCP4 molecular-graphics project. Acta Crystallogr D60:2288-2294.
45. Bond CS (2003) TopDraw: a sketchpad for protein structure topology cartoons. Bioinformatics 19:311-312.