Crystal structure of the hemoglobin dodecamer from Lumbricus erythrocruorin: Allosteric core of giant annelid respiratory complexes

Journal of Molecular Biology

Volumn 344, Issue 1, 2004, Pages 119-134

  Strand, Kristen ^a   Knapp, James E ^a   Bhyravbhatla, Balaji ^a   Royer Jr , William E ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

allostery; erythrocruorin; hemoglobin; protein crystallography

Indexed keywords

ERYTHROCRUORIN; HEMOGLOBIN;

ALLOSTERISM; ANNELID WORM; ARTICLE; CELL RESPIRATION; CRYSTAL STRUCTURE; ECHINODERM; LIGAND BINDING; MOLECULAR MODEL; MOLLUSC; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN QUATERNARY STRUCTURE; PROTEIN STRUCTURE; SPECIES COMPARISON;

ANNELIDA; ECHINODERMATA; LUMBRICUS; LUMBRICUS TERRESTRIS; MOLLUSCA;

EID: 7044270825     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.08.094     Document Type: Article

References (59)

1. K.E. van Holde, and K.I. Miller Hemocyanins Advan. Protein Chem. 47 1995 1 81
2. D.M. Kurtz Jr Oxygen-carrying proteins: three solutions to a common problem Essays Biochem. 34 1999 85 100
3. W.E. Royer Jr, J.E. Knapp, K. Strand, and H.A. Heaslet Cooperative hemoglobins: conserved fold, diverse quaternary assemblies and allosteric mechanisms Trends Biochem. Sci. 26 2001 297 304
4. M. Bolognesi, D. Bordo, M. Rizzi, C. Tarricone, and P. Ascenzi Non-vertebrate hemoglobins: structural bases for reactivity Prog. Biophys. Mol. Biol. 68 1997 29 68
5. M. Schatz, E.V. Orlova, P. Dube, J. Jager, and M. van Heel Structure of Lumbricus terrestris hemoglobin at 30 Å resolution determined using angular reconstitution J. Struct. Biol. 114 1995 28 40
6. J.C. Taveau, N. Boisset, S.N. Vinogradov, and J.N. Lamy Three-dimensional reconstruction of Lumbricus terrestris hemoglobin at 22 Å resolution: intramolecular localization of the globin and linker chains J. Mol. Biol. 289 1999 1343 1359
7. F. de Haas, F. Zal, F.H. Lallier, A. Toulmond, and J.N. Lamy Three-dimensional reconstruction of the hexagonal bilayer hemoglobin of the hydrothermal vent tube worm Riftia pachyptila by cryoelectron microscopy Proteins: Struct. Funct. Genet. 26 1996 241 256
8. F. de Haas, J.C. Taveau, N. Boisset, O. Lambert, S.N. Vinogradov, and J.N. Lamy Three-dimensional reconstruction of the chlorocruorin of the polychaete annelid Eudistylia vancouverii J. Mol. Biol. 255 1996 140 153
9. L. Jouan, J.C. Taveau, S. Marco, F.H. Lallier, and J.N. Lamy Occurrence of two architectural types of hexagonal bilayer hemoglobin in annelids: comparison of 3D reconstruction volumes of Arenicola marina and Lumbricus terrestris hemoglobins J. Mol. Biol. 305 2001 757 771
10. J.P. Harrington, Y. Gonzalez, and R.E. Hirsch Redox concerns in the use of acellular hemoglobin-based therapeutic oxygen carriers: the role of plasma components Artif. Cells Blood Substit. Immobil. Biotechnol. 28 2000 477 492
11. S.C. Dorman, C.F. Kenny, L. Miller, R.E. Hirsch, and J.P. Harrington Role of redox potential of hemoglobin-based oxygen carriers on methemoglobin reduction by plasma components Artif. Cells Blood Substit. Immobil. Biotechnol. 30 2002 39 51
12. S.C. Dorman, J.P. Harrington, M.S. Martin, and T.V. Johnson Determination of the formal reduction potential of Lumbricus terrestris hemoglobin using thin layer spectroelectrochemistry J. Inorg. Biochem. 98 2004 185 188
13. R.E. Hirsch, L.A. Jelicks, B.A. Wittenberg, D.K. Kaul, H.L. Shear, and J.P. Harrington A first evaluation of the natural high molecular weight polymeric Lumbricus terrestris hemoglobin as an oxygen carrier Artif. Cells Blood Substit. Immobil. Biotechnol. 25 1997 429 444
14. W.E. Royer Jr, K. Strand, M. van Heel, and W.A. Hendrickson Structural hierarchy in erythrocruorin, the giant respiratory assemblage of annelids Proc. Natl Acad. Sci. USA 97 2000 7107 7111
15. K. Fushitani, K. Imai, and A.F. Riggs Oxygenation properties of hemoglobin from the earthworm, Lumbricus terrestris. Effects of pH, salts, and temperature J. Biol. Chem. 261 1986 8414 8423
16. K. Fushitani, and A.F. Riggs The extracellular hemoglobin of the earthworm, Lumbricus terrestris. Oxygenation properties of isolated chains, trimer, and a reassociated product J. Biol. Chem. 266 1991 10275 10281
17. K.E. van Holde, K.I. Miller, and E. van Olden Allostery in very large molecular assemblies Biophys. Chem. 86 2000 165 172
18. K. Fushitani, M.S. Matsuura, and A.F. Riggs The amino acid sequences of chains a, b, and c that form the trimer subunit of the extracellular hemoglobin from Lumbricus terrestris J. Biol. Chem. 263 1988 6502 6517
19. X. Bailly, D. Jollivet, S. Vanin, J. Deutsch, F. Zal, F. Lallier, and A. Toulmond Evolution of the sulfide-binding function within the globin multigenic family of the deep-sea hydrothermal vent tubeworm Riftia pachyptila Mol. Biol. Evol. 19 2002 1421 1433
20. A.T. Brunger, P.D. Adams, G.M. Clore, W.L. DeLano, P. Gros, and R.W. Grosse-Kunstleve Crystallography & NMR system: a new software suite for macromolecular structure determination Acta Crystallog. sect. D 54 1998 905 921
21. G.N. Murshudov, A.A. Vagin, and E.J. Dodson Refinement of macromolcular structures by the maximum-likelihood method Acta Crystallog. sect. D 53 1997 240 255
22. Collaborative Computing Project Number 4 The CCP4 suite: programs for protein crystallography Acta Crystallog. sect. D 50 1994 760 763
23. R.A. Laskowski, M.W. MacArthur, D.S. Moss, and J.M. Thornton PROCHECK: a program to check the stereochemical quality of protein structures J. Appl. Crystallog. 26 1993 283 291
24. H.E. Aronson, W.E. Royer Jr, and W.A. Hendrickson Quantification of tertiary structural conservation despite primary sequence drift in the globin fold Protein Sci. 3 1994 1706 1711
25. F. de Haas, A. Kuchumov, J.C. Taveau, N. Boisset, S.N. Vinogradov, and J.N. Lamy Three-dimensional reconstruction of native and reassembled Lumbricus terrestris extracellular hemoglobin. Localization of the monomeric globin chains Biochemistry 36 1997 7330 7338
26. W.E. Royer Jr, K.S. Heard, D.J. Harrington, and E. Chiancone The 2.0 Å crystal structure of Scapharca tetrameric hemoglobin: cooperative dimers within an allosteric tetramer J. Mol. Biol. 253 1995 168 186
27. D.T. Mitchell, G.B. Kitto, and M.L. Hackert Structural analysis of monomeric hemichrome and dimeric cyanomet hemoglobins from Caudina arenicola J. Mol. Biol. 251 1995 421 431
28. W.E. Royer Jr High-resolution crystallographic analysis of a co-operative dimeric hemoglobin J. Mol. Biol. 235 1994 657 681
29. H.A. Heaslet, and W.E. Royer Jr The 2.7 Å crystal structure of deoxygenated hemoglobin from the sea lamprey (Petromyzon marinus): structural basis for a lowered oxygen affinity and Bohr effect Struct. Fold. Des. 7 1999 517 526
30. Y. Qiu, D.H. Maillett, J. Knapp, J.S. Olson, and A.F. Riggs Lamprey hemoglobin. Structural basis of the bohr effect J. Biol. Chem. 275 2000 13517 13528
31. J.P. Gallivan, and D.A. Dougherty Cation-pi interactions in structural biology Proc. Natl Acad. Sci. USA 96 1999 9459 9464
32. A. Tsuneshige, K. Imai, H. Hori, I. Tyuma, and T. Gotoh Spectrophotometric, electron paramagnetic resonance and oxygen binding studies on the hemoglobin from the marine polychaete Perinereis aibuhitensis (Grube): comparative physiology of hemoglobin J. Biochem. (Tokyo) 106 1989 406 417
33. R. Santucci, E. Chiancone, and B. Giardina Oxygen binding to Octolasium complanatum erythrocruorin. Modulation of homo- and heterotropic interactions by cations J. Mol. Biol. 179 1984 713 727
34. A. Pardanani, Q.H. Gibson, G. Colotti, and W.E. Royer Jr Mutation of residue Phe97 to Leu disrupts the central allosteric pathway in Scapharca dimeric hemoglobin J. Biol. Chem. 272 1997 13171 13179
35. W.E. Royer Jr, A. Pardanani, Q.H. Gibson, E.S. Peterson, and J.M. Friedman Ordered water molecules as key allosteric mediators in a cooperative dimeric hemoglobin Proc. Natl Acad. Sci. USA 93 1996 14526 14531
36. G.J. Vidugiris, J.P. Harrington, J.M. Friedman, and R.E. Hirsch Absence of ligand binding-induced tertiary changes in the multimeric earthworm Lumbricus terrestris hemoglobin. A resonance Raman study J. Biol. Chem. 268 1993 26190 26192
37. J.E. Knapp, and W.E. Royer Jr Ligand-linked structural transitions in crystals of a cooperative dimeric hemoglobin Biochemistry 42 2003 4640 4647
38. J. Yang, A.P. Kloek, D.E. Goldberg, and F.S. Mathews The structure of Ascaris hemoglobin domain I at 2.2 Å resolution: molecular features of oxygen avidity Proc. Natl Acad. Sci. USA 92 1995 4224 4228
39. D.A. Bisig, E.E. Di Iorio, K. Diederichs, K.H. Winterhalter, and K. Piontek Crystal structure of Asian elephant (Elephas maximus) cyano-metmyoglobin at 1.78-Å resolution. Phe29(B10) accounts for its unusual ligand binding properties J. Biol. Chem. 270 1995 20754 20762
40. 2 affinity and low autooxidation rate J. Biol. Chem. 267 1992 14443 14450
41. S.T. Jeong, N.T. Ho, M.P. Hendrich, and C. Ho Recombinant hemoglobin(α 29leucine→phenylalanine, α 96valine→ tryptophan, β 108asparagine→lysine) exhibits low oxygen affinity and high cooperativity combined with resistance to autoxidation Biochemistry 38 1999 13433 13442
42. J.S. Olson, R.F. Eich, L.P. Smith, J.J. Warren, and B.C. Knowles Protein engineering strategies for designing more stable hemoglobin-based blood substitutes Artif. Cells Blood Substit. Immobil. Biotechnol. 25 1997 227 241
43. Y. Dou, D.H. Maillett, R.F. Eich, and J.S. Olson Myoglobin as a model system for designing heme protein based blood substitutes Biophys. Chem. 98 2002 127 148
44. A. Rossi-Fanelli, and E. Antonini Studies on the oxygen and carbon monoxide equilibria of human myoglobin Arch. Biochem. Biophys. 77 1958 478 492
45. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276 1997 307 326
46. G.J. Kleywegt, and T.A. Jones Halloween...masks and bones S. Bailey R. Hubbard D.A. Waller From First Map to Final Model 1994 Science and Engineering Research Council Daresbury Laboratory Warrington, UK 59 66
47. T.A. Jones, J.Y. Zou, S.W. Cowan, and Kjeldgaard Improved methods for building protein models in electron density maps and the location of errors in these models Acta Crystallog. sect. A 47 1991 110 119
48. J. Vojtechovsky, K. Chu, J. Berendzen, R.M. Sweet, and I. Schlichting Crystal structures of myoglobin-ligand complexes at near-atomic resolution Biophys. J. 77 1999 2153 2174
49. R.B. Honzatko, W.A. Hendrickson, and W.E. Love Refinement of a molecular model for lamprey hemoglobin from Petromyzon marinus J. Mol. Biol. 184 1985 147 164
50. G.J. Kleywegt, and T.A. Jones Software for handling macromolecular envelopes Acta Crystallog. sect. D 55 1999 941 944
51. S. Mecozzi, A.P. West Jr, and D.A. Dougherty Cation-pi interactions in aromatics of biological and medicinal interest: electrostatic potential surfaces as a useful qualitative guide Proc. Natl Acad. Sci. USA 93 1996 10566 10571
52. H.M. Berman, J. Westbrook, Z. Feng, G. Gilliland, T.N. Bhat, and H. Weissig The Protein Data Bank Nucl. Acids Res. 28 2000 235 242
53. R.M. Esnouf Further additions to MolScript version 1.4, including reading and contouring of electron-density maps Acta Crystallog. sect. D 55 1999 938 940
54. E.A. Merritt, and D.J. Bacon Raster3D: photorealistic molecular graphics Methods Enzymol. 277 1997 505 524
55. Q. Xie, R.A. Donahue Jr, K. Schneider, U.A. Mirza, I. Haller, B.T. Chait, and A.F. Riggs Structure of chain d of the gigantic hemoglobin of the earthworm Biochim. Biophys. Acta 1337 1997 241 247
56. A.B. Edmundson Amino acid sequence of sperm whale myoglobin Nature 205 1965 883 887
57. R. Petruzzelli, B.M. Goffredo, D. Barra, F. Bossa, A. Boffi, and D. Verzili Amino acid sequence of the cooperative homodimeric hemoglobin from the mollusc Scapharca inaequivalvis and topology of the intersubunit contacts FEBS Letters 184 1985 328 332
58. F. Mauri, J. Omnaas, L. Davidson, C. Whitfill, and G.B. Kitto Amino acid sequence of a globin from the sea cucumber Caudina (Molpadia) arenicola Biochim. Biophys. Acta 1078 1991 63 67
59. T.E. Ferrin, C.C. Huang, L.E. Jarvis, and R. Langridge The MIDAS display system J. Mol. Graph. 6 1988 13 27