Crystal structure of the ferritin from the hyperthermophilic archaeal anaerobe Pyrococcus furiosus

The crystal structure of the ferritin from the archaeon, hyperthermophile and anaerobe Pyrococcus furiosus (PfFtn) is presented. While many ferritin structures from bacteria to mammals have been reported, until now only one was available from archaea, the ferritin from Archaeoglobus fulgidus (AfFtn). The PfFtn 24-mer exhibits the 432 point-group symmetry that is characteristic of most ferritins, which suggests that the 23 symmetry found in the previously reported AfFtn is not a common feature of archaeal ferritins. Consequently, the four large pores that were found in AfFtn are not present in PfFtn. The structure has been solved by molecular replacement and refined at 2.75-Å resolution to R = 0.195 and Rfree = 0.247. The ferroxidase center of the aerobically crystallized ferritin contains one iron at site A and shows sites B and C only upon iron or zinc soaking. Electron paramagnetic resonance studies suggest this iron depletion of the native ferroxidase center to be a result of a complexation of iron by the crystallization salt. The extreme thermostability of PfFtn is compared with that of eight structurally similar ferritins and is proposed to originate mostly from the observed high number of intrasubunit hydrogen bonds. A preservation of the monomer fold, rather than the 24-mer assembly, appears to be the most important factor that protects the ferritin from inactivation by heat.

[1]  P Argos,et al.  Protein thermal stability, hydrogen bonds, and ion pairs. , 1997, Journal of molecular biology.

[2]  G. Murshudov,et al.  Refinement of macromolecular structures by the maximum-likelihood method. , 1997, Acta crystallographica. Section D, Biological crystallography.

[3]  K. N. Trueblood,et al.  On the rigid-body motion of molecules in crystals , 1968 .

[4]  M. Sawaya,et al.  Crystal structures of a tetrahedral open pore ferritin from the hyperthermophilic archaeon Archaeoglobus fulgidus. , 2005, Structure.

[5]  R. Crichton.  Inorganic biochemistry of iron metabolism , 2001 .

[6]  Serdar Kuyucak,et al.  Functional properties of threefold and fourfold channels in ferritin deduced from electrostatic calculations. , 2003, Biophysical journal.

[7]  R. Crichton.  Inorganic Biochemistry of Iron Metabolism: From Molecular Mechanisms to Clinical Consequences , 2001 .

[8]  M. A. Carrondo,et al.  The nature of the di-iron site in the bacterioferritin from Desulfovibrio desulfuricans , 2003, Nature Structural Biology.

[9]  J. Tatur,et al.  The dinuclear iron‐oxo ferroxidase center of Pyrococcus furiosus ferritin is a stable prosthetic group with unexpectedly high reduction potentials , 2005, FEBS letters.

[10]  J. Powers.  p53-Mediated Apoptosis, Neuroglobin Overexpression, and Globin Deposits in a Patient With Hereditary Ferritinopathy , 2006, Journal of neuropathology and experimental neurology.

[11]  A. Brunger.  Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. , 1992 .

[12]  D. Oesterhelt,et al.  Iron-oxo clusters biomineralizing on protein surfaces: structural analysis of Halobacterium salinarum DpsA in its low- and high-iron states. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[13]  Elizabeth C. Theil,et al.  Opening protein pores with chaotropes enhances Fe reduction and chelation of Fe from the ferritin biomineral , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[14]  Jean-Michel Claverie,et al.  Genomic Correlates of Hyperthermostability, an Update* , 2003, The Journal of Biological Chemistry.

[15]  J. Tatur,et al.  A highly thermostable ferritin from the hyperthermophilic archaeal anaerobe Pyrococcus furiosus , 2006, Extremophiles.

[16]  R. Kolter,et al.  The crystal structure of Dps, a ferritin homolog that binds and protects DNA , 1998, Nature Structural Biology.

[17]  T. N. Bhat,et al.  The Protein Data Bank , 2000, Nucleic Acids Res..

[18]  V S Lamzin,et al.  ARP/wARP and molecular replacement. , 2001, Acta crystallographica. Section D, Biological crystallography.

[19]  C Combet,et al.  NPS@: network protein sequence analysis. , 2000, Trends in biochemical sciences.

[20]  Elizabeth C. Theil,et al.  Iron absorption from soybean ferritin in nonanemic women. , 2006, The American journal of clinical nutrition.

[21]  P. Arosio,et al.  Evidence that residues exposed on the three-fold channels have active roles in the mechanism of ferritin iron incorporation. , 1996, The Biochemical journal.

[22]  E. Chiancone,et al.  Thermal stability of horse spleen apoferritin and human recombinant H apoferritin. , 1996, Archives of biochemistry and biophysics.

[23]  R. Varadarajan,et al.  Elucidation of determinants of protein stability through genome sequence analysis , 2000, FEBS letters.

[24]  M. Worwood,et al.  Iron in biochemistry and medicine. , 1974 .

[25]  R. Rosenfeld.  Nature , 2009, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[26]  W. Kabsch,et al.  Dictionary of protein secondary structure: Pattern recognition of hydrogen‐bonded and geometrical features , 1983, Biopolymers.

[27]  W. Delano.  The PyMOL Molecular Graphics System , 2002 .

[28]  D. Macey,et al.  Identification of ferritin as a major high molecular weight zinc-binding protein in the tropical rock oyster,Saccostrea cuccullata , 1985 .

[29]  M. Saraste,et al.  FEBS Lett , 2000 .

[30]  F. Young.  Biochemistry , 1955, The Indian Medical Gazette.

[31]  R. Nussinov,et al.  Factors enhancing protein thermostability. , 2000, Protein engineering.

[32]  J. Thornton,et al.  Satisfying hydrogen bonding potential in proteins. , 1994, Journal of molecular biology.

[33]  G. N. Ramachandran,et al.  Conformation of polypeptides and proteins. , 1968, Advances in protein chemistry.

[34]  A M Gronenborn,et al.  Disordered water within a hydrophobic protein cavity visualized by x-ray crystallography. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[35]  D. Tsernoglou,et al.  The dodecameric ferritin from Listeria innocua contains a novel intersubunit iron-binding site , 2000, Nature Structural Biology.

[36]  G. Eichhorn,et al.  Advances in Inorganic Biochemistry , 1994 .

[37]  V S Lamzin,et al.  Automated refinement of protein models. , 1993, Acta crystallographica. Section D, Biological crystallography.

[38]  K. S. Yip,et al.  Protein thermostability above 100°C: A key role for ionic interactions , 1998 .

[39]  G. Moore,et al.  Formation of protein-coated iron minerals. , 2005, Dalton transactions.

[40]  N. Kannan,et al.  Aromatic clusters: a determinant of thermal stability of thermophilic proteins. , 2000, Protein engineering.

[41]  R. A. Scott,et al.  Dissecting contributions to the thermostability of Pyrococcus furiosus rubredoxin: beta-sheet chimeras. , 1997, Biochemistry.

[42]  G. Watt,et al.  Azotobacter cytochrome b557.5 is a bacterioferritin , 1979, Nature.

[43]  W. V. Shaw,et al.  Solving the structure of human H ferritin by genetically engineering intermolecular crystal contacts , 1991, Nature.

[44]  Collaborative Computational,et al.  The CCP4 suite: programs for protein crystallography. , 1994, Acta crystallographica. Section D, Biological crystallography.

[45]  J. Thornton,et al.  PROCHECK: a program to check the stereochemical quality of protein structures , 1993 .

[46]  K Henrick,et al.  Electronic Reprint Biological Crystallography Secondary-structure Matching (ssm), a New Tool for Fast Protein Structure Alignment in Three Dimensions Biological Crystallography Secondary-structure Matching (ssm), a New Tool for Fast Protein Structure Alignment in Three Dimensions , 2022 .

[47]  T. J. Stillman,et al.  The high-resolution X-ray crystallographic structure of the ferritin (EcFtnA) of Escherichia coli; comparison with human H ferritin (HuHF) and the structures of the Fe(3+) and Zn(2+) derivatives. , 2001, Journal of molecular biology.

[48]  N. Chasteen,et al.  Metal ion complexes of apoferritin. Evidence for initial binding in the hydrophilic channels. , 1986, The Journal of biological chemistry.

[49]  D S Moss,et al.  Rfree and the rfree ratio. I. Derivation of expected values of cross-validation residuals used in macromolecular least-squares refinement. , 1998, Acta crystallographica. Section D, Biological crystallography.

[50]  M. A. Carrondo,et al.  Crystallization and preliminary X-ray characterization of a ferritin from the hyperthermophilic archaeon and anaerobe Pyrococcus furiosus. , 2005, Acta crystallographica. Section F, Structural biology and crystallization communications.

[51]  Randy J Read,et al.  Electronic Reprint Biological Crystallography Likelihood-enhanced Fast Rotation Functions Biological Crystallography Likelihood-enhanced Fast Rotation Functions , 2003 .

[52]  Kevin Cowtan,et al.  research papers Acta Crystallographica Section D Biological , 2005 .