Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.


Science 21 August 1998:
Vol. 281. no. 5380, pp. 1197 - 1200
DOI: 10.1126/science.281.5380.1197

Reports

Prototype of a Heme Chaperone Essential for Cytochrome c Maturation

Henk Schulz, Hauke Hennecke, Linda Thöny-Meyer *

Heme, the iron-containing cofactor essential for the activity of many enzymes, is incorporated into its target proteins by unknown mechanisms. Here, an Escherichia coli hemoprotein, CcmE, was shown to bind heme in the bacterial periplasm by way of a single covalent bond to a histidine. The heme was then released and delivered to apocytochrome c. Thus, CcmE can be viewed as a heme chaperone guiding heme to its appropriate biological partner and preventing illegitimate complex formation.

Mikrobiologisches Institut, Eidgenössische Technische Hochschule, Schmelzbergstrasse 7, CH-8092 Zürich, Switzerland.
*   To whom correspondence should be addressed. E-mail: lthoeny{at}micro.biol.ethz.ch


Read the Full Text


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Cytochrome c Biogenesis: Mechanisms for Covalent Modifications and Trafficking of Heme and for Heme-Iron Redox Control.
R. G. Kranz, C. Richard-Fogal, J.-S. Taylor, and E. R. Frawley (2009)
Microbiol. Mol. Biol. Rev. 73, 510-528
   Abstract »    Full Text »    PDF »
Biogenesis of cytochrome b6 in photosynthetic membranes.
D. Saint-Marcoux, F.-A. Wollman, and C. de Vitry (2009)
J. Cell Biol. 185, 1195-1207
   Abstract »    Full Text »    PDF »
His protects heme as it crosses the membrane.
S. S. Merchant (2009)
PNAS 106, 10069-10070
   Full Text »    PDF »
Topology and Function of CcmD in Cytochrome c Maturation.
C. L. Richard-Fogal, E. R. Frawley, and R. G. Kranz (2008)
J. Bacteriol. 190, 3489-3493
   Abstract »    Full Text »    PDF »
AtCCMA Interacts with AtCcmB to Form a Novel Mitochondrial ABC Transporter Involved in Cytochrome c Maturation in Arabidopsis.
N. Rayapuram,, J. Hagenmuller,, J.-M. Grienenberger, P. Giege, and G. Bonnard (2007)
J. Biol. Chem. 282, 21015-21023
   Abstract »    Full Text »    PDF »
Dynamic Ligation Properties of the Escherichia coli Heme Chaperone CcmE to Non-covalently Bound Heme.
J. M. Stevens, T. Uchida, O. Daltrop, T. Kitagawa, and S. J. Ferguson (2006)
J. Biol. Chem. 281, 6144-6151
   Abstract »    Full Text »    PDF »
Functional Characterization of the C-terminal Domain of the Cytochrome c Maturation Protein CcmE.
E. M. Harvat, J. M. Stevens, C. Redfield, and S. J. Ferguson (2005)
J. Biol. Chem. 280, 36747-36753
   Abstract »    Full Text »    PDF »
AtCCMH, an essential component of the c-type cytochrome maturation pathway in Arabidopsis mitochondria, interacts with apocytochrome c.
E. H. Meyer, P. Giege, E. Gelhaye, N. Rayapuram, U. Ahuja, L. Thony-Meyer, J.-M. Grienenberger, and G. Bonnard (2005)
PNAS 102, 16113-16118
   Abstract »    Full Text »    PDF »
Cytochrome c Maturation and the Physiological Role of c-Type Cytochromes in Vibrio cholerae.
M. Braun and L. Thony-Meyer (2005)
J. Bacteriol. 187, 5996-6004
   Abstract »    Full Text »    PDF »
Overproduction of CcmG and CcmFHRc Fully Suppresses the c-Type Cytochrome Biogenesis Defect of Rhodobacter capsulatus CcmI-Null Mutants.
C. Sanders, M. Deshmukh, D. Astor, R. G. Kranz, and F. Daldal (2005)
J. Bacteriol. 187, 4245-4256
   Abstract »    Full Text »    PDF »
sacB-5-Fluoroorotic Acid-pyrE-Based Bidirectional Selection for Integration of Unmarked Alleles into the Chromosome of Rhodobacter capsulatus.
T. Yano, C. Sanders, J. Catalano, and F. Daldal (2005)
Appl. Envir. Microbiol. 71, 3014-3024
   Abstract »    Full Text »    PDF »
CcmD Is Involved in Complex Formation between CcmC and the Heme Chaperone CcmE during Cytochrome c Maturation.
U. Ahuja and L. Thony-Meyer (2005)
J. Biol. Chem. 280, 236-243
   Abstract »    Full Text »    PDF »
The Interaction of Covalently Bound Heme with the Cytochrome c Maturation Protein CcmE.
T. Uchida, J. M. Stevens, O. Daltrop, E. M. Harvat, L. Hong, S. J. Ferguson, and T. Kitagawa (2004)
J. Biol. Chem. 279, 51981-51988
   Abstract »    Full Text »    PDF »
KatG Is the Primary Detoxifier of Hydrogen Peroxide Produced by Aerobic Metabolism in Bradyrhizobium japonicum.
H. R. Panek and M. R. O'Brian (2004)
J. Bacteriol. 186, 7874-7880
   Abstract »    Full Text »    PDF »
Structural Basis of Redox-coupled Protein Substrate Selection by the Cytochrome c Biosynthesis Protein ResA.
A. Crow, R. M. Acheson, N. E. Le Brun, and A. Oubrie (2004)
J. Biol. Chem. 279, 23654-23660
   Abstract »    Full Text »    PDF »
Dynamic Features of a Heme Delivery System for Cytochrome c Maturation.
U. Ahuja and L. Thony-Meyer (2003)
J. Biol. Chem. 278, 52061-52070
   Abstract »    Full Text »    PDF »
Co-ordination of iron acquisition, iron porphyrin chelation and iron-protoporphyrin export via the cytochrome c biogenesis protein CcmC in Pseudomonas fluorescens.
C. Baysse, S. Matthijs, M. Schobert, G. Layer, D. Jahn, and P. Cornelis (2003)
Microbiology 149, 3543-3552
   Abstract »    Full Text »    PDF »
The C-terminally Truncated NuoL Subunit (ND5 Homologue) of the Na+-dependent Complex I from Escherichia coli Transports Na+.
J. Steuber (2003)
J. Biol. Chem. 278, 26817-26822
   Abstract »    Full Text »    PDF »
The C-Terminal Flexible Domain of the Heme Chaperone CcmE Is Important but Not Essential for Its Function.
E. Enggist and L. Thony-Meyer (2003)
J. Bacteriol. 185, 3821-3827
   Abstract »    Full Text »    PDF »
Interaction of Heme with Variants of the Heme Chaperone CcmE Carrying Active Site Mutations and a Cleavable N-terminal His Tag.
J. M. Stevens, O. Daltrop, C. W. Higham, and S. J. Ferguson (2003)
J. Biol. Chem. 278, 20500-20506
   Abstract »    Full Text »    PDF »
Cytochrome c Maturation. THE IN VITRO REACTIONS OF HORSE HEART APOCYTOCHROME c AND PARACOCCUS DENITRIFICANS APOCYTOCHROME c550 WITH HEME.
O. Daltrop and S. J. Ferguson (2003)
J. Biol. Chem. 278, 4404-4409
   Abstract »    Full Text »    PDF »
Essential Histidine and Tryptophan Residues in CcsA, a System II Polytopic Cytochrome c Biogenesis Protein.
P. P. Hamel, B. W. Dreyfuss, Z. Xie, S. T. Gabilly, and S. Merchant (2003)
J. Biol. Chem. 278, 2593-2603
   Abstract »    Full Text »    PDF »
Functional Analysis of a Divergent System II Protein, Ccs1, Involved in c-Type Cytochrome Biogenesis.
B. W. Dreyfuss, P. P. Hamel, S. S. Nakamoto, and S. Merchant (2003)
J. Biol. Chem. 278, 2604-2613
   Abstract »    Full Text »    PDF »
Biochemical and Mutational Characterization of the Heme Chaperone CcmE Reveals a Heme Binding Site.
E. Enggist, M. J. Schneider, H. Schulz, and L. Thony-Meyer (2003)
J. Bacteriol. 185, 175-183
   Abstract »    Full Text »    PDF »
Molecular and Spectroscopic Analysis of the Cytochrome cbb3 Oxidase from Pseudomonas stutzeri.
R. S. Pitcher, M. R. Cheesman, and N. J. Watmough (2002)
J. Biol. Chem. 277, 31474-31483
   Abstract »    Full Text »    PDF »
The CcmE protein of the c-type cytochrome biogenesis system: Unusual in vitro heme incorporation into apo-CcmE and transfer from holo-CcmE to apocytochrome.
O. Daltrop, J. M. Stevens, C. W. Higham, and S. J. Ferguson (2002)
PNAS 99, 9703-9708
   Abstract »    Full Text »    PDF »
In vitro formation of a c-type cytochrome.
O. Daltrop, J. W. A. Allen, A. C. Willis, and S. J. Ferguson (2002)
PNAS 99, 7872-7876
   Abstract »    Full Text »    PDF »
A Bacterial Cytochrome c Heme Lyase. CcmF FORMS A COMPLEX WITH THE HEME CHAPERONE CcmE AND CcmH BUT NOT WITH APOCYTOCHROME c.
Q. Ren, U. Ahuja, and L. Thony-Meyer (2002)
J. Biol. Chem. 277, 7657-7663
   Abstract »    Full Text »    PDF »
Interspecies Complementation of Escherichia coli ccm Mutants: CcmE (CycJ) from Bradyrhizobium japonicum Acts as a Heme Chaperone during Cytochrome c Maturation.
H. Schulz and L. Thöny-Meyer (2000)
J. Bacteriol. 182, 6831-6833
   Abstract »    Full Text »
Genetic and Biochemical Characterization of the Pathway in Pantoea citrea Leading to Pink Disease of Pineapple.
C. J. Pujol and C. I. Kado (2000)
J. Bacteriol. 182, 2230-2237
   Abstract »    Full Text »
Oxidase and periplasmic cytochrome assembly in Escherichia coli K-12: CydDC and CcmAB are not required for haem-membrane association.
G. M. Cook and R. K. Poole (2000)
Microbiology 146, 527-536
   Abstract »    Full Text »
Mutational analysis of the Paracoccus denitrificans c-type cytochrome biosynthetic genes ccmABCDG: disruption of ccmC has distinct effects suggesting a role for CcmC independent of CcmAB.
M. D. Page and S. J. Ferguson (1999)
Microbiology 145, 3047-3057
   Abstract »    Full Text »    PDF »
Heme transfer to the heme chaperone CcmE during cytochrome c maturation requires the CcmC protein, which may function independently of the ABC-transporter CcmAB.
H. Schulz, R. A. Fabianek, E. C. Pellicioli, H. Hennecke, and L. Thony-Meyer (1999)
PNAS 96, 6462-6467
   Abstract »    Full Text »    PDF »
CCME, a Nuclear-encoded Heme-binding Protein Involved in Cytochrome c Maturation in Plant Mitochondria.
N. Spielewoy, H. Schulz, J. M. Grienenberger, L. Thony-Meyer, and G. Bonnard (2001)
J. Biol. Chem. 276, 5491-5497
   Abstract »    Full Text »    PDF »
Physical Interaction of CcmC with Heme and the Heme Chaperone CcmE during Cytochrome c Maturation.
Q. Ren and L. Thony-Meyer (2001)
J. Biol. Chem. 276, 32591-32596
   Abstract »    Full Text »    PDF »



To Advertise     Find Products


Science. ISSN 0036-8075 (print), 1095-9203 (online)