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J. Biol. Chem., Vol. 278, Issue 4, 2593-2603, January 24, 2003
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From the Three distinct systems (I, II, and III) for
catalysis of heme attachment to c-type apocytochromes are
known. The CcsA and Ccs1 proteins are required in system II for the
assembly of bacterial and plastid cytochromes c. A
tryptophan-rich signature motif (WWD), also occurring in CcmC and CcmF
found in system I, and three histidinyl residues, all strictly
conserved in CcsA suggest a function in heme handling. Topological
analysis of plastid CcsA in bacteria using the PhoA and
LacZ
Essential Histidine and Tryptophan Residues in CcsA, a
System II Polytopic Cytochrome c Biogenesis
Protein*,
,,, and¶
Department of Chemistry and Biochemistry,
UCLA, Los Angeles, California 90095-1569
reporters placed the WWD motif, the conserved residues His212 and His347 on the lumen side of
the membrane, whereas His309 was assigned a location on the
stromal side. Functional analysis of CcsA through site-directed
mutagenesis enabled the designation of the initiation codon of the
ccsA gene and established the functional importance of the
WWD signature motif and the absolute requirement of all three
histidines for the assembly of plastid c-type cytochromes. In a ccsA mutant, a 200-kDa Ccs1-containing complex is
absent from solubilized thylakoid membranes, suggesting that CcsA
operates together with Ccs1. We propose a model where the WWD motif and histidine residues function in relaying heme from stroma to lumen and
we postulate the existence of a cytochrome c assembly
machinery containing CcsA, Ccs1 and additional components.
*
This work was supported by National Institutes of Health
Grant GM48350 (to S. M.) and American Heart Association Post-doctoral Fellowship 0120100Y (to P. H.).The costs of publication of this article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement" in accordance with 18 U.S.C. Section
1734 solely to indicate this fact.
The on-line version of this article (available at
http://www.jbc.org) contains a figure.
§
Present address: Biocept, 2151 Las Palmas Dr., Ste. C, Carlsbad, CA 92009.
¶
To whom correspondence should be addressed: Dept. of Chemistry
and Biochemistry, UCLA, Box 951569, Los Angeles, CA 90095-1569. Tel.:
310-825-8300; Fax: 310-206-1035; E-mail:
merchant@chem.ucla.edu.
Copyright © 2003 by The American Society for Biochemistry and Molecular Biology, Inc.
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