Paralog of the formylglycine-generating enzyme - retention in the endoplasmic reticulum by canonical and noncanonical signals

Gande SL, Mariappan M, Schmidt B, Pringle TH, von Figura K, Dierks T (2008)
FEBS JOURNAL 275(6): 1118-1130.

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Abstract
Formylglycine-generating enzyme (FGE) catalyzes in newly synthesized sulfatases the oxidation of a specific cysteine residue to formylglycine, which is the catalytic residue required for sulfate ester hydrolysis. This post-translational modification occurs in the endoplasmic reticulum (ER), and is an essential step in the biogenesis of this enzyme family. A paralog of FGE (pFGE) also localizes to the ER. It shares many properties with FGE, but lacks formylglycine-generating activity. There is evidence that FGE and pFGE act in concert, possibly by forming complexes with sulfatases and one another. Here we show that human pFGE, but not FGE, is retained in the ER through its C-terminal tetrapeptide PGEL, a noncanonical variant of the classic KDEL ER-retention signal. Surprisingly, PGEL, although having two nonconsensus residues (PG), confers efficient ER retention when fused to a secretory protein. Inducible coexpression of pFGE at different levels in FGE-expressing cells did not significantly influence the kinetics of FGE secretion, suggesting that pFGE is not a retention factor for FGE in vivo. PGEL is accessible at the surface of the pFGE structure. It is found in 21 mammalian species with available pFGE sequences. Other species carry either canonical signals (eight mammals and 26 nonmammals) or different noncanonical variants (six mammals and six nonmammals). Among the latter, SGEL was tested and found to also confer ER retention. Although evolutionarily conserved for mammalian pFGE, the PGEL signal is found only in one further human protein entering the ER. Its consequences for KDEL receptor-mediated ER retrieval and benefit for pFGE functionality remain to be fully resolved.
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Gande SL, Mariappan M, Schmidt B, Pringle TH, von Figura K, Dierks T. Paralog of the formylglycine-generating enzyme - retention in the endoplasmic reticulum by canonical and noncanonical signals. FEBS JOURNAL. 2008;275(6):1118-1130.
Gande, S. L., Mariappan, M., Schmidt, B., Pringle, T. H., von Figura, K., & Dierks, T. (2008). Paralog of the formylglycine-generating enzyme - retention in the endoplasmic reticulum by canonical and noncanonical signals. FEBS JOURNAL, 275(6), 1118-1130.
Gande, S. L., Mariappan, M., Schmidt, B., Pringle, T. H., von Figura, K., and Dierks, T. (2008). Paralog of the formylglycine-generating enzyme - retention in the endoplasmic reticulum by canonical and noncanonical signals. FEBS JOURNAL 275, 1118-1130.
Gande, S.L., et al., 2008. Paralog of the formylglycine-generating enzyme - retention in the endoplasmic reticulum by canonical and noncanonical signals. FEBS JOURNAL, 275(6), p 1118-1130.
S.L. Gande, et al., “Paralog of the formylglycine-generating enzyme - retention in the endoplasmic reticulum by canonical and noncanonical signals”, FEBS JOURNAL, vol. 275, 2008, pp. 1118-1130.
Gande, S.L., Mariappan, M., Schmidt, B., Pringle, T.H., von Figura, K., Dierks, T.: Paralog of the formylglycine-generating enzyme - retention in the endoplasmic reticulum by canonical and noncanonical signals. FEBS JOURNAL. 275, 1118-1130 (2008).
Gande, Santosh Lakshmi, Mariappan, Malaiyalam, Schmidt, Bernhard, Pringle, Thomas H., von Figura, Kurt, and Dierks, Thomas. “Paralog of the formylglycine-generating enzyme - retention in the endoplasmic reticulum by canonical and noncanonical signals”. FEBS JOURNAL 275.6 (2008): 1118-1130.
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44 References

Data provided by Europe PubMed Central.

PROSITE: a documented database using patterns and profiles as motif descriptors.
Sigrist CJ, Cerutti L, Hulo N, Gattiker A, Falquet L, Pagni M, Bairoch A, Bucher P., Brief. Bioinformatics 3(3), 2002
PMID: 12230035
Molecular characterization of the human Calpha-formylglycine-generating enzyme.
Preusser-Kunze A, Mariappan M, Schmidt B, Gande SL, Mutenda K, Wenzel D, von Figura K, Dierks T., J. Biol. Chem. 280(15), 2005
PMID: 15657036
Sorting of soluble ER proteins in yeast.
Pelham HR, Hardwick KG, Lewis MJ., EMBO J. 7(6), 1988
PMID: 3049074
Identification of amino acids in the binding pocket of the human KDEL receptor.
Scheel AA, Pelham HR., J. Biol. Chem. 273(4), 1998
PMID: 9442098
Sequence of a second human KDEL receptor.
Lewis MJ, Pelham HR., J. Mol. Biol. 226(4), 1992
PMID: 1325562
A single polypeptide acts both as the beta subunit of prolyl 4-hydroxylase and as a protein disulfide-isomerase.
Koivu J, Myllyla R, Helaakoski T, Pihlajaniemi T, Tasanen K, Kivirikko KI., J. Biol. Chem. 262(14), 1987
PMID: 3032969
Molecular cloning of the beta-subunit of human prolyl 4-hydroxylase. This subunit and protein disulphide isomerase are products of the same gene.
Pihlajaniemi T, Helaakoski T, Tasanen K, Myllyla R, Huhtala ML, Koivu J, Kivirikko KI., EMBO J. 6(3), 1987
PMID: 3034602
Thiol-mediated protein retention in the endoplasmic reticulum: the role of ERp44.
Anelli T, Alessio M, Bachi A, Bergamelli L, Bertoli G, Camerini S, Mezghrani A, Ruffato E, Simmen T, Sitia R., EMBO J. 22(19), 2003
PMID: 14517240
A C-terminal signal prevents secretion of luminal ER proteins.
Munro S, Pelham HR., Cell 48(5), 1987
PMID: 3545499
The Hera database and its use in the characterization of endoplasmic reticulum proteins.
Scott M, Lu G, Hallett M, Thomas DY., Bioinformatics 20(6), 2004
PMID: 14751973
Annotating proteins from endoplasmic reticulum and Golgi apparatus in eukaryotic proteomes.
Wrzeszczynski KO, Rost B., Cell. Mol. Life Sci. 61(11), 2004
PMID: 15170512
The dynamic organisation of the secretory pathway.
Pelham HR., Cell Struct. Funct. 21(5), 1996
PMID: 9118249
pH-dependent binding of KDEL to its receptor in vitro.
Wilson DW, Lewis MJ, Pelham HR., J. Biol. Chem. 268(10), 1993
PMID: 8385108
Sulfatase modifying factor 1 trafficking through the cells: from endoplasmic reticulum to the endoplasmic reticulum.
Zito E, Buono M, Pepe S, Settembre C, Annunziata I, Surace EM, Dierks T, Monti M, Cozzolino M, Pucci P, Ballabio A, Cosma MP., EMBO J. 26(10), 2007
PMID: 17446859
Characterization of brefeldin A induced vesicular structures containing cycling proteins of the intermediate compartment/cis-Golgi network.
Fullekrug J, Sonnichsen B, Schafer U, Nguyen Van P, Soling HD, Mieskes G., FEBS Lett. 404(1), 1997
PMID: 9074641
Exploring the sequence space for tetracycline-dependent transcriptional activators: novel mutations yield expanded range and sensitivity.
Urlinger S, Baron U, Thellmann M, Hasan MT, Bujard H, Hillen W., Proc. Natl. Acad. Sci. U.S.A. 97(14), 2000
PMID: 10859354

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