A proprotein convertase-inhibiting serpin with an ER targeting signal from Branchiostoma lanceolatum, a close relative of vertebrates

Bentele C, Krüger O, Tödtmann U, Oley M, Ragg H (2006)
Biochem. J. 395(3): 449-456.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
Download
Es wurden keine Dateien hochgeladen. Nur Publikationsnachweis!
Autor*in
Bentele, Caterina; Krüger, Olaf; Tödtmann, Ulf; Oley, Mareke; Ragg, HermannUniBi
Abstract / Bemerkung
Lancelets are considered to take a key position in the evolution of lineages leading to vertebrates. Herein, a serpin from the lancelet Branchiostoma lanceolatum, Bl-Spn1, was identified that inhibits the PCs (proprotein convertases) PC1/3 and furin. The inhibitor forms SDS-stable complexes with either of its targets. Analysis of the inhibitor/furin reaction products by mass spectroscopy assigns the enzyme's cleavage position C-terminally to Met-Met-Lys-Arg downward arrow in the reactive site loop of Spn1, in concordance with the classical recognition/cleavage site of the principal vertebrate PCs. The inhibitor is equipped with a canonical ER (endoplasmic reticulum) retrieval signal, Lys-Asp-Glu-Leu (KDEL), marking the inhibitor as a guardian of the cellular secretory routes. Deletion of the ER retrieval signal results in the export of the inhibitor into the medium of transfected COS-7 cells, consistent with the assigned intracellular location. These results identify Bl-Spn1 as the first serpin that may inhibit PC1/3-like subtilases at their natural sites of action. Phylogenetic comparisons support a concept implying a general role for ER-residing serpins in the surveillance of subtilase-like enzymes along the constitutive and regulated secretory pathways of metazoans including a role in the defence of intruders that turn PCs to their propagation.
Stichworte
furin; lancelet; Branchiostoma lanceolatum; serpin; proprotein convertase; secretory pathway
Erscheinungsjahr
2006
Zeitschriftentitel
Biochem. J.
Band
395
Ausgabe
3
Seite(n)
449-456
ISSN
0264-6021
eISSN
1470-8728
Page URI
https://pub.uni-bielefeld.de/record/1953791

Zitieren

Bentele C, Krüger O, Tödtmann U, Oley M, Ragg H. A proprotein convertase-inhibiting serpin with an ER targeting signal from Branchiostoma lanceolatum, a close relative of vertebrates. Biochem. J. 2006;395(3):449-456.
Bentele, C., Krüger, O., Tödtmann, U., Oley, M., & Ragg, H. (2006). A proprotein convertase-inhibiting serpin with an ER targeting signal from Branchiostoma lanceolatum, a close relative of vertebrates. Biochem. J., 395(3), 449-456. https://doi.org/10.1042/BJ20051947
Bentele, C., Krüger, O., Tödtmann, U., Oley, M., and Ragg, H. (2006). A proprotein convertase-inhibiting serpin with an ER targeting signal from Branchiostoma lanceolatum, a close relative of vertebrates. Biochem. J. 395, 449-456.
Bentele, C., et al., 2006. A proprotein convertase-inhibiting serpin with an ER targeting signal from Branchiostoma lanceolatum, a close relative of vertebrates. Biochem. J., 395(3), p 449-456.
C. Bentele, et al., “A proprotein convertase-inhibiting serpin with an ER targeting signal from Branchiostoma lanceolatum, a close relative of vertebrates”, Biochem. J., vol. 395, 2006, pp. 449-456.
Bentele, C., Krüger, O., Tödtmann, U., Oley, M., Ragg, H.: A proprotein convertase-inhibiting serpin with an ER targeting signal from Branchiostoma lanceolatum, a close relative of vertebrates. Biochem. J. 395, 449-456 (2006).
Bentele, Caterina, Krüger, Olaf, Tödtmann, Ulf, Oley, Mareke, and Ragg, Hermann. “A proprotein convertase-inhibiting serpin with an ER targeting signal from Branchiostoma lanceolatum, a close relative of vertebrates”. Biochem. J. 395.3 (2006): 449-456.

8 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Recent advances in the understanding of brown spider venoms: From the biology of spiders to the molecular mechanisms of toxins.
Gremski LH, Trevisan-Silva D, Ferrer VP, Matsubara FH, Meissner GO, Wille AC, Vuitika L, Dias-Lopes C, Ullah A, de Moraes FR, Chávez-Olórtegui C, Barbaro KC, Murakami MT, Arni RK, Senff-Ribeiro A, Chaim OM, Veiga SS., Toxicon 83(), 2014
PMID: 24631373
Origin of serpin-mediated regulation of coagulation and blood pressure.
Wang Y, Köster K, Lummer M, Ragg H., PLoS One 9(5), 2014
PMID: 24840053
Multiple gains of spliceosomal introns in a superfamily of vertebrate protease inhibitor genes.
Ragg H, Kumar A, Köster K, Bentele C, Wang Y, Frese MA, Prib N, Krüger O., BMC Evol Biol 9(), 2009
PMID: 19698129
Proteases for processing proneuropeptides into peptide neurotransmitters and hormones.
Hook V, Funkelstein L, Lu D, Bark S, Wegrzyn J, Hwang SR., Annu Rev Pharmacol Toxicol 48(), 2008
PMID: 18184105
Ancestry and evolution of a secretory pathway serpin.
Kumar A, Ragg H., BMC Evol Biol 8(), 2008
PMID: 18793432
Identification and characterization of a serpin from Eimeria acervulina.
Fetterer RH, Miska KB, Jenkins MC, Barfield RC, Lillehoj H., J Parasitol 94(6), 2008
PMID: 18576851

37 References

Daten bereitgestellt von Europe PubMed Central.

Interaction of subtilisins with serpins.
Komiyama T, Gron H, Pemberton PA, Salvesen GS., Protein Sci. 5(5), 1996
PMID: 8732759
The proprotein convertases.
Steiner DF., Curr Opin Chem Biol 2(1), 1998
PMID: 9667917
Molecular characterization, enzymatic analysis, and purification of murine proprotein convertase-1/3 (PC1/PC3) secreted from recombinant baculovirus-infected insect cells.
Boudreault A, Gauthier D, Rondeau N, Savaria D, Seidah NG, Chretien M, Lazure C., Protein Expr. Purif. 14(3), 1998
PMID: 9882569
Inhibition of furin by serpin Spn4A from Drosophila melanogaster.
Oley M, Letzel MC, Ragg H., FEBS Lett. 577(1-2), 2004
PMID: 15527779
Evidence for proprotein convertase activity in the endoplasmic reticulum/early Golgi.
Salvas A, Benjannet S, Reudelhuber TL, Chretien M, Seidah NG., FEBS Lett. 579(25), 2005
PMID: 16213495
Identification and characterization of proSAAS, a granin-like neuroendocrine peptide precursor that inhibits prohormone processing.
Fricker LD, McKinzie AA, Sun J, Curran E, Qian Y, Yan L, Patterson SD, Courchesne PL, Richards B, Levin N, Mzhavia N, Devi LA, Douglass J., J. Neurosci. 20(2), 2000
PMID: 10632593
A novel Drosophila serpin that inhibits serine proteases.
Han J, Zhang H, Min G, Kemler D, Hashimoto C., FEBS Lett. 468(2-3), 2000
PMID: 10692585
Evolution of the prohormone convertases: identification of a homologue of PC6 in the protochordate amphioxus.
Oliva AA Jr, Chan SJ, Steiner DF., Biochim. Biophys. Acta 1477(1-2), 2000
PMID: 10708868
Processing and sorting of the prohormone convertase 2 propeptide.
Muller L, Cameron A, Fortenberry Y, Apletalina EV, Lindberg I., J. Biol. Chem. 275(50), 2000
PMID: 10995742
Vertebrate serpins: construction of a conflict-free phylogeny by combining exon-intron and diagnostic site analyses.
Ragg H, Lokot T, Kamp PB, Atchley WR, Dress A., Mol. Biol. Evol. 18(4), 2001
PMID: 11264410
The serpins are an expanding superfamily of structurally similar but functionally diverse proteins. Evolution, mechanism of inhibition, novel functions, and a revised nomenclature.
Silverman GA, Bird PI, Carrell RW, Church FC, Coughlin PB, Gettins PG, Irving JA, Lomas DA, Luke CJ, Moyer RW, Pemberton PA, Remold-O'Donnell E, Salvesen GS, Travis J, Whisstock JC., J. Biol. Chem. 276(36), 2001
PMID: 11435447
The ordered and compartment-specfific autoproteolytic removal of the furin intramolecular chaperone is required for enzyme activation.
Anderson ED, Molloy SS, Jean F, Fei H, Shimamura S, Thomas G., J. Biol. Chem. 277(15), 2002
PMID: 11799113
Proprotein convertases in tumor progression and malignancy: novel targets in cancer therapy.
Khatib AM, Siegfried G, Chretien M, Metrakos P, Seidah NG., Am. J. Pathol. 160(6), 2002
PMID: 12057895
Ectodomain shedding of furin: kinetics and role of the cysteine-rich region.
Denault J, Bissonnette L, Longpre J, Charest G, Lavigne P, Leduc R., FEBS Lett. 527(1-3), 2002
PMID: 12220680
Furin at the cutting edge: from protein traffic to embryogenesis and disease.
Thomas G., Nat. Rev. Mol. Cell Biol. 3(10), 2002
PMID: 12360192
Precursor processing by kex2/furin proteases.
Rockwell NC, Krysan DJ, Komiyama T, Fuller RS., Chem. Rev. 102(12), 2002
PMID: 12475200
Serpin structure, mechanism, and function.
Gettins PG., Chem. Rev. 102(12), 2002
PMID: 12475206
The cystatin-related epididymal spermatogenic protein inhibits the serine protease prohormone convertase 2.
Cornwall GA, Cameron A, Lindberg I, Hardy DM, Cormier N, Hsia N., Endocrinology 144(3), 2003
PMID: 12586766
Multiple sequence alignment with the Clustal series of programs.
Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD., Nucleic Acids Res. 31(13), 2003
PMID: 12824352
Curbing activation: proprotein convertases in homeostasis and pathology.
Taylor NA, Van De Ven WJ, Creemers JW., FASEB J. 17(10), 2003
PMID: 12832286
Conserved Ser residues, the shutter region, and speciation in serpin evolution.
Krem MM, Di Cera E., J. Biol. Chem. 278(39), 2003
PMID: 12847097
Drosophila serpin 4 functions as a neuroserpin-like inhibitor of subtilisin-like proprotein convertases.
Osterwalder T, Kuhnen A, Leiserson WM, Kim YS, Keshishian H., J. Neurosci. 24(24), 2004
PMID: 15201320
The Spn4 gene of Drosophila encodes a potent furin-directed secretory pathway serpin.
Richer MJ, Keays CA, Waterhouse J, Minhas J, Hashimoto C, Jean F., Proc. Natl. Acad. Sci. U.S.A. 101(29), 2004
PMID: 15247425
Improved PC1/3 production through recombinant expression in insect cells and larvae.
Rabah N, Gauthier DJ, Gauthier D, Lazure C., Protein Expr. Purif. 37(2), 2004
PMID: 15358360
Identification and activity of a lower eukaryotic serine proteinase inhibitor (serpin) from Cyanea capillata: analysis of a jellyfish serpin, jellypin.
Cole EB, Miller D, Rometo D, Greenberg RM, Bromme D, Cataltepe S, Pak SC, Mills DR, Silverman GA, Luke CJ., Biochemistry 43(37), 2004
PMID: 15362859
The chordate amphioxus: an emerging model organism for developmental biology.
Holland LZ, Laudet V, Schubert M., Cell. Mol. Life Sci. 61(18), 2004
PMID: 15378201
The behavior and significance of slow-binding enzyme inhibitors.
Morrison JF, Walsh CT., Adv. Enzymol. Relat. Areas Mol. Biol. 61(), 1988
PMID: 3281418
Evolution of the insulin superfamily: cloning of a hybrid insulin/insulin-like growth factor cDNA from amphioxus.
Chan SJ, Cao QP, Steiner DF., Proc. Natl. Acad. Sci. U.S.A. 87(23), 1990
PMID: 1701257
Mechanism of serpin action: evidence that C1 inhibitor functions as a suicide substrate.
Patston PA, Gettins P, Beechem J, Schapira M., Biochemistry 30(36), 1991
PMID: 1888745
The neuroendocrine polypeptide 7B2 is an endogenous inhibitor of prohormone convertase PC2.
Martens GJ, Braks JA, Eib DW, Zhou Y, Lindberg I., Proc. Natl. Acad. Sci. U.S.A. 91(13), 1994
PMID: 8016065
Proprotein convertases in amphioxus: predicted structure and expression of proteases SPC2 and SPC3.
Oliva AA Jr, Steiner DF, Chan SJ., Proc. Natl. Acad. Sci. U.S.A. 92(8), 1995
PMID: 7724604
Inhibition of soluble recombinant furin by human proteinase inhibitor 8.
Dahlen JR, Jean F, Thomas G, Foster DC, Kisiel W., J. Biol. Chem. 273(4), 1998
PMID: 9442015

Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®

Quellen

PMID: 16445382
PubMed | Europe PMC

Suchen in

Google Scholar