Uhlmann et al., 2000). All members are characterised by
a catalytic dyad which is present in a His-Gly-spacer-Ala-
Cys motif. Comparison of the crystal structures of cas-
pase 1 and 3 with gingipain revealed a very similar active
centre topology where the active site residues occupy
identical positions. Intriguingly, the two active site
residues are located on opposite sides of the scissile
bond. A striking characteristic of the clan CD cysteine
peptidases is the lack of irreversible inhibition by E64, of-
ten considered to be a general inhibitor of cysteine en-
dopeptidases.
So far, synthetic inhibitors against clan CD peptidases
of the caspase, gingipain, and clostripain families have
been reported. The benzoyloxymethyl ketone inhibitor
Cbz-L-Phe-L-Lys-CH
2
O-CO-2,4,6-Me
3
-Ph specifically
inhibits gingipain K. The chloromethylketones (CMK) H-
D-Phe-L-Pro-L-Arg-CH
2
Cl and H-D-Phe-L-Phe-L-Arg-
CH
2
Cl react irreversibly with Arg-specific gingipain and
clostripain, allowing active site titration (Potempa et al.,
1997). Chloromethylketones with the core-structure H-L-
Phe-L-Ala-L-Lys-L-Arg having an ethyl residue and
methyl residue were shown to be potent irreversible in-
hibitors of clostripain (Wikstrom et al., 1989). For the cas-
pases, several different classes of inhibitors have been
described, including aldehydes (Chapman, 1992), non-
peptidic pyridone aldehydes (Golec et al., 1997), pheny-
lalkyl ketones (Mjalli et al., 1993), acyloxymethyl ketones
(Revesz et al., 1994; Thornberry et al., 1994), 1-phenyl-3-
(trifluoromethyl)-pyrazol-5-yl-oxymethyl ketones (Dolle
et al., 1994), fluoromethylketones (Revesz et al., 1994;
Hara et al., 1997), and chloromethylketones (Schulz et al.,
1996).
Legumain was first discovered in plants and the inver-
tebrate animal, Schistosoma, but was found in human
placenta by Chen et al. (1997). From all sources, legu-
main shows strict specificity for cleavage after as-
paragine residues, which suggests that the physiological
function may involve limited proteolysis. So far, there is
strong evidence in plants that legumain might be in-
volved in protein splicing (Min and Jones, 1994). An acti-
vation of precursor proteins has been reported in plants
as well (Hara-Nishimura et al., 1995). The mammalian
lysosomal enzyme was reported to play a key role in the
processing of bacterial antigen for presentation in the
MHC II class system (Manoury et al., 1998; Antoniou
et al., 2000). In addition, by screening an osteoclast
cDNA expression library, legumain has been identified in-
hibiting osteoclast formation and bone resorption (Choi
et al., 1999). The regulation of legumain activity is still un-
clear, but its inhibition by some cystatins, the general ex-
tracellular cysteine peptidase inhibitors, was reported
Biol. Chem., Vol. 383, pp. 1205 – 1214, July / August 2002 · Copyright © by Walter de Gruyter · Berlin · New York
André J. Niestroj
1
, Kirstin Feußner
1
, Ulrich
Heiser
1
, Pam M. Dando
2
, Alan Barrett
2
, Bernd
Gerhartz
1
and Hans-Ulrich Demuth
1,
*
1
Probiodrug AG, Weinbergweg 22 – Biocenter, D-06120
Halle (Saale), Germany
2
MRC Molecular Enzymology Laboratory, Babraham
Institute, Cambridge CB2 4AT, UK
* Corresponding author
Legumain is a lysosomal cysteine peptidase specific
for an asparagine residue in the P
1
-position. It has
been classified as a member of clan CD peptidases
due to predicted structural similarities to caspases
and gingipains. So far, inhibition studies on legumain
are limited by the use of endogenous inhibitors such
as cystatin C. A series of Michael acceptor inhibitors
based on the backbone Cbz-L-Ala-L-Ala-L-Asn (Cbz=
benzyloxycarbonyl) has been prepared and resulted
in an irreversible inhibition of porcine legumain. Vari-
ation of the molecular size within the ‘war head’ re-
vealed the best inhibition for the compound contain-
ing the allyl ester (k
obs
/I=766 M
–1
s
–1
). To overcome
cyclisation between the amide moiety of the Asn
residue and the ‘war head’, several asparagine ana-
logues have been synthesised. Integrated in halo-
methylketone inhibitors, azaasparagine is accepted
by legumain in the P
1
-position. The most potent
inhibitor of this series, Cbz-L-Ala-L-Ala-AzaAsn-
chloromethylketone, displays a k
obs
/I value of 139 000
M
–1
s
–1
. Other cysteine peptidases, such as papain
and cathepsin B, are not inhibited by this compound
at concentrations up to 100 μM. The synthetic in-
hibitors described here represent useful tools for the
investigation of the structural and physiological prop-
erties of this unique asparagine-specific peptidase.
Key words: α,β-Unsaturated esters / Azaasparagine /
Benzoyloxymethylketone / Cysteine protease /
Halomethylketone / Legumain / Michael acceptors.
Introduction
Cysteine peptidases grouped into the clan CD represent
a new emerging class of enzymes displaying a novel cat-
alytic mechanism different to classical papain-like pepti-
dases of clan CA. So far, five different families have been
placed in the clan CD, namely family C11 clostripain,
family C13 legumain, family C14 caspases, family C25
gingipain, and family C50 separin (Chen et al., 1998a;
Inhibition of Mammalian Legumain by Michael
Acceptors and AzaAsn-Halomethylketones
Bereitgestellt von | SUB Göttingen
Angemeldet
Heruntergeladen am | 22.01.15 10:25