Calpains (EC 3.4.22.17, Clan CA, family C02) in mammals co-exist in cells with the very specific endogenous inhibitor protein, “calpastatin”, strongly suggesting the pivotal role of this inhibitor in the regulation of calpain activity (Goll et al. 1992; Kawasaki & Kawashima 1996; Maki et al. 1991; Menard & el-Amine 1996; Nixon et al. 1994). Calpastatin was first cloned in 1987 (Emori et al. 1987) and then found not to have exact secondary structures (Uemori et al. 1990). Calpastatin contains four equivalent inhibitory domains of ca. 140 residues having three conserved regions, A, B, and C, important for inhibition (Fig. 1). A and C interact with IV and VI, respectively, in a Ca2+-dependent manner, and B shows inhibitory activity by itself probably by binding at or near the active site (Tompa et al. 2002) (Fig. 2). Presence of two calmodulin-like domains IV and VI are necessary for effective inhibition by calpastatin. Thus calpastatin inhibits only dimeric calpain, namely μ-calpain, m-calpain, and nCL-4/CAPN9 with 30K. Calpain large subunit homologues including p94/CAPN3 and nCL-2/CAPN8 are not inhibited and escape from the regulation by calpastatin (Hata et al. 2001; Ono et al. 2004; Sorimachi et al. 1993b).
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Fig. 1. Schematic structure of human calpastatin
Calpastatin has four repetitive inhibitory domains (1~4), which can inhibit one molecule of heterodimer calpains, although their inhibitory activities vary. At the N-terminus, there are two extended domains, XL and L, whose functions are unknown. Each inhibitory domain has three regions, A, B, and C, which binds to domain IV of catalytic subunit, the active site of domain II, and domain VI of regulatory subunit (see Fig. 2), respectively. Peptide corresponding to only the Region B has inhibitor activity, which is less than full-length domain. The Region B has highly conserved sequences at the center, whose consensus is GxxE/DxTIPPxYR.
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Fig. 2. Three-dimensional structure of 30K homodimer biding to calpastatin region C and synthetic calpain inhibitor molecule PD150606
A peptide corresponding to the Region B (see Fig. 1) of human calpastatin binds to the first α-helix (E-helix) of the first EF-hand motif (EF-1) of both 30K molecule. PD150606 (3-(4-iodophenyl)-2-mercapto-(Z)-2-propenoic acid), which is a unique synthetic inhibitor molecule for calpains not directing to the active site, binds close to the loop region of EF-3 and E-helix of EF-5. Cross-eye representation.
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All sections ≫ open : close
1. Structure of calpastatin
Maki’s group, the successors of the late Prof. ex-Murachi, one of the great pioneers of calpain research, examined the interaction between calpastatin and calpain subunits in a real-time biomolecular interaction analysis using a BIAcore instrument (Takano et al. 1995). They showed that three subdomains of the reactive site of calpastatin bind to domain IV of the large subunit, the active site, and domain IV’ (VI) of the small subunit, respectively, a finding consistent with their previous observations (Crawford et al. 1993; Kawasaki et al. 1993; Ma et al. 1994; Nishimura & Goll 1991; Takano et al. 1995). Interestingly, the muscle-specific homologue of calpain, p94, described below, is not inhibited by calpastatin, and, moreover, proteolyzes it in the COS-cell expression system (Ono et al. 2004; Sorimachi et al. 1995). One possible explanation for this is as follows: Calpastatin binds to the Ca2+-binding domains of both the large and small subunits, but p94 is not associated with the conventional calpain small subunit as described below, and, thus, calpastatin cannot bind firmly to p94, resulting in the digestion of rather than inhibition by calpastatin.
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Fig. 3. Three-dimensional structure of μ-calpain protease domain (domain II) with Ca2+ and inhibitor molecules
Ca2+ (dark blue ball) binds to the upper side of the active site cleft, which consists of Cys115, His 282, and Asn 296 (red ball-and-stick). E64 (upper) and leupeptin (lower) covalently bind to the sulfur atom of the active site Cys115. While E64 is an irreversible inhibitor, leupeptin dissociates from calpain when Ca2+ is depleted. Cross-eye representation.
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2. Other synthetic inhibitors of calpain
As for synthetic calpain inhibitors, their history goes back to 1980 when Sugita and colleagues used derivatives of E64 (N-(N-(L-3-trans-carboxyoxirane-2-carbonyl)-L-leucyl)agmatin) to prevent muscle degradation in patients with muscular dystrophy (Sugita et al. 1980). E64 was first isolated as a papain inhibitor from the culture medium of Aspergillus japonicus. Typical derivatives, E64c (N-(N-(L-3-trans-carboxyoxirane-2-carbonyl)-L-leucyl)isoamylamine) and E64d (N-(N-(L-3-trans-ethoxycarbonyloxyoxirane-2-carbonyl)-L-leucyl)isoamylamine), a membrane-permeable derivative of E64c, have together with E64 been widely used for various purposes (Ishiura et al. 1981; McGowan et al. 1989; Suzuki et al. 1981). Although E64, E64c, E64d, and leupeptin (N-acetyl-Leu-Leu-argininal) efficiently inhibit both μ- and m-calpains (see Fig. 3), they are not very specific as they also inhibit other cysteine proteinases. Leupeptin inhibits proteasome at the same or even lower concentrations. It is noteworthy that E-64 and leupeptin do not suppress the autolysis of p94 at all as described later (Sorimachi et al. 1993a). Calpain inhibitors I (N-acetyl-Leu-Leu-norleucinal) and II (N-acetyl-Leu-Leu-methioninal) are frequently used and commercially available (Wang 1990), but they also inhibit proteasome and other cysteine proteinases (Figueiredo-Pereira et al. 1994; Tsubuki et al. 1996). In this respect, the results concerning the differential inhibition of calpain and proteasome by di- and tri-leucyl aldehydes as shown by Tsubuki and colleagues are noteworthy (Tsubuki et al. 1996). They synthesized benzyloxycarbonyl-Leu-Leu-leucinal (ZLLLal) and benzyloxycarbonyl-Leu-leucinal (ZLLal) and showed that both ZLLLal and ZLLal strongly inhibit calpain (Ki= ca. 1 μM), but that only ZLLLal inhibits proteasome [Ki= ca. 1 μM and 0.1 μM for the ZLLL-4-methylcoumaryl-7-amide (ZLLL-MCA) and succinyl-LLVY-MCA-degrading activity of proteasome, respectively] while the Ki for ZLLal is above 100 μM for both activities. These synthetic inhibitors are potentially useful for identifying the functions of calpain and proteasome in cell biology.
Powers and coworkers (Bartus et al. 1994) developed ketoamide inhibitor molecules, AK295 (benzyloxycarbonyl-Leu-aminobutyric acid-CONH(CH2)3-morpholine), AK275 (benzyloxycarbonyl-Leu-aminobutyric acid-CONH-CH2CH3), and CX275 (the active isomer of the diastereomeric mixture of AK275), which are more effective and more calpain-specific than the above inhibitors. The Ki value of AK295 is about 30 nM for μ- and m-calpain and about 1,000 times higher for cathepsin B. The same researchers also screened derivatives of peptidyl alpha-keto compounds to improve the specificity and Ki value, and found that benzyloxycarbonyl-Leu-aminobutyric acid-CONH-CH2-CHOH-C6H5 (Ki=15 nM for m-calpain) and benzyloxycarbonyl-Leu-norvalyl-CONH-CH2-2-pyridyl (Ki=19 nM for μ-calpain) are the best inhibitors among over 100 molecules tested (Li et al. 1996; Li et al. 1993).
On the other hand, Wang and colleagues (Wang et al. 1996) developed a novel inhibitor with a distinct inhibitory mechanism compared to the other active site-directed inhibitors as described above. Their inhibitor, PD150606, shows a Ki value for μ- and m-calpains of about 0.3 μM, but greater than 100 μM for cathepsin B and papain, indicating its high specificity for calpains relative to other proteinases. It binds to the Ca2+-binding domain of calpain thus inhibiting calpastatin binding. Therefore, PD150606, when used in combination with other active site-directed inhibitors such as AK295, produces a very specific inhibition of calpain, a characteristic that is essential for in vivo studies of the physiological functions of calpain.
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