Calpastatin exon 1B-derived peptide, a selective inhibitor of calpain: Enhancing cell permeability by conjugation with penetratin

Biological Chemistry

Volumn 384, Issue 3, 2003, Pages 395-402

  Gil Parrado, Shirley ^a,b   Assfalg Machleidt, Irmgard ^a,b   Fiorino, Ferdinando ^c   Deluca, Dominga ^c   Pfeiler, Dietmar ^a,b,d   Schaschke, Norbert ^c   Moroder, Luis ^c   Machleidt, Werner ^b  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Apoptosis; Calpain; Calpain inhibitors; Calpastatin; Ionomycin; Penetratin

Indexed keywords

ALDEHYDE DERIVATIVE; CALPAIN; CALPASTATIN; CASPASE 3; CATHEPSIN; CATHEPSIN B; CATHEPSIN L; CYSTEINE; DISULFIDE; HOMEODOMAIN PROTEIN; IONOMYCIN; PENETRATIN; PEPTIDE DERIVATIVE; PROTEASOME; SYNTHETIC PEPTIDE; UNCLASSIFIED DRUG;

ACETYLATION; AMINO TERMINAL SEQUENCE; APOPTOSIS; CANCER CELL CULTURE; CELL CULTURE; CELL MEMBRANE PERMEABILITY; CONCENTRATION RESPONSE; CONJUGATION; CONTROLLED STUDY; ENZYME ACTIVATION; EXON; HUMAN; HUMAN CELL; LYSOSOME; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; REVIEW; STRUCTURE ACTIVITY RELATION; SYNTHESIS;

APOPTOSIS; CALCIUM-BINDING PROTEINS; CALPAIN; CARRIER PROTEINS; CATHEPSINS; CELL LINE; CELL MEMBRANE PERMEABILITY; CYSTEINE PROTEINASE INHIBITORS; ERYTHROCYTES; EXONS; HUMANS; IONOMYCIN; PEPTIDE FRAGMENTS;

ANIMALIA;

EID: 0038523897     PISSN: 14316730     EISSN: None     Source Type: Journal    
DOI: 10.1515/BC.2003.045     Document Type: Review

References (53)

1. Arthur, J. S., Elce, J. S., Hegadorn, C., Williams, K., and Greer, P. A. (2000). Disruption of the murine calpain small subunit gene, Capn4: calpain is essential for embryonic development but not for cell growth and division. Mol. Cell. Biol. 20, 4474-4481.
2. Bepler, G., Koehler, A., Kiefer, P., Havemann, K., Beisenherz, K., Jaques, G., Gropp, C., and Haeder, M. (1988). Characterization of the state of differentiation of six newly established human non-small-cell lung cancer cell lines. Differentiation 37, 158-171.
3. Bernatowicz, M. S., Matsueda, R., and Matsueda, G. R. (1986). Preparation of Boc-[S-(3-nitro-2-pyridinesulfenyl)]-cysteine and its use for unsymmetrical disulfide bond formation. Int. J. Pept. Protein Res. 28, 107-112.
4. Blomgren, K., Zhu, C., Wang, X., Karlsson, J. O., Leverin, A. L., Bahr, B. A., Mallard, C., and Hagberg, H. (2001). Synergistic activation of caspase-3 by m-calpain after neonatal hypoxia-ischemia: a mechanism of 'pathological apoptosis'? J. Biol. Chem. 276, 10191-10198.
5. Bordone, L., and Campbell, C. (2002). DNA ligase III is degraded by calpain during cell death induced by DNA damaging agents. J. Biol. Chem. 277, 26673-26680.
6. Carragher, N. O., Westhoff, M. A., Riley, D., Potter, D. A., Dutt, P., Elce, J. S., Greer, P. A., and Frame, M. C. (2002). v-Src-induced modulation of the calpain-calpastatin proteolytic system regulates transformation. Mol. Cell Biol. 22, 257-269.
7. Chen, M., Won, D. J., Krajewski, S., and Gottlieb, R. A. (2002). Calpain and mitochondria in ischemia/reperfusion injury. J. Biol. Chem. 277, 29181-29186.
8. Croall, D. E., and McGrody, K. S. (1994). Domain structure of calpain: mapping the binding site for calpastatin. Biochemistry 33, 13223-13230.
9. Croce, K., Flaumenhaft, R., Rivers, M., Furie, B., Furie, B. C., Herman, I. M., and Potter, D. A. (1999). Inhibition of calpain blocks platelet secretion, aggregation, and spreading. J. Biol. Chem. 274, 36321-36327.
10. Derossi, D., Chassaing, G., and Prochiantz, A. (1998). Trojan peptides: the penetratin system for intracellular delivery. Trends Cell Biol. 8, 84-87.
11. Donkor, I. O. (2000). A survey of calpain inhibitors. Curr. Med. Chem. 7, 1171-1188.
12. Eto, A., Akita, Y., Saido, T. C., Suzuki, K., and Kawashima, S. (1995). The role of the calpain-calpastatin system in thyrotropin-releasing hormone-induced selective down-regulation of a protein kinase C isozyme, nPKC epsilon, in rat pituitary GH4C1 cells. J. Biol. Chem. 270, 25115-25120.
13. Fischer, P. M., Krausz, E., and Lane, D. P. (2001). Cellular delivery of impermeable effector molecules in the form of conjugates with peptides capable of mediating membrane translocation. Bioconjug. Chem. 12, 825-841.
14. Gabrijelcic-Geiger, D., Mentele, R., Meisel, B., Hinz, H., Assfalg-Machleidt, I., Machleidt, W., Möller, A., and Auerswald, E. A. (2001). Human μ-calpain: simple isolation from erythrocytes and characterization of autolysis fragments. Biol. Chem. 382, 1733-1737.
15. Gil-Parrado, S., Fernandez-Montalvan, A., Assfalg-Machleidt, I., Popp, O., Bestvater, F., Holloschi, A., Knoch, T. A., Auerswald, E. A., Welsh, K., Reed, J. C., Fritz, H., Fuentes-Prior, P., Spiess, E., Salvesen, G. S., and Machleidt, W. (2002). Ionomycin-activated calpain triggers apoptosis: A probable role for Bcl-2 family members. J. Biol. Chem. 277, 27217-27226.
16. Glading, A., Lauffenburger, D. A., and Wells, A. (2002). Cutting to the chase: calpain proteases in cell motility. Trends Cell Biol. 12, 46-54.
17. Hällbrink, M., Floren, A., Elmquist, A., Pooga, M., Bartfai, T., and Langel, U. (2001). Cargo delivery kinetics of cell-penetrating peptides. Biochim. Biophys. Acta 1515, 101-109.
18. Hernandez, A. A., and Roush, W. R. (2002). Recent advances in the synthesis, design and selection of cysteine protease inhibitors. Curr. Opin. Chem. Biol. 6, 459-465.
19. Hiwasa, T., Nakata, M., Ohno, S., Maki, M., Suzuki, K., and Takiguchi, M. (2002). Regulation of transformed state by calpastatin via PKCepsilon in NIH3T3 mouse fibroblasts. Biochem. Biophys. Res. Commun. 290, 510-517.
20. Huang, Y., and Wang, K. K. (2001). The calpain family and human disease. Trends Mol. Med. 7, 355-362.
21. Kawasaki, H., Emori, Y., Imajoh-Ohmi, S., Minami, Y., and Suzuki, K. (1989). Identification and characterization of inhibitory sequences in four repeating domains of the endogenous inhibitor for calcium-dependent protease. J. Biochem. (Tokyo) 106, 274-281.
22. Kusakawa, G., Saito, T., Onuki, R., Ishiguro, K., Kishimoto, T., and Hisanaga, S. (2000). Calpain-dependent proteolytic cleavage of the p35 cyclin-dependent kinase 5 activator to p25. J. Biol. Chem. 275, 17166-17172.
23. Lindgren, M., Gallet, X., Soomets, U., Hallbrink, M., Brakenhielm, E., Pooga, M., Brasseur, R., and Langel, U. (2000a). Translocation properties of novel cell penetrating transportan and penetratin analogues. Bioconjug. Chem. 11, 619-626.
24. Lindgren, M., Hallbrink, M., Prochiantz, A., and Langel, U. (2000b). Cell-penetrating peptides. Trends Pharmacol. Sci. 21, 99-103.
25. Lu, T., Xu, Y., Mericle, M. T., and Mellgren, R. L. (2002). Participation of the conventional calpains in apoptosis. Biochim. Biophys. Acta 1590, 16-26.
26. Machleidt, W., Assfalg-Machleidt, I. and Auerswald, E.A. (1993). Kinetics and molecular mechanism of inhibition of cysteine proteinases by their protein inhibitors. In: Innovations in Proteases and their Inhibitors, F.X. Aviles, ed. (Berlin, Germany: Walter de Gruyter), pp. 179-196.
27. Maki, M., Takano, E., Osawa, T., Ooi, T., Murachi, T., and Hatanaka, M. (1988). Analysis of structure-function relationship of pig calpastatin by expression of mutated cDNAs in Escherichia coli. J. Biol. Chem. 263, 10254-10261.
28. Maki, M., Bagci, H., Hamaguchi, K., Ueda, M., Murachi, T., and Hatanaka, M. (1989). Inhibition of calpain by a synthetic oligopeptide corresponding to an exon of the human calpastatin gene. J. Biol. Chem. 264, 18866-18869.
29. 2+ switch aligns the active site of calpain. Cell 108, 649-660.
30. Morrison, J. F. (1982). The slow-binding and slow, tight-binding inhibition of enzyme- catalyzed reactions. Trends Biochem. Sci. 7, 102-105.
31. Naito, M., Nagashima, K., Mashima, T., and Tsuruo, T. (1997). Phosphatidylserine externalization is a downstream event of interleukin-1β-converting enzyme family protease activation during apoptosis. Blood 89, 2060-2066.
32. Rutledge, T. W., and Whiteheart, S. W. (2002). SNAP-23 is a target for calpain cleavage inactivated platelets. J. Biol. Chem., in press (July 16, 2002) 10.1074/jbc.M204526200.
33. Sasaki, T., Kishi, M., Saito, M., Tanaka, T., Higuchi, N., Kominami, E., Katunuma, N., and Murachi, T. (1990). Inhibitory effect of di- and tripeptidyl aldehydes on calpains and cathepsins. J. Enzyme Inhib. 3, 195-201.
34. Sato, K., and Kawashima, S. (2001). Calpain function in the modulation of signal transduction molecules. Biol. Chem. 382, 743-751.
35. Schaschke, N., Musiol, H. J., Assfalg-Machleidt, I., Machleidt, W., Rudolph-Bohner, S., and Moroder, L. (1996). Cyclodextrins as templates for the presentation of protease inhibitors. FEBS Lett. 391, 297-301.
36. Schaschke, N., Deluca, D., Assfalg-Machleidt, I., Hohneke, C., Sommerhoff, C. P., and Machleidt, W. (2002). Epoxysuccinyl peptide-derived cathepsin B inhibitors: modulating membrane permeability by conjugation with the C-terminal heptapeptide segment of penetratin. Biol. Chem. 383, 849-852.
37. Schoenwaelder, S. M., and Burridge, K. (1999). Evidence for a calpeptin-sensitive protein-tyrosine phosphatase upstream of the small GTPase Rho. A novel role for the calpain inhibitor calpeptin in the inhibition of protein-tyrosine phosphatases. J. Biol. Chem. 274, 14359-14367.
38. Shiraishi, S., Shibuya, I., Uezono, Y., Yokoo, H., Toyohira, Y., Yamamoto, R., Yanagita, T., Kobayashi, H., and Wada, A. (2001). Heterogeneous increases of cytoplasmic calcium: distinct effects on down-regulation of cell surface sodium channels and sodium channel subunit mRNA levels. Br. J. Pharmacol. 132, 1455-1466.
39. Sorimachi, H., and Suzuki, K. (2001). The structure of calpain. J. Biochem. (Tokyo) 129, 653-664.
40. Squier, M. K., Sehnert, A. J., Sellins, K. S., Malkinson, A. M., Takano, E., and Cohen, J. J. (1999). Calpain and calpastatin regulate neutrophil apoptosis. J. Cell Physiol. 178, 311-319.
41. Stein, R. L., Melandri, F., and Dick, L. (1996). Kinetic characterization of the chymotryptic activity of the 20S proteasome. Biochemistry 35, 3899-3908.
42. Takano, E., Ma, H., Yang, H. Q., Maki, M., and Hatanaka, M. (1995). Preference of calcium-dependent interactions between calmodulin-like domains of calpain and calpastatin subdomains. FEBS Lett. 362, 93-97.
43. Uemori, T., Shimojo, T., Asada, K., Asano, T., Kimizuka, F., Kato, I., Maki, M., Hatanaka, M., Murachi, T., Hanzawa, H., and et al. (1990). Characterization of a functional domain of human calpastatin. Biochem. Biophys. Res. Commun. 166, 1485-1493.
44. 2+ influx and not via calpain inhibition. Neuropharmacology 42, 706-713.
45. Vanderklish, P. W., and Bahr, B. A. (2000). The pathogenic activation of calpain: a marker and mediator of cellular toxicity and disease states. Int. J. Exp. Pathol. 81, 323-339.
46. Waizenegger, T., Fischer, R., and Brock, R. (2002). Intracellular concentration measurements in adherent cells: a comparison of import efficiencies of cell-permeable peptides. Biol. Chem. 383, 291-299.
47. Wang, K. K., Nath, R., Posner, A., Raser, K. J., Buroker-Kilgore, M., Hajimohammadreza, I., Probert, A. W., Jr., Marcoux, F. W., Ye, Q., Takano, E. et al. (1996). An α-mercaptoacrylic acid derivative is a selective nonpeptide cell-permeable calpain inhibitor and is neuroprotective. Proc. Natl. Acad. Sci. USA 93, 6687-6692.
48. Wang, K. K., and Yuen, P. W. (1997). Development and therapeutic potential of calpain inhibitors. Adv. Pharmacol. 37, 117-152.
49. Wang, K. K. (2000). Calpain and caspase: can you tell the difference? Trends Neurosci. 23, 20-26.
50. Yajima, Y., and Kawashima, S. (2002). Calpain function in the differentiation of mesenchymal stem cells. Biol. Chem. 383, 757-764.
51. Yamashima, T. (2000). Implication of cysteine proteases calpain, cathepsin and caspase in ischemic neuronal death of primates. Prog. Neurobiol. 62, 273-295.
52. Yamazaki, M., Ishidoh, K., Suga, Y., Saido, T. C., Kawashima, S., Suzuki, K., Kominami, E., and Ogawa, H. (1997a). Cytoplasmic processing of human profilaggrin by active μ-calpain. Biochem. Biophys. Res. Commun. 235, 652-656.
53. Yamazaki, T., Haass, C., Saido, T. C., Omura, S., and Ihara, Y. (1997b). Specific increase in amyloid β-protein 42 secretion ratio by calpain inhibition. Biochemistry 36, 8377-8383.