Endoproteinase-protein inhibitor interactions
WOLFRAM BODE,
CARLOS FERNANDEZ-CATALAN,
HIDEAKI NAGASE,
KLAUS MASKOS,
Corresponding Author
WOLFRAM BODE
Max-Planck-Institut für Biochemie, Martinsried, Germany
Max-Planck-Institut für Biochemie, D-82152 Martinsried, Germany.Search for more papers by this authorCARLOS FERNANDEZ-CATALAN
Max-Planck-Institut für Biochemie, Martinsried, Germany
Search for more papers by this authorHIDEAKI NAGASE
Department of Biochemistry and Molecular Biology, University of Kansas Medical Center, Kansas City, Kansas, USA
Search for more papers by this authorKLAUS MASKOS
Max-Planck-Institut für Biochemie, Martinsried, Germany
Search for more papers by this authorWOLFRAM BODE,
CARLOS FERNANDEZ-CATALAN,
HIDEAKI NAGASE,
KLAUS MASKOS,
Corresponding Author
WOLFRAM BODE
Max-Planck-Institut für Biochemie, Martinsried, Germany
Max-Planck-Institut für Biochemie, D-82152 Martinsried, Germany.Search for more papers by this authorCARLOS FERNANDEZ-CATALAN
Max-Planck-Institut für Biochemie, Martinsried, Germany
Search for more papers by this authorHIDEAKI NAGASE
Department of Biochemistry and Molecular Biology, University of Kansas Medical Center, Kansas City, Kansas, USA
Search for more papers by this authorKLAUS MASKOS
Max-Planck-Institut für Biochemie, Martinsried, Germany
Search for more papers by this authorAbstract
Nature uses protein inhibitors as important tools to regulate the proteolytic activity of their target proteinases. Most of these inhibitors for which 3D structures are available are directed towards serine proteinases, interacting with their active-sites in a substrate-like “canonical” manner via an exposed reactive-site loop of conserved conformation. More recently, some non-canonically binding serine proteinase inhibitors, two cysteine proteinase inhibitors, and three zinc endopeptidase inhibitors have been characterized in the free and complexed state, displaying novel mechanisms of inhibition with their target proteinases. These different interaction modes are briefly discussed, with particular emphasis on the interaction between matrix metalloproteinases (MMPs) and their endogenous tissue inhibitors of metalloproteinases (TIMPs).
REFERENCES
- 1 Neurath H.. Evolution of proteolytic enzymes. Science, 1984; 224: 350–7.
- 2 Gomez DE, Alonso DF, Yoshiji H., Thorgeirsson UP. Tissue inhibitors of metalloproteinases: structure, regulation and biological functions. Eur J Cell Biol, 1997; 74: 111–22.
- 3 Clawson GA. Protease inhibitors and carcinogenesis: a review. Cancer Invest, 1996; 14 (6): 597–608.
- 4 Laskowski M. Jr, Kato I.. Protein inhibitors of proteinases. Ann Rev Biochem, 1980; 49: 593–626.
- 5 Bode W., Huber R.. Natural protein proteinase inhibitors and their interaction with proteinases. Eur J Biochem, 1992; 204: 433–51.
- 6 Bode W., Huber R.. Proteinase-protein inhibitor interactions. Fibrinolysis, 1994; 8 (Suppl 1): 161–71.
- 7 Whisstock J., Skinner R., Lesk AM. An atlas of serpin conformations. TIBS, 1998; 23: 63–7.
- 8 Carrell RW, Stein PE. The biostructural pathology of the serpins: Critical functioning of sheet opening mechanism. Biol Chem Hoppe-Seyler, 1996; 377: 1–17.
- 9 Engh RA, Huber R., Bode W., Schulze AJ. Divining the serpin inhibition mechanism: a suicide substrate 'springe' TIBTECH, 1995; 13: 503–10.
- 10 Egelund R., Rodenburg KW, Andreasen PA, Rasmussen MS, Guldberg RE, Petersen TE. An ester bond linking a fragment of a serine proteinase to its serpin inhibitor. Biochemistry, 1998; 37: 6375–9.
- 11 Rees DC, Lipscomb WN. J Mol Biol 1982; 160: 475–98.
- 12 Rydel TJ, Ravichandran KG, Tulinsky A., Bode W., Huber R., Roitsch C., Fenton JW II. The structure of a complex of recombinant hirudin and human a-thrombin. Science, 1990; 249: 277–80.
- 13 Grütter MG, Priestle JP, Rahuel J., Grossenbacher H., Bode W., Hofsteenge J., Stone SR. Crystal structure of the thrombin-hirudin complex: A novel mode of serine protease inhibitor. EMBO J, 1990; 9: 2361–5.
- 14 Van de Locht A., Lamba D., Bauer M., Huber R., Friedrich T., Kröger B., Höffken W., Bode W.. Two heads are better than one: crystal structure of the insect derived double domain Kazal inhibitor rhodniin in complex with thrombin. EMBO J, 1995; 14: 5149–57.
- 15 Van de Locht A., Stubbs MT, Bode W., Friedrich T., Bollschweiler C., Höffken W., Huber R.. The ornithodor-in-thrombin crystal structure, a key to the TAP enigma The EMBO J, 1996; 15: 6011–7.
- 16 Fuentes-Prior P., Noeske-Jungblut C., Donner P., Schleuning W-D, Huber R., Bode W.. Structure of the thrombin complex with triabin, a lipocalin-like exosite-binding inhibitor derived from a triatomine bug. Proc Natl Acad Sci USA, 1997; 94: 11845–50.
- 17 Bode W., Engh R., Musil D., Thiele U., Huber R., Karshikov A., Brzin J., Turk V.. The 2.0 Å X-ray crystal structure of chicken egg white cystatin and its possible mode of interaction with cysteine proteinases. The EMBO J, 1988; 7: 2593–9.
- 18 Stubbs MT, Laber B., Bode W., Huber R., Jerala R., Lenarcic B., Turk V.. The refined 2.4 Å X-ray crystal structure of recombinant human stefin B in complex with the cysteine proteinase papain: a novel type of proteinase inhibitor interaction. The EMBO J, 1990; 9: 1939–47.
- 19 Gomis-Rüth FX, Maskos K., Betz M., Bergner A., Huber R., Suzuki K., Yoshida N., Nagase H., Brew K., Bourenkov GP, Bartunik H., Bode W.. Mechanism of inhibition of the human matrix metalloproteinase stromelysin-1 by TIMP-1. Nature, 1997; 389: 77–81.
- 20 Bode W., Mayr I., Baumann U., Huber R., Stone SR, Hofsteenge J.. The refined 1.9 Å crystal structure of human α-thrombin: Interaction with D-Phe-Pro-Arg chlorome-thylketone and significance of the Tyr-Pro-Pro-Trp insertion segment. EMBO J, 1989; 8: 3467–75.
- 21 Bode W., Turk D., Karshikov A.. The refined 1.9 Å X-ray crystal structure of D-PheProArg chloromethylketone inhibited human α-thrombin. Structure analysis, overall structure, electrostatic properties, detailed active site geometry, structure-function relationships. Protein Sci, 1992; 1: 426–71.
- 22 Stubbs MT, Bode W.. The clot thickens: clues provided by thrombin structure. TIBS, 1995; 20: 23–8.
- 23 Vijayalakshmi J., Padmanabhan KR, Mann KG, Tulinsky A.. The isomorphous structures of prethrombin2, hirugen-, and PPACK-thrombin: Changes accompanying activation and exosite binding to thrombin. Prot Sci, 1994; 3: 2254–71.
- 24 Bode W.. The transition of bovine trypsinogen in a trypsin-like state upon strong ligand binding. II. The binding of the pancreatic trypsin inhibitor and of isoleucinevaline and of sequentially related peptides to trypsinogen and to p-guanidnobenzoate-trypsinogen. J Mol Biol, 1979; 127: 357–74.
- 25 Turk V., Bode W.. The cystatins: protein inhibitors of cysteine proteinases. FEBS Lett, 1991; 285: 213–9.
- 26 Woessner JF, Jr. Matrix metalloproteinases and their inhibitors in connective tissue remodeling. FASEB J, 1991; 5: 2145–55.
- 27 Matrisian LM. Metalloproteinases and their inhibitors in matrix remodeling. Trends Genet, 1990; 6: 121–5.
- 28 Nagase H.. Matrix Metalloproteinases. In: NM Hooper, Ed. Francis Taylor, editors. Zinc Metalloproteases in Health and Disease, London ; 1996 p. 153–204.
- 29 Coussens LM, Werb Z.. Matrix metalloproteinases and the development of cancer. Chem Biol, 1996; 3: 895–904.
- 30 Murphy G., Willenbrock F.. Tissue inhibitors of matrix metalloendopeptidases. Meth Enzym, 1995; 248: 496–510.
- 31
Willenbrock F.,
Murphy G..
Structure-function relationships in the tissue inhibitors of metalloproteinases.
Am J Respir Crit Care Med, 1994; 150: 5165–70.
10.1164/ajrccm/150.6_Pt_2.S165 Google Scholar
- 32 Huang W., Suzuki K., Nagase H., Arumugam S., Van Doren SR, Brew K.. Folding and characterization of the amino-terminal domain of human tissue inhibitor of metalloproteinase-1 (TIMP-1) expressed at high yield in E. coli.. FEBS Lett, 1996; 384: 155–61.
- 33 Williamson RA, Martorell G., Carr MD, Murphy G., Docherty AJ, Freedman RB, Feeney J.. Solution structure of the active domain of tissue inhibitor of metalloproteinases-2. A new member of the OB fold protein family. Biochemistry, 1994; 33: 11745–59.
- 34 Bode W.. A helping hand for collagenases: the haemopexin-like domain. Structure, 1995; 3: 527–30.
- 35 Bode W., Gomis-Rüth F-X, Stöcker W.. Astacins, serralysins, snake venom and matrix metalloproteinases exhibit identical zinc-binding environments (HEXXHXXGXXH and Met-turn) and topologies and should be grouped into a common family, the ‘metzincins’. FEBS Lett, 1993; 331: 134–40.
- 36 Becker JW, Marcy AI, Rokosz LL, Axel MG, Burbaum JJ, Fitzgerald PMD, Cameron PM, Esser CK, Hagmann WK, Hermes JD, Springer JP. Stromelysin-1: Three-dimensional structure of the inhibited catalytic domain and of the C-truncated proenzyme. Prot Sci, 1995; 4: 1966–76.
- 37 Grams F., Crimmin M., Hinnes L., Huxley P., Pieper M., Tschesche H., Bode W.. Structure determination and analysis of human neutrophil collagenase complexed with a hydroxamate inhibitor. Biochemistry, 1995; 34: 14012–20.
- 38 Grams F., Reinemer P., Powers JC, Kleine T., Pieper M., Tschesche H., Huber R., Bode W.. X-ray structures of human neutrophil collagenase complexed with peptide hydroxamate and peptide thiol inhibitors. Implications for substrate binding and rational drug design. Eur J Biochem, 1995; 228: 830–41.
- 39 Matthews BW. Structural basis of the action of thermolysin and related zinc peptidases. Acc Chem Res, 1988; 21: 333–40.
- 40 Li J-Y, Brick P. O'Hare MC, Skarzynski T., Lloyd LF, Curry VA, Clark IM, Bigg HF, Hazlemen BL, Cawston TE, Blow, DM. Structure of full-length porcine synovial collagenase reveals a C-terminal domain containing a calcium-linked, four-bladed beta-propeller. Structure, 1995; 3: 541–9.
