Matrix Metalloproteinase-10/TIMP-2 Structure and Analyses Define Conserved Core Interactions and Diverse Exosite Interactions in MMP/TIMP Complexes

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Batra, Jyotica ^a,c   Soares, Alexei S ^b   Mehner, Christine ^a   Radisky, Evette S ^a  

^a MAYO CLINIC   (United States)

^b BROOKHAVEN NATIONAL LABORATORY   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGENASE 3; STROMELYSIN; STROMELYSIN 2; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME BINDING; ENZYME STRUCTURE; PROTEIN PROTEIN INTERACTION; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS;

BINDING SITES; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; HUMANS; MATRIX METALLOPROTEINASE 10; MATRIX METALLOPROTEINASES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SUBSTRATE SPECIFICITY; TISSUE INHIBITOR OF METALLOPROTEINASE-2; TISSUE INHIBITOR OF METALLOPROTEINASES;

EID: 84884490364     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075836     Document Type: Article

References (63)

1. Stamenkovic I, (2003) Extracellular matrix remodelling: the role of matrix metalloproteinases. J Pathol 200: 448-464.
2. Parks WC, Wilson CL, Lopez-Boado YS, (2004) Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat Rev Immunol 4: 617-629.
3. Van Wart HE, Birkedal-Hansen H, (1990) The cysteine switch: a principle of regulation of metalloproteinase activity with potential applicability to the entire matrix metalloproteinase gene family. Proc Natl Acad Sci U S A 87: 5578-5582.
4. Rosenblum G, Van den Steen PE, Cohen SR, Grossmann JG, Frenkel J, et al. (2007) Insights into the structure and domain flexibility of full-length pro-matrix metalloproteinase-9/gelatinase B. Structure. 15: 1227-1236.
5. Brew K, Nagase H, (2010) The tissue inhibitors of metalloproteinases (TIMPs): an ancient family with structural and functional diversity. Biochim Biophys Acta 1803: 55-71.
6. Murphy G, (2011) Tissue inhibitors of metalloproteinases. Genome Biology 12: 233.
7. Murphy G, Nagase H, (2008) Progress in matrix metalloproteinase research. Mol Aspects Med 29: 290-308.
8. Nicholson R, Murphy G, Breathnach R, (1989) Human and rat malignant-tumor-associated mRNAs encode stromelysin-like metalloproteinases. Biochemistry 28: 5195-5203.
9. Nakamura H, Fujii Y, Ohuchi E, Yamamoto E, Okada Y, (1998) Activation of the precursor of human stromelysin 2 and its interactions with other matrix metalloproteinases. Eur J Biochem 253: 67-75.
10. Pilcher BK, Wang M, Qin XJ, Parks WC, Senior RM, et al. (1999) Role of matrix metalloproteinases and their inhibition in cutaneous wound healing and allergic contact hypersensitivity. Ann N Y Acad Sci 878: 12-24.
11. Saarialho-Kere UK, Pentland AP, Birkedal-Hansen H, Parks WC, Welgus HG, (1994) Distinct populations of basal keratinocytes express stromelysin-1 and stromelysin-2 in chronic wounds. J Clin Invest 94: 79-88.
12. Bord S, Horner A, Hembry RM, Compston JE, (1998) Stromelysin-1 (MMP-3) and stromelysin-2 (MMP-10) expression in developing human bone: potential roles in skeletal development. Bone 23: 7-12.
13. Chang S, Young BD, Li S, Qi X, Richardson JA, et al. (2006) Histone deacetylase 7 maintains vascular integrity by repressing matrix metalloproteinase 10. Cell 126: 321-334.
14. Rodriguez JA, Orbe J, Martinez de Lizarrondo S, Calvayrac O, Rodriguez C, et al. (2008) Metalloproteinases and atherothrombosis: MMP-10 mediates vascular remodeling promoted by inflammatory stimuli. Front Biosci 13: 2916-2921.
15. Gill JH, Kirwan IG, Seargent JM, Martin SW, Tijani S, et al. (2004) MMP-10 is overexpressed, proteolytically active, and a potential target for therapeutic intervention in human lung carcinomas. Neoplasia 6: 777-785.
16. Frederick LA, Matthews JA, Jamieson L, Justilien V, Thompson EA, et al. (2008) Matrix metalloproteinase-10 is a critical effector of protein kinase Ciota-Par6alpha-mediated lung cancer. Oncogene 27: 4841-4853.
17. Regala RP, Justilien V, Walsh MP, Weems C, Khoor A, et al. (2011) Matrix metalloproteinase-10 promotes Kras-mediated bronchio-alveolar stem cell expansion and lung cancer formation. PloS One 6: e26439.
18. Justilien V, Regala RP, Tseng IC, Walsh MP, Batra J, et al. (2012) Matrix metalloproteinase-10 is required for lung cancer stem cell maintenance, tumor initiation and metastatic potential. PLoS One 7: e35040.
19. Deraz EM, Kudo Y, Yoshida M, Obayashi M, Tsunematsu T, et al. (2011) MMP-10/stromelysin-2 promotes invasion of head and neck cancer. PloS One 6: e25438.
20. Van Themsche C, Alain T, Kossakowska AE, Urbanski S, Potworowski EF, et al. (2004) Stromelysin-2 (matrix metalloproteinase 10) is inducible in lymphoma cells and accelerates the growth of lymphoid tumors in vivo. J Immunol 173: 3605-3611.
21. Rawlings ND, Barrett AJ, Bateman A, (2012) MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res 40: D343-350.
22. Kveiborg M, Jacobsen J, Lee MH, Nagase H, Wewer UM, et al. (2010) Selective inhibition of ADAM12 catalytic activity through engineering of tissue inhibitor of metalloproteinase 2 (TIMP-2). Biochem J 430: 79-86.
23. Hutton M, Willenbrock F, Brocklehurst K, Murphy G, (1998) Kinetic analysis of the mechanism of interaction of full-length TIMP-2 and gelatinase A: evidence for the existence of a low-affinity intermediate. Biochemistry 37: 10094-10098.
24. Batra J, Robinson J, Soares AS, Fields AP, Radisky DC, et al. (2012) Matrix metalloproteinase-10 (MMP-10) interaction with tissue inhibitors of metalloproteinases TIMP-1 and TIMP-2: binding studies and crystal structure. J Biol Chem 287: 15935-15946.
25. Stetler-Stevenson WG, (2008) The tumor microenvironment: regulation by MMP-independent effects of tissue inhibitor of metalloproteinases-2. Cancer Metastasis Rev 27: 57-66.
26. Gomis-Ruth FX, Maskos K, Betz M, Bergner A, Huber R, et al. (1997) Mechanism of inhibition of the human matrix metalloproteinase stromelysin-1 by TIMP-1. Nature 389: 77-81.
27. Fernandez-Catalan C, Bode W, Huber R, Turk D, Calvete JJ, et al. (1998) Crystal structure of the complex formed by the membrane type 1-matrix metalloproteinase with the tissue inhibitor of metalloproteinases-2, the soluble progelatinase A receptor. Embo J 17: 5238-5248.
28. Maskos K, Lang R, Tschesche H, Bode W, (2007) Flexibility and variability of TIMP binding: X-ray structure of the complex between collagenase-3/MMP-13 and TIMP-2. J Mol Biol 366: 1222-1231.
29. Grossman M, Tworowski D, Dym O, Lee MH, Levy Y, et al. (2010) The intrinsic protein flexibility of endogenous protease inhibitor TIMP-1 controls its binding interface and affects its function. Biochemistry 49: 6184-6192.
30. Iyer S, Wei S, Brew K, Acharya KR, (2007) Crystal structure of the catalytic domain of matrix metalloproteinase-1 in complex with the inhibitory domain of tissue inhibitor of metalloproteinase-1. J Biol Chem 282: 364-371.
31. Willenbrock F, Crabbe T, Slocombe PM, Sutton CW, Docherty AJ, et al. (1993) The activity of the tissue inhibitors of metalloproteinases is regulated by C-terminal domain interactions: a kinetic analysis of the inhibition of gelatinase A. Biochemistry. 32: 4330-4337.
32. Otwinowski Z, Minor W (1993) DENZO: A film Processing for Macromolecular Crystallography. New Haven, CT: Yale University.
33. McCoy AJ, Grosse-Kunstleve RW, Storoni LC, Read RJ, (2005) Likelihood-enhanced fast translation functions. Acta Crystallogr D Biol Crystallogr 61: 458-464.
34. Tuuttila A, Morgunova E, Bergmann U, Lindqvist Y, Maskos K, et al. (1998) Three-dimensional structure of human tissue inhibitor of metalloproteinases-2 at 2.1 A resolution. J Mol Biol 284: 1133-1140.
35. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
36. Murshudov GN, Vagin AA, Dodson EJ, (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255.
37. Kleywegt GJ, (1996) Use of non-crystallographic symmetry in protein structure refinement. Acta Crystallogr D Biol Crystallogr 52: 842-857.
38. Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, et al. (2007) MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 35: W375-383.
39. Krissinel E, Henrick K, (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372: 774-797.
40. Tallant C, Marrero A, Gomis-Ruth FX, (2010) Matrix metalloproteinases: fold and function of their catalytic domains. Biochim Biophys Acta 1803: 20-28.
41. Bertini I, Calderone V, Fragai M, Luchinat C, Mangani S, et al. (2004) Crystal structure of the catalytic domain of human matrix metalloproteinase 10. J Mol Biol 336: 707-716.
42. Williamson RA, Martorell G, Carr MD, Murphy G, Docherty AJ, et al. (1994) Solution structure of the active domain of tissue inhibitor of metalloproteinases-2. A new member of the OB fold protein family. Biochemistry 33: 11745-11759.
43. DeClerck YA, Yean TD, Lee Y, Tomich JM, Langley KE, (1993) Characterization of the functional domain of tissue inhibitor of metalloproteinases-2 (TIMP-2). Biochem J 289 (Pt 1): 65-69.
44. Morgunova E, Tuuttila A, Bergmann U, Tryggvason K, (2002) Structural insight into the complex formation of latent matrix metalloproteinase 2 with tissue inhibitor of metalloproteinase 2. Proc Natl Acad Sci U S A 99: 7414-7419.
45. Lambert E, Dasse E, Haye B, Petitfrere E, (2004) TIMPs as multifacial proteins. Crit Rev Oncol Hematol 49: 187-198.
46. Gomis-Ruth FX, Botelho TO, Bode W, (2012) A standard orientation for metallopeptidases. Biochim Biophys Acta 1824: 157-163.
47. Troeberg L, Tanaka M, Wait R, Shi YE, Brew K, et al. (2002) E. coli expression of TIMP-4 and comparative kinetic studies with TIMP-1 and TIMP-2: insights into the interactions of TIMPs and matrix metalloproteinase 2 (gelatinase A). Biochemistry 41: 15025-15035.
48. Williamson RA, Hutton M, Vogt G, Rapti M, Knauper V, et al. (2001) Tyrosine 36 plays a critical role in the interaction of the AB loop of tissue inhibitor of metalloproteinases-2 with matrix metalloproteinase-14. J Biol Chem 276: 32966-32970.
49. Cohen M, Reichmann D, Neuvirth H, Schreiber G, (2008) Similar chemistry, but different bond preferences in inter versus intra-protein interactions. Proteins 72: 741-753.
50. Scrutton NS, Raine AR, (1996) Cation-pi bonding and amino-aromatic interactions in the biomolecular recognition of substituted ammonium ligands. Biochem J 319 (Pt1): 1-8.
51. Krissinel E, Henrick K, (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372: 774-797.
52. Bertini I, Calderone V, Cosenza M, Fragai M, Lee YM, et al. (2005) Conformational variability of matrix metalloproteinases: beyond a single 3D structure. Proc Natl Acad Sci U S A 102: 5334-5339.
53. Moy FJ, Chanda PK, Chen J, Cosmi S, Edris W, et al. (2002) Impact of mobility on structure-based drug design for the MMPs. J Am Chem Soc 124: 12658-12659.
54. Udi Y, Fragai M, Grossman M, Mitternacht S, Arad-Yellin R, et al. (2013) Unraveling hidden regulatory sites in structurally homologous metalloproteases. J Mol Biol 425: 2330-2346.
55. Baker AH, Edwards DR, Murphy G, (2002) Metalloproteinase inhibitors: biological actions and therapeutic opportunities. J Cell Sci 115: 3719-3727.
56. Nagase H, Brew K (2003) Designing TIMP (tissue inhibitor of metalloproteinases) variants that are selective metalloproteinase inhibitors. Biochem Soc Symp: 201-212.
57. Lee MH, Rapti M, Knauper V, Murphy G, (2004) Threonine 98, the pivotal residue of tissue inhibitor of metalloproteinases (TIMP)-1 in metalloproteinase recognition. J Biol Chem 279: 17562-17569.
58. Lee MH, Rapti M, Murphy G, (2003) Unveiling the surface epitopes that render tissue inhibitor of metalloproteinase-1 inactive against membrane type 1-matrix metalloproteinase. J Biol Chem 278: 40224-40230.
59. Lee MH, Rapti M, Murphy G, (2005) Total conversion of tissue inhibitor of metalloproteinase (TIMP) for specific metalloproteinase targeting: fine-tuning TIMP-4 for optimal inhibition of tumor necrosis factor-{alpha}-converting enzyme. J Biol Chem 280: 15967-15975.
60. Bahudhanapati H, Zhang Y, Sidhu SS, Brew K, (2011) Phage display of tissue inhibitor of metalloproteinases-2 (TIMP-2): identification of selective inhibitors of collagenase-1 (metalloproteinase 1 (MMP-1)). J Biol Chem 286: 31761-31770.
61. Batra J, Robinson J, Mehner C, Hockla A, Miller E, et al. (2012) PEGylation extends circulation half-life while preserving in vitro and in vivo activity of tissue inhibitor of metalloproteinases-1 (TIMP-1). PloS One 7: e50028.
62. Chaturvedi M, Figiel I, Sreedhar B, Kaczmarek L, (2012) Neuroprotection from tissue inhibitor of metalloproteinase-1 and its nanoparticles. Neurochem Int 61: 1065-1071.
63. Lee MS, Kim YH, Kim YJ, Kwon SH, Bang JK, et al. (2011) Pharmacokinetics and biodistribution of human serum albumin-TIMP-2 fusion protein using near-infrared optical imaging. Journal of Pharmacy & Pharmaceutical Sciences 14: 368-377.