Extra-and intracellular imaging of human matrix metalloprotease 11 (hMMP-11) with a cell-penetrating FRET substrate

Journal of Biological Chemistry

Volumn 287, Issue 45, 2012, Pages 37857-37867

  Meyer, B Sina ^a,b   Rademann, Jörg ^b,c  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

^c UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL-PERMEABLE; HUMAN MATRIX; IMAGING TOOLS; IN-VITRO; INTRACELLULAR IMAGING; MATRIX METALLOPROTEASE; RATIONAL DESIGN; TUMORIGENESIS;

TISSUE;

SUBSTRATES;

ARGININE; STROMELYSIN 3;

ARTICLE; BINDING AFFINITY; BREAST ADENOCARCINOMA; CANCER INVASION; CARCINOGENESIS; CELL ASSAY; CELL MEMBRANE PERMEABILITY; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; ENZYME SUBSTRATE; FLUORESCENCE RESONANCE ENERGY TRANSFER; IN VITRO STUDY; LEUKEMIA CELL LINE; MOLECULAR IMAGING; PANCREAS ADENOCARCINOMA; PRIORITY JOURNAL; PROCESS DEVELOPMENT; PROTEIN BINDING; PROTEIN EXPRESSION;

BIOCATALYSIS; BLOTTING, WESTERN; CELL LINE, TUMOR; DIPEPTIDES; EXTRACELLULAR SPACE; FLUORESCEINS; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMANS; INTRACELLULAR SPACE; JURKAT CELLS; KINETICS; MATRIX METALLOPROTEINASE 11; MCF-7 CELLS; MICROSCOPY, CONFOCAL; MOLECULAR IMAGING; P-DIMETHYLAMINOAZOBENZENE; PROTEASE INHIBITORS; SUBSTRATE SPECIFICITY;

EID: 84868314908     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.371500     Document Type: Article

References (52)

1. Snoek-van Beurden, P. A., and Von den Hoff, J. W. (2005) Zymographic techniques for the analysis of matrix metalloproteinases and their inhibitors. BioTechniques 38, 73-833
2. Andreini, C., Banci, L., Bertini, I., Luchinat, C., and Rosato, A. (2004) Bioinformatic comparison of structures and homology-models of matrix metalloproteinases. J. Proteome Res. 3, 21-311
3. Masson, R., Lefebvre, O., Noël, A., Fahime, M. E., Chenard, M. P., Wendling, C., Kebers, F., LeMeur, M., Dierich, A., Foidart, J. M., Basset, P., and Rio, M. C. (1998) In vivo evidence that the stromelysin-3 metalloproteinase contributes in a paracrine manner to epithelial cell malignancy. J. Cell Biol. 140, 1535-15411
4. Arora, S., Kaur, J., Sharma, C., Mathur, M., Bahadur, S., Shukla, N. K., Deo, S. V., and Ralhan, R. (2005) Stromelysin 3, Ets-1, and vascular endothelial growth factor expression in oral precancerous and cancerous lesions. Correlation with microvessel density, progression, and prognosis. Clin. Cancer Res. 11, 2272-22844
5. Baldini, E., Toller, M., Graziano, F. M., Russo, F. P., Pepe, M., Biordi, L., Marchioni, E., Curcio, F., Ulisse, S., Ambesi-Impiombato, F. S., and D'Armiento, M. (2004) Expression of matrix metalloproteinases and their specific inhibitors in normal and different human thyroid tumor cell lines. Thyroid 14, 881-8888
6. Leivo, I., Jee, K., Heikinheimo, K., Laine, M., Ollila, J., Nagy, B., and Knuutila, S. (2005) Characterization of gene expression in major types of salivary gland carcinomas with epithelial differentiation. Cancer Gen. Cytogen. 156, 104-1133
7. Denys, H., De Wever, O., Nusgens, B., Kong, Y., Sciot, R., Le, A. T., Van Dam, K., Jadidizadeh, A., Tejpar, S., Mareel, M., Alman, B., and Cassiman, J. J. (2004) Invasion and MMP expression profile in desmoid tumours. Br. J. Cancer 90, 1443-14499
8. Yamashita, K., Tanaka, Y., Mimori, K., Inoue, H., and Mori, M. (2004) Differential expression of MMP and uPA systems and prognostic relevance of their expression in esophageal squamous cell carcinoma. Int. J. Cancer 110, 201-2077
9. Basset, P., Bellocq, J. P., Wolf, C., Stoll, I., Hutin, P., and Limacher, J. M. (1990) A novel metalloproteinase gene specifically expressed in stromal cells of breast carcinomas. Nature 348, 699-7044
10. Jones, L. E., Humphreys, M. J., Campbell, F., Neoptolemos, J. P., and Boyd, M. T. (2004) Comprehensive analysis of matrix metalloproteinase and tissue inhibitor expression in pancreatic cancer. Increased expression of matrix metalloproteinase-7 predicts poor survival. Clin. Cancer Res. 10, 2832-28455
11. Ahmad, A., Hanby, A., Dublin, E., Poulsom, R., Smith, P., Barnes, D., Rubens, R., Anglard, P., and Hart, I. (1998) Stromelysin 3. An independent prognostic factor for relapse-free survival in node-positive breast cancer and demonstration of novel breast carcinoma cell expression. Am. J. Pathol. 152, 721-7288
12. Rouyer, N., Wolf, C., Chenard, M. P., Rio, M. C., Chambon, P., Bellocq, J. P., and Basset, P. (1994) Stromelysin-3 gene expression in human cancer. An overview. Invasion Metastasis 14, 269-2755
13. Thewes, M., Pohlmann, G., Atkinson, M., Mueller, J., Pütz, B., and Höfler, H. (1996) Stromelysin-3 (ST-3) mRNA expression in colorectal carcinomas. Localization and clinicopathologic correlations. Diagn. Mol. Pathol. 5, 284-2900
14. Peruzzi, D., Mori, F., Conforti, A., Lazzaro, D., De Rinaldis, E., Ciliberto, G., La Monica, N., and Aurisicchio, L. (2009) MMP-11. A novel target antigen for cancer immunotherapy. Clin. Cancer Res. 15, 4104-41133
15. Laurell, H., Bouisson, M., Berthelemy, P., Rochaix, P., Dejean, S., Besse, P., Susini, C., Pradayrol, L., Vaysse, N., and Buscail, L. (2006) Identification of biomarkers of human pancreatic adenocarcinomas by expression profiling and validation with gene expression analysis in endoscopic ultrasound-guided fine needle aspiration samples. World J. Gastroenterol., 12, 3344-33511
16. Fromigué, O., Louis, K., Wu, E., Belhacène, N., Loubat, A., Shipp, M., Auberger, P., and Mari, B. (2003) Active stromelysin-3 (MMP-11) increases MCF-7 survival in three-dimensional Matrigel culture via activation of p42/p44 MAP-kinase. Int. J. Cancer 106, 355-3633
17. Pei, D., and Weiss, S. J. (1995) Furin-dependent intracellular activation of the human stromelysin-3 zymogen. Nature 375, 244-2477
18. Noël, A., Santavicca, M., Stoll, I., L'Hoir, C., Staub, A., Murphy, G., Rio, M. C., and Basset, P. (1995) Identification of structural determinants controlling human and mouse stromelysin-3 proteolytic activities. J. Biol. Chem. 270, 22866-228722
19. Pan, W., Arnone, M., Kendall, M., Grafstrom, R. H., Seitz, S. P., Wasserman, Z. R., and Albright, C. F. (2003) Identification of peptide substrates for human MMP-11 (stromelysin-3) using phage display. J. Biol. Chem. 278, 27820-278277
20. Chaussain-Miller, C., Fioretti, F., Goldberg, M., and Menashi, S. (2006) The role of matrix metalloproteinases (MMPs) in human caries. J. Dent. Res. 85, 22-322
21. Delain, E., Pochon, F., Barray, M., and Van Leuven, F. (1992) Ultrastructure of α2-macroglobulins. Electron Microsc. Rev. 5, 231-2811
22. del Mar Barbacid, M., Fernández-Resa, P., Buesa, J. M., Márquez, G., Aracil, M., Quesadaand, A. R., and Mira, E. (1998) Expression and purification of human stromelysin 1 and 3 from baculovirus-infected insect cells. Protein Expr. Purif. 13, 243-2500
23. Schmitt, M., Harbeck, N., Thomssen, C., Wilhelm, O., Magdolen, V., Reuning, U., Ulm, K., Höfler, H., Jänicke, F., and Graeff, H. (1997) Clinical impact of the plasminogen activation system in tumor invasion and metastasis. Prognostic relevance and target for therapy. Thromb. Haemost. 78, 285-2966
24. Luo, D., Mari, B., Stoll, I., and Anglard, P. (2002) Alternative splicing and promoter usage generates an intracellular stromelysin 3 isoform directly translated as an active matrix metalloproteinase. J. Biol. Chem. 277, 25527-255366
25. Visse, R., and Nagase, H. (2003) Matrix metalloproteinases and tissue inhibitors of metalloproteinases. Structure, function, and biochemistry. Circ. Res. 92, 827-8399
26. Weissleder, R., and Mahmood, U. (2001) Molecular imaging. Radiology 219, 316-3333
27. Kovar, J. L., Simpson, M.A., Schutz-Geschwender, A., and Olive, D.M.(2007) A systematic approach to the development of fluorescent contrast agents for optical imaging of mouse cancer models. Anal. Biochem. 367, 1-122
28. Lee, S., Xie, J., and Chen, X. (2010) Peptides and peptide hormones for molecular imaging and disease diagnosis. Chem. Rev. 110, 3087-31111
29. Förster, T. (1948) Intermolecular energy transfer and fluorescence. Annals of Physics 6, 55-755
30. Kannan, R., Ruff, M., Kochins, J. G., Manly, S. P., Stoll, I., El Fahime, M., Noël, A., Foidart, J. M., Rio, M. C., Dive, V., and Basset, P. (1999) Purification of active matrix metalloproteinase catalytic domains and its use for screening of specific stromelysin-3 inhibitors. Protein Expr. Purif. 16, 76-833
31. Monici, M. (2005) Cell and tissue autofluorescence research and diagnostic applications. Biotechnol. Annu. Rev. 11, 227-2566
32. Uryga-Polowy, V., Kosslick, D., Freund, C., and Rademann, J. (2008) Resin-bound aminofluorescein for C-terminal labeling of peptides. High-affinity polarization probes binding to polyproline-specific GYF domains. ChemBioChem 9, 2452-24622
33. Coin, I., Beyermann, M., and Bienert, M. (2007) Solid-phase peptide synthesis. From standard procedures to the synthesis of difficult sequences. Nat. Protoc. 2, 3247-32566
34. Wood, W. J., Patterson, A. W., Tsuruoka, H., Jain, R. K., Ellman, J. A. (2005) Substrate activity screening. A fragment-based method for the rapid identification of nonpeptidic protease inhibitors. J. Am. Chem. Soc. 127, 15521-155277
35. Nuti, E., Panelli, L., Casalini, F., Avramova, S. I., Orlandini, E., Santamaria, S., Nencetti, S., Tuccinardi, T., Martinelli, A., Cercignani, G., D'Amelio, N., Maiocchi, A., Uggeri, F., and Rossello, A. (2009) Design, synthesis, biological evaluation, and NMR studies of a new series of arylsulfones as selective and potent matrix metalloproteinase-12 inhibitors. J. Med. Chem. 52, 6347-63611
36. Mucha, A., Cuniasse, P., Kannan, R., Beau, F., Yiotakis, A., Basset, P., and Dive, V. (1998) Membrane type-1 matrix metalloprotease and stromelysin-3 cleave more efficiently synthetic substrates containing unusual amino Acids in their P1' positions. J. Biol. Chem. 273, 2763-27688
37. Holtz, B., Cuniasse, P., Boulay, A., Kannan, R., Mucha, A., Beau, F., Basset, P., and Dive, V. (1999) Role of the S1' subsite glutamine 215 in activity and specificity of stromelysin-3 by site-directed mutagenesis. Biochemistry 38, 12174-121799
38. Nazarenko, I. A., Bhatnagar, S. K., and Hohman, R. J. (1997) A closed tube format for amplification and detection of DNA based on energy transfer. Nucleic Acids Res. 25, 2516-25211
39. Fuchs, S. M., Rutkoski, T. J., Kung, V. M., Groeschl, R. T., and Raines, R. T. (2007) Increasing the potency of a cytotoxin with an arginine graft. Protein Eng. Des. Sel. 20, 505-5099
40. Ramage, R., Green, J., and Blake, A. J. (1991) An acid labile arginine derivative for peptide synthesis. NG-2, 2, 5, 7, 8-pentamethylchroman-6- sulphonyl-L-arginine. Tetrahedron 47, 6353-63700
41. Isidro-Llobet, A., Alvarez, M., and Albericio, F. (2009) Amino acid-protecting groups. Chem. Rev. 109, 2455-25044
42. Apte, S. S., Fukai, N., Beier, D. R., and Olsen, B. R. (1997) The matrix metalloproteinase-14 (MMP-14) gene is structurally distinct from other MMP genes and is co-expressed with the TIMP-2 gene during mouse embryogenesis. J. Biol. Chem. 272, 25511-255177
43. Saghatelian, A., Jessani, N., Joseph, A., Humphrey, M., and Cravatt, B. F. (2004) Activity-based probes for the proteomic profiling of metalloproteases. Proc. Natl. Acad. Sci. U.S.A. 101, 10000-100055
44. Yang, J., Zhang, Z., Lin, J., Lu, J., Liu, B. F., Zeng, S., and Luo, Q. (2007) Detection ofMMPactivity in living cells by a genetically encoded surfacedisplayed FRET sensor. Biochim. Biophys. Acta 1773, 400-4077
45. Ledour, G., Moroy, G., Rouffet, M., Bourguet, E., Guillaume, D., Decarme, M., Elmourabit, H., Augé, F., Alix, A. J., Laronze, J. Y., Bellon, G., Hornebeck, W., Sapi, J. (2008) Introduction of the 4-(4-bromophenyl) benzenesulfonyl group to hydrazide analogs of ilomastat leads to potent gelatinase B (MMP-9) inhibitors with improved selectivity. Bioorg. Med. Chem. 16, 8745-87599
46. Balakrishnan, A., Patel, B., Sieber, S. A., Chen, D., Pachikara, N., Zhong, G., Cravatt, B. F., and Fan, H. (2006) Metalloprotease inhibitors GM6001 and TAPI-0 inhibit the obligate intracellular human pathogen Chlamydia trachomatis by targeting peptide deformylase of the bacterium. J. Biol. Chem. 281, 16691-166999
47. Gall, A. L., Ruff, M., Kannan, R., Cuniasse, P., Yiotakis, A., Dive, V., Rio, M. C., Basset, P., and Moras, D. (2001) Crystal structure of the stromelysin-3 (MMP-11) catalytic domain complexed with a phosphinic inhibitor mimicking the transition-state. J. Mol. Biol. 301, 577-5866
48. Bremer, C., Bredow, S., Mahmood, U., Weissleder, R., and Tung, C. H. (2001) Optical imaging of matrix metalloproteinase-2 activity in tumors. Feasibility study in a mouse model. Radiology 221, 523-5299
49. Egeblad, M., and Werb, Z. (2002) New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer 2, 161-1744
50. Hartmann, W., Koch, A., Brune, H., Waha, A., Schüller, U., Dani, I., Denkhaus, D., Langmann, W., Bode, U., Wiestler, O. D., Schilling, K., and Pietsch, T. (2005) Insulin-like growth factor II is involved in the proliferation control of medulloblastoma and its cerebellar precursor cells. Am. J. Pathol. 166, 1153-11622
51. Mañes, S., Mira, E., Barbacid, M. M., Ciprés, A., Fernández-Resa, P., Buesa, J. M., Mérida, I., Aracil, M., Márquez, G., Martínez-A, C. (1997) Identification of insulin-like growth factor-binding protein-1 as a potential physiological substrate for human stromelysin-3. J. Biol. Chem. 272, 25706-257122
52. Kleifeld, O., Doucet, A., auf dem Keller, U., Prudova, A., Schilling, O., Kainthan, R. K., Starr, A. E., Foster, L. J., Kizhakkedathu, J. N., and Overall, C. M. (2010) Isotopic labeling of terminal amines in complex samples identifies protein N-termini and protease cleavage products. Nat. Biotechnol. 28, 281-2888