Metabolic mapping of proteinase activity with emphasis on in situ zymography of gelatinases: Review and protocols

Journal of Histochemistry and Cytochemistry

Volumn 52, Issue 6, 2004, Pages 711-722

  Frederiks, Wilma M ^a,b   Mook, Olaf R F ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

Gelatinase; In situ zymography; Metabolic mapping; Proteinase

Indexed keywords

CASEIN; FIBRIN; FLUORESCEIN ISOTHIOCYANATE; GELATIN; GELATINASE; MATRIX METALLOPROTEINASE; PROTEINASE;

BIOPROCESS; EMULSION; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME SUBSTRATE; IMMUNOHISTOCHEMISTRY; MACROMOLECULE; NONPHOTOCHEMICAL QUENCHING; PATHOGENESIS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW; TECHNIQUE; ZYMOGRAPHY;

ANIMALS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENDOPEPTIDASES; FLUORESCENT DYES; GELATIN; GELATINASES; IMMUNOHISTOCHEMISTRY; SENSITIVITY AND SPECIFICITY;

EID: 2542569423     PISSN: 00221554     EISSN: None     Source Type: Journal    
DOI: 10.1369/jhc.4R6251.2004     Document Type: Review

References (98)

1. Barrett AJ, Rawlings ND, Woessner JF (1998) Handbook of Proteolytic Enzymes. 1st ed. London, Academic Press
2. Boonacker E, Elferink S, Bardai A, Fleischer B, Van Noorden CJ (2003) Fluorogenic substrate [Ala-Pro]2-cresyl violet but not Ala-Pro-rhodamine 110 is cleaved specifically by DPPIV activity: a study in living Jurkat cells and CD26/DPPIV-transfected Jurkat cells. J Histochem Cytochem 51:959-968
3. Boonacker E, Van Noorden CJ (2001) Enzyme cytochemical techniques for metabolic mapping in living cells, with special reference to proteolysis. J Histochem Cytochem 49:1473-1486
4. Bremer C, Bredow S, Mahmood U, Weissleder R, Tung CH (2001a) Optical imaging of matrix metalloproteinase-2 activity in tumors: feasibility study in a mouse model. Radiology 221:523-529
5. Bremer C, Tung CH, Weissleder R (2001b) In vivo molecular target assessment of matrix metalloproteinase inhibition. Nature Med 7:743-748
6. Bruno G, Todor R, Lewis I, Chyatte D (1998) Vascular extracellular matrix remodeling in cerebral aneurysms. J Neurosurg 89: 431-440
7. Catterall JB, Cawston TE (2003) Assays of matrix metalloproteinases (MMPs) and MMP inhibitors: bioassays and immunoassays applicable to cell culture medium, serum, and synovial fluid. Methods Mol Biol 225:353-364
8. Curry TE Jr, Song L, Wheeler SE (2001) Cellular localization of gelatinases and tissue inhibitors of metalloproteinases during follicular growth, ovulation, and early luteal formation in the rat. Biol Reprod 65:855-865
9. de Vries TJ, Kitson JL, Silvers WK, Mintz B (1995) Expression of plasminogen activators and plasminogen activator inhibitors in cutaneous melanomas of transgenic melanoma-susceptible mice. Cancer Res 55:4681-4687
10. Dolbeare FA, Smith RE (1977) Flow cytometric measurement of peptidases with use of 5-nitrosalicylaldehyde and 4-methoxy-beta-naphthylamine derivatives. Clin Chem 23:1485-1491
11. Duchossoy Y, Arnaud S, Feldblum S (2001) Matrix metalloproteinases: potential therapeutic target in spinal cord injury. Clin Chem Lab Med 39:362-367
12. Elner SG (2002) Human retinal pigment epithelial lysis of extracellular matrix: functional urokinase plasminogen activator receptor, collagenase, and elastase. Trans Am Ophthalmol Soc 100: 273-299
13. Faia KL, Davis WP, Marone AJ, Foxall TL (2002) Matrix metalloproteinases and tissue inhibitors of metalloproteinases in hamster aortic atherosclerosis: correlation with in-situ zymography. Atherosclerosis 160:325-337
14. Fernandez HA, Kallenbach K, Seghezzi G, Mehrara B, Apazidis A, Baumann FG, Grossi EA, et al. (1998) Modulation of matrix metalloproteinase activity in human saphenous vein grafts using adenovirus-mediated gene transfer. Surgery 124:129-136
15. Fisher GJ, Wang ZQ, Datta SC, Varani J, Kang S, Voorhees JJ (1997) Pathophysiology of premature skin aging induced by ultraviolet light. N Engl J Med 337:1419-1428
16. Freemont AJ, Byers RJ, Taiwo YO, Hoyland JA (1999) In situ zymographic localisation of type II collagen degrading activity in osteoarthritic human articular cartilage. Ann Rheum Dis 58: 357-365
17. Furuya M, Ishikura H, Nemori R, Shibata M, Fujimoto S, Yoshiki T (2001) Clarification of the active gelatinolytic sites in human ovarian neoplasms using in situ zymography. Hum Pathol 32: 163-168
18. Galis ZS, Sukhova GK, Lark MW, Libby P (1994) Increased expression of matrix metalloproteinases and matrix degrading activity in vulnerable regions of human atherosclerotic plaques. J Clin Invest 94:2493-2503
19. Galis ZS, Sukhova GK, Libby P (1995) Microscopic localization of active proteases by in situ zymography: detection of matrix metalloproteinase activity in vascular tissue. FASEB J 9:974-980
20. George SJ, Baker AH, Angelini GD, Newby AC (1998) Gene transfer of tissue inhibitor of metalloproteinase-2 inhibits metalloproteinase activity and neointima formation in human saphenous veins. Gene Ther 5:1552-1560
21. Goodall S, Crowther M, Hemingway DM, Bell PR, Thompson MM (2001) Ubiquitous elevation of matrix metalloproteinase-2 expression in the vasculature of patients with abdominal aneurysms. Circulation 104:304-309
22. Hanyu T (1999) The effects of single mitomycin C application on the expression of matrix metalloproteinase in the sclera and aqueous of albino rabbits. Nippon Ganka Gakkai Zasshi 103: 186-192
23. Heussen C, Dowdle EB (1980) Electrophoretic analysis of plasminogen activators in polyacrylamide gels containing sodium dodecyl sulfate and copolymerized substrates. Anal Biochem 102:196-202
24. Horino K, Kindezelskii AL, Elner VM, Hughes BA, Petty HR (2001) Tumor cell invasion of model 3-dimensional matrices: demonstration of migratory pathways, collagen disruption, and intercellular cooperation. FASEB J 15:932-939
25. Ikeda M, Maekawa R, Tanaka H, Matsumoto M, Takeda Y, Tamura Y, Nemori R, et al. (2000) Inhibition of gelatinolytic activity in tumor tissues by synthetic matrix metalloproteinase inhibitor: application of film in situ zymography. Clin Cancer Res 6:3290-3296
26. Iwata H, Yamamoto M, Nemori R, Mizutani M, Iwase T, Miura S, Obata Y, et al. (2001) Localization of gelatinolytic activity can be detected in breast cancer tissues by film in situ zymography. Breast Cancer 8:111-115
27. Jones LJ, Upson RH, Haugland RP, Panchuk-Voloshina N, Zhou M (1997) Quenched BODIPY dye-labeled casein substrates for the assay of protease activity by direct fluorescence measurement. Anal Biochem 251:144-152
28. Kaji M, Moriyama S, Sasaki H, Saitoh Y, Kiriyama M, Fukai I, Yamakawa Y, et al. (2003) Gelatinolytic activity of matrix metalloproteinase in lung cancer studied using film in situ zymography stamp method. Lung Cancer 39:125-130
29. Kamiya N, Kishimoto T, Suzuki H, Sekita N, Nagai Y, Oosumi N, Kito H, et al. (2003) Increased in situ gelatinolytic activity in renal cell tumor tissues correlates with tumor size, grade and vessel invasion. Int J Cancer 106:480-485
30. Kaneyoshi T, Nakatsukasa H, Higashi T, Fujiwara K, Naito I, Nouso K, Kariyama K, et al. (2001) Actual invasive potential of human hepatocellular carcinoma revealed by in situ gelatin zymography. Clin Cancer Res 7:4027-4032
31. Khandoker MA, Imai K, Takahashi T, Hashizume K (2001) Role of gelatinase on follicular atresia in the bovine ovary. Biol Reprod 65:726-732
32. Kieseier BC, Schneider C, Clements JM, Gearing AJ, Gold R, Toyka KV, Hartung HP (2001) Expression of specific matrix metalloproteinases in inflammatory myopathies. Brain 124:341-351
33. Kim SH, Choi NS, Lee WY (1998) Fibrin zymography: a direct analysis of fibrinolytic enzymes on gels. Anal Biochem 263:115-116
34. Knox JB, Sukhova GK, Whittemore AD, Libby P (1997) Evidence for altered balance between matrix metalloproteinases and their inhibitors in human aortic diseases. Circulation 95:205-212
35. Koblinski JE, Ahram M, Sloane BF (2000) Unraveling the role of proteases in cancer. Clin Chim Acta 291:113-135
36. Kohler C, Orrenius S, Zhivotovsky B (2002) Evaluation of caspase activity in apoptotic cells. J Immunol Methods 265:97-110
37. Komoriya A, Packard BZ, Brown MJ, Wu ML, Henkart PA (2000) Assessment of caspase activities in intact apoptotic thymocytes using cell-permeable fluorogenic caspase substrates. J Exp Med 191:1819-1828
38. Koyama H, Iwata H, Kuwabara Y, Iwase H, Kobayashi S, Fujii Y (2000) Gelatinolytic activity of matrix metalloproteinase-2 and -9 in oesophageal carcinoma; a study using in situ zymography. Eur J Cancer 36:2164-2170
39. Kranzhofer A, Baker AH, George SJ, Newby AC (1999) Expression of tissue inhibitor of metalloproteinase-1, -2, and -3 during neointima formation in organ cultures of human saphenous vein. Arterioscler Thromb Vasc Biol 19:255-265
40. Krejci-Papa NC, Paus R (1998) A novel in-situ-zymography technique localizes gelatinolytic activity in human skin to mast cells. Exp Dermatol 7:321-326
41. Kurschat P, Wickenhauser C, Groth W, Krieg T, Mauch C (2002) Identification of activated matrix metalloproteinase-2 (MMP-2) as the main gelatinolytic enzyme in malignant melanoma by in situ zymography. J Pathol 197:179-187
42. Leber TM, Balkwill FR (1997) Zymography: a single-step staining method for quantitation of proteolytic activity on substrate gels. Anal Biochem 249:24-28
43. Leco KJ, Waterhouse P, Sanchez OH, Gowing KL, Poole AR, Wakeham A, Mak TW, et al. (2001) Spontaneous air space enlargement in the lungs of mice lacking tissue inhibitor of metalloproteinases-3 (TIMP-3). J Clin Invest 108:817-829
44. Lee BW, Johnson GL, Hed SA, Darzynkiewicz Z, Talhouk JW, Mehrotra S (2003) DEVDase detection in intact apoptotic cells using the cell permeant fluorogenic substrate, (z-DEVD)2-cresyl violet. BioTechniques 35:1080-1085
45. Lee SR, Tsuji K, Lee SR, Lo EH (2004) Role of matrix metalloproteinases in delayed neuronal damage after transient global cerebral ischemia. J Neurosci 24:671-678
46. Lengyel E, Schmalfeldt B, Konik E, Spathe K, Harting K, Fenn A, Berger U, et al. (2001) Expression of latent matrix metalloproteinase 9 (MMP-9) predicts survival in advanced ovarian cancer. Gynecol Oncol 82:291-298
47. Leytus SP, Melhado LL, Mangel WF (1983) Rhodamine-based compounds as fluorogenic substrates for serine proteinases. Biochem J 209:299-307
48. Lindsey M, Wedin K, Brown MD, Keller C, Evans AJ, Smolen J, Burns AR, et al. (2001) Matrix-dependent mechanism of neutrophil-mediated release and activation of matrix metalloproteinase 9 in myocardial ischemia/reperfusion. Circulation 103:2181-2187
49. Lojda Z (1984) Histochemistry of proteases. Acta Histochem 30:9-28
50. Lojda Z (1996) The use of substrates with 7-amino-3-trifluoromethylcoumarine (AFC) leaving group in the localization of protease activities in situ. Acta Histochem Armed Forces Inst. of Pathology 98:215-228
51. Lopez-Otin C, Overall CM (2002) Protease degradomics: a new challenge for proteomics. Nature Rev Mol Cell Biol 3:509-519
52. Loy M, Burggraf D, Martens KH, Liebetrau M, Wunderlich N, Bultemeier G, Nemori R, et al. (2002) A gelatin in situ-overlay technique localizes brain matrix metalloproteinase activity in experimental focal cerebral ischemia. J Neurosci Methods 116: 125-133
53. Maquoi E, Munaut C, Colige A, Collen D, Lijnen HR (2002) Modulation of adipose tissue expression of murine matrix metalloproteinases and their tissue inhibitors with obesity. Diabetes 51: 1093-1101
54. Minami R, Tsunoda H, Iijima T, Yoshikawa H, Nemori R, Noguchi M (2003) Early acquisition of gelatinolytic activity in carcinogenesis of the uterine cervix. Mod Pathol 16:1164-1170
55. Mook OR, Van Overbeek C, Ackema EG, Van Maldegem F, Frederiks WM (2003) In situ localization of gelatinolytic activity in the extracellular matrix of metastases of colon cancer in rat liver using quenched fluorogenic DQ-gelatin. J Histochem Cytochem 51:821-829
56. Mungall BA, Pollitt CC, Collins R (1998) Localisation of gelatinase activity in epidermal hoof lamellae by in situ zymography. Histochem Cell Biol 110:535-540
57. Mungall BA, Pollitt CC (1999) Zymographic analysis of equine laminitis. Histochem Cell Biol 112:467-472
58. Mungall BA, Pollitt CC (2001) In situ zymography: topographical considerations. J Biochem Biophys Methods 47:169-176
59. Nakada M, Nakamura H, Ikeda E, Fujimoto N, Yamashita J, Sato H, Seiki M, et al. (1999) Expression and tissue localization of membrane-type 1, 2, and 3 matrix metalloproteinases in human astrocytic tumors. Am J Pathol 154:417-428
60. Nakamura H, Ueno H, Yamashita K, Shimada T, Yamamoto E, Noguchi M, Fujimoto N, et al. (1999) Enhanced production and activation of progelatinase A mediated by membrane-type 1 matrix metalloproteinase in human papillary thyroid carcinomas. Cancer Res 59:467-473
61. Oh LY, Larsen PH, Krekoski CA, Edwards DR, Donovan F, Werb Z, Yong VW (1999) Matrix metalloproteinase-9/gelatinase B is required for process outgrowth by oligodendrocytes. J Neurosci 19:8464-8475
62. Pardo A, Selman M, Ridge K, Barrios R, Sznajder JI (1996) Increased expression of gelatinases and collagenase in rat lungs exposed to 100% oxygen. Am J Respir Crit Care Med 154:1067-1075
63. Pirila E, Maisi P, Salo T, Koivunen E, Sorsa T (2001) In vivo localization of gelatinases (MMP-2 and -9) by in situ zymography with a selective gelatinase inhibitor. Biochem Biophys Res Commun 287:766-774
64. Platt CI, Krekoski CA, Ward RV, Edwards DR, Gavrilovic J (2003) Extracellular matrix and matrix metalloproteinases in sciatic nerve. J Neurosci Res 74:417-429
65. Premzl A, Zavasnik-Bergant V, Turk V, Kos J (2003) Intracellular and extracellular cathepsin B facilitate invasion of MCF-10A neoT cells through reconstituted extracellular matrix in vitro. Exp Cell Res 283:206-214
66. Ratnikov B, Deryugina E, Leng J, Marchenko G, Dembrow D, Strongin A (2000) Determination of matrix metalloproteinase activity using biotinylated gelatin. Anal Biochem 286:149-155
67. Ratnikov BI, Deryugina EI, Strongin AY (2002) Gelatin zymography and substrate cleavage assays of matrix metalloproteinase-2 in breast carcinoma cells overexpressing membrane type-1 matrix metalloproteinase. Lab Invest 82:1583-1590
68. Robert V, Besse S, Sabri A, Silvestre JS, Assayag P, Nguyen VT, Swynghedauw B, et al. (1997) Differential regulation of matrix metalloproteinases associated with aging and hypertension in the rat heart. Lab Invest 76:729-738
69. Sameni M, Dosescu J, Sloane BF (2001) Imaging proteolysis by living human glioma cells. Biol Chem 382:785-788
70. Sameni M, Moin K, Sloane BF (2000) Imaging proteolysis by living human breast cancer cells. Neoplasia 2:496-504
71. Sappino AP, Belin D, Huarte J, Hirschel-Scholz S, Saurat JH, Vassalli JD (1991) Differential protease expression by cutaneous squamous and basal cell carcinomas. J Clin Invest 88:1073-1079
72. Schellens JP, Vreeling-Sindelarova H, Frederiks WM (2003) Electron microscopical enzyme histochemistry on unfixed tissues and cells. Bridging the gap between LM and EM enzyme histochemistry. Acta Histochem 105:1-19
73. Schroeder J, Gossrau R (1982) Electron microscopic localization of proteases by the direct azo dye staining method. Acta Histochem 25:147-152
74. Shimada T, Nakamura H, Yamashita K, Kawata R, Murakami Y, Fujimoto N, Sato H, et al. (2000) Enhanced production and activation of progelatinase A mediated by membrane-type 1 matrix metalloproteinase in human oral squamous cell carcinomas: implications for lymph node metastasis. Clin Exp Metastasis 18: 179-188
75. Siebert H, Dippel N, Mader M, Weber F, Bruck W (2001) Matrix metalloproteinase expression and inhibition after sciatic nerve axotomy. J Neuropathol Exp Neurol 60:85-93
76. Smith RE, Smithwick EL, Allen CH (1972) A new assay for cathepsin B1 using CBZ-Ala-Arg-Arg-4-Me0-β-NA. J Histochem Cytochem 20:843
77. Smith RE, Van Frank RM (1975) The use of amino acid derivatives of 4-methoxy-β-naphthylamine for the assay and subcellular localization of tissue proteinases. In Dingle JT, Dean RJ, eds. Lysosomes in Biology and Pathology. Amsterdam, North-Holland, 193
78. Stoward PJ (1980) Criteria for the validation of quantitative histochemical enzyme techniques. In Everid D, O'Connor M, eds. Trends in Enzyme Histochemistry and Cytochemistry. Amsterdam, Excerpta Medica, 11-31
79. Tarlton JF, Whiting CV, Tunmore D, Bregenholt S, Reimann J, Claesson MH, Bland PW (2000) The role of up-regulated serine proteases and matrix metalloproteinases in the pathogenesis of a murine model of colitis. Am J Pathol 157:1927-1935
80. Teesalu T, Hinkkanen AE, Vaheri A (2001) Coordinated induction of extracellular proteolysis systems during experimental autoimmune encephalomyelitis in mice. Am J Pathol 159:2227-2237
81. Thomas M, Barker G, Furness PN (1998) A semi-quantitative approach to in situ zymography using tissue sections. J Pathol 186:4A
82. Tyagi SC, Kumar SG, Haas SJ, Reddy HK, Voelker DJ, Hayden MR, Demmy TL, et al. (1996) Post-transcriptional regulation of extracellular matrix metalloproteinase in human heart end-stage failure secondary to ischemic cardiomyopathy. J Mol Cell Cardiol 28:1415-1428
83. Van Noorden CJ, Boonacker E, Bissell ER, Meijer AJ, van Marle J, Smith RE (1997) Ala-Pro-cresyl violet, a synthetic fluorogenic substrate for the analysis of kinetic parameters of dipeptidyl peptidase IV (CD26) in individual living rat hepatocytes. Anal Biochem 252:71-77
84. Van Noorden CJ, Jonges TG, Van Marle J, Bissell ER, Griffini P, Jans M, Snel J, et al. (1998) Heterogeneous suppression of experimentally induced colon cancer metastasis in rat liver lobes by inhibition of extracellular cathepsin B. Clin Exp Metastasis 16: 159-167
85. Van Noorden CJ, Vogels IM, Everts V, Beertsen W (1987) Localization of cathepsin B activity in fibroblasts and chondrocytes by continuous monitoring of the formation of a final fluorescent reaction product using 5-nitrosalicylaldehyde. Histochem J 19: 483-487
86. Van Noorden CJ, Vogels IM, Smith RE (1989) Localization and cytophotometric analysis of cathepsin B activity in unfixed and undecalcified cryostat sections of whole rat knee joints. J Histochem Cytochem 37:617-624
87. Van Noorden CJF, Frederiks WM (1992) Enzyme Histochemistry. A Laboratory Manual of Current Methods. Oxford, Oxford University Press
88. Visse R, Nagase H (2003) Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res 92:827-839
89. Wada N, Otani Y, Kubota T, Kimata M, Minagawa A, Yoshimizu N, Kameyama K, et al. (2003) Reduced angiogenesis in peritoneal dissemination of gastric cancer through gelatinase inhibition. Clin Exp Metastasis 20:431-435
90. Wang M, Lakatta EG (2002) Altered regulation of matrix metalloproteinase-2 in aortic remodeling during aging. Hypertension 39: 865-873
91. Weissleder R, Tung CH, Mahmood U, Bogdanov A Jr (1999) In vivo imaging of tumors with protease-activated near-infrared fluorescent probes. Nature Biotechnol 17:375-378
92. Yamanaka H, Makino K, Takizawa M, Nakamura H, Fujimoto N, Moriya H, Nemori R, et al. (2000) Expression and tissue localization of membrane-types 1, 2, and 3 matrix metalloproteinases in rheumatoid synovium. Lab Invest 80:677-687
93. Yan SJ, Blomme EA (2003) In situ zymography: a molecular pathology technique to localize endogenous protease activity in tissue sections. Vet Pathol 40:227-236
94. Yi CF, Gosiewska A, Burtis D, Geesin J (2001) Incorporation of fluorescent enzyme substrates in agarose gel for in situ zymography. Anal Biochem 291:27-33
95. Zhang J, Salamonsen LA (2002) In vivo evidence for active matrix metalloproteinases in human endometrium supports their role in tissue breakdown at menstruation. J Clin Endocrinol Metab 87: 2346-2351
96. Zheng K, Nagai Y, Kishimoto T, Yamazawa K, Tate S, Nemori R, Hirai Y, et al. (2002) A quantitative evaluation of active gelatinolytic sites in uterine endometrioid adenocarcinoma using film in situ zymography: association of stronger gelatinolysis with myometrial invasion. Jpn J Cancer Res 93:516-522
97. Zhou L, Sawaguchi S, Twining SS, Sugar J, Feder RS, Yue BY (1998) Expression of degradative enzymes and protease inhibitors in corneas with keratoconus. Invest Ophthalmol Vis Sci 39: 1117-1124
98. Zucker S, Lysik RM, Gurfinkel M, Zarrabi MH, Stetler-Stevenson W, Liotta LA, Birkedal-Hansen H, et al. (1992) Immunoassay of type IV collagenase/gelatinase (MMP-2) in human plasma. J Immunol Methods 148:189-198