Matrix metalloproteinases in cancer: Their value as diagnostic and prognostic markers and therapeutic targets

Tumor Biology

Volumn 34, Issue 4, 2013, Pages 2041-2051

  Hadler Olsen, Elin ^a   Winberg, Jan Olof ^a   Uhlin Hansen, Lars ^a,b  

^a UNIVERSITY OF TROMSØ   (Norway)

^b UNIVERSITY HOSPITAL OF NORTH NORWAY   (Norway)

Author keywords

Biomarkers; Cancer; Drug design; Matrix metalloproteinase

Indexed keywords

ANGIOGENESIS INHIBITOR; ANTINEOPLASTIC AGENT; COLLAGENASE 3; GELATINASE A; GELATINASE B; HORMONE; INTERSTITIAL COLLAGENASE; MACROPHAGE ELASTASE; MATRILYSIN; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE 26; MATRIX METALLOPROTEINASE INHIBITOR; MESSENGER RNA; PHOSPHOTRANSFERASE INHIBITOR; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2;

ANTINEOPLASTIC ACTIVITY; BREAST CANCER; CANCER GROWTH; CANCER PATIENT; CANCER PROGNOSIS; CARCINOGENESIS; CLINICAL TRIAL (TOPIC); COLORECTAL CANCER; DIAGNOSTIC VALUE; DISEASE FREE SURVIVAL; DRUG EFFICACY; DRUG TARGETING; ENZYME ANALYSIS; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; HUMAN; IMMUNOHISTOCHEMISTRY; LUNG CANCER; MALIGNANT NEOPLASTIC DISEASE; MEDICAL DECISION MAKING; NONHUMAN; OVERALL SURVIVAL; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; REVIEW; SENSITIVITY AND SPECIFICITY; UNSPECIFIED SIDE EFFECT; WESTERN BLOTTING;

EID: 84881481410     PISSN: 10104283     EISSN: 14230380     Source Type: Journal    
DOI: 10.1007/s13277-013-0842-8     Document Type: Review

References (128)

1. Brinckerhoff CE, Matrisian LM. Matrix metalloproteinases: a tail of a frog that became a prince. Nat Rev Mol Cell Biol. 2002;3(3):207-14.
2. Hadler-Olsen E, Fadnes B, Sylte I, Uhlin-Hansen L, Winberg JO. Regulation of matrix metalloproteinase activity in health and disease. FEBS J. 2011;278(1):28-45.
3. Nagase H, Visse R, Murphy G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res. 2006;69(3):562-73.
4. Butler GS, Overall CM. Proteomic identification of multitasking proteins in unexpected locations complicates drug targeting. Nat Rev Drug Discov. 2009;8(12):935-48.
5. Butler GS, Overall CM. Updated biological roles for matrix metalloproteinases and new "intracellular" substrates revealed by degradomics. Biochemistry. 2009;48(46):10830-45.
6. Clark IM, Swingler TE, Sampieri CL, Edwards DR. The regulation of matrix metalloproteinases and their inhibitors. Int J Biochem Cell Biol. 2008;40(6-7):1362-78. doi: 10.1016/j.biocel.2007.12.006.
7. Murphy G. Tissue inhibitors of metalloproteinases. Genome Biol. 2011;12(11):233. doi: 10.1186/gb-2011-12-11-233.
8. Stetler-Stevenson WG. Tissue inhibitors of metalloproteinases in cell signaling: metalloproteinase-independent biological activities. Sci Signal. 2008;1(27):re6. doi: 10.1126/scisignal.127re6.
9. Cawston TE, Wilson AJ. Understanding the role of tissue degrading enzymes and their inhibitors in development and disease. Best Pract Res Clin Rheumatol. 2006;20(5):983-1002.
10. Duffy M, McGowan P, Gallagher W. Cancer invasion and metastasis: changing views. J Pathol. 2008;214(3):283-93.
11. Kessenbrock K, Plaks V, Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell. 2010;141(1):52-67.
12. Gialeli C, Theocharis AD, Karamanos NK. Roles of matrix metalloproteinases in cancer progression and their pharmacological targeting. FEBS J. 2011;278(1):16-27.
13. Folgueras AR, Pendas AM, Sanchez LM, Lopez-Otin C. Matrix metalloproteinases in cancer: from new functions to improved inhibition strategies. Int J Dev Biol. 2004;48(5-6):411-24.
14. Egeblad M, Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer. 2002;2(3):161-74.
15. Yu Q, Stamenkovic I. Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis. Genes Dev. 2000;14(2):163-76.
16. Belotti D, Paganoni P, Manenti L, Garofalo A, Marchini S, Taraboletti G, et al. Matrix metalloproteinases (MMP9 and MMP2) induce the release of vascular endothelial growth factor (VEGF) by ovarian carcinoma cells: implications for ascites formation. Cancer Res. 2003;63(17):5224-9.
17. van Hinsbergh VW, Engelse MA, Quax PH. Pericellular proteases in angiogenesis and vasculogenesis. Arterioscler Thromb Vasc Biol. 2006;26(4):716-28. doi: 10.1161/01.ATV.0000209518.58252.17.
18. Fingleton B. Matrix metalloproteinases: roles in cancer and metastasis. Front Biosci. 2006;11:479-91.
19. Lopez-Otin C, Matrisian LM. Emerging roles of proteases in tumour suppression. Nat Rev Cancer. 2007;7(10):800-8.
20. Ha HY, Moon HB, Nam MS, Lee JW, Ryoo ZY, Lee TH, et al. Overexpression of membrane-type matrix metalloproteinase-1 gene induces mammary gland abnormalities and adenocarcinoma in transgenic mice. Cancer Res. 2001;61(3):984-90.
21. Rudolph-Owen LA, Chan R, Muller WJ, Matrisian LM. The matrix metalloproteinase matrilysin influences early-stage mammary tumorigenesis. Cancer Res. 1998;58(23):5500-6.
22. Sternlicht MD, Lochter A, Sympson CJ, Huey B, Rougier JP, Gray JW, et al. The stromal proteinase MMP3/stromelysin-1 promotes mammary carcinogenesis. Cell. 1999;98(2):137-46.
23. Witty JP, Lempka T, Coffey Jr RJ, Matrisian LM. Decreased tumor formation in 7,12-dimethylbenzanthracene-treated stromelysin-1 transgenic mice is associated with alterations in mammary epithelial cell apoptosis. Cancer Res. 1995;55(7):1401-6.
24. Bergers G, Brekken R, McMahon G, Vu TH, Itoh T, Tamaki K, et al. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol. 2000;2(10):737-44.
25. Itoh T, Tanioka M, Yoshida H, Yoshioka T, Nishimoto H, Itohara S. Reduced angiogenesis and tumor progression in gelatinase A-deficient mice. Cancer Res. 1998;58(5):1048-51.
26. Itoh T, Tanioka M, Matsuda H, Nishimoto H, Yoshioka T, Suzuki R, et al. Experimental metastasis is suppressed in MMP-9-deficient mice. Clin Exp Metastasis. 1999;17(2):177-81.
27. Wilson CL, Heppner KJ, Labosky PA, Hogan BL, Matrisian LM. Intestinal tumorigenesis is suppressed in mice lacking the metalloproteinase matrilysin. Proc Natl Acad Sci USA. 1997;94(4):1402-7.
28. Acuff HB, Sinnamon M, Fingleton B, Boone B, Levy SE, Chen X, et al. Analysis of host- and tumor-derived proteinases using a custom dual species microarray reveals a protective role for stromal matrix metalloproteinase-12 in non-small cell lung cancer. Cancer Res. 2006;66(16):7968-75. doi: 10.1158/0008-5472.CAN-05-4279.
29. Balbin M, Fueyo A, Tester AM, Pendas AM, Pitiot AS, Astudillo A, et al. Loss of collagenase-2 confers increased skin tumor susceptibility to male mice. Nat Genet. 2003;35(3):252-7.
30. McCawley LJ, Crawford HC, King Jr LE, Mudgett J, Matrisian LM. A protective role for matrix metalloproteinase-3 in squamous cell carcinoma. Cancer Res. 2004;64(19):6965-72.
31. Hadler-Olsen E, Kanapathippillai P, Berg E, Svineng G, Winberg JO, Uhlin-Hansen L. Gelatin In situ zymography on fixed, paraffin-embedded tissue: zinc and ethanol fixation preserve enzyme activity. J Histochem Cytochem. 2009;58(1):29-39. doi: 10.1369/jhc.2009.954354.
32. Snoek-van Beurden PA, Von den Hoff JW. Zymographic techniques for the analysis of matrix metalloproteinases and their inhibitors. Biotechniques. 2005;38(1):73-83.
33. Oliver GW, Leferson JD, Stetler-Stevenson WG, Kleiner DE. Quantitative reverse zymography: analysis of picogram amounts of metalloproteinase inhibitors using gelatinase A and B reverse zymograms. Anal Biochem. 1997;244(1):161-6. doi: 10.1006/abio.1996.9895.
34. Mathisen B, Lindstad RI, Hansen J, El-Gewely SA, Maelandsmo GM, Hovig E, et al. S100A4 regulates membrane induced activation of matrix metalloproteinase-2 in osteosarcoma cells. Clin Exp Metastasis. 2003;20(8):701-11.
35. Hattori S, Fujisaki H, Kiriyama T, Yokoyama T, Irie S. Real-time zymography and reverse zymography: a method for detecting activities of matrix metalloproteinases and their inhibitors using FITC-labeled collagen and casein as substrates. Anal Biochem. 2002;301(1):27-34. doi: 10.1006/abio.2001.5479.
36. Hurst NG, Stocken DD, Wilson S, Keh C, Wakelam MJ, Ismail T. Elevated serum matrix metalloproteinase 9 (MMP-9) concentration predicts the presence of colorectal neoplasia in symptomatic patients. Br J Cancer. 2007;97(7):971-7.
37. Wilson S, Wakelam MJ, Hobbs RF, Ryan AV, Dunn JA, Redman VD, et al. Evaluation of the accuracy of serum MMP-9 as a test for colorectal cancer in a primary care population. BMC Cancer. 2006;6:258. doi: 10.1186/1471-2407-6-258.
38. Eissa S, Ali-Labib R, Swellam M, Bassiony M, Tash F, El-Zayat TM. Noninvasive diagnosis of bladder cancer by detection of matrix metalloproteinases (MMP-2 and MMP-9) and their inhibitor (TIMP-2) in urine. Eur Urol. 2007;52(5):1388-96. doi: 10.1016/j.eururo.2007.04.006.
39. Roy R, Louis G, Loughlin KR, Wiederschain D, Kilroy SM, Lamb CC, et al. Tumor-specific urinary matrix metalloproteinase fingerprinting: identification of high molecular weight urinary matrix metalloproteinase species. Clin Cancer Res. 2008;14(20):6610-7. doi: 10.1158/1078-0432.CCR-08-1136.
40. Fernandez CA, Yan L, Louis G, Yang J, Kutok JL, Moses MA. The matrix metalloproteinase-9/neutrophil gelatinase-associated lipocalin complex plays a role in breast tumor growth and is present in the urine of breast cancer patients. Clin Cancer Res. 2005;11(15):5390-5.
41. Incorvaia L, Badalamenti G, Rini G, Arcara C, Fricano S, Sferrazza C, et al. MMP-2, MMP-9 and activin A blood levels in patients with breast cancer or prostate cancer metastatic to the bone. Anticancer Res. 2007;27(3B):1519-25.
42. Lukaszewicz-Zajac M, Mroczko B, Kozlowski M, Niklinski J, Laudanski J, Szmitkowski M. Elevated levels of serum metalloproteinase 9 in patients with esophageal squamous cell carcinoma. Pol Arch Med Wewn. 2009;119(9):558-63.
43. Mroczko B, Kozlowski M, Groblewska M, Lukaszewicz M, Niklinski J, Jelski W, et al. The diagnostic value of the measurement of matrix metalloproteinase 9 (MMP-9), squamous cell cancer antigen (SCC) and carcinoembryonic antigen (CEA) in the sera of esophageal cancer patients. Clin Chim Acta. 2008;389(1-2):61-6.
44. Mroczko B, Lukaszewicz-Zajac M, Wereszczynska-Siemiatkowska U, Groblewska M, Gryko M, Kedra B, et al. Clinical significance of the measurements of serum matrix metalloproteinase-9 and its inhibitor (tissue inhibitor of metalloproteinase-1) in patients with pancreatic cancer: metalloproteinase-9 as an independent prognostic factor. Pancreas. 2009;38(6):613-8.
45. Patel S, Sumitra G, Koner BC, Saxena A. Role of serum matrix metalloproteinase-2 and -9 to predict breast cancer progression. Clin Biochem. 2011;44(10-11):869-72.
46. Provatopoulou X, Gounaris A, Kalogera E, Zagouri F, Flessas I, Goussetis E, et al. Circulating levels of matrix metalloproteinase-9 (MMP-9), neutrophil gelatinase-associated lipocalin (NGAL) and their complex MMP-9/NGAL in breast cancer disease. BMC Cancer. 2009;9:390.
47. Ramankulov A, Lein M, Johannsen M, Schrader M, Miller K, Jung K. Plasma matrix metalloproteinase-7 as a metastatic marker and survival predictor in patients with renal cell carcinomas. Cancer Sci. 2008;99(6):1188-94.
48. Sarkissian G, Fergelot P, Lamy PJ, Patard JJ, Culine S, Jouin P, et al. Identification of pro-MMP-7 as a serum marker for renal cell carcinoma by use of proteomic analysis. Clin Chem. 2008;54(3):574-81.
49. Shpitzer T, Hamzany Y, Bahar G, Feinmesser R, Savulescu D, Borovoi I, et al. Salivary analysis of oral cancer biomarkers. Br J Cancer. 2009;101(7):1194-8.
50. Smith ER, Zurakowski D, Saad A, Scott RM, Moses MA. Urinary biomarkers predict brain tumor presence and response to therapy. Clin Cancer Res. 2008;14(8):2378-86.
51. Cribier B, Noacco G, Peltre B, Grosshans E. Stromelysin 3 expression: a useful marker for the differential diagnosis dermatofibroma versus dermatofibrosarcoma protuberans. J Am Acad Dermatol. 2002;46(3):408-13.
52. Kim HJ, Lee JY, Kim SH, Seo YJ, Lee JH, Park JK, et al. Stromelysin-3 expression in the differential diagnosis of dermatofibroma and dermatofibrosarcoma protuberans: comparison with factor XIIIa and CD34. Br J Dermatol. 2007;157(2):319-24.
53. Gouyer V, Conti M, Devos P, Zerimech F, Copin MC, Creme E, et al. Tissue inhibitor of metalloproteinase 1 is an independent predictor of prognosis in patients with nonsmall cell lung carcinoma who undergo resection with curative intent. Cancer. 2005;103(8):1676-84.
54. Hofmann HS, Bartling B, Simm A, Murray R, Aziz N, Hansen G, et al. Identification and classification of differentially expressed genes in non-small cell lung cancer by expression profiling on a global human 59.620-element oligonucleotide array. Oncol Rep. 2006;16(3):587-95.
55. Hsu CP, Shen GH, Ko JL. Matrix metalloproteinase-13 expression is associated with bone marrow microinvolvement and prognosis in non-small cell lung cancer. Lung Cancer. 2006;52(3):349-57.
56. Li L, Mei TH, Zhou XD, Zhang XG. Expression and clinical significance of matrix metalloproteinase (MMP)-26 protein in non-small cell lung cancer. Ai Zheng. 2009;28(1):60-3.
57. Safranek J, Pesta M, Holubec L, Kulda V, Dreslerova J, Vrzalova J, et al. Expression of MMP-7, MMP-9, TIMP-1 and TIMP-2 mRNA in lung tissue of patients with non-small cell lung cancer (NSCLC) and benign pulmonary disease. Anticancer Res. 2009;29(7):2513-7.
58. Li M, Xiao T, Zhang Y, Feng L, Lin D, Liu Y, et al. Prognostic significance of matrix metalloproteinase-1 levels in peripheral plasma and tumour tissues of lung cancer patients. Lung Cancer. 2010;69(3):341-7.
59. Qian Q, Wang Q, Zhan P, Peng L, Wei SZ, Shi Y, et al. The role of matrix metalloproteinase 2 on the survival of patients with non-small cell lung cancer: a systematic review with meta-analysis. Cancer Invest. 2010;28(6):661-9.
60. Kim SJ, Rabbani ZN, Dewhirst MW, Vujaskovic Z, Vollmer RT, Schreiber EG, et al. Expression of HIF-1alpha, CA IX, VEGF, and MMP-9 in surgically resected non-small cell lung cancer. Lung Cancer. 2005;49(3):325-35.
61. Leinonen T, Pirinen R, Bohm J, Johansson R, Ropponen K, Kosma VM. Expression of matrix metalloproteinases 7 and 9 in non-small cell lung cancer: relation to clinicopathological factors, beta-catenin and prognosis. Lung Cancer. 2006;51(3):313-21.
62. Matsuyama M, Chijiwa T, Inoue Y, Abe Y, Nishi M, Miyazaki N, et al. Alternative splicing variant of vascular endothelial growth factor-A is a critical prognostic factor in non-small cell lung cancer. Oncol Rep. 2009;22(6):1407-13.
63. Shimanuki Y, Takahashi K, Cui R, Hori S, Takahashi F, Miyamoto H, et al. Role of serum vascular endothelial growth factor in the prediction of angiogenesis and prognosis for non-small cell lung cancer. Lung. 2005;183(1):29-42.
64. Takemoto N, Tada M, Hida Y, Asano T, Cheng S, Kuramae T, et al. Low expression of reversion-inducing cysteine-rich protein with Kazal motifs (RECK) indicates a shorter survival after resection in patients with adenocarcinoma of the lung. Lung Cancer. 2007;58(3):376-83.
65. Grossi F, Spizzo R, Bordo D, Cacitti V, Valent F, Rossetto C, et al. Prognostic stratification of stage IIIA pN2 non-small cell lung cancer by hierarchical clustering analysis of tissue microarray immunostaining data: an Alpe Adria Thoracic Oncology Multidisciplinary Group study (ATOM 014). J Thorac Oncol. 2010;5(9):1354-60.
66. Hoikkala S, Paakko P, Soini Y, Makitaro R, Kinnula V, Turpeenniemi-Hujanen T. Tissue MMP-2 and MMP-9 [corrected] are better prognostic factors than serum MMP-2/TIMP-2 - complex or TIMP-1 [corrected] in stage [corrected] I-III lung carcinoma. Cancer Lett. 2006;236(1):125-32. doi: 10.1016/j.canlet.2005.05.012.
67. Martins SJ, Takagaki TY, Silva AG, Gallo CP, Silva FB, Capelozzi VL. Prognostic relevance of TTF-1 and MMP-9 expression in advanced lung adenocarcinoma. Lung Cancer. 2009;64(1):105-9.
68. Ylisirnio S, Hoyhtya M, Turpeenniemi-Hujanen T. Serum matrix metalloproteinases -2, -9 and tissue inhibitors of metalloproteinases -1, -2 in lung cancer - TIMP-1 as a prognostic marker. Anticancer Res. 2000;20(2B):1311-6.
69. Zheng S, Chang Y, Hodges KB, Sun Y, Ma X, Xue Y, et al. Expression of KISS1 and MMP-9 in non-small cell lung cancer and their relations to metastasis and survival. Anticancer Res. 2010;30(3):713-8.
70. Peng WJ, Zhang JQ, Wang BX, Pan HF, Lu MM, Wang J. Prognostic value of matrix metalloproteinase 9 expression in patients with non-small cell lung cancer. Clin Chim Acta: Int J Clin Chem. 2012. doi: 10.1016/j.cca.2012.03.012.
71. Zhu ZH, Sun BY, Ma Y, Shao JY, Long H, Zhang X, et al. Three immunomarker support vector machines-based prognostic classifiers for stage IB non-small-cell lung cancer. J Clin Oncol. 2009;27(7):1091-9.
72. Liu D, Nakano J, Ishikawa S, Yokomise H, Ueno M, Kadota K, et al. Overexpression of matrix metalloproteinase-7 (MMP-7) correlates with tumor proliferation, and a poor prognosis in non-small cell lung cancer. Lung Cancer. 2007;58(3):384-91.
73. Liu H, Zhang T, Li X, Huang J, Wu B, Huang X, et al. Predictive value of MMP-7 expression for response to chemotherapy and survival in patients with non-small cell lung cancer. Cancer Sci. 2008;99(11):2185-92.
74. Garcia-Albeniz X, Pericay C, Alonso-Espinaco V, Alonso V, Escudero P, Fernandez-Martos C, et al. Serum matrilysin correlates with poor survival independently of KRAS and BRAF status in refractory advanced colorectal cancer patients treated with irinotecan plus cetuximab. Tumour Biol: J Int Soc Oncodev Biol Med. 2011;32(2):417-24. doi: 10.1007/s13277-010-0136-3.
75. Hilska M, Roberts PJ, Collan YU, Laine VJ, Kossi J, Hirsimaki P, et al. Prognostic significance of matrix metalloproteinases-1, -2, -7 and -13 and tissue inhibitors of metalloproteinases-1, -2, -3 and -4 in colorectal cancer. Int J Cancer. 2007;121(4):714-23.
76. Koskensalo S, Louhimo J, Nordling S, Hagstrom J, Haglund C. MMP-7 as a prognostic marker in colorectal cancer. Tumour Biol: J Int Soc Oncodev Biol Med. 2011;32(2):259-64. doi: 10.1007/s13277-010-0080-2.
77. Ring P, Johansson K, Hoyhtya M, Rubin K, Lindmark G. Expression of tissue inhibitor of metalloproteinases TIMP-2 in human colorectal cancer - a predictor of tumour stage. Br J Cancer. 1997;76(6):805-11.
78. Tahara K, Mimori K, Iinuma H, Iwatsuki M, Yokobori T, Ishii H, et al. Serum matrix-metalloproteinase-1 is a bona fide prognostic marker for colorectal cancer. Ann Surg Oncol. 2010;17(12):3362-9.
79. Murray GI, Duncan ME, O'Neil P, Melvin WT, Fothergill JE. Matrix metalloproteinase-1 is associated with poor prognosis in colorectal cancer. Nat Med. 1996;2(4):461-2.
80. Sunami E, Tsuno N, Osada T, Saito S, Kitayama J, Tomozawa S, et al. MMP-1 is a prognostic marker for hematogenous metastasis of colorectal cancer. Oncologist. 2000;5(2):108-14.
81. Hettiaratchi A, Hawkins NJ, McKenzie G, Ward RL, Hunt JE, Wakefield D, et al. The collagenase-1 (MMP-1) gene promoter polymorphism - 1607/2G is associated with favourable prognosis in patients with colorectal cancer. Br J Cancer. 2007;96(5):783-92.
82. Bendardaf R, Buhmeida A, Hilska M, Laato M, Syrjanen S, Syrjanen K, et al. MMP-9 (gelatinase B) expression is associated with disease-free survival and disease-specific survival in colorectal cancer patients. Cancer Invest. 2010;28(1):38-43.
83. Schwandner O, Schlamp A, Broll R, Bruch HP. Clinicopathologic and prognostic significance of matrix metalloproteinases in rectal cancer. Int J Colorectal Dis. 2007;22(2):127-36.
84. Svagzdys S, Lesauskaite V, Pangonyte D, Saladzinskas Z, Tamelis A, Pavalkis D. Matrix metalloproteinase-9 is a prognostic marker to predict survival of patients who underwent surgery due to rectal carcinoma. Tohoku J Exp Med. 2011;223(1):67-73.
85. Waas ET, Lomme RM, DeGroot J, Wobbes T, Hendriks T. Tissue levels of active matrix metalloproteinase-2 and -9 in colorectal cancer. Br J Cancer. 2002;86(12):1876-83.
86. Adachi Y, Yamamoto H, Itoh F, Arimura Y, Nishi M, Endo T, et al. Clinicopathologic and prognostic significance of matrilysin expression at the invasive front in human colorectal cancers. Int J Cancer. 2001;95(5):290-4.
87. Masaki T, Matsuoka H, Sugiyama M, Abe N, Goto A, Sakamoto A, et al. Matrilysin (MMP-7) as a significant determinant of malignant potential of early invasive colorectal carcinomas. Br J Cancer. 2001;84(10):1317-21.
88. Wang WS, Chen PM, Wang HS, Liang WY, Su Y. Matrix metalloproteinase-7 increases resistance to Fas-mediated apoptosis and is a poor prognostic factor of patients with colorectal carcinoma. Carcinogenesis. 2006;27(5):1113-20.
89. Yang W, Arii S, Gorrin-Rivas MJ, Mori A, Onodera H, Imamura M. Human macrophage metalloelastase gene expression in colorectal carcinoma and its clinicopathologic significance. Cancer. 2001;91(7):1277-83.
90. Cheng CW, Yu JC, Wang HW, Huang CS, Shieh JC, Fu YP, et al. The clinical implications of MMP-11 and CK-20 expression in human breast cancer. Clin Chim Acta. 2010;411(3-4):234-41.
91. Jiang WG, Davies G, Martin TA, Parr C, Watkins G, Mason MD, et al. Expression of membrane type-1 matrix metalloproteinase, MT1-MMP in human breast cancer and its impact on invasiveness of breast cancer cells. Int J Mol Med. 2006;17(4):583-90.
92. Kohrmann A, Kammerer U, Kapp M, Dietl J, Anacker J. Expression of matrix metalloproteinases (MMPs) in primary human breast cancer and breast cancer cell lines: new findings and review of the literature. BMC Cancer. 2009;9:188.
93. Somiari SB, Somiari RI, Heckman CM, Olsen CH, Jordan RM, Russell SJ, et al. Circulating MMP2 and MMP9 in breast cancer - potential role in classification of patients into low risk, high risk, benign disease and breast cancer categories. Int J Cancer. 2006;119(6):1403-11.
94. Stankovic S, Konjevic G, Gopcevic K, Jovic V, Inic M, Jurisic V. Activity of MMP-2 and MMP-9 in sera of breast cancer patients. Pathol Res Pract. 2010;206(4):241-7.
95. Zhao YG, Xiao AZ, Ni J, Man YG, Sang QX. Expression of matrix metalloproteinase-26 in multiple human cancer tissues and smooth muscle cells. Ai Zheng. 2009;28(11):1168-75.
96. McGowan PM, Duffy MJ. Matrix metalloproteinase expression and outcome in patients with breast cancer: analysis of a published database. Ann Oncol. 2008;19(9):1566-72.
97. del Casar JM, Gonzalez LO, Alvarez E, Junquera S, Marin L, Gonzalez L, et al. Comparative analysis and clinical value of the expression of metalloproteases and their inhibitors by intratumor stromal fibroblasts and those at the invasive front of breast carcinomas. Breast Cancer Res Treat. 2009;116(1):39-52.
98. Vizoso FJ, Gonzalez LO, Corte MD, Rodriguez JC, Vazquez J, Lamelas ML, et al. Study of matrix metalloproteinases and their inhibitors in breast cancer. Br J Cancer. 2007;96(6):903-11.
99. Mylona E, Nomikos A, Magkou C, Kamberou M, Papassideri I, Keramopoulos A, et al. The clinicopathological and prognostic significance of membrane type 1 matrix metalloproteinase (MT1-MMP) and MMP-9 according to their localization in invasive breast carcinoma. Histopathology. 2007;50(3):338-47.
100. Pellikainen JM, Ropponen KM, Kataja VV, Kellokoski JK, Eskelinen MJ, Kosma VM. Expression of matrix metalloproteinase (MMP)-2 and MMP-9 in breast cancer with a special reference to activator protein-2, HER2, and prognosis. Clin Cancer Res. 2004;10(22):7621-8.
101. Beeghly-Fadiel A, Shu XO, Long J, Li C, Cai Q, Cai H, et al. Genetic polymorphisms in the MMP-7 gene and breast cancer survival. Int J Cancer. 2009;124(1):208-14.
102. Zhang B, Cao X, Liu Y, Cao W, Zhang F, Zhang S, et al. Tumor-derived matrix metalloproteinase-13 (MMP-13) correlates with poor prognoses of invasive breast cancer. BMC Cancer. 2008;8:83.
103. Savinov AY, Remacle AG, Golubkov VS, Krajewska M, Kennedy S, Duffy MJ, et al. Matrix metalloproteinase 26 proteolysis of the NH2-terminal domain of the estrogen receptor beta correlates with the survival of breast cancer patients. Cancer Res. 2006;66(5):2716-24.
104. del Casar JM, Carreno G, Gonzalez LO, Junquera S, Gonzalez-Reyes S, Gonzalez JM, et al. Expression of metalloproteases and their inhibitors in primary tumors and in local recurrences after mastectomy for breast cancer. J Cancer Res Clin Oncol. 2010;136(7):1049-58.
105. Escaff S, Fernandez JM, Gonzalez LO, Suarez A, Gonzalez-Reyes S, Gonzalez JM, et al. Study of matrix metalloproteinases and their inhibitors in prostate cancer. Br J Cancer. 2010;102(5):922-9.
106. Escaff S, Fernandez JM, Gonzalez LO, Suarez A, Gonzalez-Reyes S, Gonzalez JM, et al. Collagenase-3 expression by tumor cells and gelatinase B expression by stromal fibroblast-like cells are associated with biochemical recurrence after radical prostatectomy in patients with prostate cancer. World J Urol. 2011;29(5):657-63. doi: 10.1007/s00345-010-0595-6.
107. Morgia G, Falsaperla M, Malaponte G, Madonia M, Indelicato M, Travali S, et al. Matrix metalloproteinases as diagnostic (MMP-13) and prognostic (MMP-2, MMP-9) markers of prostate cancer. Urol Res. 2005;33(1):44-50.
108. Zhong WD, Han ZD, He HC, Bi XC, Dai QS, Zhu G, et al. CD147, MMP-1, MMP-2 and MMP-9 protein expression as significant prognostic factors in human prostate cancer. Oncology. 2008;75(3-4):230-6.
109. Szarvas T, Becker M, Vom DF, Meschede J, Scherag A, Bankfalvi A, et al. Elevated serum matrix metalloproteinase 7 levels predict poor prognosis after radical prostatectomy. Int J Cancer. 2011;128(6):1486-92.
110. Szarvas T, Jager T, Becker M, Tschirdewahn S, Niedworok C, Kovalszky I, et al. Validation of circulating MMP-7 level as an independent prognostic marker of poor survival in urinary bladder cancer. Pathol Oncol Res. 2011;17(2):325-32.
111. Zhang L, Shi J, Feng J, Klocker H, Lee C, Zhang J. Type IV collagenase (matrix metalloproteinase-2 and -9) in prostate cancer. Prostate Cancer Prostatic Dis. 2004;7(4):327-32.
112. Miyake H, Muramaki M, Kurahashi T, Takenaka A, Fujisawa M. Expression of potential molecular markers in prostate cancer: correlation with clinicopathological outcomes in patients undergoing radical prostatectomy. Urol Oncol. 2010;28(2):145-51.
113. Boxler S, Djonov V, Kessler TM, Hlushchuk R, Bachmann LM, Held U, et al. Matrix metalloproteinases and angiogenic factors: predictors of survival after radical prostatectomy for clinically organ-confined prostate cancer? Am J Pathol. 2010;177(5):2216-24.
114. De CC, Ravasi L, Zorzino L, Sandri MT, Botteri E, Verweij F, et al. Circulating levels of VCAM and MMP-2 may help identify patients with more aggressive prostate cancer. Curr Cancer Drug Targets. 2008;8(3):199-206.
115. Coussens LM, Fingleton B, Matrisian LM. Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science. 2002;295(5564):2387-92.
116. Martin MD, Matrisian LM. The other side of MMPs: protective roles in tumor progression. Cancer Metastasis Rev. 2007;26(3-4):717-24.
117. Overall CM, Lopez-Otin C. Strategies for MMP inhibition in cancer: innovations for the post-trial era. Nat Rev Cancer. 2002;2(9):657-72.
118. Morrison CJ, Butler GS, Rodriguez D, Overall CM. Matrix metalloproteinase proteomics: substrates, targets, and therapy. Curr Opin Cell Biol. 2009;21(5):645-53.
119. Terp GE, Cruciani G, Christensen IT, Jorgensen FS. Structural differences of matrix metalloproteinases with potential implications for inhibitor selectivity examined by the GRID/CPCA approach. J Med Chem. 2002;45(13):2675-84.
120. Cuniasse P, Devel L, Makaritis A, Beau F, Georgiadis D, Matziari M, et al. Future challenges facing the development of specific active-site-directed synthetic inhibitors of MMPs. Biochimie. 2005;87(3-4):393-402.
121. Chung L, Shimokawa K, Dinakarpandian D, Grams F, Fields GB, Nagase H. Identification of the (183)RWTNNFREY(191) region as a critical segment of matrix metalloproteinase 1 for the expression of collagenolytic activity. J Biol Chem. 2000;275(38):29610-7.
122. Chung L, Dinakarpandian D, Yoshida N, Lauer-Fields JL, Fields GB, Visse R, et al. Collagenase unwinds triple-helical collagen prior to peptide bond hydrolysis. EMBO J. 2004;23(15):3020-30.
123. Manka SW, Carafoli F, Visse R, Bihan D, Raynal N, Farndale RW, et al. Structural insights into triple-helical collagen cleavage by matrix metalloproteinase 1. Proc Natl Acad Sci U S A. 2012;109(31):12461-6. doi: 10.1073/pnas.1204991109.
124. Bertini I, Fragai M, Luchinat C, Melikian M, Toccafondi M, Lauer JL, et al. Structural basis for matrix metalloproteinase 1-catalyzed collagenolysis. J Am Chem Soc. 2012;134(4):2100-10. doi: 10.1021/ja208338j.
125. Kousidou OC, Mitropoulou TN, Roussidis AE, Kletsas D, Theocharis AD, Karamanos NK. Genistein suppresses the invasive potential of human breast cancer cells through transcriptional regulation of metalloproteinases and their tissue inhibitors. Int J Oncol. 2005;26(4):1101-9.
126. Mitropoulou TN, Tzanakakis GN, Kletsas D, Kalofonos HP, Karamanos NK. Letrozole as a potent inhibitor of cell proliferation and expression of metalloproteinases (MMP-2 and MMP-9) by human epithelial breast cancer cells. Int J Cancer J Int du Cancer. 2003;104(2):155-60. doi: 10.1002/ijc.10941.
127. Aikawa Y, Morimoto K, Yamamoto T, Chaki H, Hashiramoto A, Narita H, et al. Treatment of arthritis with a selective inhibitor of c-Fos/activator protein-1. Nat Biotechnol. 2008;26(7):817-23. doi: 10.1038/nbt1412.
128. Iliopoulos D, Malizos KN, Tsezou A. Epigenetic regulation of leptin affects MMP-13 expression in osteoarthritic chondrocytes: possible molecular target for osteoarthritis therapeutic intervention. Ann Rheum Dis. 2007;66(12):1616-21. doi: 10.1136/ard.2007.069377.