Role of microRNA-mediated MMP regulation in the treatment and diagnosis of malignant tumors

Cancer Biology and Therapy

Volumn 14, Issue 9, 2013, Pages 796-805

  Li, Liqin ^a   Li, Heng ^b  

^a HUZHOU CENTRAL HOSPITAL   (China)

^b HUZHOU UNIVERSITY   (China)

Author keywords

Angiogenesis; Extracellular matrix; Invasion; Matrix metalloproteinase; MicroRNAs; Migration; Tumor growth

Indexed keywords

ALPHA 2 MACROGLOBULIN; ANTISENSE OLIGONUCLEOTIDE; COLLAGENASE 3; GELATINASE; GELATINASE A; GELATINASE B; INTERLEUKIN 1BETA; INTERSTITIAL COLLAGENASE; MACROPHAGE ELASTASE; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE 14; MATRIX METALLOPROTEINASE 20; MATRIX METALLOPROTEINASE 27; MESSENGER RNA; MICRORNA; MICRORNA 125B; MICRORNA 143; MICRORNA 196B; MICRORNA 206; MICRORNA 21; MICRORNA 340; MICRORNA 451; MICRORNA 7; MICRORNA 9; NEUTROPHIL COLLAGENASE; STROMELYSIN; STROMELYSIN 2; TISSUE INHIBITOR OF METALLOPROTEINASE; TISSUE INHIBITOR OF METALLOPROTEINASE 1; UNCLASSIFIED DRUG; UVOMORULIN; ANTINEOPLASTIC AGENT; FURIN; MATRIX METALLOPROTEINASE INHIBITOR;

3' UNTRANSLATED REGION; BREAST TUMOR; CANCER DIAGNOSIS; CANCER GROWTH; CANCER SURVIVAL; CANCER THERAPY; EPITHELIAL MESENCHYMAL TRANSITION; GLIOBLASTOMA; HUMAN; MALIGNANT NEOPLASTIC DISEASE; METASTASIS; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PANCREAS CANCER; PROTEIN EXPRESSION; REVIEW; TUMOR INVASION; UPREGULATION; ANIMAL; DISEASE COURSE; GENETICS; METABOLISM; NEOPLASMS; PATHOLOGY;

ANIMALS; ANTINEOPLASTIC AGENTS; DISEASE PROGRESSION; FURIN; HUMANS; MATRIX METALLOPROTEINASE INHIBITORS; MATRIX METALLOPROTEINASES; MICRORNAS; NEOPLASMS;

EID: 84883435027     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.25936     Document Type: Review

References (114)

1. Visse R, Nagase H. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res 2003; 92:827-39; PMID:12730128; http://dx.doi.org/10.1161/01. RES.0000070112.80711.3D
2. Murphy G, Nagase H. Progress in matrix metalloproteinase research. Mol Aspects Med 2008; 29:290-308; PMID:18619669; http://dx.doi.org/10.1016/j. mam.2008.05.002
3. Gomis-Rüth FX. Catalytic domain architecture of metzincin metalloproteases. J Biol Chem 2009; 284:15353-7; PMID:19201757; http://dx.doi.org/10.1074/jbc.R800069200
4. Curran S, Murray GI. Matrix metalloproteinases: molecular aspects of their roles in tumour invasion and metastasis. Eur J Cancer 2000; 36(13 Spec No):1621-30; PMID:10959048; http://dx.doi.org/10.1016/ S0959-8049(00)00156-8
5. Egeblad M, Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2002; 2:161-74; PMID:11990853; http:// dx.doi.org/10.1038/nrc745
6. López-Otín C, Matrisian LM. Emerging roles of proteases in tumour suppression. Nat Rev Cancer 2007; 7:800-8; PMID:17851543; http://dx.doi.org/10.1038/ nrc2228
7. Ra HJ, Parks WC. Control of matrix metalloproteinase catalytic activity. Matrix Biol 2007; 26:587-96; PMID:17669641; http://dx.doi.org/10.1016/j.matbio. 2007.07.001
8. Clark IM, Swingler TE, Sampieri CL, Edwards DR. The regulation of matrix metalloproteinases and their inhibitors. Int J Biochem Cell Biol 2008; 40:1362-78; PMID:18258475; http://dx.doi.org/10.1016/j. biocel.2007.12.006
9. Mannello F, Medda V. Nuclear localization of matrix metalloproteinases. Prog Histochem Cytochem 2012; 47:27-58; PMID:22226510; http://dx.doi.org/10. 1016/j.proghi.2011.12.002
10. Sbardella D, Fasciglione GF, Gioia M, Ciaccio C, Tundo GR, Marini S, et al. Human matrix metalloproteinases: an ubiquitarian class of enzymes involved in several pathological processes. Mol Aspects Med 2012; 33:119-208; PMID:22100792; http://dx.doi.org/10.1016/j.mam.2011.10.015
11. Chaudhary A, Pandya S, Ghosh K, Nadkarni A. Matrix metalloproteinase and its drug targets therapy in solid and hematological malignancies: An overview. Mutat Res Rev Mutat Res 2013 http//dx.doi.org/10.1016/j.mrrev.2013.01.002
12. Hubmacher D, Apte SS. The biology of the extracellular matrix: novel insights. Curr Opin Rheumatol 2013; 25:65-70; PMID:23143224; http://dx.doi.org/10.1097/BOR.0b013e32835b137b
13. Murphy G. Tissue inhibitors of metalloproteinases. Genome Biol 2011; 12:233; PMID:22078297; http:// dx.doi.org/10.1186/gb-2011-12-11-233
14. Dalmay T, Edwards DR. MicroRNAs and the hallmarks of cancer. Oncogene 2006; 25:6170-5; PMID:17028596; http://dx.doi.org/10.1038/ sj.onc.1209911
15. Croce CM. Oncogenes and cancer. N Engl J Med 2008; 358:502-11; PMID:18234754; http://dx.doi.org/10.1056/NEJMra072367
16. Esquela-Kerscher A, Slack FJ. Oncomirs -microRNAs with a role in cancer. Nat Rev Cancer 2006; 6:259-69; PMID:16557279; http://dx.doi.org/10.1038/nrc1840
17. He L, He X, Lowe SW, Hannon GJ. microRNAs join the p53 network - another piece in the tumoursuppression puzzle. Nat Rev Cancer 2007; 7:819-22; PMID:17914404; http://dx.doi.org/10.1038/nrc2232
18. Kent OA, Mendell JT. A small piece in the cancer puzzle: microRNAs as tumor suppressors and oncogenes. Oncogene 2006; 25:6188-96; PMID:17028598; http://dx.doi.org/10.1038/sj.onc.1209913
19. Osaki M, Takeshita F, Ochiya T. MicroRNAs as biomarkers and therapeutic drugs in human cancer. Biomarkers 2008; 13:658-70; PMID:19096960; http://dx.doi.org/10.1080/13547500802646572
20. Fanjul-Fernández M, Folgueras AR, Cabrera S, López- Otín C. Matrix metalloproteinases: evolution, gene regulation and functional analysis in mouse models. Biochim Biophys Acta 2010; 1803:3-19; PMID:19631700; http://dx.doi.org/10.1016/j.bbamcr. 2009.07.004
21. Piperi C, Papavassiliou AG. Molecular mechanisms regulating matrix metalloproteinases. Curr Top Med Chem 2012; 12:1095-112; PMID:22519442; http:// dx.doi.org/10.2174/1568026611208011095
22. Overall CM. Molecular determinants of metalloproteinase substrate specificity: matrix metalloproteinase substrate binding domains, modules, and exosites. Mol Biotechnol 2002; 22:51-86; PMID:12353914; http:// dx.doi.org/10.1385/MB:22:1:051
23. Huang L, Dai T, Lin X, Zhao X, Chen X, Wang C, et al. MicroRNA-224 targets RKIP to control cell invasion and expression of metastasis genes in human breast cancer cells. Biochem Biophys Res Commun 2012; 425:127-33; PMID:22809510; http://dx.doi.org/10.1016/j.bbrc.2012.07.025
24. Hwang SJ, Seol HJ, Park YM, Kim KH, Gorospe M, Nam DH, et al. MicroRNA-146a suppresses metastatic activity in brain metastasis. Mol Cells 2012; 34:329-34; PMID:22949171; http://dx.doi.org/10.1007/s10059-012-0171-6
25. Wu J, Wu G, Lv L, Ren YF, Zhang XJ, Xue YF, et al. MicroRNA-34a inhibits migration and invasion of colon cancer cells via targeting to Fra-1. Carcinogenesis 2012; 33:519-28; PMID:22198213; http://dx.doi.org/10.1093/carcin/ bgr304
26. Liu X, Yu J, Jiang L, Wang A, Shi F, Ye H, et al. MicroRNA-222 regulates cell invasion by targeting matrix metalloproteinase 1 (MMP1) and manganese superoxide dismutase 2 (SOD2) in tongue squamous cell carcinoma cell lines. Cancer Genomics Proteomics 2009; 6:131-9; PMID:19487542
27. Xu N, Zhang L, Meisgen F, Harada M, Heilborn J, Homey B, et al. MicroRNA-125b down-regulates matrix metallopeptidase 13 and inhibits cutaneous squamous cell carcinoma cell proliferation, migration, and invasion. J Biol Chem 2012; 287:29899-908; PMID:22782903; http://dx.doi.org/10.1074/jbc. M112.391243
28. Chang HJ, Yang MJ, Yang YH, Hou MF, Hsueh EJ, Lin SR. MMP13 is potentially a new tumor marker for breast cancer diagnosis. Oncol Rep 2009; 22:1119-27; PMID:19787229
29. Impola U, Uitto VJ, Hietanen J, Hakkinen L, Zhang L, Larjava H, et al. Differential expression of matrilysin-1 (MMP-7), 92 kD gelatinase (MMP-9), and metalloelastase (MMP-12) in oral verrucous and squamous cell cancer. J Pathol 2004; 202:14-22; PMID:14694517; http://dx.doi.org/10.1002/path.1479
30. Boström PJ, Ravanti L, Reunanen N, Aaltonen V, Söderström KO, Kähäri VM, et al. Expression of collagenase-3 (matrix metalloproteinase-13) in transitionalcell carcinoma of the urinary bladder. Int J Cancer 2000; 88:417-23; PMID:11054671; http://dx.doi.org/10.1002/1097- 0215(20001101)88:3<417::AIDIJC14> 3.0.CO;2-G
31. Osaki M, Takeshita F, Sugimoto Y, Kosaka N, Yamamoto Y, Yoshioka Y, et al. MicroRNA-143 regulates human osteosarcoma metastasis by regulating matrix metalloprotease-13 expression. Mol Ther 2011; 19:1123-30; PMID:21427707; http://dx.doi.org/10.1038/mt.2011.53
32. Moilanen M, Pirilä E, Grénman R, Sorsa T, Salo T. Expression and regulation of collagenase-2 (MMP-8) in head and neck squamous cell carcinomas. J Pathol 2002; 197:72-81; PMID:12081207; http://dx.doi.org/10.1002/ path.1078
33. Stadlmann S, Pollheimer J, Moser PL, Raggi A, Amberger A, Margreiter R, et al. Cytokine-regulated expression of collagenase-2 (MMP-8) is involved in the progression of ovarian cancer. Eur J Cancer 2003; 39:2499-505; PMID:14602136; http://dx.doi.org/10.1016/j.ejca.2003.08.011
34. Balbín M, Fueyo A, Tester AM, Pendás AM, Pitiot AS, Astudillo A, et al. Loss of collagenase-2 confers increased skin tumor susceptibility to male mice. Nat Genet 2003; 35:252-7; PMID:14517555; http:// dx.doi.org/10.1038/ng1249
35. Gearing AJ, Beckett P, Christodoulou M, Churchill M, Clements J, Davidson AH, et al. Processing of tumour necrosis factoralpha precursor by metalloproteinases. Nature 1994; 6490:555-7; http://dx.doi.org/10.1038/370555a0
36. Zheng X, Chopp M, Lu Y, Buller B, Jiang F. MiR-15b and miR-152 reduce glioma cell invasion and angiogenesis via NRP-2 and MMP-3. Cancer Lett 2013; 329:146-54; PMID:23142217; http://dx.doi.org/10.1016/j.canlet.2012.10.026
37. Graff JW, Powers LS, Dickson AM, Kim J, Reisetter AC, Hassan IH, et al. Cigarette smoking decreases global microRNA expression in human alveolar macrophages. PLoS One 2012; 7:e44066; PMID:22952876; http://dx.doi.org/10.1371/ journal.pone.0044066
38. Yu Q, Stamenkovic I. Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis. Genes Dev 2000; 14:163-76; PMID:10652271
39. McQuibban GA, Gong JH, Wong JP, Wallace JL, Clark-Lewis I, Overall CM. Matrix metalloproteinase processing of monocyte chemoattractant proteins generates CC chemokine receptor antagonists with anti-inflammatory properties in vivo. Blood 2002; 100:1160-7; PMID:12149192
40. Han L, Zhang A, Zhou X, Xu P, Wang GX, Pu PY, et al. Downregulation of Dicer enhances tumor cell proliferation and invasion. Int J Oncol 2010; 37:299-305; PMID:20596657
41. Shi L, Wan Y, Sun G, Gu X, Qian C, Yan W, et al. Functional differences of miR-125b on the invasion of primary glioblastoma CD133-negative cells and CD133-positive cells. Neuromolecular Med 2012; 14:303-16; PMID:22711523; http://dx.doi.org/10.1007/s12017-012-8188-8
42. Alpini G, Glaser SS, Zhang JP, Francis H, Han Y, Gong J, et al. Regulation of placenta growth factor by microRNA-125b in hepatocellular cancer. J Hepatol 2011; 55:1339-45; PMID:21703189; http://dx.doi.org/10.1016/j.jhep. 2011.04.015
43. Zhu Q, Wang Z, Hu Y, Li J, Li X, Zhou L, et al. miR-21 promotes migration and invasion by the miR-21-PDCD4-AP-1 feedback loop in human hepatocellular carcinoma. Oncol Rep 2012; 27:1660-8; PMID:22322403
44. Giovannetti E, Funel N, Peters GJ, Del Chiaro M, Erozenci LA, Vasile E, et al. MicroRNA-21 in pancreatic cancer: correlation with clinical outcome and pharmacologic aspects underlying its role in the modulation of gemcitabine activity. Cancer Res 2010; 70:4528-38; PMID:20460539; http://dx.doi.org/10.1158/ 0008-5472.CAN-09-4467
45. Hu Y, Ou Y, Wu K, Chen Y, Sun W. miR-143 inhibits the metastasis of pancreatic cancer and an associated signaling pathway. Tumour Biol 2012; 33:1863-70; PMID:23070684; http://dx.doi.org/10.1007/s13277-012-0446-8
46. Nan Y, Han L, Zhang A, Wang G, Jia Z, Yang Y, et al. MiRNA-451 plays a role as tumor suppressor in human glioma cells. Brain Res 2010; 1359:14-21; PMID:20816946; http://dx.doi.org/10.1016/j. brainres.2010.08.074
47. Wu DG, Wang YY, Fan LG, Luo H, Han B, Sun LH, et al. MicroRNA-7 regulates glioblastoma cell invasion via targeting focal adhesion kinase expression. Chin Med J (Engl) 2011; 124:2616-21; PMID:22040413
48. Liu H, Cao YD, Ye WX, Sun YY. Effect of microRNA-206 on cytoskeleton remodelling by downregulating Cdc42 in MDA-MB-231 cells. Tumori 2010; 96:751-5; PMID:21302623
49. Wu ZS, Wu Q, Wang CQ, Wang XN, Huang J, Zhao JJ, et al. miR-340 inhibition of breast cancer cell migration and invasion through targeting of oncoprotein c-Met. Cancer 2011; 117:2842-52; PMID:21692045; http://dx.doi.org/ 10.1002/cncr.25860
50. Liu N, Sun Q, Chen J, Li J, Zeng Y, Zhai S, et al. MicroRNA-9 suppresses uveal melanoma cell migration and invasion through the NF-?B1 pathway. Oncol Rep 2012; 28:961-8; PMID:22825752
51. Liao YL, Hu LY, Tsai KW, Wu CW, Chan WC, Li SC, et al. Transcriptional regulation of miR-196b by ETS2 in gastric cancer cells. Carcinogenesis 2012; 33:760-9; PMID:22298639; http://dx.doi.org/10.1093/carcin/ bgs023
52. Steele R, Mott JL, Ray RB. MBP-1 upregulates miR-29b that represses Mcl-1, collagens, and matrixmetalloproteinase-2 in prostate cancer cells. Genes Cancer 2010; 1:381-7; PMID:20657750; http:// dx.doi.org/10.1177/1947601910371978
53. Fang JH, Zhou HC, Zeng C, Yang J, Liu Y, Huang X, et al. MicroRNA-29b suppresses tumor angiogenesis, invasion, and metastasis by regulating matrix metalloproteinase 2 expression. Hepatology 2011; 54:1729-40; PMID:21793034; http://dx.doi.org/10.1002/ hep.24577
54. Ding Q, Chang CJ, Xie X, Xia W, Yang JY, Wang SC, et al. APOBEC3G promotes liver metastasis in an orthotopic mouse model of colorectal cancer and predicts human hepatic metastasis. J Clin Invest 2011; 121:4526-36; PMID:21985787; http://dx.doi.org/10.1172/JCI45008
55. Dong CG, Wu WK, Feng SY, Wang XJ, Shao JF, Qiao J. Co-inhibition of microRNA-10b and microRNA-21 exerts synergistic inhibition on the proliferation and invasion of human glioma cells. Int J Oncol 2012; 41:1005-12; PMID:22766763
56. Ren J, Sun Y, Zhao X, Wang X, Feng J, Liu M, et al. Downregulation of miR-21 regulates MMP-2 expression and suppress migration of Laryngeal squamous cell carcinoma. Head Neck Oncol 2012; 4:65; PMID:23104547
57. Shen K, Liang Q, Xu K, Cui D, Jiang L, Yin P, et al. MiR-139 inhibits invasion and metastasis of colorectal cancer by targeting the type I insulin-like growth factor receptor. Biochem Pharmacol 2012; 84:320-30; PMID:22580051; http://dx.doi.org/10.1016/j. bcp.2012.04.017
58. Cho HM, Jeon HS, Lee SY, Jeong KJ, Park SY, Lee HY, et al. microRNA-101 inhibits lung cancer invasion through the regulation of enhancer of zeste homolog 2. xp Ther Med 2011; 2:963-7; PMID:22977606
59. Liu P, Wilson MJ. miR-520c and miR-373 upregulate MMP9 expression by targeting mTOR and SIRT1, and activate the Ras/Raf/MEK/Erk signaling pathway and NF-?B factor in human fibrosarcoma cells. J Cell Physiol 2012; 227:867-76; PMID:21898400; http:// dx.doi.org/10.1002/jcp.22993
60. Liu B, Wu X, Liu B, Wang C, Liu Y, Zhou Q, et al. MiR-26a enhances metastasis potential of lung cancer cells via AKT pathway by targeting PTEN. Biochim Biophys Acta 2012; 1822:1692-704; PMID:22885155; http://dx.doi.org/10. 1016/j.bbadis.2012.07.019
61. Yan W, Zhang W, Sun L, Liu Y, You G, Wang Y, et al. Identification of MMP-9 specific microRNA expression profile as potential targets of anti-invasion therapy in glioblastoma multiforme. Brain Res 2011; 1411:108-15; PMID:21831363
62. Wan Y, Fei XF, Wang ZM, Jiang DY, Chen HC, Yang J, et al. Expression of miR-125b in the new, highly invasive glioma stem cell and progenitor cell line SU3. Chin J Cancer 2012; 31:207-14; PMID:22360855; http://dx.doi.org/10.5732/ cjc.011.10336
63. Song L, Huang Q, Chen K, Liu L, Lin C, Dai T, et al. miR-218 inhibits the invasive ability of glioma cells by direct downregulation of IKK-β. Biochem Biophys Res Commun 2010; 402:135-40; PMID:20933503; http://dx.doi.org/ 10.1016/j.bbrc.2010.10.003
64. Liu Y, Yan W, Zhang W, Chen L, You G, Bao Z, et al. MiR-218 reverses high invasiveness of glioblastoma cells by targeting the oncogenic transcription factor LEF1. Oncol Rep 2012; 28:1013-21; PMID:22766851
65. Huang XH, Chen JS, Wang Q, Chen XL, Wen L, Chen LZ, et al. miR-338-3p suppresses invasion of liver cancer cell by targeting smoothened. J Pathol 2011; 225:463-72; PMID:21671467; http://dx.doi.org/10.1002/path.2877
66. Li Q, Wang G, Shan JL, Yang ZX, Wang HZ, Feng J, et al. MicroRNA-224 is upregulated in HepG2 cells and involved in cellular migration and invasion. J Gastroenterol Hepatol 2010; 25:164-71; PMID:19793168; http://dx.doi.org/10.1111/ j.1440-1746.2009.05971.x
67. Gao P, Xing AY, Zhou GY, Zhang TG, Zhang JP, Gao C, et al. The molecular mechanism of microRNA-145 to suppress invasion-metastasis cascade in gastric cancer. Oncogene 2013; 32:491-501; PMID:22370644; http://dx.doi.org/10.1038/onc. 2012.61
68. Lohi J, Wilson CL, Roby JD, Parks WCE. Epilysin, a novel human matrix metalloproteinase (MMP-28) expressed in testis and keratinocytes and in response to injury. J Biol Chem 2001; 276:10134-44; PMID:11121398; http://dx.doi.org/10. 1074/jbc. M001599200
69. Velasco G, Pendás AM, Fueyo A, Knäuper V, Murphy G, López-Otín C. Cloning and characterization of human MMP-23, a new matrix metalloproteinase predominantly expressed in reproductive tissues and lacking conserved domains in other family members. J Biol Chem 1999; 274:4570-6; PMID:9988691; http:// dx.doi.org/10.1074/jbc.274.8.4570
70. Uchibori M, Nishida Y, Nagasaka T, Yamada Y, Nakanishi K, Ishiguro N. Increased expression of membrane-type matrix metalloproteinase-1 is correlated with poor prognosis in patients with osteosarcoma. Int J Oncol 2006; 28:33-42; PMID:16327977
71. Ip YC, Cheung ST, Fan ST. Atypical localization of membrane type 1-matrix metalloproteinase in the nucleus is associated with aggressive features of hepatocellular carcinoma. Mol Carcinog 2007; 46:225-30; PMID:17219425; http://dx.doi.org/10.1002/ mc.20270
72. Wolf K, Wu YI, Liu Y, Geiger J, Tam E, Overall C, et al. Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat Cell Biol 2007; 9:893-904; PMID:17618273; http://dx.doi.org/10.1038/ncb1616
73. Bartolomé RA, Ferreiro S, Miquilena-Colina ME, Martínez-Prats L, Soto-Montenegro ML, García-Bernal D, et al. The chemokine receptor CXCR4 and the metalloproteinase MT1-MMP are mutually required during melanoma metastasis to lungs. Am J Pathol 2009; 174:602-12; PMID:19147814; http:// dx.doi.org/10.2353/ajpath.2009.080636
74. Sohail A, Sun Q, Zhao H, Bernardo MM, Cho JA, Fridman R. MT4-(MMP17) and MT6-MMP (MMP25), A unique set of membrane-Anchored matrix metalloproteinases: properties and expression in cancer. Cancer Metastasis Rev 2008; 27:289-302; PMID:18286233; http://dx.doi.org/10.1007/s10555-008-9129-8
75. Seiki MEA, Yana I. Roles of pericellular proteolysis by membrane type-1 matrix metalloproteinase in cancer invasion and angiogenesis. Cancer Sci 2003; 94:569-74; PMID:12841863; http://dx.doi.org/10.1111/j.1349-7006.2003.tb01484.x
76. Al-Raawi DEA, Abu-El-Zahab H, El-Shinawi M, Mohamed MM. Membrane type-1 matrix metalloproteinase (MT1-MMP) correlates with the expression and activation of matrix metalloproteinase-2 (MMP-2) in inflammatory breast cancer. Int J Clin Exp Med 2011; 4:265-75; PMID:22140598
77. Furuichi KEA, Hisada Y, Shimizu M, Okumura T, Kitagawa K, Yoshimoto K, et al. Matrix metalloproteinase-2 (MMP-2) and membrane-type 1 MMP (MT1-MMP) affect the remodeling of glomerulosclerosis in diabetic OLETF rats. Nephrol Dial Transplant 2011; 26:3124-31; PMID:21414971; http://dx.doi.org/10.1093/ndt/gfr125
78. Kachgal SEA, Carrion B, Janson IA, Putnam AJ. Bone marrow stromal cells stimulate an angiogenic program that requires endothelial MT1-MMP. J Cell Physiol 2012; 227:3546-55; PMID:22262018; http://dx.doi.org/10.1002/jcp.24056
79. Soubani O, Ali AS, Logna F, Ali S, Philip PA, Sarkar FH. Re-expression of miR-200 by novel approaches regulates the expression of PTEN and MT1-MMP in pancreatic cancer. Carcinogenesis 2012; 33:1563-71; PMID:22637745; http://dx.doi.org/10.1093/carcin/ bgs189
80. Dangi-Garimella S, Strouch MJ, Grippo PJ, Bentrem DJ, Munshi HG. Collagen regulation of let-7 in pancreatic cancer involves TGF-β1-mediated membrane type 1-matrix metalloproteinase expression. Oncogene 2011; 30:1002-8; PMID:21057545; http://dx.doi.org/10.1038/onc.2010.485
81. Ali S, Banerjee S, Logna F, Bao B, Philip PA, Korc M, et al. Inactivation of Ink4a/Arf leads to deregulated expression of miRNAs in K-Ras transgenic mouse model of pancreatic cancer. J Cell Physiol 2012; 227:3373-80; PMID:22213426; http://dx.doi.org/10.1002/jcp.24036
82. Dong QEA, Yu D, Yang CM, Jiang B, Zhang H. Expression of the reversion-inducing cysteine-rich protein with Kazal motifs and matrix metalloproteinase-14 in neuroblastoma and the role in tumour metastasis. Int J Exp Pathol 2010; 91:368-73; PMID:20579139; http://dx.doi.org/10.1111/j.1365- 2613.2010.00724.x
83. Sun L, Yan W, Wang Y, Sun G, Luo H, Zhang J, et al. MicroRNA-10b induces glioma cell invasion by modulating MMP-14 and uPAR expression via HOXD10. Brain Res 2011; 1389:9-18; PMID:21419107; http:// dx.doi.org/10.1016/j.brainres.2011. 03.013
84. Zhang H, Qi M, Li S, Qi T, Mei H, Huang K, et al. microRNA-9 targets matrix metalloproteinase 14 to inhibit invasion, metastasis, and angiogenesis of neuroblastoma cells. Mol Cancer Ther 2012; 11:1454-66; PMID:22564723; http://dx.doi.org/10.1158/1535-7163.MCT-12-0001
85. Arai I, Nagano H, Kondo M, Yamamoto H, Hiraoka N, Sugita Y, et al. Overexpression of MT3-MMP in hepatocellular carcinoma correlates with capsular invasion. Hepatogastroenterology 2007; 54:167-71; PMID:17419254
86. Lowy AM, Clements WM, Bishop J, Kong L, Bonney T, Sisco K, et al. beta-Catenin/Wnt signaling regulates expression of the membrane type 3 matrix metalloproteinase in gastric cancer. Cancer Res 2006; 66:4734-41; PMID:16651426; http://dx.doi.org/10.1158/0008-5472.CAN-05-4268
87. Astarci E, Erson-Bensan AE, Banerjee S. Matrix metalloprotease 16 expression is downregulated by microRNA-146a in spontaneously differentiating Caco-2 cells. Dev Growth Differ 2012; 54:216-26; PMID:22348245; http://dx.doi.org/10.1111/j.1440-169X.2011.01324.x
88. Xia H, Qi Y, Ng SS, Chen X, Li D, Chen S, et al. microRNA-146b inhibits glioma cell migration and invasion by targeting MMPs. Brain Res 2009; 1269:158-65; PMID:19265686; http://dx.doi.org/10.1016/j.brainres.2009.02.037
89. Belguise KEA, Kersual N, Galtier F, Chalbos D. FRA-1 expression level regulates proliferation and invasiveness of breast cancer cells. Oncogene 2005; 24:1434-44; PMID:15608675; http://dx.doi.org/10.1038/ sj.onc.1208312
90. Xu B, Wang N, Wang X, Tong N, Shao N, Tao J, et al. MiR-146a suppresses tumor growth and progression by targeting EGFR pathway and in a p-ERK-dependent manner in castration-resistant prostate cancer. Prostate 2012; 72:1171-8; PMID:22161865; http://dx.doi.org/10.1002/pros.22466
91. Collette T, Bellehumeur C, Kats R, Maheux R, Mailloux J, Villeneuve M, et al. Evidence for an increased release of proteolytic activity by the ectopic endometrial tissue in women with endometriosis and for involvement of matrix metalloproteinase-9. Hum Reprod 2004; 6:1257-64; http://dx.doi.org/10.1093/ humrep/deh290
92. Folgueras AR, Pendás AM, Sánchez LM, López- Otín C. Matrix metalloproteinases in cancer: from new functions to improved inhibition strategies. Int J Dev Biol 2004; 48:411-24; PMID:15349816; http://dx.doi.org/10.1387/ijdb.041811af
93. Qi JH, Ebrahem Q, Moore N, Murphy G, Claesson-Welsh L, Bond M, et al. A novel function for tissue inhibitor of metalloproteinases-3 (TIMP3): inhibition of angiogenesis by blockage of VEGF binding to VEGF receptor-2. Nat Med 2003; 9:407-15; PMID:12652295; http://dx.doi.org/10.1038/nm846
94. Brew K, Nagase H. The tissue inhibitors of metalloproteinases (TIMPs): an ancient family with structural and functional diversity. Biochim Biophys Acta 2010; 1803:55-71; PMID:20080133; http://dx.doi.org/10.1016/j.bbamcr.2010.01.003
95. Yu D, Zhou H, Xun Q, Xu X, Ling J, Hu Y. microRNA-103 regulates the growth and invasion of endometrial cancer cells through the downregulation of tissue inhibitor of metalloproteinase 3. Lincol Lett 2012; 3:1221-6; PMID:22783422
96. Wang B, Hsu SH, Majumder S, Kutay H, Huang W, Jacob ST, et al. TGFbeta-mediated upregulation of hepatic miR-181b promotes hepatocarcinogenesis by targeting TIMP3. Oncogene 2010; 29:1787-97; PMID:20023698; http://dx.doi.org/10.1038/ onc.2009.468
97. He Y, Cui Y, Wang W, Gu J, Guo S, Ma K, et al. Hypomethylation of the hsa-miR-191 locus causes high expression of hsa-mir-191 and promotes the epithelialto-mesenchymal transition in hepatocellular carcinoma. Neoplasia 2011; 13:841-53; PMID:21969817
98. Almog N, Ma L, Schwager C, Brinkmann BG, Beheshti A, Vajkoczy P, et al. Consensus micro RNAs governing the switch of dormant tumors to the fast-growing angiogenic phenotype. PLoS One 2012; 7:e44001; PMID:22952847; http://dx.doi.org/10.1371/journal. pone.0044001
99. Garofalo M, Di Leva G, Romano G, Nuovo G, Suh SS, Ngankeu A, et al. miR-221&222 regulate TRAIL resistance and enhance tumorigenicity through PTEN and TIMP3 downregulation. Cancer Cell 2009; 16:498-509; PMID:19962668; http://dx.doi.org/10.1016/j. ccr.2009.10.014
100. Gabriely G, Wurdinger T, Kesari S, Esau CC, Burchard J, Linsley PS, et al. MicroRNA 21 promotes glioma invasion by targeting matrix metalloproteinase regulators. Mol Cell Biol 2008; 28:5369-80; PMID:18591254; http://dx.doi.org/10. 1128/MCB.00479-08
101. Oh J, Takahashi R, Kondo S, Mizoguchi A, Adachi E, Sasahara RM, et al. The membrane-Anchored MMP inhibitor RECK is a key regulator of extracellular matrix integrity and angiogenesis. Cell 2001; 107:789-800; PMID:11747814; http://dx.doi.org/10.1016/ S0092-8674(01)00597-9
102. Clark JC, Thomas DM, Choong PF, Dass CR. RECK - a newly discovered inhibitor of metastasis with prognostic significance in multiple forms of cancer. Cancer Metastasis Rev 2007; 26:675-83; PMID:17828469; http://dx.doi.org/10.1007/s10555-007-9093-8
103. Zhang Z, Li Z, Gao C, Chen P, Chen J, Liu W, et al. miR-21 plays a pivotal role in gastric cancer pathogenesis and progression. Lab Invest 2008; 88:1358-66; PMID:18794849; http://dx.doi.org/10.1038/labinvest. 2008.94
104. Reis ST, Pontes-Junior J, Antunes AA, Dall'Oglio MF, Dip N, Passerotti CC, et al. miR-21 may acts as an oncomir by targeting RECK, a matrix metalloproteinase regulator, in prostate cancer. BMC Urol 2012; 12:14; PMID:22642976; http://dx.doi.org/10.1186/1471-2490-12-14
105. Zhu Y, Yu X, Fu H, Wang H, Wang P, Zheng X, et al. MicroRNA-21 is involved in ionizing radiation-promoted liver carcinogenesis. Int J Clin Exp Med 2010; 3:211-22; PMID:20827319
106. Liu C, Yu J, Yu S, Lavker RM, Cai L, Liu W, et al. MicroRNA-21 acts as an oncomir through multiple targets in human hepatocellular carcinoma. J Hepatol 2010; 53:98-107; PMID:20447717; http://dx.doi.org/10.1016/j.jhep.2010.02.021
107. Han L, Yue X, Zhou X, Lan FM, You G, Zhang W, et al. MicroRNA-21 expression is regulated by β-catenin/STAT3 pathway and promotes glioma cell invasion by direct targeting RECK. CNS Neurosci Ther 2012; 18:573-83; PMID:22630347; http:// dx.doi.org/10.1111/j.1755-5949.2012.00344.x
108. Ziyan W, Shuhua Y, Xiufang W, Xiaoyun L. MicroRNA-21 is involved in osteosarcoma cell invasion and migration. Med Oncol 2011; 28:1469-74; PMID:20480266; http://dx.doi.org/10.1007/s12032-010-9563-7
109. Park JK, Lee EJ, Esau C, Schmittgen TD. Antisense inhibition of microRNA-21 or -221 arrests cell cycle, induces apoptosis, and sensitizes the effects of gemcitabine in pancreatic adenocarcinoma. Pancreas 2009; 38:e190-9; PMID:19730150; http://dx.doi.org/10.1097/MPA.0b013e3181ba82e1
110. Jung HM, Phillips BL, Patel RS, Cohen DM, Jakymiw A, Kong WW, et al. Keratinization-Associated miR-7 and miR-21 regulate tumor suppressor reversioninducing cysteine-rich protein with kazal motifs (RECK) in oral cancer. J Biol Chem 2012; 287:29261-72; PMID:22761427; http://dx.doi.org/10.1074/jbc. M112.366518
111. Loayza-Puch F, Yoshida Y, Matsuzaki T, Takahashi C, Kitayama H, Noda M. Hypoxia and RASsignaling pathways converge on, and cooperatively downregulate, the RECK tumor-suppressor protein through microRNAs. Oncogene 2010; 29:2638-48; PMID:20154725; http://dx.doi.org/10.1038/ onc.2010.23
112. Li N, Tang B, Zhu ED, Li BS, Zhuang Y, Yu S, et al. Increased miR-222 in H. pylori-Associated gastric cancer correlated with tumor progression by promoting cancer cell proliferation and targeting RECK. FEBS Lett 2012; 586:722-8; PMID:22321642; http:// dx.doi.org/10.1016/j.febslet.2012.01.025
113. Bauvois B. New facets of matrix metalloproteinases MMP-2 and MMP-9 as cell surface transducers: outside-in signaling and relationship to tumor progression. Biochim Biophys Acta 2012; 1825:29-36; PMID:22020293
114. Wang H, Wu J, Meng X, Ying X, Zuo Y, Liu R, et al. MicroRNA-342 inhibits colorectal cancer cell proliferation and invasion by directly targeting DNA methyltransferase 1. Carcinogenesis 2011; 32:1033-42; PMID:21565830; http://dx.doi.org/10.1093/carcin/ bgr081