Epigenetic regulation of matrix metalloproteinases and their collagen substrates in cancer

Biomolecular Concepts

Volumn 2, Issue 3, 2011, Pages 135-147

  Chernov, Andrei V ^a   Strongin, Alex Y ^a  

^a BURNHAM INSTITUTE   (United States)

Author keywords

cancer; cell migration; collagen; DNA methylation; epigenetics; extracellular matrix; glioblastoma; glioma; histone modification; MMP

Indexed keywords

EID: 84861019337     PISSN: 18685021     EISSN: 1868503X     Source Type: Journal    
DOI: 10.1515/bmc.2011.017     Document Type: Review

References (118)

1. Garzon R, Calin GA, Croce CM. MicroRNAs in cancer. Annu Rev Med 2009; 60: 167-79
2. Fry CJ, Peterson CL. Chromatin remodeling enzymes: who's on first? Curr Biol 2001; 11: R185-97
3. Swigut T, Wysocka J. H3K27 demethylases, at long last. Cell 2007; 131: 29-32
4. Turner BM. Reading signals on the nucleosome with a new nomenclature for modified histones. Nat Struct Mol Biol 2005; 12: 110-2
5. Kouzarides T. Chromatin modifications and their function. Cell 2007; 128: 693-705
6. Zhang Y, Reinberg D. Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tails. Genes Dev 2001; 15: 2343-60
7. Bannister AJ, Zegerman P, Partridge JF, Miska EA, Thomas JO, Allshire RC, Kouzarides T. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 2001; 410: 120-4
8. Lachner M, O'Carroll D, Rea S, Mechtler K, Jenuwein T. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 2001; 410: 116-20
9. Nakayama J, Rice JC, Strahl BD, Allis CD, Grewal SI. Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 2001; 292: 110-3
10. Peters AH, Mermoud JE, O'Carroll D, Pagani M, Schweizer D, Brockdorff N, Jenuwein T. Histone H3 lysine 9 methylation is an epigenetic imprint of facultative heterochromatin. Nat Genet 2002; 30: 77-80
11. Chernov AV, Sounni NE, Remacle AG, Strongin AY. Epigenetic control of the invasion-promoting MT1-MMP/MMP-2/TIMP-2 axis in cancer cells. J Biol Chem 2009; 284: 12727-34
12. Cartwright JE, Keogh RJ, Tissot van Patot MC. Hypoxia and placental remodelling. Adv Exp Med Biol 2007; 618: 113-26
13. Erler JT, Bennewith KL, Cox TR, Lang G, Bird D, Koong A, Le QT, Giaccia AJ. Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche. Cancer Cell 2009; 15: 35-44
14. Sorokin L. The impact of the extracellular matrix on inflammation. Nat Rev Immunol 2010; 10: 712-23
15. Gordon MK, Hahn RA. Collagens. Cell Tissue Res 2010; 339: 247-57
16. Kessenbrock K, Plaks V, Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 2010; 141: 52-67
17. Gomis-Ruth, FX. Structural aspects of the metzincin clan of metalloendopeptidases. Mol Biotechnol 2003; 24: 157-202
18. Egeblad M, Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2002; 2: 161-74
19. Nagase H, Woessner JF Jr. Matrix metalloproteinases. J Biol Chem 1999; 274: 21491-4
20. Sternlicht MD, Werb Z. How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 2001; 17: 463-516
21. Zucker S, Pei D, Cao J, Lopez-Otin C. Membrane type-matrix metalloproteinases (MT-MMP). Curr Top Dev Biol 2003; 54: 1-74
22. McQuibban GA, Gong JH, Tam EM, McCulloch CA, Clark-Lewis I, Overall CM. Inflammation dampened by gelatinase A cleavage of monocyte chemoattractant protein-3. Science 2000; 289: 1202-6
23. Van Wart HE, Birkedal-Hansen H. The cysteine switch: a principle of regulation of metalloproteinase activity with potential applicability to the entire matrix metalloproteinase gene family. Proc Natl Acad Sci USA 1990; 87: 5578-82
24. Murphy G, Stanton H, Cowell S, Butler G, Knauper V, Atkinson S, Gavrilovic J. Mechanisms for pro matrix metalloproteinase activation. APMIS 1999; 107: 38-44
25. Pei D, Weiss SJ. Furin-dependent intracellular activation of the human stromelysin-3 zymogen. Nature 1995; 375: 244-7
26. Golubkov VS, Cieplak P, Chekanov AV, Ratnikov BI, Aleshin AE, Golubkova NV, Postnova TI, Radichev IA, Rozanov DV, Zhu W, Motamedchaboki K, Strongin AY. Internal cleavages of the autoinhibitory prodomain are required for membrane type 1 matrix metalloproteinase activation, although furin cleavage alone generates inactive proteinase. J Biol Chem 2010; 285: 27726-36
27. Holmbeck K, Bianco P, Caterina J, Yamada S, Kromer M, Kuznetsov SA, Mankani M, Robey PG, Poole AR, Pidoux I, Ward JM, Birkedal-Hansen H. MT1-MMP-deficient mice develop dwarfism, osteopenia, arthritis, and connective tissue disease due to inadequate collagen turnover. Cell 1999; 99: 81-92
28. Holmbeck K, Bianco P, Yamada S, Birkedal-Hansen H. MT1-MMP: a tethered collagenase. J Cell Physiol 2004; 200: 11-9
29. Coyle RC, Latimer A, Jessen JR. Membrane-Type 1 matrix metalloproteinase regulates cell migration during zebrafish gastrulation: evidence for an interaction with non-canonical Wnt signaling. Exp Cell Res 2008; 314: 2150-62
30. Golubkov VS, Chekanov AV, Cieplak P, Aleshin AE, Chernov AV, Zhu W, Radichev IA, Zhang D, Dong PD, Strongin AY. The Wnt/planar cell polarity protein-Tyrosine kinase-7 (PTK7) is a highly efficient proteolytic target of membrane type-1 matrix metalloproteinase: implications in cancer and embryogenesis. J Biol Chem 2010; 285: 35740-9
31. Oh J, Takahashi R, Adachi E, Kondo S, Kuratomi S, Noma A, Alexander DB, Motoda H, Okada A, Seiki M, Itoh T, Itohara S, Takahashi C, Noda M. Mutations in two matrix metalloproteinase genes, MMP-2 and MT1-MMP, are synthetic lethal in mice. Oncogene 2004; 23: 5041-8
32. 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
33. Nagase H, Visse R, Murphy G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res 2006; 69: 562-73
34. Lopez-Otin C, Palavalli LH, Samuels Y. Protective roles of matrix metalloproteinases: from mouse models to human cancer. Cell Cycle 2009; 8: 3657-62
35. Gutierrez-Fernandez A, Fueyo A, Folgueras AR, Garabaya C, Pennington CJ, Pilgrim S, Edwards DR, Holliday DL, Jones JL, Span PN, Sweep FC, Puente XS, Lopez-Otin C. Matrix metalloproteinase-8 functions as a metastasis suppressor through modulation of tumor cell adhesion and invasion. Cancer Res 2008; 68: 2755-63
36. Korpi JT, Kervinen V, Maklin H, Vaananen A, Lahtinen M, Laara E, Ristimaki A, Thomas G, Ylipalosaari M, Astrom P, Lopez-Otin C, Sorsa T, Kantola S, Pirila E, Salo T. Collagenase-2 (matrix metalloproteinase-8) plays a protective role in tongue cancer. Br J Cancer 2008; 98: 766-75
37. Decock J, Long JR, Laxton RC, Shu XO, Hodgkinson C, Hendrikx W, Pearce EG, Gao YT, Pereira AC, Paridaens R, Zheng W, Ye S. Association of matrix metalloproteinase-8 gene variation with breast cancer prognosis. Cancer Res 2007; 67: 10214-21
38. Houghton AM, Grisolano JL, Baumann ML, Kobayashi DK, Hautamaki RD, Nehring LC, Cornelius LA, Shapiro SD. Macrophage elastase (matrix metalloproteinase-12) suppresses growth of lung metastases. Cancer Res 2006; 66: 6149-55
39. Acuff HB, Sinnamon M, Fingleton B, Boone B, Levy SE, Chen X, Pozzi A, Carbone DP, Schwartz DR, Moin K, Sloane BF, Matrisian LM. 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: 7968-75
40. Savinov AY, Remacle AG, Golubkov VS, Krajewska M, Kennedy S, Duffy MJ, Rozanov DV, Krajewski S, Strongnin AY. 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: 2716-24
41. Lopez-Otin C, Matrisian LM. Emerging roles of proteases in tumour suppression. Nat Rev Cancer 2007; 7: 800-8
42. McCawley LJ, Wright J, LaFleur BJ, Crawford HC, Matrisian LM. Keratinocyte expression of MMP3 enhances differentiation and prevents tumor establishment. Am J Pathol 2008; 173: 1528-39
43. Martins VL, Vyas JJ, Chen M, Purdie K, Mein CA, South AP, Storey A, McGrath JA, O'Toole EA. Increased invasive behaviour in cutaneous squamous cell carcinoma with loss of basement-membrane type VII collagen. J Cell Sci 2009; 122: 1788-99
44. Yoder JA, Soman NS, Verdine GL, Bestor TH. DNA (cytosine-5)-methyltransferases in mouse cells and tissues. Studies with a mechanism-based probe. J Mol Biol 1997; 270: 385-95
45. Xie S, Wang Z, Okano M, Nogami M, Li Y, He WW, Okumura K, Li E. Cloning, expression and chromosome locations of the human DNMT3 gene family. Gene 1999; 236: 87-95
46. Coulondre C, Miller JH, Farabaugh PJ, Gilbert W. Molecular basis of base substitution hotspots in Escherichia coli. Nature 1978; 274: 775-80
47. Law JA, Jacobsen SE. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 2010; 11: 204-220
48. Gardiner-Garden M, Frommer M. CpG islands in vertebrate genomes. J Mol Biol 1987; 196: 261-82
49. Illingworth RS, Bird AP. CpG islands-'a rough guide'. FEBS Lett 2009; 583: 1713-20
50. Tost J. DNA methylation: an introduction to the biology and the disease-Associated changes of a promising biomarker. Methods Mol Biol 2009; 507: 3-20
51. Lopez J, Percharde M, Coley HM, Webb A, Crook T. The context and potential of epigenetics in oncology. Br J Cancer 2009; 100: 571-7
52. Azuara V, Perry P, Sauer S, Spivakov M, Jorgensen HF, John RM, Gouti M, Casanova M, Warnes G, Merkenschlager M, Fisher AG. Chromatin signatures of pluripotent cell lines. Nat Cell Biol 2006; 8: 532-8
53. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, Jaenisch R, Wagschal A, Feil R, Schreiber SL, Lander ES. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 2006; 125: 315-26
54. Roh TY, Cuddapah S, Cui K, Zhao K. The genomic landscape of histone modifications in human T cells. Proc Natl Acad Sci USA 2006; 103: 15782-7
55. Yan C, Wang H, Toh Y, Boyd DD. Repression of 92-kDa type IV collagenase expression by MTA1 is mediated through direct interactions with the promoter via a mechanism, which is both dependent on and independent of histone deacetylation. J Biol Chem 2003; 278: 2309-16
56. Barrett T, Troup DB, Wilhite SE, Ledoux P, Rudnev D, Evangelista C, Kim IF, Soboleva A, Tomashevsky M, Marshall KA, Phillippy KH, Sherman PM, Muertter RN, Edgar R. NCBI GEO: archive for high-Throughput functional genomic data. Nucleic Acids Res 2009; 37: D885-90
57. Sun T, Gao Y, Tan W, Ma S, Zhang X, Wang Y, Zhang Q, Guo Y, Zhao D, Zeng C, Lin D. Haplotypes in matrix metalloproteinase gene cluster on chromosome 11q22 contribute to the risk of lung cancer development and progression. Clin Cancer Res 2006; 12: 7009-17
58. Tsuchiya N, Narita S, Kumazawa T, Inoue T, Ma Z, Tsuruta H, Saito M, Horikawa Y, Yuasa T, Satoh S, Ogawa O, Habuchi T. Clinical significance of a single nucleotide polymorphism and allelic imbalance of matrix metalloproteinase-1 promoter region in prostate cancer. Oncol Rep 2009; 22: 493-9
59. Shimizu C, Matsubara T, Onouchi Y, Jain S, Sun S, Nievergelt CM, Shike H, Brophy VH, Takegawa T, Furukawa S, Akagi T, Newburger JW, Baker AL, Burgner D, Hibberd ML, Davila S, Levin M, Mamtani M, He W, Ahuja SK, Burns JC. Matrix metalloproteinase haplotypes associated with coronary artery aneurysm formation in patients with Kawasaki disease. J Hum Genet 2010; 55: 779-84
60. Wang H, Ogawa M, Wood JR, Bartolomei MS, Sammel MD, Kusanovic JP, Walsh SW, Romero R, Strauss JF 3rd. Genetic and epigenetic mechanisms combine to control MMP1 expression and its association with preterm premature rupture of membranes. Hum Mol Genet 2008; 17: 1087-96
61. Couillard J, Demers M, Lavoie G, St-Pierre Y. The role of DNA hypomethylation in the control of stromelysin gene expression. Biochem Biophys Res Commun 2006; 342: 1233-9
62. Yue W, Sun Q, Landreneau R, Wu C, Siegfried JM, Yu J, Zhang L. Fibulin-5 suppresses lung cancer invasion by inhibiting matrix metalloproteinase-7 expression. Cancer Res 2009; 69: 6339-46
63. Eiseler T, Doppler H, Yan IK, Goodison S, Storz P. Protein kinase D1 regulates matrix metalloproteinase expression and inhibits breast cancer cell invasion. Breast Cancer Res 2009; 11: R13
64. Chernov AV, Baranovskaya S, Golubkov VS, Wakeman DR, Snyder EY, Williams R, Strongin AY. Microarray-based transcriptional and epigenetic profiling of matrix metalloproteinases, collagens, and related genes in cancer. J Biol Chem 2010; 285: 19647-59
65. Bernstein BE, Kamal M, Lindblad-Toh K, Bekiranov S, Bailey DK, Huebert DJ, McMahon S, Karlsson EK, Kulbokas EJ 3rd, Gingeras TR, Schreiber SL, Lander ES. Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 2005; 120: 169-81
66. Birney E, Stamatoyannopoulos JA, Dutta A, Guigo R, Gingeras TR, Margulies EH, Weng Z, Snyder M, Dermitzakis ET, Thurman RE, Kuehn MS, Taylor CM, Neph S, Koch CM, Asthana S, Malhotra A, Adzhubei I, Greenbaum JA, Andrews RM, Flicek P, Boyle PJ, Cao H, Carter NP, Clelland GK, Davis S, Day N, Dhami P, Dillon SC, Dorschner MO, Fiegler H, Giresi PG, Goldy J, Hawrylycz M, Haydock A, Humbert R, James KD, Johnson BE, Johnson EM, Frum TT, Rosenzweig ER, Karnani N, Lee K, Lefebvre GC, Navas PA, Neri F, Parker SC, Sabo PJ, Sandstrom R, Shafer A, Vetrie D, Weaver M, Wilcox S, Yu M, Collins FS. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 2007; 447: 799-816
67. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim TK, Koche RP, Lee W, Mendenhall E, O'Donovan A, Presser A, Russ C, Xie X, Meissner A, Wernig M, Jaenisch R, Nusbaum C, Lander ES, Bernstein BE. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 2007; 448: 553-60
68. Takeshima H, Yamashita S, Shimazu T, Niwa T, Ushijima T. The presence of RNA polymerase II, active or stalled, predicts epigenetic fate of promoter CpG islands. Genome Res 2009; 19: 1974-82
69. Shukeir N, Pakneshan P, Chen G, Szyf M, Rabbani SA. Alteration of the methylation status of tumor-promoting genes decreases prostate cancer cell invasiveness and tumorigenesis in vitro and in vivo. Cancer Res 2006; 66: 9202-10
70. Sato N, Maehara N, Su GH, Goggins M. Effects of 5-Aza-29-deoxycytidine on matrix metalloproteinase expression and pancreatic cancer cell invasiveness. J Natl Cancer Inst 2003; 95: 327-30
71. Ailenberg M, Silverman, M. Trichostatin A-histone deacetylase inhibitor with clinical therapeutic potential-is also a selective and potent inhibitor of gelatinase A expression. Biochem Biophys Res Commun 2002; 298: 110-5
72. Andarawewa KL, Boulay A, Masson R, Mathelin C, Stoll I, Tomasetto C, Chenard MP, Gintz M, Bellocq JP, Rio MC. Dual stromelysin-3 function during natural mouse mammary tumor virus-ras tumor progression. Cancer Res 2003; 63: 5844-9
73. Brasse D, Mathelin C, Leroux K, Chenard MP, Blaise S, Stoll I, Tomasetto C, Rio MC. Matrix metalloproteinase 11/stromelysin-3 exerts both activator and repressor functions during the hematogenous metastatic process in mice. Int J Cancer 2010; 127: 1347-55
74. Chicoine E, Esteve PO, Robledo O, Van Themsche C, Potworowski EF, St-Pierre Y. Evidence for the role of promoter methylation in the regulation of MMP-9 gene expression. Biochem Biophys Res Commun 2002; 297: 765-72
75. Patra SK, Bettuzzi S. Epigenetic DNA-methylation regulation of genes coding for lipid raft-Associated components: a role for raft proteins in cell transformation and cancer progression (review). Oncol Rep 2007; 17: 1279-90
76. Du R, Lu KV, Petritsch C, Liu P, Ganss R, Passegue E, Song H, Vandenberg S, Johnson RS, Werb Z, Bergers G. HIF1alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell 2008; 13: 206-20
77. Liu MC, Choong DY, Hooi CS, Williams LH, Campbell IG. Genetic and epigenetic analysis of the TIMP-3 gene in ovarian cancer. Cancer Lett 2007; 247: 91-7
78. Masson D, Rioux-Leclercq N, Fergelot P, Jouan F, Mottier S, Theoleyre S, Bach-Ngohou K, Patard JJ, Denis MG. Loss of expression of TIMP3 in clear cell renal cell carcinoma. Eur J Cancer 2010; 46: 1430-7
79. Anderson CL, Brown CJ. Epigenetic predisposition to expression of TIMP1 from the human inactive X chromosome. BMC Genet 2005; 6: 48
80. Pulukuri SM, Patibandla S, Patel J, Estes N, Rao JS. Epigenetic inactivation of the tissue inhibitor of metalloproteinase-2 (TIMP-2) gene in human prostate tumors. Oncogene 2007; 26: 5229-37
81. Galm O, Suzuki H, Akiyama Y, Esteller M, Brock MV, Osieka R, Baylin SB, Herman JG. Inactivation of the tissue inhibitor of metalloproteinases-2 gene by promoter hypermethylation in lymphoid malignancies. Oncogene 2005; 24: 4799-805
82. Ivanova T, Vinokurova S, Petrenko A, Eshilev E, Solovyova N, Kisseljov F, Kisseljova N. Frequent hypermethylation of 59 flanking region of TIMP-2 gene in cervical cancer. Int J Cancer 2004; 108: 882-6
83. Paulus W, Sage EH, Liszka U, Iruela-Arispe ML, Jellinger K. Increased levels of type VIII collagen in human brain tumours compared to normal brain tissue and non-neoplastic cerebral disorders. Br J Cancer 1991; 63: 367-71
84. Huijbers IJ, Iravani M, Popov S, Robertson D, Al-Sarraj S, Jones C, Isacke CM. A role for fibrillar collagen deposition and the collagen internalization receptor endo180 in glioma invasion. PLoS One 2010; 5: e9808
85. Nacu N, Luzina IG, Highsmith K, Lockatell V, Pochetuhen K, Cooper ZA, Gillmeister MP, Todd NW, Atamas SP. Macrophages produce TGF-beta-induced (beta-ig-h3) following ingestion of apoptotic cells and regulate MMP14 levels and collagen turnover in fibroblasts. J Immunol 2008; 180: 5036-44
86. Shelton L, Rada JA. Inhibition of human scleral fibroblast cell attachment to collagen type I by TGFBIp. Invest Ophthalmol Vis Sci 2009; 50: 3542-52
87. Messaritou G, East L, Roghi C, Isacke CM, Yarwood H. Membrane type-1 matrix metalloproteinase activity is regulated by the endocytic collagen receptor Endo180. J Cell Sci 2009; 122: 4042-8
88. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009; 136: 215-33
89. Kim VN, Han J, Siomi MC. Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 2009; 10: 126-39
90. Carthew RW, Sontheimer EJ. Origins and mechanisms of miRNAs and siRNAs. Cell 2009; 136: 642-55
91. Eulalio A, Huntzinger E, Izaurralde E. Getting to the root of miRNA-mediated gene silencing. Cell 2008; 132: 9-14
92. Wentz-Hunter KK, Potashkin JA. Role of miRNAs as key regulators in the neoplastic microenvironment. Mol Biol Int 2011; 2011: 839872
93. Gabriely G, Wurdinger T, Kesari S, Esau CC, Burchard J, Linsley PS, Krichevsky AM. MicroRNA 21 promotes glioma invasion by targeting matrix metalloproteinase regulators. Mol Cell Biol 2008; 28: 5369-80
94. Sun L, Yan W, Wang Y, Sun G, Luo H, Zhang J, Wang X, You Y, Liu N, Yang Z. MicroRNA-10b induces glioma cell invasion by modulating MMP-14 and uPAR expression via HOXD10. Brain Res 2011; 1389: 9-18
95. Osaki M, Takeshita F, Sugimoto Y, Kosaka N, Yamamoto Y, Yoshioka Y, Kobayashi E, Yamada T, Kawai A, Inoue T, Ito H, Oshimura M, Ochiya T. MicroRNA-143 regulates human osteosarcoma metastasis by regulating matrix metalloprotease-13 expression. Mol Ther 2011 (in press
96. Xia H, Qi Y, Ng SS, Chen X, Li D, Chen S, Ge R, Jiang S, Li G, Chen Y, He ML, Kung HF, Lai L, Lin MC. microRNA-146b inhibits glioma cell migration and invasion by targeting MMPs. Brain Res 2009; 1269: 158-65
97. Wang B, Hsu SH, Majumder S, Kutay H, Huang W, Jacob ST, Ghoshal K. TGFbeta-mediated upregulation of hepatic miR-181b promotes hepatocarcinogenesis by targeting TIMP3. Oncogene 2010; 29: 1787-97
98. Liu H, Cao YD, Ye WX, Sun YY. Effect of microRNA-206 on cytoskeleton remodelling by downregulating Cdc42 in MDAMB-231 cells. Tumori 2010; 96: 751-5
99. Kato M, Wang L, Putta S, Wang M, Yuan H, Sun G, Lanting L, Todorov I, Rossi JJ, Natarajan R. Post-Transcriptional upregulation of Tsc-22 by Ybx1, a target of miR-216a, mediates TGF-{beta}-induced collagen expression in kidney cells. J Biol Chem 2010; 285: 34004-15
100. Song L, Huang Q, Chen K, Liu L, Lin C, Dai T, Yu C, Wu Z, Li J. miR-218 inhibits the invasive ability of glioma cells by direct downregulation of IKK-beta. Biochem Biophys Res Commun 2010; 402: 135-40
101. Selaru FM, Olaru AV, Kan T, David S, Cheng Y, Mori Y, Yang J, Paun B, Jin Z, Agarwal R, Hamilton JP, Abraham J, Georgiades C, Alvarez H, Vivekanandan P, Yu W, Maitra A, Torbenson M, Thuluvath PJ, Gores GJ, LaRusso NF, Hruban R, Meltzer SJ. MicroRNA-21 is overexpressed in human cholangiocarcinoma and regulates programmed cell death 4 and tissue inhibitor of metalloproteinase 3. Hepatology 2009; 49: 1595-601
102. Song B, Wang C, Liu J, Wang X, Lv L, Wei L, Xie L, Zheng Y, Song X. MicroRNA-21 regulates breast cancer invasion partly by targeting tissue inhibitor of metalloproteinase 3 expression. J Exp Clin Cancer Res 2010; 29: 29
103. Ucar A, Vafaizadeh V, Jarry H, Fiedler J, Klemmt PA, Thum T, Groner B, Chowdhury K. miR-212 and miR-132 are required for epithelial stromal interactions necessary for mouse mammary gland development. Nat Genet 2010; 42: 1101-8
104. Garofalo M, Di Leva G, Romano G, Nuovo G, Suh SS, Ngankeu A, Taccioli C, Pichiorri F, Alder H, Secchiero P, Gasparini P, Gonelli A, Costinean S, Acunzo M, Condorelli G, Croce CM. miR-221&222 regulate TRAIL resistance and enhance tumorigenicity through PTEN and TIMP3 downregulation. Cancer Cell 2009; 16: 498-509
105. Akhtar N, Rasheed Z, Ramamurthy S, Anbazhagan AN, Voss FR, Haqqi TM. MicroRNA-27b regulates the expression of matrix metalloproteinase 13 in human osteoarthritis chondrocytes. Arthritis Rheum 2010; 62: 1361-71
106. Maurer B, Stanczyk J, Jungel A, Akhmetshina A, Trenkmann M, Brock M, Kowal-Bielecka O, Gay RE, Michel BA, Distler JH, Gay S, Distler O. MicroRNA-29, a key regulator of collagen expression in systemic sclerosis. Arthritis Rheum 2010; 62: 1733-43
107. Du B, Ma LM, Huang MB, Zhou H, Huang HL, Shao P, Chen YQ, Qu LH. High glucose down-regulates miR-29a to increase collagen IV production in HK-2 cells. FEBS Lett 2010; 584: 811-6
108. Chen Y, Liu W, Chao T, Zhang Y, Yan X, Gong Y, Qiang B, Yuan J, Sun M, Peng X. MicroRNA-21 down-regulates the expression of tumor suppressor PDCD4 in human glioblastoma cell T98G. Cancer Lett 2008; 272: 197-205
109. Liu Y, Taylor NE, Lu L, Usa K, Cowley AW Jr, Ferreri NR, Yeo NC, Liang M. Renal medullary microRNAs in Dahl saltsensitive rats: miR-29b regulates several collagens and related genes. Hypertension 2010; 55: 974-82
110. Steele R, Mott JL, Ray RB. MBP-1 upregulates miR-29b that represses Mcl-1, collagens, and matrix-metalloproteinase-2 in prostate cancer cells. Genes Cancer 2010; 1: 381-387
111. Ogawa T, Iizuka M, Sekiya Y, Yoshizato K, Ikeda K, Kawada N. Suppression of type I collagen production by microRNA-29b in cultured human stellate cells. Biochem Biophys Res Commun 2010; 391: 316-21
112. Chen KC, Wang YS, Hu CY, Chang WC, Liao YC, Dai CY, Juo SH. OxLDL up-regulates microRNA-29b, leading to epigenetic modifications of MMP-2/MMP-9 genes: a novel mechanism for cardiovascular diseases. FASEB J 2011; 25: 1718-28
113. Nan Y, Han L, Zhang A, Wang G, Jia Z, Yang Y, Yue X, Pu P, Zhong Y, Kang C. MiRNA-451 plays a role as tumor suppressor in human glioma cells. Brain Res 2010; 1359: 14-21
114. Song J, Kim D, Jin EJ. MicroRNA-488 suppresses cell migration through modulation of the focal adhesion activity during chondrogenic differentiation of chick limb mesenchymal cells. Cell Biol Int 2010; 35: 179-85
115. Dudek KA, Lafont JE, Martinez-Sanchez A, Murphy CL. Type II collagen expression is regulated by tissue-specific miR-675 in human articular chondrocytes. J Biol Chem 2010; 285: 24381-7
116. Tuuttila A, Morgunova E, Bergmann U, Lindqvist Y, Maskos K, Fernandez-Catalan C, Bode W, Tryggvason K, Schneider G. Three-dimensional structure of human tissue inhibitor of metalloproteinases-2 at 2.1 A resolution. J Mol Biol 1998; 284: 1133-40
117. Fernandez-Catalan C, Bode W, Huber R, Turk D, Calvete JJ, Lichte A, Tschesche H, Maskos K. Crystal structure of the complex formed by the membrane type 1-matrix metalloproteinase with the tissue inhibitor of metalloproteinases-2, the soluble progelatinase A receptor. EMBO J 1998; 17: 5238-48
118. Maunakea AK, Nagarajan RP, Bilenky M, Ballinger TJ, D'Souza C, Fouse SD, Johnson BE, Hong C, Nielsen C, Zhao Y, Turecki G, Delaney A, Varhol R, Thiessen N, Shchors K, Heine VM, Rowitch DH, Xing X, Fiore C, Schillebeeckx M, Jones SJ, Haussler D, Marra MA, Hirst M, Wang T, Costello JF. Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature 2010; 466: 253-7