Metalloproteinases involvement in liver tumoral pathology- an update

Elena-Roxana Avădănei, Simona-Eliza Giușcă, Irina-Draga Căruntu, Cornelia Amălinei

Abstract


MMPs and TIMPs involvement in tissue destruction may be incriminated in malignant invasion and metastasis, showing correlations between the overexpression, aggressiveness, tumor stage and prognosis. Recent data provide evidence of their complex role in creating an auspicious microenvironment for tumor growth in primary and metastatic sites. The investigation of MMPs and TIMPs functional interdependency is an important direction, useful in carcinogenesis intrinsic mechanisms deciphering, its apparently paradoxical role being incompletely defined. Literature review regarding MMPs and TIMPs study in primary and secondary hepatic tumors allows us to affirm that defining a precise profile of their activities is extremely difficult. The most studied metalloproteinase, in liver tumoral microenvironment, were MMP2 and MMP9 together with their inhibitors TIMP 2 and TIMP1, respectively. The expression variability of both MMPs and TIMPs is associated to promoter or inhibitor action of stromal cells and / or tumor cells, as liver microenvironment has a modulatory action for MMPs and TIMPs. MMPs capacity to intervene in many biological processes is attributed to their ability of ECM proteolysis, as a possible initiator of unrevealed functions. The understanding of biochemical and structural aspects of MMPs, and the capacity to form molecular complexes with TIMPs open the perspectives of design of potent specific inhibitors for MMPs and, thus, the development of new therapies for primary and metastatic liver cancers.

Keywords


matrix metalloproteinases (MMPs), tissue inhibitors of metalloproteinases (TIMPs), HCC, liver metastasis, carcinogenesis

Full Text:

PDF

References


Mbeunkui F, Johann DJ. Cancer and the tumor microenvironment: a review of an essential relationship. Cancer Chemother Pharmacol 2009; 63:571-582.

Hanahan D, Coussens LM. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell 2012; 21:309–322.

Witz IP, Levy-Nissenbaum O. The tumor microenvironment in the post-PAGET era. Cancer Lett 2006; 242:1-10.

Leonardi GC, Candido S, Cervello M, et al. The tumor microenvironment in hepatocellular carcinoma. Int J Oncol 2012; 40:1733–1747.

Hernandez–Gea V, Toffanin S, Friedman SL, Llovet JM. Role of the microenvironment in the pathogenesis and treatment of hepatocellular carcinoma. Gastroenterology 2013; 144:512–527.

Yang JD, Nakamura I, Roberts LR. The tumor microenvironment in hepatocellular carcinoma: current status and therapeutic targets. Semin Cancer Biol 2011; 21(1):35–43.

Roskams T, Kojiro M. Pathology of early hepatocellular carcinoma: conventional and molecular diagnosis. Semin Liver Dis 2010; 30:17–25.

El-Serag HB. Epidemiology of hepatocellular carcinoma in USA. Hepatol Res 2007; 37:88-94.

Jemal A, Siegel R, Ward E, et al. Cancer statistics, 2009. CA Cancer J Clin 2009; 59:225-249.

Dooley S, Weng H, Mertens PR. Hypotheses on the role of transforming growth factor-β in the onset and progression of hepatocellular carcinoma. Dig Dis 2009; 27:93-101.

Hoshida Y, Toffanin S, Lachenmayer A, et al. Molecular classification and novel targets in hepatocellular carcinoma: recent advancements. Semin Liver Dis 2010; 30:35–51.

Whittaker S, Marais R, Zhu AX. The role of signaling pathways in the development and treatment of hepatocellular carcinoma. Oncogene 2010; 29:4989–5005.

Lee JS, Thorgeirsson SS. Comparative and integrative functional genomics of HCC. Oncogene 2006; 25:3801–3809.

Mohla S, Witz IP. The 5th International Conference on Tumor Microenvironment: Progression, Therapy and Prevention Versailles, France, October 20-24, 2009: conference summary. Cancer Microenviron 2010; 3:1-5.

Sternlicht MD, Werb Z. How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 2001; 17:463–516.

Bruner-Tran K, Eisenberg E, Yeaman GR, et al. Steroid and Cytokine Regulation of Matrix Metalloproteinase Expression in Endometriosis and the Establishment of Experimental Endometriosis in Nude Mice. J Clin Endocrinol Metab 2002; 87(10):4782-4791.

Chung HW, Lee JY, Moon HS, et al. Matrix metalloproteinase-2, membranous type 1 matrix metalloproteinase,and tissue inhibitor of metalloproteinase-2 expression in ectopic and eutopic endometrium. Fertil Steril 2002; 78:787–795.

Visse R, Nagase H. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function and biochemistry. Circ Res 2003; 92:827-839.

Gross J, Lapiere C. Collagenolytic activity in amphibian tissues: a tissue culture assay. Proc Natl Acad Sci USA 1962; 48(6):1014–1022.

Ii M, Yamamoto H, Adachi Y, et al. Role of MMP-7 (Matrilysin) in human cancer invasion, apoptosis, growth, and angiogenesis. Exp Biol Med 2005; 231:20-27.

Brummer O, Bohmer G, Hollwitz B, et al. MMP-1 and MMP-2 in the cervix uteri in different steps of malignant transformation-an immunohistochemical study. Gynecol Oncol 2002; 84(2):222-227.

Curry TE, Osteen KG. The matrix metalloproteinase system: changes, regulation, and impact throughout the ovarian and uterine reproductive cycle. Endocrine Reviews 2003; 24:428-465.

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; 48:411-424.

Hashizume K. Analysis of utero-placental-specific molecules and their functions during implantation and placentation in the bovine. J Reprod Dev 2007; 53(1):1-11.

Kessenbrock K, Plaks V, Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 2010; 141:52–67.

Osteen KG, Igarashi TM, Bruner-Tran KL. Progesterone action in the human endometrium: induction of a unique tissue environment which limits matrix metalloproteinase (MMP) expression. Front Biosci 2003; 8:78-86.

Overall CM. Molecular determinants of metalloproteinase substrate specificity: matrix metalloproteinase substrate binding domains, modules, and exosites. Mol Biotechnol 2002; 22:51-86.

Yadav SS, Mandal RK, Singh MK, Usman K, Khattri S. Genetic variants of matrix metalloproteinase (MMP2) gene influence metabolic syndrome susceptibility. Genet Test Mol Biomarkers 2014; 18(2):88-92.

Edwards DR, Handsley MM, Pennington CJ. The ADAM metalloproteinases. Mol Aspects Med 2008; 29:258–289.

Brew K, Dinakarpandian D, Nagase H. Tissue inhibitors of metalloproteinases: evolution, structure and function. Biochim Biophys Acta 2000; 1477(1–2):267–283.

Murphy G. Tissue inhibitors of metalloproteinases. Genome Biol 2011; 12(11):233-241.

Baker A, Edwards D, Murphy G. Metalloproteinase inhibitors: biological actions and therapeutic opportunities. J Cell Sci 2002; 115:3719–3727.

Edwards DR, Beaudry PP, Laing TD, et al. The roles of tissue inhibitors of metalloproteinases in tissue remodelling and cell growth. Int J Obes Relat Metab Disord 1996; 20(3):9–15.

Arpino V, Brock M, Gill SE. The role of TIMPs in regulation of extracellular matrix proteolysis. In: Matrix Biology, Parks wc, Apte S. (eds.), Philadelphia: Elsevier B.V., 2015; 44–46:247–254.

McLennan SV, Wang XY, Moreno V, Yue DK, Twigg SM. Connective tissue growth factor mediates high glucose effects on matrix degradation through tissue inhibitor of matrix metalloproteinase type 1: implications for diabetic nephropathy. Endocrinology 2004; 145:5646–5655.

Lieu S, Hansen E, Dedini R, et al. Impaired remodeling phase of fracture repair in the absence of matrix metalloproteinase-2. Dis Model Mech 2011; 4:203–211.

Aoki M, Miyake K, Ogawa R, et al. siRNA knockdown of tissue inhibitor of metalloproteinase-1 in keloid fibroblasts leads to degradation of collagen type I. J Invest Dermatol 2014; 134:818–826.

Yang J, Zheng J, Wu L, et al. NDRG2 ameliorates hepatic fibrosis by inhibiting the TGF-β1/Smad pathway and altering the MMP2/TIMP2 ratio in rats. PLoS One 2011; 6:e27710. http://dx.doi.org/10.1371/journal. pone.0027710.

Sokolović A, Rodriguez-Ortigosa CM, Ten Bloemendaal L, Oude Elferink RPJ, Prieto J, Bosma PJ. Insulin-like growth factor 1 enhances bile-duct proliferation and fibrosis in Abcb4(−/−) mice. Biochim Biophys Acta 2013; 1832:697–704.

Pushpakumar S, Kundu S, Pryor T, et al. Angiotensin-II induced hypertension and renovascular remodelling in tissue inhibitor of metalloproteinase 2 knockout mice. J Hypertens 2013; 31:2270–2281.

Ratajczak-Wielgomas K, Gosk J, Rabczyński J, et al. Expression of MMP- 2, TIMP-2, TGF-β1, and decorin in Dupuytren's contracture. Connect Tissue Res 2012; 53:469–477.

Georgescu SP, Aronovitz MJ, Iovanna JL, Patten RD, Kyriakis JM, Goruppi S. Decreased metalloprotease 9 induction, cardiac fibrosis, and higher autophagy after pressure overload in mice lacking the transcriptional regulator p8. Am J Physiol Cell Physiol 2011; 301:1046–56.

Black RA. TIMP3 checks inflammation. Nat Genet 2004; 36:934–935.

Watanabe-Takano H, Takano K, et al. DA-Raf-dependent inhibition of the Ras-ERK signaling pathway in type 2 alveolar epithelial cells controls alveolar formation. Proc Natl Acad Sci U S A 2014; 111:E2291–300.

Shynlova O, Bortolini MAT, Alarab M. Genes responsible for vaginal extracellular matrix metabolism are modulated by women's reproductive cycle and menopause. Int Braz J Urol 2013; 39:257–267.

Fountoulakis N, Labiris G, Aristeidou A, et al. Tissue inhibitor of metalloproteinase 4 in aqueous humor of patients with primary open angle glaucoma, pseudoexfoliation syndrome and pseudoexfoliative glaucoma and its role in proteolysis imbalance. BMC Ophthalmol 2013;13:69. http://dx.doi.org/10.1186/1471-2415-13-69.

Kyle DJT, Harvey AG, Shih B, Tan KT, Chaudhry IH, Bayat A. Identification of molecular phenotypic descriptors of breast capsular contracture formation using informatics analysis of the whole genome transcriptome. Wound Repair Regen 2013; 21:762–769.

Zeng ZS, Shu WP, Cohen AM, Guillem JG. Matrix metalloproteinase-7 expression in colorectal cancer liver metastases: evidence for involvement of MMP-7 activation in human cancer metastases. Clin Cancer Res 2002; 8(1):144–148.

Qi JH, Ebrahem Q, Moore N, 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; 9:407–415.

Collette T, Bellehumeur C, Kats R, 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; 19(6):1257–1264.

Butler GS, Overall CM. Updated biological roles for matrix metalloproteinases and new “intracellular” substrates revealed by degradomics. Biochemistry 2009; 48(46):10830–10845.

Klein T, Bischoff R. Physiology and pathophysiology of matrix metalloproteases. Amino Acids 2011; 41(2):271–290.

Poswar FO, Fraga CA, Farias LC, et al. Immunohistochemical analysis of TIMP-3 and MMP-9 in actinic keratosis, squamous cell carcinoma of the skin, and basal cell carcinoma. Pathol Res Pract 2013; 209(11):705-709.

Zucker S, Vacirca J. Role of matrix metalloproteinases (MMPs) in colorectal cancer. Cancer Metastasis Rev 2004; 23(1–2):101–117.

Basset P, Bellocq JP, Wolf C, et al. A novel metalloproteinase gene specifically expressed in stromal cells of breast carcinomas. Nature 1990; 348(6303):699–704.

Hashimoto K, Kihira Y, Matuo Y, Usui T. Expression of matrix metalloproteinase-7 and tissue inhibitor of metalloproteinase-1 in human prostate. J Urol 1998; 160(5):1872–1876.

Oikonomidi S, Kostikas K, Tsilioni I, Tanou K, Gourgoulianis KI, Kiropoulos TS. Matrix metalloproteinases in respiratory diseases: from pathogenesis to potential clinical implications. Curr Med Chem 2009; 16:1214–1228.

Groblewska M, Siewko M, Mroczko B, Szmitkowski M. The role of matrix metalloproteinases (MMPs) and their inhibitors (TIMPs) in the development of esophageal cancer. Folia Histochem Cytobiol 2012; 50:12-19.

Zhang M, Zhu GY, Gao HY, Zhao SP, Xue Y. Expression of tissue levels of matrix metalloproteinases and tissue inhibitorsof metalloproteinases in gastric adenocarcinoma. J Surg Oncol 2011; 103(3):243–247.

Zhang QW, Liu L, Chen R, et al. Matrix metalloproteinase-9 as a prognostic factor in gastric cancer: a meta-analysis. Asian Pac J Cancer Prev 2012; 13(6):2903–2908.

Ueno H, Yamashita K, Azumano I, Inoue M, Okada Y. Enhanced production and activation of matrix metaslloproteinase-7 (matrilysin) in human endometrial carcinomas. Int J Cancer 1999; 84:470-477.

Sakata K, Shigemasa K, Nagai N, Ohama K. Expression of matrix metalloproteinases (MMP-2, MMP-9, MT1-MMP) and their inhibitors (TIMP-1, TIMP-2) in common epithelial tumors of the ovary. Int J Oncol 2000; 17(4):673–681.

Saito K, Takeha S, Shiba K, et al. Clinicopathologic significance of urokinase receptorand MMP-9-positive stromal cells in human colorectal cancer: functional multiplicity of matrix degradation on hematogenous metastasis. Int J Cancer 2000; 86(1):24–29.

Poulsom R, Pignatelli M, Stetler-Stevenson WG, et al. Stromal expression of 72 Kda type IV collagenase (MMP-2) and TIMP-2 mRNAs in colorectal neoplasia. Am J Pathol 1992; 141(2):389–396.

Frich L, Bjørnland K, Pettersen S, Clausen OP, Gladhaug IP. Increased activity of matrix metalloproteinase 2 and 9 after hepatic radiofrequency ablation. J Surg Res 2006; 135:297–304.

Johansson N, Ala-Aho R, Uitto V, et al. Expression of collagenase-3 (MMP-13) and collagenase-1 (MMP-1) by transformed keratinocytes is dependent on the activity of p38 mitogen-activated protein kinase. J Cell Sci 2000; 113(2):227-235.

Liu D, Guo H, Li Y, Xu X, Yang K, Bai Y. Association between polymorphisms in the promoter regions of matrix metalloproteinases (MMPs) and risk of cancer metastasis: a meta-analysis. PLoS ONE 2012; 7:e31251.

O'byrne EM, Parker DT, Roberts ED, et al. Oral administration of a matrix metalloproteinase inhibitor, CGS 27023A, protects the cartilage proteoglycan matrix in a partial meniscectomy model of osteoarthritis in rabbits. Inflam Res 1995; 44:117-118.

Cawston TE. Metalloproteinase inhibitors and the prevention of tissue breakdown. Pharm Ther 1996; 70:163-182.

Saarialho-Kere UK, Vaalamo M, Karjalainen-Lindsberg ML, Airola K, Parks WC, Puolakkainen P. Enhanced expression of matrilysin, collagenase, and stromelysin-1 in gastrointestinal ulcers. Am J Pathol 1996; 148:519-526.

Rosenberg GA. Matrix metalloproteinases in brain injury. J Neurotrauma 1995; 12:833-842.

Chandler S, Coates R, Gearing A, Lury J, Wells G, Bone E. Matrix metalloproteinases degrade myelin basic protein. Neurosci Lett 1995; 201:223-226.

Woessner JF. The Matrix Metalloproteinase Family. In: Parks WC, Mecham RP. (eds.), Matrix metalloproteinases. San Diego, California: Academic Press; 1998:1-14.

Thompson RW, Parks WC. Role of matrix metalloproteinases in abdominalaortic aneurysms. Ann N Y Acad Sci 1996; 800:157-174.

Strauss BH, Robinson R, Batchelor WB. In vivo collagen turnover following experimental balloon angioplasty injury and the role of matrix. Circulation Research 1996; 79:541-550.

Nelson AR, Fingleton B, Rothenberg ML, Matrisian LM. Matrix metalloproteinases: biologic activity and clinical implications. J Clin Oncol 2000; 18(5):1135-1149.

Noe V, Fingleton B, Jacobs K, et al. Release of an invasion promoter E-cadherin fragment by matrilysin and stromelysin-1. J Cell Sci 2001; 114:111-118.

Lynch CC, Hikosaka A, Acuff HB. MMP-7 promotes prostate cancer-induced osteolysis via the solubilization of RANKL. Cancer Cell 2005; 7(5):485-496.

Shiomi T, Okada Y. MT1-MMP and MMP-7 in invasion and metastasis of human cancers. Cancer and Metastasis Rev 2003; 22:145-152.

Mannello F, Gazzanelli G. Tissue inhibitors of metalloproteinases and programmed cell death: conundrums, controversies and potential implications. Apoptosis 2001; 6:479–482.

Gersch I, Catchpole HR. The organization of ground substance and basement membrane and its significance in tissue injury, disease and growth. Am J Anat 1949; 85:457-507.

Deryugina EI, Quigley JP. Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev 2006; 25(1):9-34.

Heppner KJ, Matrisian LM, Jensen RA, Rodgers WH. Expression of most matrix metalloproteinase family members in breast cancer respresents a tumor-induced host response. Am J Pathol 1996; 149:273-282.

Okada N, Ishida H, Murata N, Hashimoto D, Seyama Y, Kubota S. Matrix metalloproteinase-2 and -9 in bile as a marker of liver metastasis in colorectal cancer. Biochem Biophys Res Commun 2001; 288(1):212-216.

Ray JM, Stetler-Stevenson WG. Gelatinase A activity directly modulates melanoma cell adhesion and spreading. EMBO J 1995; 14:908-917.

Giannelli G, Falk-Marzillier J, Schiraldi O, Stetler-Stevenson WG, Quaranta V. Induction of cell migration by matrix metalloproteinase-2 cleavage of laminin-5. Science 1997; 277:225-228.

Laurie GW, Leblond CP, Martin GR. Localization of type IV collagen, laminin, heparan sulfate proteoglycan, and fibronectin to the basal lamina of basement membranes. J Cell Biol 1982; 95:340-344.

Burgeson, RE, Chiquet M, Deutzmann R, et al. A new nomenclature for the laminins. Matrix Biol 1994; 14:209-211.

Stefansson S, Lawrence DA. The serpin PAI-1 inhibits cell migration by blocking integrin alpha V beta 3 binding to vitronectin. Nature 1996; 383:441-443.

Nagase H, Visse R, Murphy G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovascular Research 2006; 69:562-573.

Gress TM, Muller-Pillasch F, Lerch MM, Friess H, Buchler M, Adler G. Expression and in-situ localization of genes coding for extracellular matrix proteins and extracellular matrix degrading proteases in pancreatic cancer. Int J Cancer 1995; 2:407-413.

Pei D. Leukolysin/MMP25/MT6-MMP: a novel matrix metalloproteinase specifically expressed in the leukocyte lineage. Cell Res 1999; 9(4):291-303.

Zeng ZS, Huang Y, Cohen AM, Guillem JG. Prediction of colorectalcancer relapse and survival via tissue RNA levels of matrix metalloproteinase-9. J Clin Oncol 1996; 14:3133-3140.

Zeng Z, Cohen AM, Zhang Z, Stetler-Stevenson WG, Guillem JG. Elevated tissue inhibitor of metalloproteinase 1 RNA in colorectal cancer stroma correlates with lymph node and distant metastases. Clin Cancer Res 1995; 1:899-906.

Sier CFM, Kubben FJGM, Ganesh S, et al. Tissue levels of matrix metalloproteinases MMP-2 and MMP-9 are related to the overall survival of patients with gastric carcinoma. Br J Cancer 1996; 74:413-417.

Chenard MP, O'siorain L, Shering S, et al. High levels of stromelysin-3 correlate with poor prognosis in patients with breast carcinoma. Int J Cancer 1996; 69:448-451.

Fong KM, Kida Y, Zimmerman PV, Smith PJ. TIMP1 and adverse prognosis in non-small cell lung cancer. Clin Cancer Res 1996; 2:1369-1372.

Grignon DJ, Sakr W, Toth M. High levels of tissue inhibitor ofmetalloproteinase-2 (TIMP-2) expression are associated with poor outcome in invasive bladder cancer. Cancer Res 1996; 56:1654-1659.

Murray GI, Duncan ME, O'neil P, Melvin WT, Fothergill JE. Matrix metalloproteinase-1 is associated with poor prognosis in colorectal cancer. Nature Med 1996; 2:461-462.

Gallegos NC, Smales C, Savage FG, Hembry RM, Boulos PB. The distribution of matrix metalloproteinases and tissue inhibitor of metalloproteinases in colorectal cancer. Surgical Oncol 1995; 4:21-29.

Brooks PC, Stromblad S, Sanders LC. Localization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin alpha v beta 3. Cell 1996; 85:683-693.

Macdougall JR, Matrisian LM. Contributions of tumor and stromal matrix metalloproteinases to tumor progression, invasion and metastasis. Cancer Metast Rev 1995; 14:351-362.

Houghton AM, Grisolano JL, Baumann ML. Macrophage elastase (matrix metalloproteinase-12) suppresses growth of lung metastases. Cancer Res 2006; 66(12):6149-6155.

Shapiro SD, Kobayashi DK, Ley TJ. Cloning and characterization of a unique elastolytic metalloproteinase produced by human alveolar macrophages. J Biol Chem 1993; 268:23824-23829.

Heppner KJ, Matrisian LM, Jensen RA, Rodgers WH. Expression of most matrix metalloproteinase family members in breast cancer respresents a tumor-induced host response. Am J Pathol 1996; 149:273-282.

Strongin AY, Collier I, Bannikov G, Marmer BL, Grant GA, Goldberg GI. Mechanism of cell surface activation of 72-kDa type IV collagenase. Isolation of the activated form of the membrane metalloprotease. J Biol Chem 1995; 270:5331-5338.

Gohji K, Fujimoto N, Fujii A, Komiyama T, Okawa J, Nakajima M. Prognostic significance of circulating matrix metalloproteinase-2 to tissue inhibitor of metalloproteinase-2 ratio in recurrence ofurothelial cancer after complete resection. Cancer Res 1996; 56:3196-3198.

Onisto M, Riccio MP, Scannapieco P, et al. Gelatinase A/TIMP-2 imbalance in lymphnode- positive breast carcinomas, as measured by RT-PCR. Int J Cancer 1995; 3:621-626.

Egeblad M, Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat Rev Canc 2002; 2(3):161-174.

Hojilla CV, Mohammed FF, Khokha R. Matrix metalloproteinases and their tissue inhibitors direct cell fate during cancer development. Br J Canc 2003; 10:1817-1821.

Rundhaug JE. Matrix metalloproteinases and angiogenesis. J Cell Mol Med 2005; 9(2):267-285.

Yu Q, Stamenkovic I. Cell surface-localized Matrix Metalloproteinase-9 proteolytically activates TGF- and promotes tumor invasion and angiogenesis. Genes & Development 2000; 14:163–176.

Huo N, Ichikawa Y, Kamiyama M, et al. MMP-7 (matrilysin) accelerated growth of human umbilical vein endothelial cells. Cancer Lett 2002; 177(1):95-100.

Pozzi A, Levine WF, Gradner HA. Low plasma levels of MMP9 permit increased tumor angiogenesis. Oncogene 2002; 21:272-281.

Thorns V, Walter GF, Thorns C. Expression of MMP-2, MMP-7, MMP-9, MMP-10 and MMP-11 in human astrocytic and oligodendroglial gliomas. Anticancer Res 2003; 23(5A):3937-3944.

Lee MH, Murphy G. Matrix metalloproteinases at a glance. J Cell Science 2004; 117:4015-4016.

Cornelius LA, Nehring LC, Harding E, et al. Matrix metalloproteinases generate angiostatin: effects on neovascularization. J Immunol 1998; 161(12):6845-6852.

Ferreras M, Felbor U, Lenhard T, Olsen BR, Delaissé JM. Generation and degradation of human endostatin proteins by various proteinases. FEBS Letters 2000; 486:247-251.

Heljasvaara R, Nyberg P, Luostarinen J, et al. Generation of biologically active endostatin fragments from human collagen XVIII by distinct matrix metalloproteases. Exp Cell Res 2005; 307(2):292-304.

Chang JH, Javier JA, Chang GY, Oliveira HB, Azar DT. Functional characterization of neostatins, the MMP-derived, enzymatic cleavage products of type XVIII collagen. FEBS Lett 2005; 579(17):3601-3606.

Hamano Y, Zeisberg M, Sugimoto H. Physiological levels of tumstatin, a fragment of collagen IV alpha3 chain, are generated by MMP-9 proteolysis and suppress angiogenesis via alphaV beta3 integrin. Cancer Cell 2003; 3:589-601.

Sounni NE, Dehne K, van Kempen LLCL, et al. Stromal regulation of vessel stability by MMP9 and TGFβ. Dis Model Mech 2010; 3(5-6):317-332

Bruyere F, Melen-Lamalle L, Blacher S, et al. Modeling lymphangiogenesis in a three-dimensional culture system. Nat Methods 2008; 5:431–437.

Langenskiold M, Holmdahl L, Falk P, Ivarsson ML. Increased plasma MMP-2 protein expression in lymph node-positive patients with colorectal cancer. Int J Colorectal Dis 2005; 20:245–252.

Islekel H, Oktay G, Terzi C, Canda AE, Fuzun M, Kupelioglu A. Matrix metalloproteinase-9,-3 and tissue inhibitor of matrix metalloproteinase-1 in colorectal cancer: relationship to clinicopathological variables. Cell Biochem Funct 2007; 25:433–441.

Nakamura ES, Koizumi K, Kobayashi M, Saiki I. Inhibition of lymphangiogenesis-related properties of murine lymphatic endothelial cells and lymph node metastasis of lung cancer by the matrix metalloproteinase inhibitor MMI270. Cancer Sci 2004; 95:25–31.

Vargo-Gogola T, Fingleton B, Crawford HC, Matrisian LM. Matrilysin (matrix metalloproteinase-7) selects for apoptosis-resistant mammary cells in vivo. Cancer Res 2002; 62(19):5559-5563.

Mitsiades N, Yu WH, Poulaki V, Tsokos M, Stamenkovic I. Matrix metalloproteinase-7-mediated cleavage of Fas ligand protects tumor cells from chemotherapeutic drug cytotoxicity. Cancer Res 2001; 61(2):577-5781.

Liu H, Zhang T, Li 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; 99:2185–2192.

Andarawewa KL, Boulay A, Masson R, et al. Dual stromelysin-3 function during natural mouse mammary tumor virus-ras tumor progression. Cancer Res 2003; 63:5844-5849.

Waas ET, Wobbes T, Lomme RM, et al Matrix metalloproteinase 2 and 9 activity in patients with colorectal cancer liver metastasis. Br J Surg 2003; 90(12):1556–1564.

Illemann M, Bird N, Majeed A, et al. MMP-9 is differentially expressed in primary human colorectal adenocarcinomas and their metastases. Mol Cancer Res 2006; 4(5):293–302.

Parsons SL, Watson SA, Collins HM, et al. Gelatinase (MMP-2 and -9) expression in gastrointestinal malignancy. Br J Cancer 1998; 78(11):1495–1502.

Ring P, Johansson K, Höyhtyä 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):805–811.

Joo YE, Seo KS, Kim J, et al. Role of tissue inhibitors of metalloproteinases (TIMPs) in colorectal carcinoma. J Korean Med Sci 1999; 14(4):417–442.

Lyall MS, Dundas SR, Curran S, Murray GI. Profiling markers of prognosis in colorectal cancer. Clin Cancer Res 2006; 12(4):1184–1191.

Nielsen BS, Timshel S, Kjeldsen L, et al. 92 kDa type IV collagenase (MMP-9) is expressed in neutrophils and macrophages but not in malignant epithelilal cells in human colon cancer. Int J Cancer 1999; 365:57–62.

Howell R, Roche W, Rees M, Blaydes J, Primrose J. TIMP-1 expression in colorectal cancer liver metastases is associated with poor outcome. Proc Am Soc Clin Oncol 2002; 21:1758.

Barozzi C, Ravaioli M, D’Errico A, et al. Relevance of biological markers in colorectal carcinoma. A comparative study of a broad panel. Cancer 2002; 94:647–657.

Illemann M, Eefsen RH, Bird NC, et al. Tissue inhibitor of matrix metalloproteinase-1 expression in colorectal cancer liver metastases is associated with vascular structures. Mol Carcinog 2015; 1-16. Doi:10.1002/mc.22269.

Giuşcă SE, Căruntu ID, Amălinei C, Avădănei ER. Prognostic significance of MMP-9 and TIMP-1 in liver metastases. Rom J Morphol Embryol 2015, 56(2):357–364.

Roderfeld M, Weiskirchen R, Wagner S, et al. Inhibition of hepatic fibrogenesis by matrix metalloproteinase-9 mutants in mice. Faseb J 2006; 20:444–454.

Cheng JC, Chou CH, Kuo ML, Hsieh CY. Radiation-enhanced hepatocellular carcinoma cellinvasion with MMP-9 expression through PI3K/Akt/NF-kappaB signal transduction pathway. Oncogene 2006; 25:7009–7018.

Chen JS, Wang Q, Fu XH, et al. Involvement of PI3K/PTEN/AKT/mTOR pathway in invasion and metastasis in hepatocellular carcinoma: Association with MMP-9. Hepatol Res 2009; 39:177–86.

Littlepage LE, Sternlicht MD, Rougier N, et al. Matrix metalloproteinases contribute distinct roles in neuroendocrine prostate carcinogenesis, metastasis, and angiogenesis progression. Cancer Res 2010; 70: 2224–2234.

Kohga K, Tatsumi T, Takehara T, et al. Expression of CD133 confers malignant potential by regulating metalloproteinases in human hepatocellular carcinoma. J Hepatol 2010; 52:872–879.

Parks WC, Wilson CL, Lopez-Boado YS. Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat Rev Immunol 2004; 4:617–629.

Lin WW, Karim M. A cytokine-mediated link between innate immunity, inflammation, and cancer. J Clin Invest 2007; 117:1175–1183.

Manicone AM, McGuire JK. Matrix metalloproteinases as modulators of inflammation, Semin Cel Dev Biol 2008; 19:34–41.

Arii S, Mise M, Harada T, et al. Overexpression of matrix metalloproteinase 9 gene in hepatocellular carcinoma with invasive potential. Hepatology 1996; 24:316–322.

Takafuji V, Forgues M, Unsworth E, Goldsmith P, Wang XW. An osteopontin fragment is essential for tumor cell invasion in hepatocellular carcinoma. Oncogene 2007, 26:6361–6371.

Yu FL, Liu HJ, Lee JW, et al. Hepatitis B virus X protein promotes cell migration by inducing matrix metalloproteinase-3. J Hepatol 2005; 42:520–527.

Ou DP, Tao YM, Tang FQ, Yang LY. The hepatitis B virus X protein promotes hepatocellular carcinoma metastasis by upregulation of matrix metalloproteinases. Int J Cancer 2007; 120:1208–1214.

Woo HG, Park ES, Cheon JH, et al. Gene expression-based recurrence prediction of hepatitis B virus-related human hepatocellular carcinoma. Clin Cancer Res 2008; 14:2056–2064.

Zhao XL, Sun T, Che N, et al. Promotion of hepatocellular carcinoma metastasis through matrix metalloproteinase activation by epithelial-mesenchymal transition regulator twist1. J Cell Mol Med 2011; 15(3):691-700.

Taras D, Blanc JF, Rullier A, Dugot-Senant N, et al. Pravastatin reduces lung metastasis of rat hepatocellular carcinoma via a coordinated decrease of MMP expression and activity. J Hepatol 2007; 46:69–76.

Zhang H, Wang YS, Han G, Shi Y. TIMP-3 gene transfection suppresses invasive and metastatic capacity of human hepatocarcinoma cell line HCC-7721. Hepatobiliary Pancreat Dis Int 2007; 6:487–491.

Kim JR, Kim CH. Association of a high activity of matrix metalloproteinase-9 to low levels of tissue inhibitors of metalloproteinase-1 and -3 in human hepatitis B-viral hepatoma cells. Int J Biochem Cell Biol 2004; 36:2293–306.

Xia D, Yan LN, Xie JG, et al. Overexpression of TIMP-1 mediated by recombinant adenovirus in hepatocellular carcinoma cells inhibits proliferation and invasion in vitro. Hepatobiliary Pancreat Dis Int 2006; 5:409–415.

Kinoshita T, Sato H, Okada A, et al. TIMP-2 promotes activation of progelatinase A by membrane-type 1 matrix metalloproteinase immobilized on agarose beads. J Biol Chem 1998; 273:16098–16103

Gorden DL, Fingleton B, Crawford HC, et al. Resident stromal cell-derived MMP-9 promotes the growth of colorectal metastases in the liver microenvironment. Int J Cancer 2007; 121(3):495–500.

Nart D, Yaman B, Yilmaz F, et al. Expression of matrix metalloproteinase-9 in predicting prognosis of hepatocellular carcinoma after liver transplantation. Liver Transp 2010; 16(5):621-630.

Giannelli G, Fransvea E, Bergamini C, et al. Laminin-5 chains are expressed differentially in metastatic and nonmetastatic hepatocellular carcinoma. Clin Cancer Res 2003; 9:3684–3691.

Ng KT, Qi X, Kong KL, et al. Overexpression of matrix metalloproteinase-12 (MMP-12) correlates with poor prognosis of hepatocellular carcinoma. Eur J Cancer 2011; 47(15):2299-2305.

Thieringer FR, Maass T, Anthon B, et al. Liver-specific overexpression of matrix metalloproteinase 9 (MMP-9) in transgenic mice accelerates development of hepatocellular carcinoma. Mol Carcinog 2012; 51(6):439-448.

Lempinen M, Lyytinen I, Nordin A. Prognostic value of serum MMP-8, -9 and TIMP-1 in patients with hepatocellular carcinoma. Ann Med 2013; 45(7):482-487.

Ogawa M, Ikeuchi K, Watanabe M, et al. Expression of matrix metalloproteinase 7, laminin and type IV collagen-associated liver metastasis in human colorectal cancer: immunohistochemical approach, Hepato-gastroenterol 2005; 52(63):875–880.

Sutnar A, Pesta M, Liska V, et al. Clinical relevance of the expression of mRNA of MMP-7, MMP-9, TIMP-1, TIMP-2 and CEA tissue samples from colorectal liver metastases. Tumour Biol 2007; 28(5):247–252.

Oshima T, Kunisaki C, Yoshihara K, et al. Clinicopathological significance of the gene expression of matrix metalloproteinases and reversioninducing cysteine-rich protein with Kazal motifs in patients with colorectal cancer: MMP-2 gene expression is a useful predictor of liver metastasis from colorectal cancer. Oncol Rep 2008; 19(5):1285–1291.

Kim YW, Ko YT, Kim NK, et al. A comparative study of protein expression in primary colorectal cancer and synchronous hepatic metastases: the significance of matrix metalloproteinase-1 expression as a predictor of liver metastasis. Scand J Gastroenterol 2010; 45(2):217–225.

Yamada T, Oshima T, Yoshihara K, et al. Overexpression of MMP-13 gene in colorectal cancer with liver metastasis. Anticancer Res 2010; 30(7):2693–2699.




DOI: http://dx.doi.org/10.22551/2015.07.0203.10050

Copyright (c) 2015 Archive of Clinical Cases

Creative Commons License
Archive of Clinical Cases is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

 

ISSN: 2360-6975