Metalloproteinases in Ovarian Cancer
Abstract
:1. Introduction
2. Tumorigenesis
2.1. Epithelial-to-Mesenchymal Transition
2.2. Proteolytic Effects on the TGF-β Signaling Pathway
3. Metastasis
3.1. Adhesion
3.2. Invasion
3.3. Angiogenesis
4. Host Factors Influencing Proteolysis
5. Conclusions
Funding
Acknowledgments
Conflicts of Interest
References
- Howlader, N.; Noone, A.M.; Krapcho, M.; Miller, D.; Brest, A.; Yu, M.; Ruhl, J.; Tatalovich, Z.; Mariotto, A.; Lewis, D.R. SEER Cancer Statistics Review, 1975–2017; National Cancer Institute: Bethesda, MD, USA, 2019. Available online: https://seer.cancer.gov/csr/1975_2017/ (accessed on 1 November 2020).
- Luo, Z.; Wang, Q.; Lau, W.B.; Lau, B.; Xu, L.; Zhao, L.; Yang, H.; Feng, M.; Xuan, Y.; Yang, Y.; et al. Tumor microenvironment: The culprit for ovarian cancer metastasis? Cancer Lett. 2016, 377, 174–182. [Google Scholar] [CrossRef]
- Barbolina, M.V.; Moss, N.M.; Westfall, S.D.; Liu, Y.; Burkhalter, R.J.; Marga, F.; Forgacs, G.; Hudson, L.G.; Stack, M.S. Microenvironmental Regulation of Ovarian Cancer Metastasis. Cancer Treat. Res. 2009, 149, 319–334. [Google Scholar] [CrossRef] [PubMed]
- Kenny, H.A.; Krausz, T.; Yamada, S.D.; Lengyel, E. Use of a novel 3D culture model to elucidate the role of mesothelial cells, fibroblasts and extra-cellular matrices on adhesion and invasion of ovarian cancer cells to the omentum. Int. J. Cancer 2007, 121, 1463–1472. [Google Scholar] [CrossRef] [PubMed]
- López-Otín, C.; Bond, J.S. Proteases: Multifunctional Enzymes in Life and Disease. J. Biol. Chem. 2008, 283, 30433–30437. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Antalis, T.M.; Bugge, T. Proteases and Cancer. In Methods and Protocols; Humana Press: New York, NY, USA, 2009; Volume 539. [Google Scholar]
- Al-Alem, L.; Curry, T.E. Ovarian cancer: Involvement of the matrix metalloproteinases. Reproduction 2015, 150, R55–R64. [Google Scholar] [CrossRef] [Green Version]
- Zhang, Y.; Chen, Q. Relationship between matrix metalloproteinases and the occurrence and development of ovarian cancer. Br. J. Med. Biol. Res. 2017, 50, e6104. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hua, H.; Li, M.; Luo, T.; Yin, Y.; Jiang, Y. Matrix metalloproteinases in tumorigenesis: An evolving paradigm. Cell. Mol. Life Sci. 2011, 68, 3853–3868. [Google Scholar] [CrossRef] [PubMed]
- Page-McCaw, A.; Ewald, A.J.; Werb, Z. Matrix metalloproteinases and the regulation of tissue remodelling. Nat. Rev. Mol. Cell Biol. 2007, 8, 221–233. [Google Scholar] [CrossRef]
- Nagase, H.; Visse, R.; Murphy, G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc. Res. 2006, 69, 562–573. [Google Scholar] [CrossRef] [Green Version]
- Nelson, A.R.; Fingleton, B.; Rothenberg, M.L.; Matrisian, L.M. Matrix Metalloproteinases: Biologic Activity and Clinical Implications. J. Clin. Oncol. 2000, 18, 1135. [Google Scholar] [CrossRef]
- Barbolina, M.V.; Adley, B.P.; Ariztia, E.V.; Liu, Y.; Stack, M.S. Microenvironmental Regulation of Membrane Type 1 Matrix Metalloproteinase Activity in Ovarian Carcinoma Cells via Collagen-induced EGR1 Expression. J. Biol. Chem. 2007, 282, 4924–4931. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lengyel, E.; Burdette, J.E.; Kenny, H.A.; Matei, D.; Pilrose, J.; Haluska, P.; Nephew, K.P.; Hales, D.B.; Stack, M.S. Epithelial ovarian cancer experimental models. Oncogene 2013, 33, 3619–3633. [Google Scholar] [CrossRef] [Green Version]
- Klymenko, Y.; Kim, O.; Loughran, E.; Yang, J.; Lombard, R.; Alber, M.; Stack, M.S. Cadherin composition and multicellular aggregate invasion in organotypic models of epithelial ovarian cancer intraperitoneal metastasis. Oncogene 2017, 36, 5840–5851. [Google Scholar] [CrossRef] [Green Version]
- Fishman, D.A.; Bafetti, L.M.; Stack, M.S. Membrane-type matrix metalloproteinase expression and matrix metalloproteinase-2 activation in primary human ovarian epithelial carcinoma cells. Invasion Metastasis 1996, 16, 150–159. [Google Scholar] [PubMed]
- Moss, N.M.; Barbolina, M.V.; Liu, Y.; Sun, L.; Munshi, H.G.; Stack, M.S. Ovarian Cancer Cell Detachment and Multicellular Aggregate Formation Are Regulated by Membrane Type 1 Matrix Metalloproteinase: A Potential Role in I.p. Metastatic Dissemination. Cancer Res. 2009, 69, 7121–7129. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ellerbroek, S.M.; Fishman, D.A.; Kearns, A.S.; Bafetti, L.M.; Stack, M.S. Ovarian carcinoma regulation of matrix metalloproteinase-2 and membrane type 1 matrix metalloproteinase through beta1 integrin. Cancer Res. 1999, 59, 1635–1641. [Google Scholar]
- Schmalfeldt, B.; Prechtel, D.; Härting, K.; Späthe, K.; Rutke, S.; Konik, E.; Fridman, R.; Berger, U.; Schmitt, M.; Kuhn, W.; et al. Increased expression of matrix metalloproteinases (MMP)-2, MMP-9, and the urokinase-type plasminogen activator is associated with progression from benign to advanced ovarian cancer. Clin. Cancer Res. 2001, 7, 2396–2404. [Google Scholar]
- Lengyel, E.; Schmalfeldt, B.; Konik, E.; Späthe, K.; Härting, K.; Fenn, A.; Berger, U.; Fridman, R.; Schmitt, M.; Prechtel, D.; et al. Expression of Latent Matrix Metalloproteinase 9 (MMP-9) Predicts Survival in Advanced Ovarian Cancer. Gynecol. Oncol. 2001, 82, 291–298. [Google Scholar] [CrossRef]
- Radisky, D.C.; Levy, D.D.; Littlepage, L.E.; Liu, H.; Nelson, C.M.; Fata, J.E.; Leake, D.; Godden, E.L.; Albertson, D.G.; Nieto, M.A.; et al. Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability. Nat. Cell Biol. 2005, 436, 123–127. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kenny, H.A.; Kaur, S.; Coussens, L.M.; Lengyel, E. The initial steps of ovarian cancer cell metastasis are mediated by MMP-2 cleavage of vitronectin and fibronectin. J. Clin. Investig. 2008, 118, 1367–1379. [Google Scholar] [CrossRef] [PubMed]
- Kenny, H.A.; Lengyel, E. MMP-2 functions as an early response protein in ovarian cancer metastasis. Cell Cycle 2009, 8, 683–688. [Google Scholar] [CrossRef] [Green Version]
- Jabłońska-Trypuć, A.; Matejczyk, M.; Rosochacki, S. Matrix metalloproteinases (MMPs), the main extracellular matrix (ECM) enzymes in collagen degradation, as a target for anticancer drugs. J. Enzym. Inhib. Med. Chem. 2016, 31, 177–183. [Google Scholar] [CrossRef] [Green Version]
- Hanahan, D.; Weinberg, R.A. The Hallmarks of Cancer. Cell 2000, 100, 57–70. [Google Scholar] [CrossRef] [Green Version]
- Deryugina, E.I.; Quigley, J.P. Tumor angiogenesis: MMP-mediated induction of intravasation- and metastasis-sustaining neovasculature. Matrix Biol. 2015, 44–46, 94–112. [Google Scholar] [CrossRef]
- Thaker, P.H.; Han, L.Y.; Kamat, A.A.; Arevalo, J.M.; Takahashi, R.; Lu, C.; Jennings, N.B.; Armaiz-Pena, G.; Bankson, J.A.; Ravoori, M.; et al. Chronic stress promotes tumor growth and angiogenesis in a mouse model of ovarian carcinoma. Nat. Med. 2006, 12, 939–944. [Google Scholar] [CrossRef]
- Wu, W.; Yamaura, T.; Murakami, K.; Ogasawara, M.; Hayashi, K.; Murata, J.; Saiki, I. Involvement of TNF-alpha in enhancement of invasion and metastasis of colon 26-L5 carcinoma cells in mice by social isolation stress. Oncol. Res. Featur. Preclin. Clin. Cancer Ther. 1999, 11, 461–469. [Google Scholar]
- Lengyel, E. Ovarian Cancer Development and Metastasis. Am. J. Pathol. 2010, 177, 1053–1064. [Google Scholar] [CrossRef]
- Singer, G.; Oldt, R.; Cohen, Y.; Wang, B.G.; Sidransky, D.; Kurman, R.J.; Shih, I.-M. Mutations in BRAF and KRAS Characterize the Development of Low-Grade Ovarian Serous Carcinoma. J. Natl. Cancer Inst. 2003, 95, 484–486. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shih, I.-M.; Kurman, R.J. Ovarian Tumorigenesis. Am. J. Pathol. 2004, 164, 1511–1518. [Google Scholar] [CrossRef]
- Alwosaibai, K.; Abedini, A.; Al-Hujaily, E.M.; Tang, Y.; Garson, K.; Collins, O.; Vanderhyden, B.C. PAX2 maintains the differentiation of mouse oviductal epithelium and inhibits the transition to a stem cell-like state. Oncotarget 2017, 8, 76881–76897. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xu, J.; Lamouille, S.; Derynck, R. TGF-β-induced epithelial to mesenchymal transition. Cell Res. 2009, 19, 156–172. [Google Scholar] [CrossRef] [PubMed]
- Larre, I.; Lazaro, A.; Contreras, R.G.; Balda, M.S.; Matter, K.; Flores-Maldonado, C.; Ponce, A.; Flores-Benitez, D.; Rincon-Heredia, R.; Padilla-Benavides, T.; et al. Ouabain modulates epithelial cell tight junction. Proc. Natl. Acad. Sci. USA 2010, 107, 11387–11392. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- McNeil, E.; Capaldo, C.T.; Macara, I.G. Zonula Occludens-1 Function in the Assembly of Tight Junctions in Madin-Darby Canine Kidney Epithelial Cells. Mol. Biol. Cell 2006, 17, 1922–1932. [Google Scholar] [CrossRef] [Green Version]
- Qian, X.; Karpova, T.; Sheppard, A.M.; McNally, J.; Lowy, D.R. E-cadherin-mediated adhesion inhibits ligand-dependent activation of diverse receptor tyrosine kinases. EMBO J. 2004, 23, 1739–1784. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Adams, C.L.; Chen, Y.-T.; Smith, S.J.; Nelson, W.J. Mechanisms of Epithelial Cell–Cell Adhesion and Cell Compaction Revealed by High-resolution Tracking of E-Cadherin– Green Fluorescent Protein. J. Cell Biol. 1998, 142, 1105–1119. [Google Scholar] [CrossRef] [PubMed]
- Rickelt, S.; Kuhn, C.; Winter-Simanowski, S.; Zimbelmann, R.; Frey, N.; Franke, W.W. Protein myozap—A late addition to the molecular ensembles of various kinds of adherens junctions. Cell Tissue Res. 2011, 346, 347–359. [Google Scholar] [CrossRef] [PubMed]
- Tisza, M.J.; Zhao, W.; Fuentes, J.S.R.; Prijic, S.; Chen, X.; Levental, I.; Chang, J.T. Motility and stem cell properties induced by the epithelial-mesenchymal transition require destabilization of lipid rafts. Oncotarget 2016, 7, 51553–51568. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kalluri, R.; Weinberg, R.A. The basics of epithelial-mesenchymal transition. J. Clin. Investig. 2009, 119, 1420–1428. [Google Scholar] [CrossRef] [Green Version]
- Lepzelter, D.; Zaman, M.H. Modeling Persistence in Mesenchymal Cell Motility Using Explicit Fibers. Langmuir 2014, 30, 5506–5509. [Google Scholar] [CrossRef]
- Moser, T.L.; Young, T.N.; Rodriguez, G.C.; Pizzo, S.V.; Bast, R.C.; Stack, M.S. Secretion of extracellular matrix-degrading proteinases is increased in epithelial ovarian carcinoma. Int. J. Cancer 1994, 56, 552–559. [Google Scholar] [CrossRef]
- Powell, W.C.; Knox, J.D.; Navre, M.; Grogan, T.M.; Kittelson, J.; Nagle, R.B.; Bowden, G.T. Expression of the metalloproteinase matrilysin in DU-145 cells increases their invasive potential in severe combined immunodeficient mice. Cancer Res. 1993, 53, 417–422. [Google Scholar] [PubMed]
- Lin, C.-Y.; Tsai, P.-H.; Kandaswami, C.C.; Lee, P.-P.; Huang, C.-J.; Hwang, J.-J.; Lee, M.-T. Matrix metalloproteinase-9 cooperates with transcription factor Snail to induce epithelial-mesenchymal transition. Cancer Sci. 2011, 102, 815–827. [Google Scholar] [CrossRef] [PubMed]
- Vallorosi, C.J.; Day, K.C.; Zhao, X.; Rashid, M.G.; Rubin, M.A.; Johnson, K.R.; Wheelock, M.J.; Day, M.L. Truncation of the β-Catenin Binding Domain of E-cadherin Precedes Epithelial Apoptosis during Prostate and Mammary Involution. J. Biol. Chem. 2000, 275, 3328–3334. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Symowicz, J.; Adley, B.P.; Gleason, K.J.; Johnson, J.J.; Ghosh, S.; Fishman, D.A.; Hudson, L.G.; Stack, M.S. Engagement of Collagen-Binding Integrins Promotes Matrix Metalloproteinase-9–Dependent E-Cadherin Ectodomain Shedding in Ovarian Carcinoma Cells. Cancer Res. 2007, 67, 2030–2039. [Google Scholar] [CrossRef] [Green Version]
- Murthy, S.; Ryan, A.J.; Carter, A.B. SP-1 regulation of MMP-9 expression requires Ser586 in the PEST domain. Biochem. J. 2012, 445, 229–236. [Google Scholar] [CrossRef] [Green Version]
- Lubbe, W.J.; Zhou, Z.Y.; Fu, W.; Zuzga, D.; Schulz, S.; Fridman, R.; Muschel, R.J.; Waldman, S.A.; Pitari, G.M. Tumor Epithelial Cell Matrix Metalloproteinase 9 Is a Target for Antimetastatic Therapy in Colorectal Cancer. Clin. Cancer Res. 2006, 12, 1876–1882. [Google Scholar] [CrossRef] [Green Version]
- Moirangthem, A.; Bondhopadhyay, B.; Mukherjee, M.; Bandyopadhyay, A.; Mukherjee, N.; Konar, K.; Bhattacharya, S.; Basu, A. Simultaneous knockdown of uPA and MMP9 can reduce breast cancer progression by increasing cell-cell adhesion and modulating EMT genes. Sci. Rep. 2016, 6, 21903. [Google Scholar] [CrossRef] [Green Version]
- Rosso, M.; Majem, B.; Devis, L.; Lapyckyj, L.; Besso, M.J.; Llauradó, M.; Abascal, M.F.; Matos, M.L.; Lanau, L.; Castellví, J.; et al. E-cadherin: A determinant molecule associated with ovarian cancer progression, dissemination and aggressiveness. PLoS ONE 2017, 12, e0184439. [Google Scholar] [CrossRef] [Green Version]
- Miyoshi, A.; Kitajima, Y.; Sumi, K.; Sato, K.; Hagiwara, A.; Koga, Y.; Miyazaki, K. Snail and SIP1 increase cancer invasion by upregulating MMP family in hepatocellular carcinoma cells. Br. J. Cancer 2004, 90, 1265–1273. [Google Scholar] [CrossRef] [Green Version]
- Rodriguez, G.C.; Haisley, C.; Hurteau, J.; Moser, T.L.; Whitaker, R.; Bast, R.C.; Stack, M.S. Regulation of Invasion of Epithelial Ovarian Cancer by Transforming Growth Factor-β. Gynecol. Oncol. 2001, 80, 245–253. [Google Scholar] [CrossRef]
- Perez-Yepez, E.A.; Ayala-Sumuano, J.-T.; Lezama, R.; Meza, I. A novel β-catenin signaling pathway activated by IL-1β leads to the onset of epithelial–mesenchymal transition in breast cancer cells. Cancer Lett. 2014, 354, 164–171. [Google Scholar] [CrossRef]
- Lochter, A.; Galosy, S.; Muschler, J.; Freedman, N.; Werb, Z.; Bissell, M.J. Matrix Metalloproteinase Stromelysin-1 Triggers a Cascade of Molecular Alterations That Leads to Stable Epithelial-to-Mesenchymal Conversion and a Premalignant Phenotype in Mammary Epithelial Cells. J. Cell Biol. 1997, 139, 1861–1872. [Google Scholar] [CrossRef] [PubMed]
- Li, W.; Li, S.; Deng, L.; Yang, S.; Li, M.; Long, S.; Chen, S.; Lin, F.; Xiao, L. Decreased MT1-MMP in gastric cancer suppressed cell migration and invasion via regulating MMPs and EMT. Tumor Biol. 2015, 36, 6883–6889. [Google Scholar] [CrossRef]
- Yang, J.; Kasberg, W.C.; Celo, A.; Liang, Z.; Quispe, K.; Stack, M.S. Post-translational modification of the membrane type 1 matrix metalloproteinase (MT1-MMP) cytoplasmic tail impacts ovarian cancer multicellular aggregate dynamics. J. Biol. Chem. 2017, 292, 13111–13121. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bruney, L.; Conley, K.C.; Moss, N.M.; Liu, Y.; Stack, M.S. Membrane-type I matrix metalloproteinase-dependent ectodomain shedding of mucin16/ CA-125 on ovarian cancer cells modulates adhesion and invasion of peritoneal mesothelium. Biol. Chem. 2014, 395, 1221–1231. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bast, R.C.; Klug, T.L.; John, E.S.; Jenison, E.; Niloff, J.M.; Lazarus, H.; Berkowitz, R.S.; Leavitt, T.; Griffiths, C.T.; Parker, L.; et al. A Radioimmunoassay Using a Monoclonal Antibody to Monitor the Course of Epithelial Ovarian Cancer. N. Engl. J. Med. 1983, 309, 883–887. [Google Scholar] [CrossRef] [PubMed]
- Rump, A.; Morikawa, Y.; Tanaka, M.; Minami, S.; Umesaki, N.; Takeuchi, M.; Miyajima, A. Binding of Ovarian Cancer Antigen CA125/MUC16 to Mesothelin Mediates Cell Adhesion. J. Biol. Chem. 2004, 279, 9190–9198. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Thériault, C.; Pinard, M.; Comamala, M.; Migneault, M.; Beaudin, J.; Matte, I.; Boivin, M.; Piché, A.; Rancourt, C. MUC16 (CA125) regulates epithelial ovarian cancer cell growth, tumorigenesis and metastasis. Gynecol. Oncol. 2011, 121, 434–443. [Google Scholar] [CrossRef]
- Jiao, Y.; Feng, X.; Zhan, Y.; Wang, R.; Zheng, S.; Liu, W.; Zeng, X. Matrix metalloproteinase-2 Promotes αvβ3 Integrin-Mediated Adhesion and Migration of Human Melanoma Cells by Cleaving Fibronectin. PLoS ONE 2012, 7, e41591. [Google Scholar] [CrossRef] [PubMed]
- Ellerbroek, S.M.; Wu, Y.I.; Overall, C.M.; Stack, M.S. Functional Interplay between Type I Collagen and Cell Surface Matrix Metalloproteinase Activity. J. Biol. Chem. 2001, 276, 24833–24842. [Google Scholar] [CrossRef] [Green Version]
- Mitra, A.K. Ovarian Cancer Metastasis: A Unique Mechanism of Dissemination. In Tumor Metastasis; Xu, K., Ed.; InTech: London, UK, 2016. [Google Scholar]
- Mitra, A.; Chiang, C.; Tiwari, P.; Tomar, S.L.; Watters, K.M.; Peter, M.E.; Lengyel, E. Microenvironment-induced downregulation of miR-193b drives ovarian cancer metastasis. Oncogene 2015, 34, 5923–5932. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tang, C.-H.; Hill, M.L.; Brumwell, A.N.; Chapman, H.A.; Wei, Y. Signaling through urokinase and urokinase receptor in lung cancer cells requires interactions with beta1 integrins. J. Cell Sci. 2008, 121, 3747–3756. [Google Scholar] [CrossRef] [Green Version]
- Li, X.-F.; Yan, P.-J.; Shao, Z.-M. Downregulation of miR-193b contributes to enhance urokinase-type plasminogen activator (uPA) expression and tumor progression and invasion in human breast cancer. Oncogene 2009, 28, 3937–3948. [Google Scholar] [CrossRef] [Green Version]
- Wang, L.; Madigan, M.C.; Chen, H.; Liu, F.; Patterson, K.I.; Beretov, J.; O’Brien, P.M.; Li, Y. Expression of urokinase plasminogen activator and its receptor in advanced epithelial ovarian cancer patients. Gynecol. Oncol. 2009, 114, 265–272. [Google Scholar] [CrossRef]
- Duffy, M.J. The Urokinase Plasminogen Activator System: Role in Malignancy. Curr. Pharm. Des. 2004, 10, 39–49. [Google Scholar] [CrossRef] [PubMed]
- Ko, S.Y.; Naora, H. Adaptation of ovarian cancer cells to the peritoneal environment: Multiple mechanisms of the developmental patterning gene HOXA9. Cancer Cell Microenviron. 2014, 1, e379. [Google Scholar]
- Ko, S.Y.; Barengo, N.; Ladanyi, A.; Lee, J.-S.; Marini, F.; Lengyel, E.; Naora, H. HOXA9 promotes ovarian cancer growth by stimulating cancer-associated fibroblasts. J. Clin. Investig. 2012, 122, 3603–3617. [Google Scholar] [CrossRef] [Green Version]
- Kaimal, R.; Aljumaily, R.; Tressel, S.L.; Pradhan, R.V.; Covic, L.; Kuliopulos, A.; Zarwan, C.; Kim, Y.B.; Sharifi, S.; Agarwal, A. Selective Blockade of Matrix Metalloprotease-14 with a Monoclonal Antibody Abrogates Invasion, Angiogenesis, and Tumor Growth in Ovarian Cancer. Cancer Res. 2013, 73, 2457–2467. [Google Scholar] [CrossRef] [Green Version]
- Young, T.N.; Rodriguez, G.C.; Rinehart, A.R.; Bast, J.R.C.; Pizzo, S.V.; Stack, M. Characterization of Gelatinases Linked to Extracellular Matrix Invasion in Ovarian Adenocarcinoma: Purification of Matrix Metalloproteinase 2. Gynecol. Oncol. 1996, 62, 89–99. [Google Scholar] [CrossRef] [PubMed]
- Fishman, D.A.; Bafetti, L.M.; Banionis, S.; Kearns, A.S.; Chilukuri, K.; Stack, M.S. Production of extracellular matrix-degrading proteinases by primary cultures of human epithelial ovarian carcinoma cells. Cancer 1997, 80, 1457–1463. [Google Scholar] [CrossRef]
- Moss, N.M.; Wu, Y.I.; Liu, Y.; Munshi, H.; Stack, M.S. Modulation of the Membrane Type 1 Matrix Metalloproteinase Cytoplasmic Tail Enhances Tumor Cell Invasion and Proliferation in Three-dimensional Collagen Matrices. J. Biol. Chem. 2009, 284, 19791–19799. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Burger, R.A.; Brady, M.F.; Bookman, M.A.; Fleming, G.F.; Monk, B.J.; Huang, H.; Mannel, R.S.; Homesley, H.D.; Fowler, J.; Greer, B.E.; et al. Incorporation of Bevacizumab in the Primary Treatment of Ovarian Cancer. N. Engl. J. Med. 2011, 365, 2473–2483. [Google Scholar] [CrossRef] [Green Version]
- Monk, B.J.; Minion, L.E.; Coleman, R.L. Anti-angiogenic agents in ovarian cancer: Past, present, and future. Ann. Oncol. 2016, 27, i33–i39. [Google Scholar] [CrossRef]
- Geva, E.; Jaffe, R.B. Role of vascular endothelial growth factor in ovarian physiology and pathology. Fertil. Steril. 2000, 74, 429–438. [Google Scholar] [CrossRef]
- Nishida, N.; Yano, H.; Komai, K.; Nishida, T.; Kamura, T.; Kojiro, M. Vascular endothelial growth factor C and vascular endothelial growth factor receptor 2 are related closely to the prognosis of patients with ovarian carcinoma. Cancer 2004, 101, 1364–1374. [Google Scholar] [CrossRef]
- Duyndam, M.C.A.; Hilhorst, M.C.G.W.; Schlüper, H.M.M.; Verheul, H.M.W.; Van Diest, P.J.; Kraal, G.; Pinedo, H.M.; Boven, E. Vascular Endothelial Growth Factor-165 Overexpression Stimulates Angiogenesis and Induces Cyst Formation and Macrophage Infiltration in Human Ovarian Cancer Xenografts. Am. J. Pathol. 2002, 160, 537–548. [Google Scholar] [CrossRef] [Green Version]
- Ke, L.D.; Shi, Y.-X.; Yung, W.K.A. VEGF(121), VEGF(165) overexpression enhances tumorigenicity in U251 MG but not in NG-1 glioma cells. Cancer Res. 2002, 62, 1854–1861. [Google Scholar]
- Zhang, L.; Yang, N.; Park, J.-W.; Katsaros, D.; Fracchioli, S.; Cao, G.; O’Brien-Jenkins, A.; Randall, T.C.; Rubin, S.C.; Coukos, G. Tumor-derived vascular endothelial growth factor up-regulates angiopoietin-2 in host endothelium and destabilizes host vasculature, supporting angiogenesis in ovarian cancer. Cancer Res. 2003, 63, 3403–3412. [Google Scholar] [PubMed]
- Villegas, G.; Lange-Sperandio, B.; Tufro, A. Autocrine and paracrine functions of vascular endothelial growth factor (VEGF) in renal tubular epithelial cells. Kidney Int. 2005, 67, 449–457. [Google Scholar] [CrossRef] [Green Version]
- Fang, J.; Shing, Y.; Wiederschain, D.; Yan, L.; Butterfield, C.; Jackson, G.; Harper, J.; Tamvakopoulos, G.; Moses, M.A. Matrix metalloproteinase-2 is required for the switch to the angiogenic phenotype in a tumor model. Proc. Natl. Acad. Sci. USA 2000, 97, 3884–3889. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- 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, 1048–1051. [Google Scholar]
- Gálvez, B.G.; Matías-Román, S.; Albar, J.P.; Sánchez-Madrid, F.; Arroyo, A.G. Membrane Type 1-Matrix Metalloproteinase Is Activated during Migration of Human Endothelial Cells and Modulates Endothelial Motility and Matrix Remodeling. J. Biol. Chem. 2001, 276, 37491–37500. [Google Scholar] [CrossRef] [Green Version]
- Vu, T.H.; Shipley, J.; Bergers, G.; Berger, J.E.; Helms, J.A.; Hanahan, D.; Shapiro, S.D.; Senior, R.M.; Werb, Z. MMP-9/Gelatinase B is a Key Regulator of Growth Plate Angiogenesis and Apoptosis of Hypertrophic Chondrocytes. Cell 1998, 93, 411–422. [Google Scholar] [CrossRef] [Green Version]
- Zhou, Z.; Apte, S.S.; Soininen, R.; Cao, R.; Baaklini, G.Y.; Rauser, R.W.; Wang, J.; Cao, Y.; Tryggvason, K. Impaired endochondral ossification and angiogenesis in mice deficient in membrane-type matrix metalloproteinase I. Proc. Natl. Acad. Sci. USA 2000, 97, 4052–4057. [Google Scholar] [CrossRef] [Green Version]
- Huang, S.; Van Arsdall, M.; Tedjarati, S.; Mccarty, M.; Wu, W.; Langley, R.; Fidler, I.J. Contributions of Stromal Metalloproteinase-9 to Angiogenesis and Growth of Human Ovarian Carcinoma in Mice. J. Natl. Cancer Inst. 2002, 94, 1134–1142. [Google Scholar] [CrossRef] [PubMed]
- Deryugina, E.I.; Soroceanu, L.; Strongin, A.Y. Up-regulation of vascular endothelial growth factor by membrane-type 1 matrix metalloproteinase stimulates human glioma xenograft growth and angiogenesis. Cancer Res. 2002, 62, 580–588. [Google Scholar] [PubMed]
- Sounni, N.E.; Devy, L.; Hajitou, A.; Frankenne, F.; Munaut, C.; Gilles, C.; Deroanne, C.; Thompson, E.W.; Foidart, J.M.; Noel, A. MT1-MMP expression promotes tumor growth and angiogenesis through an up-regulation of vascular endothelial growth factor expression. FASEB J. 2002, 16, 555–564. [Google Scholar] [CrossRef]
- Sounni, N.E.; Roghi, C.; Chabottaux, V.; Janssen, M.; Munaut, C.; Maquoi, E.; Galvez, B.G.; Gilles, C.; Frankenne, F.; Murphy, G.; et al. Up-regulation of Vascular Endothelial Growth Factor-A by Active Membrane-type 1 Matrix Metalloproteinase through Activation of Src-Tyrosine Kinases. J. Biol. Chem. 2004, 279, 13564–13574. [Google Scholar] [CrossRef] [Green Version]
- Bergers, G.; Brekken, R.A.; McMahon, G.; Vu, T.H.; Itoh, T.; Tamaki, K.; Tanzawa, K.; Thorpe, P.E.; Itohara, S.; Werb, Z.; et al. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat. Cell Biol. 2000, 2, 737–744. [Google Scholar] [CrossRef]
- Belotti, D.; Calcagno, C.; Garofalo, A.; Caronia, D.; Riccardi, E.; Giavazzi, R.; Taraboletti, G. Vascular Endothelial Growth Factor Stimulates Organ-Specific Host Matrix Metalloproteinase-9 Expression and Ovarian Cancer Invasion. Mol. Cancer Res. 2008, 6, 525–534. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ugarte-Berzal, E.; Redondo-Muñoz, J.; Eroles, P.; Del Cerro, M.H.; García-Marco, J.A.; Terol, M.J.; García-Pardo, A. VEGF/VEGFR2 interaction down-regulates matrix metalloproteinase–9 via STAT1 activation and inhibits B chronic lymphocytic leukemia cell migration. Blood 2010, 115, 846–849. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chetty, C.; Lakka, S.S.; Bhoopathi, P.; Rao, J.S. MMP-2 alters VEGF expression via αVβ3 integrin-mediated PI3K/AKT signaling in A549 lung cancer cells. Int. J. Cancer 2009, 127, 1081–1095. [Google Scholar] [CrossRef] [Green Version]
- Xu, J.; Rodriguez, D.; Petitclerc, E.; Kim, J.J.; Hangai, M.; Yuen, S.M.; Davis, G.E.; Brooks, P.C. Proteolytic exposure of a cryptic site within collagen type IV is required for angiogenesis and tumor growth in vivo. J. Cell Biol. 2001, 154, 1069–1080. [Google Scholar] [CrossRef] [PubMed]
- Keyt, B.A.; Berleau, L.T.; Nguyen, H.V.; Chen, H.; Heinsohn, H.; Vandlen, R.; Ferrara, N. The Carboxyl-terminal Domain(111–165) of Vascular Endothelial Growth Factor Is Critical for Its Mitogenic Potency. J. Biol. Chem. 1996, 271, 7788–7795. [Google Scholar] [CrossRef] [Green Version]
- Lutgendorf, S.K.; Cole, S.; Costanzo, E.; Bradley, S.; Coffin, J.; Jabbari, S.; Rainwater, K.; Ritchie, J.M.; Yang, M.; Sood, A.K. Stress-related mediators stimulate vascular endothelial growth factor secretion by two ovarian cancer cell lines. Clin. Cancer Res. 2003, 9, 4514–4521. [Google Scholar] [PubMed]
- Sood, A.K.; Bhatty, R.; Kamat, A.A.; Landen, C.N.; Han, L.; Thaker, P.H.; Li, Y.; Gershenson, D.M.; Lutgendorf, S.; Cole, S.W. Stress Hormone–Mediated Invasion of Ovarian Cancer Cells. Clin. Cancer Res. 2006, 12, 369–375. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lutgendorf, S.K.; DeGeest, K.; Dahmoush, L.; Farley, D.; Penedo, F.; Bender, D.; Goodheart, M.; Buekers, T.E.; Mendez, L.; Krueger, G. Social isolation is associated with elevated tumor norepinephrine in ovarian carcinoma patients. Brain Behav. Immun. 2011, 25, 250–255. [Google Scholar] [CrossRef] [Green Version]
- Lutgendorf, S.K.; Johnsen, E.L.; Cooper, B.; Anderson, B.; Sorosky, J.I.; Buller, R.E.; Sood, A.K. Vascular endothelial growth factor and social support in patients with ovarian carcinoma. Cancer 2002, 95, 808–815. [Google Scholar] [CrossRef]
- Yang, E.V.; Sood, A.K.; Chen, M.; Li, Y.; Eubank, T.D.; Marsh, C.B.; Jewell, S.; Flavahan, N.A.; Morrison, C.; Yeh, P.-E.; et al. Norepinephrine Up-regulates the Expression of Vascular Endothelial Growth Factor, Matrix Metalloproteinase (MMP)-2, and MMP-9 in Nasopharyngeal Carcinoma Tumor Cells. Cancer Res. 2006, 66, 10357–10364. [Google Scholar] [CrossRef] [Green Version]
- Yang, E.V.; Bane, C.M.; Maccallum, R.C.; Kiecolt-Glaser, J.K.; Malarkey, W.B.; Glaser, R. Stress-related modulation of matrix metalloproteinase expression. J. Neuroimmunol. 2002, 133, 144–150. [Google Scholar] [CrossRef]
- Drell, T.L., IV; Joseph, J.; Lang, K.; Niggemann, B.; Zaenker, K.S.; Entschladen, F. Effects of Neurotransmitters on the Chemokinesis and Chemotaxis of MDA-MB-468 Human Breast Carcinoma Cells. Breast Cancer Res. Treat. 2003, 80, 63–70. [Google Scholar] [CrossRef] [PubMed]
- Masur, K.; Niggemann, B.; Zanker, K.S.; Entschladen, F. Norepinephrine-induced migration of SW 480 colon carcinoma cells is inhibited by beta-blockers. Cancer Res. 2001, 61, 2866–2869. [Google Scholar] [PubMed]
- Nankova, B.; Kvetnansky, R.; Hiremagalur, B.; Sabban, B.; Rusnak, M.; Sabban, E.L. Immobilization stress elevates gene expression for catecholamine biosynthetic enzymes and some neuropeptides in rat sympathetic ganglia: Effects of adrenocorticotropin and glucocorticoids. Endocrinology 1996, 137, 5597–5604. [Google Scholar] [CrossRef]
- Paredes, A.; Galvez, A.; Leyton, V.; Aravena, G.; Fiedler, J.L.; Bustamante, D.; Lara, H.E. Stress Promotes Development of Ovarian Cysts in Rats: The Possible Role of Sympathetic Nerve Activation. Endocrine 1998, 8, 309–316. [Google Scholar] [CrossRef]
- Lara, H.E.; Porcile, A.; Espinoza, J.; Romero, C.; Luza, S.M.; Fuhrer, J.; Miranda, C.; Roblero, L. Release of Norepinephrine from Human Ovary: Coupling to Steroidogenic Response. Endocrine 2001, 15, 187–192. [Google Scholar] [CrossRef]
- Mayerhofer, A.; Smith, G.D.; Danilchik, M.V.; Levine, J.E.; Wolf, D.P.; Dissen, G.A.; Ojeda, S.R. Oocytes are a source of catecholamines in the primate ovary: Evidence for a cell-cell regulatory loop. Proc. Natl. Acad. Sci. USA 1998, 95, 10990–10995. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lutgendorf, S.K.; Lamkin, D.M.; Jennings, N.B.; Arevalo, J.M.G.; Penedo, F.; DeGeest, K.; Langley, R.R.; Lucci, J.A.; Cole, S.W.; Lubaroff, D.M.; et al. Biobehavioral Influences on Matrix Metalloproteinase Expression in Ovarian Carcinoma. Clin. Cancer Res. 2008, 14, 6839–6846. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pollard, J.W. Tumour-educated macrophages promote tumour progression and metastasis. Nat. Rev. Cancer 2004, 4, 71–78. [Google Scholar] [CrossRef]
- Loughran, E.A.; Leonard, A.K.; Hilliard, T.S.; Phan, R.C.; Yemc, M.G.; Harper, E.; Sheedy, E.; Klymenko, Y.; Asem, M.; Liu, Y.; et al. Aging Increases Susceptibility to Ovarian Cancer Metastasis in Murine Allograft Models and Alters Immune Composition of Peritoneal Adipose Tissue. Neoplasia 2018, 20, 621–631. [Google Scholar] [CrossRef]
- Harper, E.I.; Sheedy, E.F.; Stack, M.S. With Great Age Comes Great Metastatic Ability: Ovarian Cancer and the Appeal of the Aging Peritoneal Microenvironment. Cancers 2018, 10, 230. [Google Scholar] [CrossRef] [Green Version]
- Vaughan-Thomas, A.; Gilbert, S.J.; Duance, V.C. Elevated levels of proteolytic enzymes in the aging human vitreous. Investig. Ophthalmol. Vis. Sci. 2000, 41, 3299–3304. [Google Scholar]
- Quigley, J.P.; Gold, L.I.; Schwimmer, R.; Sullivan, L.M. Limited cleavage of cellular fibronectin by plasminogen activator purified from transformed cells. Proc. Natl. Acad. Sci. USA 1987, 84, 2776–2780. [Google Scholar] [CrossRef] [Green Version]
- Deryugina, E.I.; Quigley, J.P. Cell Surface Remodeling by Plasmin: A New Function for an Old Enzyme. J. Biomed. Biotechnol. 2012, 2012, 1–21. [Google Scholar] [CrossRef] [Green Version]
- Parrinello, S.; Coppe, J.-P.; Krtolica, A.; Campisi, J. Stromal-epithelial interactions in aging and cancer: Senescent fibroblasts alter epithelial cell differentiation. J. Cell Sci. 2005, 118, 485–496. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fisher, G.J.; Wang, Z.; Datta, S.C.; Varani, J.; Kang, S.; Voorhees, J.J. Pathophysiology of Premature Skin Aging Induced by Ultraviolet Light. N. Engl. J. Med. 1997, 337, 1419–1429. [Google Scholar] [CrossRef] [PubMed]
- Brenneisen, P.; Sies, H.; Scharffetter-Kochanek, K. Ultraviolet-B Irradiation and Matrix Metalloproteinases. Ann. N. Y. Acad. Sci. 2002, 973, 31–43. [Google Scholar] [CrossRef]
- Quan, T.; Qin, Z.; Xia, W.; Shao, Y.; Voorhees, J.J.; Fisher, G.J. Matrix-Degrading Metalloproteinases in Photoaging. J. Investig. Dermatol. Symp. Proc. 2009, 14, 20–24. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Baramova, E.; Bajou, K.; Remacle, A.; L’Hoir, C.; Krell, H.; Weidle, U.; Noel, A.; Foidart, J. Involvement of PA/plasmin system in the processing of pro-MMP-9 and in the second step of pro-MMP-2 activation. FEBS Lett. 1997, 405, 157–162. [Google Scholar] [CrossRef] [Green Version]
- Sodek, K.L.; Ringuette, M.J.; Brown, T.J. MT1-MMP is the critical determinant of matrix degradation and invasion by ovarian cancer cells. Br. J. Cancer 2007, 97, 358–367. [Google Scholar] [CrossRef] [Green Version]
- Seandel, M.; Noack-Kunnmann, K.; Zhu, D.; Aimes, R.T.; Quigley, J.P. Growth factor–induced angiogenesis in vivo requires specific cleavage of fibrillar type I collagen. Blood 2001, 97, 2323–2332. [Google Scholar] [CrossRef] [Green Version]
- Mahner, S.; Woelber, L.; Eulenburg, C.; Schwarz, J.; Carney, W.; Jaenicke, F.; Milde-Langosch, K.; Mueller, V. TIMP-1 and VEGF-165 serum concentration during first-line therapy of ovarian cancer patients. BMC Cancer 2010, 10, 139. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Santamaria, S.; De Groot, R. Monoclonal antibodies against metzincin targets. Br. J. Pharmacol. 2019, 176, 52–66. [Google Scholar] [CrossRef]
- Devy, L.; Huang, L.; Naa, L.; Yanamandra, N.; Pieters, H.; Frans, N.; Chang, E.; Tao, Q.; Vanhove, M.; Lejeune, A.; et al. Selective Inhibition of Matrix Metalloproteinase-14 Blocks Tumor Growth, Invasion, and Angiogenesis. Cancer Res. 2009, 69, 1517–1526. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ager, E.I.; Kozin, S.V.; Kirkpatrick, N.D.; Seano, G.; Kodack, D.P.; Askoxylakis, V.; Huang, Y.; Goel, S.; Snuderl, M.; Muzikansky, A.; et al. Blockade of MMP14 Activity in Murine Breast Carcinomas: Implications for Macrophages, Vessels, and Radiotherapy. J. Natl. Cancer Inst. 2015, 107. [Google Scholar] [CrossRef] [PubMed]
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Carey, P.; Low, E.; Harper, E.; Stack, M.S. Metalloproteinases in Ovarian Cancer. Int. J. Mol. Sci. 2021, 22, 3403. https://doi.org/10.3390/ijms22073403
Carey P, Low E, Harper E, Stack MS. Metalloproteinases in Ovarian Cancer. International Journal of Molecular Sciences. 2021; 22(7):3403. https://doi.org/10.3390/ijms22073403
Chicago/Turabian StyleCarey, Preston, Ethan Low, Elizabeth Harper, and M. Sharon Stack. 2021. "Metalloproteinases in Ovarian Cancer" International Journal of Molecular Sciences 22, no. 7: 3403. https://doi.org/10.3390/ijms22073403