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Research Paper

The fibrinolysis inhibitor α2-antiplasmin restricts lymphatic remodelling and metastasis in a mouse model of cancer

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Pages 61-75 | Received 22 Mar 2017, Accepted 28 Jun 2017, Published online: 11 Jul 2017

References

  • Achen MG, Gad JM, Stacker SA, Wilks AF. 1997. Placenta growth factor and vascular endothelial growth factor are co-expressed during early embryonic development. Growth Factors 15:69–80.
  • Achen MG, Jeltsch M, Kukk E, Makinen T, Vitali A, Wilks AF, Alitalo K, Stacker SA. 1998. Vascular endothelial growth factor D (VEGF-D) is a ligand for the tyrosine kinases VEGF receptor 2 (Flk1) and VEGF receptor 3 (Flt4). Proc Natl Acad Sci USA 95:548–553.
  • Achen MG, Mann GB, Stacker SA. 2006. Targeting lymphangiogenesis to prevent tumour metastasis. Br J Cancer 94:1355–1360.
  • Achen MG, McColl BK, Stacker SA. 2005. Focus on lymphangiogenesis in tumor metastasis. Cancer Cell 7:121–127.
  • Achen MG, Roufail S, Domagala T, Catimel B, Nice EC, Geleick DM, Murphy R, Scott AM, Caesar C, Makinen T, Alitalo K, Stacker SA. 2000. Monoclonal antibodies to vascular endothelial growth factor-D block its interactions with both VEGF receptor-2 and VEGF receptor-3. Eur J Biochem 267:2505–2515.
  • Achen MG, Stacker SA. 2012. Vascular endothelial growth factor-D: signalling mechanisms, biology and clinical relevance. Growth Factors 30:283–296.
  • Alitalo K. 2011. The lymphatic vasculature in disease. Nat Med 17:1371–1380.
  • Baldwin ME, Roufail S, Halford MM, Alitalo K, Stacker SA, Achen MG. 2001. Multiple forms of mouse vascular endothelial growth factor-D are generated by RNA splicing and proteolysis. J Biol Chem 276:44307–44314.
  • Banerji S, Ni J, Wang SX, Clasper S, Su J, Tammi R, Jones M, Jackson DG. 1999. LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. J Cell Biol 144:789–801.
  • Basak A, Khatib AM, Mohottalage D, Basak S, Kolajova M, Bag SS, Basak A. 2009. A novel enediynyl peptide inhibitor of furin that blocks processing of proPDGF-A, B and proVEGF-C. PLoS One 4:e7700.
  • Bui HM, Enis D, Robciuc MR, Nurmi HJ, Cohen J, Chen M, Yang Y, et al. 2016. Proteolytic activation defines distinct lymphangiogenic mechanisms for VEGFC and VEGFD. J Clin Invest 126:2167–2180.
  • Byzova TV, Goldman CK, Jankau J, Chen J, Cabrera G, Achen MG, Stacker SA, et al. 2002. Adenovirus encoding vascular endothelial growth factor-D induces tissue-specific vascular patterns in vivo. Blood 99:4434–4442.
  • Carpenter SL, Mathew P. 2008. Alpha2-antiplasmin and its deficiency: fibrinolysis out of balance. Haemophilia 14:1250–1254.
  • Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, Aksoy BA, Jacobsen A, et al. 2012. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov 2:401–404.
  • Dadras SS, Paul T, Bertoncini PT, Brown LF, Muzikansky A, Jackson DG, Ellwanger U, et al. 2003. Tumor lymphangiogenesis: a novel prognostic indicator for cutaneous melanoma metastasis and survival. Am J Pathol 162:1951–1960.
  • Davydova N, Harris NC, Roufail S, Paquet-Fifield S, Ishaq M, Streltsov VA, Williams SP, et al. 2016. Differential receptor binding and regulatory mechanisms for the lymphangiogenic growth factors vascular endothelial growth factor (VEGF)-C and -D. J Biol Chem 291:27265–27278.
  • Davydova N, Roufail S, Streltsov VA, Stacker SA, Achen MG. 2011. The VD1 neutralizing antibody to vascular endothelial growth factor-D: binding epitope and relationship to receptor binding. J Mol Biol 407:581–593.
  • Davydova N, Streltsov VA, Roufail S, Lovrecz GO, Stacker SA, Adams TE, Achen MG. 2012. Preparation of human vascular endothelial growth factor-D for structural and preclinical therapeutic studies. Protein Expr Purif 82:232–239.
  • Doucet A, Overall CM. 2008. Protease proteomics: revealing protease in vivo functions using systems biology approaches. Mol Aspects Med 29:339–358.
  • Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B, Sumer SO, Sun Y, et al. 2013. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal 6:pl1.
  • Harris NC, Davydova N, Roufail S, Paquet-Fifield S, Paavonen K, Karnezis T, Zhang YF, et al. 2013. The propeptides of VEGF-D determine heparin binding, receptor heterodimerization, and effects on tumor biology. J Biol Chem 288:8176–8186.
  • Harris NC, Paavonen K, Davydova N, Roufail S, Sato T, Zhang YF, Karnezis T, et al. 2011. Proteolytic processing of vascular endothelial growth factor-D is essential for its capacity to promote the growth and spread of cancer. FASEB J 25:2615–2625.
  • Hayashido Y, Hamana T, Ishida Y, Shintani T, Koizumi K, Okamoto T. 2007. Induction of alpha2-antiplasmin inhibits E-cadherin processing mediated by the plasminogen activator/plasmin system, leading to suppression of progression of oral squamous cell carcinoma via upregulation of cell-cell adhesion. Oncol Rep 17:417–423.
  • He Y, Kozaki K, Karpanen T, Koshikawa K, Yla-Herttuala S, Takahashi T, Alitalo K. 2002. Suppression of tumor lymphangiogenesis and lymph node metastasis by blocking vascular endothelial growth factor receptor 3 signaling. J Natl Cancer Inst 94:819–825.
  • He Y, Rajantie I, Pajusola K, Jeltsch M, Holopainen T, Yla-Herttuala S, Harding T, et al. 2005. Vascular endothelial cell growth factor receptor 3-mediated activation of lymphatic endothelium is crucial for tumor cell entry and spread via lymphatic vessels. Cancer Res 65:4739–4746.
  • Heckman CA, Holopainen T, Wirzenius M, Keskitalo S, Jeltsch M, Yla-Herttuala S, Wedge SR, et al. 2008. The tyrosine kinase inhibitor cediranib blocks ligand-induced vascular endothelial growth factor receptor-3 activity and lymphangiogenesis. Cancer Res 68:4754–4762.
  • Heinemann V, Ebert MP, Laubender RP, Bevan P, Mala C, Boeck S. 2013. Phase II randomised proof-of-concept study of the urokinase inhibitor upamostat (WX-671) in combination with gemcitabine compared with gemcitabine alone in patients with non-resectable, locally advanced pancreatic cancer. Br J Cancer 108:766–770.
  • Heissig B, Eiamboonsert S, Salama Y, Shimazu H, Dhahri D, Munakata S, Tashiro Y, Hattori K. 2016. Cancer therapy targeting the fibrinolytic system. Adv Drug Deliv Rev 99:172–179.
  • Hendry SA, Farnsworth RH, Solomon B, Achen MG, Stacker SA, Fox SB. 2016. The role of the tumor vasculature in the host immune response: implications for therapeutic strategies targeting the tumor microenvironment. Front Immunol 7:621.
  • Jain RK, Padera TP. 2002. Prevention and treatment of lymphatic metastasis by antilymphangiogenic therapy. J Natl Cancer Inst 94:785–787.
  • Jeltsch M, Jha SK, Tvorogov D, Anisimov A, Leppanen VM, Holopainen T, Kivela R, et al. 2014. CCBE1 enhances lymphangiogenesis via a disintegrin and metalloprotease with thrombospondin motifs-3-mediated vascular endothelial growth factor-C activation. Circulation 129:1962–1971.
  • Joukov V, Sorsa T, Kumar V, Jeltsch M, Claesson-Welsh L, Cao Y, Saksela O, Kalkkinen N, Alitalo K. 1997. Proteolytic processing regulates receptor specificity and activity of VEGF-C. EMBO J 16:3898–3911.
  • Karnezis T, Shayan R, Caesar C, Roufail S, Harris NC, Ardipradja K, Zhang YF, et al. 2012. VEGF-D promotes tumor metastasis by regulating prostaglandins produced by the collecting lymphatic endothelium. Cancer Cell 21:181–195.
  • Karpanen T, Egeblad M, Karkkainen MJ, Kubo H, Yla-Herttuala S, Jaattela M, Alitalo K. 2001. Vascular endothelial growth factor C promotes tumor lymphangiogenesis and intralymphatic tumor growth. Cancer Res 61:1786–1790.
  • Khatib AM, Lahlil R, Scamuffa N, Akimenko MA, Ernest S, Lomri A, Lalou C, et al. 2010. Zebrafish proVEGF-C expression, proteolytic processing and inhibitory effect of unprocessed proVEGF-C during fin regeneration. PLoS One 5:10.
  • Kwaan HC, McMahon B. 2009. The role of plasminogen-plasmin system in cancer. Cancer Treat Res 148:43–66.
  • Law RH, Sofian T, Kan WT, Horvath AJ, Hitchen CR, Langendorf CG, Buckle AM, et al. 2008. X-ray crystal structure of the fibrinolysis inhibitor alpha2-antiplasmin. Blood 111:2049–2052.
  • Lin J, Lalani AS, Harding TC, Gonzalez M, Wu WW, Luan B, Tu GH, et al. 2005. Inhibition of lymphogenous metastasis using adeno-associated virus-mediated gene transfer of a soluble VEGFR-3 decoy receptor. Cancer Res 65:6901–6909.
  • Longstaff C, Kolev K. 2015. Basic mechanisms and regulation of fibrinolysis. J Thromb Haemost 13 Suppl 1:S98–S105.
  • Lu BG, Sofian T, Law RH, Coughlin PB, Horvath AJ. 2011. Contribution of conserved lysine residues in the alpha2-antiplasmin C terminus to plasmin binding and inhibition. J Biol Chem 286:24544–24552.
  • Lund AW, Duraes FV, Hirosue S, Raghavan VR, Nembrini C, Thomas SN, Issa A, et al. 2012. VEGF-C promotes immune tolerance in B16 melanomas and cross-presentation of tumor antigen by lymph node lymphatics. Cell Rep 1:191–199.
  • Lund AW, Wagner M, Fankhauser M, Steinskog ES, Broggi MA, Spranger S, Gajewski TF, et al. 2016. Lymphatic vessels regulate immune microenvironments in human and murine melanoma. J Clin Invest 126:3389–3402.
  • Makinen T, Adams RH, Bailey J, Lu Q, Ziemiecki A, Alitalo K, Klein R, Wilkinson GA. 2005. PDZ interaction site in ephrinB2 is required for the remodeling of lymphatic vasculature. Genes Dev 19:397–410.
  • Makinen T, Veikkola T, Mustjoki S, Karpanen T, Catimel B, Nice EC, Wise L, et al. 2001. Isolated lymphatic endothelial cells transduce growth, survival and migratory signals via the VEGF-C/D receptor VEGFR-3. EMBO J 20:4762–4773.
  • Mandriota SJ, Jussila L, Jeltsch M, Compagni A, Baetens D, Prevo R, Banerji S, et al. 2001. Vascular endothelial growth factor-C-mediated lymphangiogenesis promotes tumour metastasis. EMBO J 20:672–682.
  • Matsumoto M, Roufail S, Inder R, Caesar C, Karnezis T, Shayan R, Farnsworth RH, et al. 2013. Signaling for lymphangiogenesis via VEGFR-3 is required for the early events of metastasis. Clin Exp Metastasis 30:819–832.
  • McColl BK, Baldwin ME, Roufail S, Freeman C, Moritz RL, Simpson RJ, Alitalo K, et al. 2003. Plasmin activates the lymphangiogenic growth factors VEGF-C and VEGF-D. J Exp Med 198:863–868.
  • McColl BK, Paavonen K, Karnezis T, Harris NC, Davydova N, Rothacker J, Nice EC, et al. 2007. Proprotein convertases promote processing of VEGF-D, a critical step for binding the angiogenic receptor VEGFR-2. FASEB J 21:1088–1098.
  • Mekkawy AH, Morris DL, Pourgholami MH. 2009. Urokinase plasminogen activator system as a potential target for cancer therapy. Future Oncol 5:1487–1499.
  • Mekkawy AH, Pourgholami MH, Morris DL. 2014. Involvement of urokinase-type plasminogen activator system in cancer: an overview. Med Res Rev 34:918–956.
  • Paavonen K, Puolakkainen P, Jussila L, Jahkola T, Alitalo K. 2000. Vascular endothelial growth factor receptor-3 in lymphangiogenesis in wound healing. Am J Pathol 156:1499–1504.
  • Paquet-Fifield S, Levy SM, Sato T, Shayan R, Karnezis T, Davydova N, Nowell CJ, et al. 2013. Vascular endothelial growth factor-d modulates caliber and function of initial lymphatics in the dermis. J Invest Dermatol 133:2074–2084.
  • Pytowski B, Goldman J, Persaud K, Wu Y, Witte L, Hicklin DJ, Skobe M, et al. 2005. Complete and specific inhibition of adult lymphatic regeneration by a novel VEGFR-3 neutralizing antibody. J Natl Cancer Inst 97:14–21.
  • Rissanen TT, Markkanen JE, Gruchala M, Heikura T, Puranen A, Kettunen MI, Kholova I, et al. 2003. VEGF-D is the strongest angiogenic and lymphangiogenic effector among VEGFs delivered into skeletal muscle via adenoviruses. Circ Res 92:1098–1106.
  • Rogers LD, Overall CM. 2013. Proteolytic post-translational modification of proteins: proteomic tools and methodology. Mol Cell Proteomics 12:3532–3542.
  • Saif MW, Knost JA, Chiorean EG, Kambhampati SR, Yu D, Pytowski B, Qin A, et al. 2016. Phase 1 study of the anti-vascular endothelial growth factor receptor 3 monoclonal antibody LY3022856/IMC-3C5 in patients with advanced and refractory solid tumors and advanced colorectal cancer. Cancer Chemother Pharmacol 78:815–824.
  • Sato T, Paquet-Fifield S, Harris NC, Roufail S, Turner DJ, Yuan Y, Zhang YF, et al. 2016. VEGF-D promotes pulmonary oedema in hyperoxic acute lung injury. J Pathol 239:152–161.
  • Schaller J, Gerber SS. 2011. The plasmin-antiplasmin system: structural and functional aspects. Cell Mol Life Sci 68:785–801.
  • Shayan R, Inder R, Karnezis T, Caesar C, Paavonen K, Ashton MW, Mann GB, et al. 2013. Tumor location and nature of lymphatic vessels are key determinants of cancer metastasis. Clin Exp Metastasis 30:345–356.
  • Shayan R, Karnezis T, Murali R, Wilmott JS, Ashton MW, Taylor GI, Thompson JF, et al. 2012. Lymphatic vessel density in primary melanomas predicts sentinel lymph node status and risk of metastasis. Histopathology 61:702–710.
  • Shimamura K, Nakatani T, Ueda A, Sugama J, Okuwa M. 2009. Relationship between lymphangiogenesis and exudates during the wound-healing process of mouse skin full-thickness wound. Wound Repair Regen 17:598–605.
  • Siegfried G, Basak A, Cromlish JA, Benjannet S, Marcinkiewicz J, Chretien M, Seidah NG, Khatib AM. 2003. The secretory proprotein convertases furin, PC5, and PC7 activate VEGF-C to induce tumorigenesis. J Clin Invest 111:1723–1732.
  • Skobe M, Hawighorst T, Jackson DG, Prevo R, Janes L, Velasco P, Riccardi L, et al. 2001. Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis. Nat Med 7:192–198.
  • Stacker SA, Baldwin ME, Achen MG. 2002. The role of tumor lymphangiogenesis in metastatic spread. FASEB J 16:922–934.
  • Stacker SA, Caesar C, Baldwin ME, Thornton GE, Williams RA, Prevo R, Jackson DG, et al. 2001. VEGF-D promotes the metastatic spread of tumor cells via the lymphatics. Nat Med 7:186–191.
  • Stacker SA, Stenvers K, Caesar C, Vitali A, Domagala T, Nice E, Roufail S, et al. 1999. Biosynthesis of vascular endothelial growth factor-D involves proteolytic processing which generates non-covalent homodimers. J Biol Chem 274:32127–32136.
  • Stacker SA, Williams RA, Achen MG. 2004. Lymphangiogenic growth factors as markers of tumor metastasis. Apmis 112:539–549.
  • Stacker SA, Williams SP, Karnezis T, Shayan R, Fox SB, Achen MG. 2014. Lymphangiogenesis and lymphatic vessel remodelling in cancer. Nat Rev Cancer 14:159–172.
  • Swartz MA. 2014. Immunomodulatory roles of lymphatic vessels in cancer progression. Cancer Immunol Res 2:701–707.
  • Swedberg JE, Harris JM. 2012. Natural and engineered plasmin inhibitors: applications and design strategies. Chembiochem 13:336–348.
  • Vercauteren E, Peeters M, Hoylaerts MF, Lijnen HR, Meijers JC, Declerck PJ, Gils A. 2012. The hyperfibrinolytic state of mice with combined thrombin-activatable fibrinolysis inhibitor (TAFI) and plasminogen activator inhibitor-1 gene deficiency is critically dependent on TAFI deficiency. J Thromb Haemost 10:2555–2562.
  • Wise LM, Ueda N, Dryden NH, Fleming SB, Caesar C, Roufail S, Achen MG, et al. 2003. Viral vascular endothelial growth factors vary extensively in amino acid sequence, receptor-binding specificities, and the ability to induce vascular permeability yet are uniformly active mitogens. J Biol Chem 278:38004–38014.