Generic placeholder image

Current Pharmaceutical Design

Editor-in-Chief

ISSN (Print): 1381-6128
ISSN (Online): 1873-4286

Review Article

Heparanase Inhibitors in Cancer Progression: Recent Advances

Author(s): Rajwinder Kaur*, Pran Kishore Deb, Vishal Diwan and Balraj Saini*

Volume 27 , Issue 1 , 2021

Published on: 13 November, 2020

Page: [43 - 68] Pages: 26

DOI: 10.2174/1381612826666201113105250

Price: $65

Abstract

Background: An endo-β-glucuronidase enzyme, Heparanase (HPSE), degrades the side chains of polymeric heparan sulfate (HS), a glycosaminoglycan formed by alternate repetitive units of D-glucosamine and D-glucuronic acid/L-iduronic acid. HS is a major component of the extracellular matrix and basement membranes and has been implicated in processes of the tissue’s integrity and functional state. The degradation of HS by HPSE enzyme leads to conditions like inflammation, angiogenesis, and metastasis. An elevated HPSE expression with a poor prognosis and its multiple roles in tumor growth and metastasis has attracted significant interest for its inhibition as a potential anti-neoplastic target.

Methods: We reviewed the literature from journal publication websites and electronic databases such as Bentham, Science Direct, PubMed, Scopus, USFDA, etc., about HPSE, its structure, functions, and role in cancer.

Results: The present review is focused on Heparanase inhibitors (HPIns) that have been isolated from natural resources or chemically synthesized as new therapeutics for metastatic tumors and chronic inflammatory diseases in recent years. The recent developments made in the HPSE structure and function are also discussed, which can lead to the future design of HPIns with more potency and specificity for the target.

Conclusion: HPIns can be a better target to be explored against various cancers.

Keywords: Heparanase inhibitors, Suramin, PI-88, SST0001, M402, PG545, AS1411.

[1]
Avendano C, Menendez JC. Introduction Medicinal Chemistry of Anticancer Drugs. Elsevier 2015.
[2]
Cheng B, Gao F, Maissy E, Xu P. Repurposing suramin for the treatment of breast cancer lung metastasis with glycol chitosan-based nanoparticles. Acta Biomater 2019; 84: 378-90.
[http://dx.doi.org/10.1016/j.actbio.2018.12.010] [PMID: 30528604]
[3]
Quesada AR, Medina MA, Muñoz-Chápuli R, Ponce ÁL. Do not say ever never more: the ins and outs of antiangiogenic therapies. Curr Pharm Des 2010; 16(35): 3932-57.
[http://dx.doi.org/10.2174/138161210794454950] [PMID: 21158731]
[4]
Kim AW, Xu X, Hollinger EF, Gattuso P, Godellas CV, Prinz RA. Human heparanase-1 gene expression in pancreatic adenocarcinoma. J Gastrointest Surg 2002; 6(2): 167-72.
[http://dx.doi.org/10.1016/S1091-255X(01)00087-7] [PMID: 11992801]
[5]
Bandari SK, Purushothaman A, Ramani VC, et al. Chemotherapy induces secretion of exosomes loaded with heparanase that degrades extracellular matrix and impacts tumor and host cell behavior. Matrix Biol 2018; 65: 104-18.
[http://dx.doi.org/10.1016/j.matbio.2017.09.001] [PMID: 28888912]
[6]
Davidson B, Shafat I, Risberg B, et al. Heparanase expression correlates with poor survival in metastatic ovarian carcinoma. Gynecol Oncol 2007; 104(2): 311-9.
[http://dx.doi.org/10.1016/j.ygyno.2006.08.045] [PMID: 17030350]
[7]
Vlodavsky I, Singh P, Boyango I, et al. Heparanase: From basic research to therapeutic applications in cancer and inflammation. Drug Resist Updat 2016; 29: 54-75.
[http://dx.doi.org/10.1016/j.drup.2016.10.001] [PMID: 27912844]
[8]
Mohan CD, Hari S, Preetham HD, et al. Targeting heparanase in cancer: inhibition by synthetic, chemically modified, and natural compounds. iScience 2019; 15: 360-90.
[http://dx.doi.org/10.1016/j.isci.2019.04.034] [PMID: 31103854]
[9]
Coombe DR, Gandhi NS. Heparanase: A challenging cancer drug target. Front Oncol 2019; 9: 1316.
[http://dx.doi.org/10.3389/fonc.2019.01316] [PMID: 31850210]
[10]
El-Nadi M, Hassan H, Saleh ME, et al. Induction of heparanase via IL-10 correlates with a high infiltration of CD163+ M2-type tumor-associated macrophages in inflammatory breast carcinomas. Matrix Biol Plus 2020; p. 100030.
[11]
Masola V, Bellin G, Gambaro G, Onisto M. Heparanase: A multitasking protein involved in extracellular matrix (ECM) remodeling and intracellular events. Cells 2018; 7(12): 236.
[http://dx.doi.org/10.3390/cells7120236] [PMID: 30487472]
[12]
Kusindarta DL, Wihadmadyatami H. The role of extracellular matrix in tissue regeneration. Tissue Regeneration 2018; p. 65.
[http://dx.doi.org/10.5772/intechopen.75728]
[13]
Wu L, Viola CM, Brzozowski AM, Davies GJ. Structural characterization of human heparanase reveals insights into substrate recognition. Nat Struct Mol Biol 2015; 22(12): 1016-22.
[http://dx.doi.org/10.1038/nsmb.3136] [PMID: 26575439]
[14]
Ding J. Heparanase inhibitors Encyclopedia of Cancer ed M Schwab:. Springer Berlin Heidelberg 2016; pp. 1-7.
[15]
Vlodavsky I, Fuks Z, Ishai-Michaeli R, et al. Extracellular matrix-resident basic fibroblast growth factor: implication for the control of angiogenesis. J Cell Biochem 1991; 45(2): 167-76.
[http://dx.doi.org/10.1002/jcb.240450208] [PMID: 1711529]
[16]
Ashikari-Hada S, Habuchi H, Kariya Y, Itoh N, Reddi AH, Kimata K. Characterization of growth factor-binding structures in heparin/heparan sulfate using an octasaccharide library. J Biol Chem 2004; 279(13): 12346-54.
[http://dx.doi.org/10.1074/jbc.M313523200] [PMID: 14707131]
[17]
Robinson CJ, Mulloy B, Gallagher JT, Stringer SE. VEGF165-binding sites within heparan sulfate encompass two highly sulfated domains and can be liberated by K5 lyase. J Biol Chem 2006; 281(3): 1731-40.
[http://dx.doi.org/10.1074/jbc.M510760200] [PMID: 16258170]
[18]
Eccles SA. Heparanase: breaking down barriers in tumors. Nat Med 1999; 5(7): 735-6.
[http://dx.doi.org/10.1038/10455] [PMID: 10395313]
[19]
Overall CM, López-Otín C. Strategies for MMP inhibition in cancer: innovations for the post-trial era. Nat Rev Cancer 2002; 2(9): 657-72.
[http://dx.doi.org/10.1038/nrc884] [PMID: 12209155]
[20]
Li JP. Heparin, heparan sulfate and heparanase in cancer: remedy for metastasis? Anticancer Agents Med Chem 2008; 8(1): 64-76.
[http://dx.doi.org/10.2174/187152008783330824] [PMID: 18220506]
[21]
Vlodavsky I, Friedmann Y. Molecular properties and involvement of heparanase in cancer metastasis and angiogenesis. J Clin Invest 2001; 108(3): 341-7.
[http://dx.doi.org/10.1172/JCI13662] [PMID: 11489924]
[22]
Bohlmann L, Tredwell GD, Yu X, et al. Functional and structural characterization of a heparanase. Nat Chem Biol 2015; 11(12): 955-7.
[http://dx.doi.org/10.1038/nchembio.1956] [PMID: 26565989]
[23]
Rivara S, Milazzo FM, Giannini G. Heparanase: a rainbow pharmacological target associated to multiple pathologies including rare diseases. Future Med Chem 2016; 8(6): 647-80.
[http://dx.doi.org/10.4155/fmc-2016-0012] [PMID: 27057774]
[24]
Avendano C, Menendez JC. Other nonbiological approaches to targeted cancer chemotherapy. eds Avendaño, C Menéndez,. (Second E.). JCBT- Medicinal chemistry of anticancer drugs 2015; 493-560.
[25]
Sanderson RD, Yang Y. Syndecan-1: a dynamic regulator of the myeloma microenvironment. Clin Exp Metastasis 2008; 25(2): 149-59.
[http://dx.doi.org/10.1007/s10585-007-9125-3] [PMID: 18027090]
[26]
Richardson TP, Trinkaus-Randall V, Nugent MA. Regulation of heparan sulfate proteoglycan nuclear localization by fibronectin. J Cell Sci 2001; 114(Pt 9): 1613-23.
[PMID: 11309193]
[27]
Fux L, Ilan N, Sanderson RD, Vlodavsky I. Heparanase: busy at the cell surface. Trends Biochem Sci 2009; 34(10): 511-9.
[http://dx.doi.org/10.1016/j.tibs.2009.06.005] [PMID: 19733083]
[28]
Ilan N, Elkin M, Vlodavsky I. Regulation, function and clinical significance of heparanase in cancer metastasis and angiogenesis. Int J Biochem Cell Biol 2006; 38(12): 2018-39.
[http://dx.doi.org/10.1016/j.biocel.2006.06.004] [PMID: 16901744]
[29]
Reiland J, Kempf D, Roy M, Denkins Y, Marchetti D. FGF2 binding, signaling, and angiogenesis are modulated by heparanase in metastatic melanoma cells. Neoplasia 2006; 8(7): 596-606.
[http://dx.doi.org/10.1593/neo.06244] [PMID: 16867222]
[30]
Reiland J, Sanderson RD, Waguespack M, et al. Heparanase degrades syndecan-1 and perlecan heparan sulfate: functional implications for tumor cell invasion. J Biol Chem 2004; 279(9): 8047-55.
[http://dx.doi.org/10.1074/jbc.M304872200] [PMID: 14630925]
[31]
Cassinelli G, Zaffaroni N, Lanzi C. The heparanase/heparan sulfate proteoglycan axis: A potential new therapeutic target in sarcomas. Cancer Lett 2016; 382(2): 245-54.
[http://dx.doi.org/10.1016/j.canlet.2016.09.004] [PMID: 27666777]
[32]
Parish CR, Freeman C, Hulett MD. Heparanase: a key enzyme involved in cell invasion. Biochim Biophys Acta 2001; 1471(3): M99-M108.
[PMID: 11250066]
[33]
Vlodavsky I, Eldor A, Haimovitz-Friedman A, et al. Expression of heparanase by platelets and circulating cells of the immune system: possible involvement in diapedesis and extravasation. Invasion Metastasis 1992; 12(2): 112-27.
[PMID: 1399400]
[34]
McKenzie E, Tyson K, Stamps A, et al. Cloning and expression profiling of Hpa2, a novel mammalian heparanase family member. Biochem Biophys Res Commun 2000; 276(3): 1170-7.
[http://dx.doi.org/10.1006/bbrc.2000.3586] [PMID: 11027606]
[35]
Mahmood S, Beetz C, Tahir MM, et al. First HPSE2 missense mutation in urofacial syndrome. Clin Genet 2012; 81(1): 88-92.
[http://dx.doi.org/10.1111/j.1399-0004.2011.01649.x] [PMID: 21332471]
[36]
Levy-Adam F, Feld S, Cohen-Kaplan V, et al. Heparanase 2 interacts with heparan sulfate with high affinity and inhibits heparanase activity. J Biol Chem 2010; 285(36): 28010-9.
[http://dx.doi.org/10.1074/jbc.M110.116384] [PMID: 20576607]
[37]
Roberts NA, Woolf AS, Stuart HM, et al. Heparanase 2, mutated in urofacial syndrome, mediates peripheral neural development in Xenopus. Hum Mol Genet 2014; 23(16): 4302-14.
[http://dx.doi.org/10.1093/hmg/ddu147] [PMID: 24691552]
[38]
Jin H, Cui M. New Advances of Heparanase and Heparanase-2 in Human Diseases. Arch Med Res 2018; 49(7): 423-9.
[http://dx.doi.org/10.1016/j.arcmed.2019.02.004] [PMID: 30850186]
[39]
Vlodavsky I, Gross-Cohen M, Weissmann M, Ilan N, Sanderson RD. Opposing functions of Heparanase-1 and Heparanase-2 in cancer progression. Trends Biochem Sci 2018; 43(1): 18-31.
[http://dx.doi.org/10.1016/j.tibs.2017.10.007] [PMID: 29162390]
[40]
Heyman B, Yang Y. Mechanisms of heparanase inhibitors in cancer therapy. Exp Hematol 2016; 44(11): 1002-12.
[http://dx.doi.org/10.1016/j.exphem.2016.08.006] [PMID: 27576132]
[41]
Masola V, Zaza G, Gambaro G, Franchi M, Onisto M. Role of heparanase in tumor progression: Molecular aspects and therapeutic options. Semin Cancer Biol 2020; 62: 86-98.
[http://dx.doi.org/10.1016/j.semcancer.2019.07.014] [PMID: 31348993]
[42]
Ricciuti B, Foglietta J, Chiari R, et al. Emerging enzymatic targets controlling angiogenesis in cancer: preclinical evidence and potential clinical applications. Med Oncol 2017; 35(1): 4.
[PMID: 29209837]
[43]
Zetser A, Bashenko Y, Edovitsky E, Levy-Adam F, Vlodavsky I, Ilan N. Heparanase induces vascular endothelial growth factor expression: correlation with p38 phosphorylation levels and Src activation. Cancer Res 2006; 66(3): 1455-63.
[http://dx.doi.org/10.1158/0008-5472.CAN-05-1811] [PMID: 16452201]
[44]
Gingis-Velitski S, Zetser A, Flugelman MY, Vlodavsky I, Ilan N. Heparanase induces endothelial cell migration via protein kinase B/Akt activation. J Biol Chem 2004; 279(22): 23536-41.
[http://dx.doi.org/10.1074/jbc.M400554200] [PMID: 15044433]
[45]
Zetser A, Bashenko Y, Miao HQ, Vlodavsky I, Ilan N. Heparanase affects adhesive and tumorigenic potential of human glioma cells. Cancer Res 2003; 63(22): 7733-41.
[PMID: 14633698]
[46]
Purushothaman A, Babitz SK, Sanderson RD. Heparanase enhances the insulin receptor signaling pathway to activate extracellular signal-regulated kinase in multiple myeloma. J Biol Chem 2012; 287(49): 41288-96.
[http://dx.doi.org/10.1074/jbc.M112.391417] [PMID: 23048032]
[47]
Cohen-Kaplan V, Doweck I, Naroditsky I, Vlodavsky I, Ilan N. Heparanase augments epidermal growth factor receptor phosphorylation: correlation with head and neck tumor progression. Cancer Res 2008; 68(24): 10077-85.
[http://dx.doi.org/10.1158/0008-5472.CAN-08-2910] [PMID: 19074873]
[48]
Ramani VC, Zhan F, He J, et al. Targeting heparanase overcomes chemoresistance and diminishes relapse in myeloma. Oncotarget 2016; 7(2): 1598-607.
[http://dx.doi.org/10.18632/oncotarget.6408] [PMID: 26624982]
[49]
Ramani VC, Vlodavsky I, Ng M, et al. Chemotherapy induces expression and release of heparanase leading to changes associated with an aggressive tumor phenotype. Matrix Biol 2016; 55: 22-34.
[http://dx.doi.org/10.1016/j.matbio.2016.03.006] [PMID: 27016342]
[50]
Li J, Pan Q, Rowan PD, et al. Heparanase promotes myeloma progression by inducing mesenchymal features and motility of myeloma cells. Oncotarget 2016; 7(10): 11299-309.
[http://dx.doi.org/10.18632/oncotarget.7170] [PMID: 26849235]
[51]
Shteingauz A, Boyango I, Naroditsky I, et al. Heparanase enhances tumor growth and chemoresistance by promoting autophagy. Cancer Res 2015; 75(18): 3946-57.
[http://dx.doi.org/10.1158/0008-5472.CAN-15-0037] [PMID: 26249176]
[52]
Levy-Adam F, Ilan N, Vlodavsky I. Tumorigenic and adhesive properties of heparanase. Semin Cancer Biol 2010; 20(3): 153-60.
[http://dx.doi.org/10.1016/j.semcancer.2010.06.005] [PMID: 20619346]
[53]
Nadir Y, Brenner B, Zetser A, et al. Heparanase induces tissue factor expression in vascular endothelial and cancer cells. J Thromb Haemost 2006; 4(11): 2443-51.
[http://dx.doi.org/10.1111/j.1538-7836.2006.02212.x] [PMID: 16970801]
[54]
Nadir Y, Brenner B, Fux L, Shafat I, Attias J, Vlodavsky I. Heparanase enhances the generation of activated factor X in the presence of tissue factor and activated factor VII. Haematologica 2010; 95(11): 1927-34.
[http://dx.doi.org/10.3324/haematol.2010.023713] [PMID: 20634491]
[55]
Nadir Y, Brenner B, Gingis-Velitski S, et al. Heparanase induces tissue factor pathway inhibitor expression and extracellular accumulation in endothelial and tumor cells. Thromb Haemost 2008; 99(1): 133-41.
[http://dx.doi.org/10.1055/s-0037-1608919] [PMID: 18217145]
[56]
Cui H, Tan YX, Österholm C, et al. Heparanase expression upregulates platelet adhesion activity and thrombogenicity. Oncotarget 2016; 7(26): 39486-96.
[http://dx.doi.org/10.18632/oncotarget.8960] [PMID: 27129145]
[57]
Kogan I, Chap D, Hoffman R, Axelman E, Brenner B, Nadir Y. JAK-2 V617F mutation increases heparanase procoagulant activity. Thromb Haemost 2016; 115(1): 73-80.
[http://dx.doi.org/10.1160/TH15-04-0320] [PMID: 26489695]
[58]
Ruan J, Trotter TN, Nan L, et al. Heparanase inhibits osteoblastogenesis and shifts bone marrow progenitor cell fate in myeloma bone disease. Bone 2013; 57(1): 10-7.
[http://dx.doi.org/10.1016/j.bone.2013.07.024] [PMID: 23895995]
[59]
Sanderson RD, Elkin M, Rapraeger AC, Ilan N, Vlodavsky I. Heparanase regulation of cancer, autophagy and inflammation: new mechanisms and targets for therapy. FEBS J 2017; 284(1): 42-55.
[http://dx.doi.org/10.1111/febs.13932] [PMID: 27758044]
[60]
Coombe DR, Kett WC. Heparan sulfate-protein interactions: therapeutic potential through structure-function insights. Cell Mol Life Sci 2005; 62(4): 410-24.
[http://dx.doi.org/10.1007/s00018-004-4293-7] [PMID: 15719168]
[61]
Bathini R, Fatima S, Sivan SK, Manga V. 3D QSAR based design of novel substituted urea molecules as heparanase inhibitors. J Pharm Res 2013; 7: 754-61.
[http://dx.doi.org/10.1016/j.jopr.2013.08.024]
[63]
Naggi A. Glycol-splitting as a device for modulating inhibition of growth factors and heparanase by heparin and heparin derivatives Chemistry and biology of heparin and heparan sulfate. Elsevier Science 2005; pp. 461-81.
[http://dx.doi.org/10.1016/B978-008044859-6/50017-4]
[64]
Casu B, Vlodavsky I, Sanderson RD. Non-anticoagulant heparins and inhibition of cancer. Pathophysiol Haemost Thromb 2008; 36(3-4): 195-203.
[PMID: 19176992]
[65]
Green D. The heparins: Basic and clinical aspects. Academic Press 2020.
[66]
Hammond E, Handley P, Dredge K, Bytheway I. Mechanisms of heparanase inhibition by the heparan sulfate mimetic PG545 and three structural analogues. FEBS Open Bio 2013; 3: 346-51.
[PMID: 24251094]
[67]
Jia L, Ma S. Recent advances in the discovery of heparanase inhibitors as anti-cancer agents. Eur J Med Chem 2016; 121: 209-20.
[http://dx.doi.org/10.1016/j.ejmech.2016.05.052] [PMID: 27240275]
[68]
Lazo-Langner A, Goss GD, Spaans JN, Rodger MA. The effect of low-molecular-weight heparin on cancer survival. A systematic review and meta-analysis of randomized trials. J Thromb Haemost 2007; 5(4): 729-37.
[http://dx.doi.org/10.1111/j.1538-7836.2007.02427.x] [PMID: 17408406]
[69]
Kuderer NM, Khorana AA, Lyman GH, Francis CW. A meta-analysis and systematic review of the efficacy and safety of anticoagulants as cancer treatment: impact on survival and bleeding complications. Cancer 2007; 110(5): 1149-61.
[http://dx.doi.org/10.1002/cncr.22892] [PMID: 17634948]
[70]
Cassinelli G, Dal Bo L, Favini E, et al. Supersulfated low-molecular weight heparin synergizes with IGF1R/IR inhibitor to suppress synovial sarcoma growth and metastases. Cancer Lett 2018; 415: 187-97.
[http://dx.doi.org/10.1016/j.canlet.2017.12.009] [PMID: 29225052]
[71]
Sanford D, Naidu A, Alizadeh N, Lazo-Langner A. The effect of low molecular weight heparin on survival in cancer patients: an updated systematic review and meta-analysis of randomized trials. J Thromb Haemost 2014; 12(7): 1076-85.
[http://dx.doi.org/10.1111/jth.12595] [PMID: 24796727]
[72]
Macbeth F, Noble S, Evans J, et al. Randomized phase III trial of standard therapy plus low molecular weight heparin in patients with lung cancer: FRAGMATIC trial. J Clin Oncol 2016; 34(5): 488-94.
[http://dx.doi.org/10.1200/JCO.2015.64.0268] [PMID: 26700124]
[73]
Oduah EI, Linhardt RJ, Sharfstein ST. Heparin: past, present, and future. Pharmaceuticals (Basel) 2016; 9(3): 38.
[http://dx.doi.org/10.3390/ph9030038] [PMID: 27384570]
[74]
Franchini M, Mannucci PM. Low-molecular-weight heparins and cancer: focus on antitumoral effect. Ann Med 2015; 47(2): 116-21.
[http://dx.doi.org/10.3109/07853890.2015.1004361] [PMID: 25766973]
[75]
Gomes AM, Kozlowski EO, Borsig L, Teixeira FC, Vlodavsky I, Pavão MS. Antitumor properties of a new non-anticoagulant heparin analog from the mollusk Nodipecten nodosus: Effect on P-selectin, heparanase, metastasis and cellular recruitment. Glycobiology 2015; 25(4): 386-93.
[http://dx.doi.org/10.1093/glycob/cwu119] [PMID: 25367817]
[76]
Mohamed S, Coombe DR. Heparin mimetics: Their therapeutic potential. Pharmaceuticals (Basel) 2017; 10(4): 78.
[http://dx.doi.org/10.3390/ph10040078] [PMID: 28974047]
[77]
A Study of Standard Treatment +/- Enoxaparin in Small Cell Lung Cancer (RASTEN) Available from: https://clinicaltrials.gov/ct2/show/NCT00717938?term=enoxaparin+in+cancer&draw=2&rank=42020
[78]
Djaafar S, Dunand-Sautier I, Gonelle-Gispert C, et al. Enoxaparin attenuates mouse colon cancer liver metastases by inhibiting heparanase and interferon-γ-inducible chemokines. Anticancer Res 2016; 36(8): 4019-32.
[PMID: 27466508]
[79]
Achour O, Poupard N, Bridiau N, et al. Anti-heparanase activity of ultra-low-molecular-weight heparin produced by physicochemical depolymerization. Carbohydr Polym 2016; 135: 316-23.
[http://dx.doi.org/10.1016/j.carbpol.2015.08.041] [PMID: 26453883]
[80]
Alekseeva A, Mazzini G, Giannini G, Naggi A. Structural features of heparanase-inhibiting non-anticoagulant heparin derivative Roneparstat. Carbohydr Polym 2017; 156: 470-80.
[http://dx.doi.org/10.1016/j.carbpol.2016.09.032] [PMID: 27842848]
[81]
Cassinelli G, Lanzi C, Tortoreto M, et al. Antitumor efficacy of the heparanase inhibitor SST0001 alone and in combination with antiangiogenic agents in the treatment of human pediatric sarcoma models. Biochem Pharmacol 2013; 85(10): 1424-32.
[http://dx.doi.org/10.1016/j.bcp.2013.02.023] [PMID: 23466421]
[82]
Alekseeva A, Casu B, Cassinelli G, Guerrini M, Torri G, Naggi A. Structural features of glycol-split low-molecular-weight heparins and their heparin lyase generated fragments. Anal Bioanal Chem 2014; 406(1): 249-65.
[http://dx.doi.org/10.1007/s00216-013-7446-4] [PMID: 24253408]
[83]
Park PW. Isolation and functional analysis of syndecans. Methods Cell Biol 2018; 143: 317-33.
[http://dx.doi.org/10.1016/bs.mcb.2017.08.019] [PMID: 29310785]
[84]
Ritchie JP, Ramani VC, Ren Y, et al. SST0001, a chemically modified heparin, inhibits myeloma growth and angiogenesis via disruption of the heparanase/syndecan-1 axis. Clin Cancer Res 2011; 17(6): 1382-93.
[http://dx.doi.org/10.1158/1078-0432.CCR-10-2476] [PMID: 21257720]
[85]
Galli M, Chatterjee M, Grasso M, et al. Phase I study of the heparanase inhibitor roneparstat: an innovative approach for ultiple myeloma therapy. Haematologica 2018; 103(10): e469-72.
[http://dx.doi.org/10.3324/haematol.2017.182865] [PMID: 29700168]
[86]
Cassinelli G, Favini E, Dal Bo L, et al. Antitumor efficacy of the heparan sulfate mimic roneparstat (SST0001) against sarcoma models involves multi-target inhibition of receptor tyrosine kinases. Oncotarget 2016; 7(30): 47848-63.
[http://dx.doi.org/10.18632/oncotarget.10292] [PMID: 27374103]
[87]
Pala D, Rivara S, Mor M, et al. Kinetic analysis and molecular modeling of the inhibition mechanism of roneparstat (SST0001) on human heparanase. Glycobiology 2016; 26(6): 640-54.
[http://dx.doi.org/10.1093/glycob/cww003] [PMID: 26762172]
[88]
Naggi A, Casu B, Perez M, et al. Modulation of the heparanase-inhibiting activity of heparin through selective desulfation, graded N-acetylation, and glycol splitting. J Biol Chem 2005; 280(13): 12103-13.
[http://dx.doi.org/10.1074/jbc.M414217200] [PMID: 15647251]
[89]
Esposito E, Vlodavsky I, Barash U, et al. Novel N-acetyl-Glycol-split heparin biotin-conjugates endowed with anti-heparanase activity. Eur J Med Chem 2020; 186111831
[http://dx.doi.org/10.1016/j.ejmech.2019.111831] [PMID: 31740052]
[90]
Zhou H, Roy S, Cochran E, et al. M402, a novel heparan sulfate mimetic, targets multiple pathways implicated in tumor progression and metastasis. PLoS One 2011; 6(6)e21106
[http://dx.doi.org/10.1371/journal.pone.0021106] [PMID: 21698156]
[91]
Krause S, Weyers A, Loveluck K, Schultes B. Abstract 5499: necuparanib affects tumor progression and invasion in a 3D co-culture system of pancreatic cancer cells and stellate cells. Cancer Res 2015; 75(15)(Suppl.): 5499.
[92]
O’Reilly EM, Roach J, Miller P, et al. Safety, pharmacokinetics, pharmacodynamics, and antitumor activity of Necuparanib combined with nab-paclitaxel and gemcitabine in patients with metastatic pancreatic cancer: Phase I results. Oncologist 2017; 22(12): 1429-e139.
[http://dx.doi.org/10.1634/theoncologist.2017-0472] [PMID: 29158367]
[93]
Parish CR, Freeman C, Brown KJ, Francis DJ, Cowden WB. Identification of sulfated oligosaccharide-based inhibitors of tumor growth and metastasis using novel in vitro assays for angiogenesis and heparanase activity. Cancer Res 1999; 59(14): 3433-41.
[PMID: 10416607]
[94]
Ferro V, Fewings K, Palermo MC, Li C. Large-scale preparation of the oligosaccharide phosphate fraction of Pichia holstii NRRL Y-2448 phosphomannan for use in the manufacture of PI-88. Carbohydr Res 2001; 332(2): 183-9.
[http://dx.doi.org/10.1016/S0008-6215(01)00061-1] [PMID: 11434376]
[95]
Karoli T, Liu L, Fairweather JK, et al. Synthesis, biological activity, and preliminary pharmacokinetic evaluation of analogues of a phosphosulfomannan angiogenesis inhibitor (PI-88). J Med Chem 2005; 48(26): 8229-36.
[http://dx.doi.org/10.1021/jm050618p] [PMID: 16366604]
[96]
Fairweather JK, Hammond E, Johnstone KD, Ferro V. Synthesis and heparanase inhibitory activity of sulfated mannooligosaccharides related to the antiangiogenic agent PI-88. Bioorg Med Chem 2008; 16(2): 699-709.
[http://dx.doi.org/10.1016/j.bmc.2007.10.044] [PMID: 17967543]
[97]
Cochran S, Li C, Fairweather JK, Kett WC, Coombe DR, Ferro V. Probing the interactions of phosphosulfomannans with angiogenic growth factors by surface plasmon resonance. J Med Chem 2003; 46(21): 4601-8.
[http://dx.doi.org/10.1021/jm030180y] [PMID: 14521421]
[98]
Ferro V, Dredge K, Liu L, et al. PI-88 and novel heparan sulfate mimetics inhibit angiogenesis. Semin Thromb Hemost 2007; 33(5): 557-68.
[http://dx.doi.org/10.1055/s-2007-982088] [PMID: 17629854]
[99]
Kudchadkar R, Gonzalez R, Lewis KD. PI-88: a novel inhibitor of angiogenesis. Expert Opin Investig Drugs 2008; 17(11): 1769-76.
[http://dx.doi.org/10.1517/13543784.17.11.1769] [PMID: 18922112]
[100]
Wood JP, Ellery PER, Maroney SA, Mast AE. Biology of tissue factor pathway inhibitor. Blood 2014; 123(19): 2934-43.
[http://dx.doi.org/10.1182/blood-2013-11-512764] [PMID: 24620349]
[101]
Demir M, Iqbal O, Hoppensteadt DA, et al. Anticoagulant and antiprotease profiles of a novel natural heparinomimetic mannopentaose phosphate sulfate (PI-88). Clin Appl Thromb Hemost 2001; 7(2): 131-40.
[http://dx.doi.org/10.1177/107602960100700210] [PMID: 11292191]
[102]
Iversen PO, Sorensen DR, Benestad HB. Inhibitors of angiogenesis selectively reduce the malignant cell load in rodent models of human myeloid leukemias. Leukemia 2002; 16(3): 376-81.
[http://dx.doi.org/10.1038/sj.leu.2402376] [PMID: 11896541]
[103]
Joyce JA, Freeman C, Meyer-Morse N, Parish CR, Hanahan D. A functional heparan sulfate mimetic implicates both heparanase and heparan sulfate in tumor angiogenesis and invasion in a mouse model of multistage cancer. Oncogene 2005; 24(25): 4037-51.
[http://dx.doi.org/10.1038/sj.onc.1208602] [PMID: 15806157]
[104]
Hossain MM, Hosono-Fukao T, Tang R, et al. Direct detection of HSulf-1 and HSulf-2 activities on extracellular heparan sulfate and their inhibition by PI-88. Glycobiology 2010; 20(2): 175-86.
[http://dx.doi.org/10.1093/glycob/cwp159] [PMID: 19822709]
[105]
Basche M, Gustafson DL, Holden SN, et al. A phase I biological and pharmacologic study of the heparanase inhibitor PI-88 in patients with advanced solid tumors. Clin Cancer Res 2006; 12(18): 5471-80.
[http://dx.doi.org/10.1158/1078-0432.CCR-05-2423] [PMID: 17000682]
[106]
Khasraw M, Pavlakis N, McCowatt S, et al. Multicentre phase I/II study of PI-88, a heparanase inhibitor in combination with docetaxel in patients with metastatic castrate-resistant prostate cancer. Ann Oncol 2010; 21(6): 1302-7.
[http://dx.doi.org/10.1093/annonc/mdp524] [PMID: 19917571]
[107]
Chen PJ, Lee PH, Han KH, et al. 624PDA A phase III trial of muparfostat (PI-88) as adjuvant therapy in patients with hepatitis virus related hepatocellular carcinoma (HV-HCC) after resection. Ann Oncol 2017; 28(Suppl. 5): v209-68.
[http://dx.doi.org/10.1093/annonc/mdx369.008]
[108]
Xie L, Shen M, Hong Y, Ye H, Huang L, Xie J. Chemical modifications of polysaccharides and their anti-tumor activities. Carbohydr Polym 2020; 229115436
[http://dx.doi.org/10.1016/j.carbpol.2019.115436] [PMID: 31826393]
[109]
Abaterusso C, Gambaro G. The role of glycosaminoglycans and sulodexide in the treatment of diabetic nephropathy. Treat Endocrinol 2006; 5(4): 211-22.
[http://dx.doi.org/10.2165/00024677-200605040-00002] [PMID: 16879000]
[110]
Masola V, Zaza G, Gambaro G. Sulodexide and glycosaminoglycans in the progression of renal disease. Nephrol Dial Transplant 2014; 29(Suppl. 1): 74-9.
[http://dx.doi.org/10.1093/ndt/gft389]
[111]
Masola V, Onisto M, Zaza G, Lupo A, Gambaro G. A new mechanism of action of sulodexide in diabetic nephropathy: inhibits heparanase-1 and prevents FGF-2-induced renal epithelial-mesenchymal transition. J Transl Med 2012; 10: 213.
[http://dx.doi.org/10.1186/1479-5876-10-213] [PMID: 23095131]
[112]
Zhao H, Liu H, Chen Y, et al. Oligomannurarate sulfate, a novel heparanase inhibitor simultaneously targeting basic fibroblast growth factor, combats tumor angiogenesis and metastasis. Cancer Res 2006; 66(17): 8779-87.
[http://dx.doi.org/10.1158/0008-5472.CAN-06-1382] [PMID: 16951194]
[113]
Li JP, Vlodavsky I. Heparin, heparan sulfate and heparanase in inflammatory reactions. Thromb Haemost 2009; 102(5): 823-8.
[PMID: 19888515]
[114]
Zhang J, Chen Y, Xin XL, et al. Oligomannurarate sulfate blocks tumor growth by inhibiting NF-kappaB activation. Acta Pharmacol Sin 2010; 31(3): 375-81.
[http://dx.doi.org/10.1038/aps.2010.13] [PMID: 20154712]
[115]
Zhang J, Xin X, Chen Q, et al. Oligomannurarate sulfate sensitizes cancer cells to doxorubicin by inhibiting atypical activation of NF-κB via targeting of Mre11. Int J Cancer 2012; 130(2): 467-77.
[http://dx.doi.org/10.1002/ijc.26021] [PMID: 21387297]
[116]
Miao B, Chen Y, Li J, et al. Oligomannurarate sulfate, a novel antimitotic agent, exerts anti-cancer activity by binding to tubulin on novel site. Cancer Biol Ther 2010; 10(1): 89-98.
[http://dx.doi.org/10.4161/cbt.10.1.12167] [PMID: 20495375]
[117]
Dredge K, Hammond E, Davis K, et al. The PG500 series: novel heparan sulfate mimetics as potent angiogenesis and heparanase inhibitors for cancer therapy. Invest New Drugs 2010; 28(3): 276-83.
[http://dx.doi.org/10.1007/s10637-009-9245-5] [PMID: 19357810]
[118]
Dredge K, Hammond E, Handley P, et al. PG545, a dual heparanase and angiogenesis inhibitor, induces potent anti-tumour and anti-metastatic efficacy in preclinical models. Br J Cancer 2011; 104(4): 635-42.
[http://dx.doi.org/10.1038/bjc.2011.11] [PMID: 21285983]
[119]
Ostapoff KT, Awasthi N, Cenik BK, et al. PG545, an angiogenesis and heparanase inhibitor, reduces primary tumor growth and metastasis in experimental pancreatic cancer. Mol Cancer Ther 2013; 12(7): 1190-201.
[http://dx.doi.org/10.1158/1535-7163.MCT-12-1123] [PMID: 23696215]
[120]
Hammond E, Brandt R, Dredge K. PG545, a heparan sulfate mimetic, reduces heparanase expression in vivo, blocks spontaneous metastases and enhances overall survival in the 4T1 breast carcinoma model. PLoS One 2012; 7(12)e52175
[http://dx.doi.org/10.1371/journal.pone.0052175] [PMID: 23300607]
[121]
Jung DB, Yun M, Kim EO, et al. The heparan sulfate mimetic PG545 interferes with Wnt/β-catenin signaling and significantly suppresses pancreatic tumorigenesis alone and in combination with gemcitabine. Oncotarget 2015; 6(7): 4992-5004.
[http://dx.doi.org/10.18632/oncotarget.3214] [PMID: 25669977]
[122]
Winterhoff B, Freyer L, Hammond E, et al. PG545 enhances anti-cancer activity of chemotherapy in ovarian models and increases surrogate biomarkers such as VEGF in preclinical and clinical plasma samples. Eur J Cancer 2015; 51(7): 879-92.
[http://dx.doi.org/10.1016/j.ejca.2015.02.007] [PMID: 25754234]
[123]
Barash U, Lapidot M, Zohar Y, et al. Involvement of heparanase in the pathogenesis of mesothelioma: basic aspects and clinical applications. J Natl Cancer Inst 2018; 110(10): 1102-14.
[http://dx.doi.org/10.1093/jnci/djy032] [PMID: 29579286]
[124]
Katz A, Barash U, Boyango I, et al. Patient derived xenografts (PDX) predict an effective heparanase-based therapy for lung cancer. Oncotarget 2018; 9(27): 19294-306.
[http://dx.doi.org/10.18632/oncotarget.25022] [PMID: 29721203]
[125]
Spyrou A, Kundu S, Haseeb L, et al. Inhibition of heparanase in pediatric brain tumor cells attenuates their proliferation, invasive capacity, and in vivo tumor growth. Mol Cancer Ther 2017; 16(8): 1705-16.
[http://dx.doi.org/10.1158/1535-7163.MCT-16-0900] [PMID: 28716813]
[126]
Brennan TV, Lin L, Brandstadter JD, et al. Heparan sulfate mimetic PG545-mediated antilymphoma effects require TLR9-dependent NK cell activation. J Clin Invest 2016; 126(1): 207-19.
[http://dx.doi.org/10.1172/JCI76566] [PMID: 26649979]
[127]
Weissmann M, Bhattacharya U, Feld S, Hammond E, Ilan N, Vlodavsky I. The heparanase inhibitor PG545 is a potent anti-lymphoma drug: Mode of action. Matrix Biol 2019; 77: 58-72.
[http://dx.doi.org/10.1016/j.matbio.2018.08.005] [PMID: 30096360]
[128]
Supramaniam A, Liu X, Ferro V, Herrero LJ. Prophylactic antiheparanase activity by PG545 is antiviral in vitro and protects against Ross River virus disease in mice. Antimicrob Agents Chemother 2018; 62(4): e01959-17.
[http://dx.doi.org/10.1128/AAC.01959-17] [PMID: 29437628]
[129]
Singh P, Blatt A, Feld S, et al. The heparanase inhibitor PG545 attenuates colon cancer initiation and growth, associating with increased p21 expression. Neoplasia 2017; 19(3): 175-84.
[http://dx.doi.org/10.1016/j.neo.2016.12.001] [PMID: 28147305]
[130]
Hoffmann R, Sarkar Bhattacharya S, Roy D, et al. Sulfated glycolipid PG545 induces endoplasmic reticulum stress and augments autophagic flux by enhancing anticancer chemotherapy efficacy in endometrial cancer. Biochem Pharmacol 2020; 178114003
[http://dx.doi.org/10.1016/j.bcp.2020.114003] [PMID: 32360360]
[131]
Hoffman R, Burns WW III, Paper DH. Selective inhibition of cell proliferation and DNA synthesis by the polysulphated carbohydrate l-carrageenan. Cancer Chemother Pharmacol 1995; 36(4): 325-34.
[http://dx.doi.org/10.1007/BF00689050] [PMID: 7628052]
[132]
Parish CR, Coombe DR, Jakobsen KB, Bennett FA, Underwood PA. Evidence that sulphated polysaccharides inhibit tumour metastasis by blocking tumour-cell-derived heparanases. Int J Cancer 1987; 40(4): 511-8.
[http://dx.doi.org/10.1002/ijc.2910400414] [PMID: 3666989]
[133]
Poupard N, Badarou P, Fasani F, et al. Assessment of heparanase-mediated angiogenesis using microvascular endothelial cells: Identification of λ-Carrageenan derivative as a potent anti angiogenic agent. Mar Drugs 2017; 15(5): 134.
[http://dx.doi.org/10.3390/md15050134] [PMID: 28486399]
[134]
Poupard N, Groult H, Bodin J, et al. Production of heparin and λ-carrageenan anti-heparanase derivatives using a combination of physicochemical depolymerization and glycol splitting. Carbohydr Polym 2017; 166: 156-65.
[http://dx.doi.org/10.1016/j.carbpol.2017.02.040] [PMID: 28385219]
[135]
Chen H, Yan X, Lin J, Wang F, Xu W. Depolymerized products of λ-carrageenan as a potent angiogenesis inhibitor. J Agric Food Chem 2007; 55(17): 6910-7.
[http://dx.doi.org/10.1021/jf070183+] [PMID: 17661479]
[136]
Alban S, Ludwig RJ, Bendas G, et al. PS3, a semisynthetic beta-1,3-glucan sulfate, diminishes contact hypersensitivity responses through inhibition of L- and P-selectin functions. J Invest Dermatol 2009; 129(5): 1192-202.
[http://dx.doi.org/10.1038/jid.2008.358] [PMID: 19052560]
[137]
Schoenfeld AK, Vierfuß S, Lühn S, Alban S. Testing of potential glycan-based heparanase inhibitors in a fluorescence activity assay using either bacterial heparinase II or human heparanase. J Pharm Biomed Anal 2014; 95: 130-8.
[http://dx.doi.org/10.1016/j.jpba.2014.02.021] [PMID: 24667567]
[138]
Groth I, Grünewald N, Alban S. Pharmacological profiles of animal- and nonanimal-derived sulfated polysaccharides--comparison of unfractionated heparin, the semisynthetic glucan sulfate PS3, and the sulfated polysaccharide fraction isolated from Delesseria sanguinea. Glycobiology 2009; 19(4): 408-17.
[http://dx.doi.org/10.1093/glycob/cwn151] [PMID: 19106233]
[139]
Borsig L, Vlodavsky I, Ishai-Michaeli R, Torri G, Vismara E. Sulfated hexasaccharides attenuate metastasis by inhibition of P-selectin and heparanase. Neoplasia 2011; 13(5): 445-52.
[http://dx.doi.org/10.1593/neo.101734] [PMID: 21532885]
[140]
Coletti A, Elli S, Macchi E, et al. Conformational changes of 1-4-glucopyranosyl residues of a sulfated C-C linked hexasaccharide. Carbohydr Res 2014; 389: 134-40.
[http://dx.doi.org/10.1016/j.carres.2014.02.009] [PMID: 24680506]
[141]
Shiozawa H, Takahashi M, Takatsu T, et al. Trachyspic acid, a new metabolite produced by Talaromyces trachyspermus, that inhibits tumor cell heparanase: taxonomy of the producing strain, fermentation, isolation, structural elucidation, and biological activity. J Antibiot (Tokyo) 1995; 48(5): 357-62.
[http://dx.doi.org/10.7164/antibiotics.48.357] [PMID: 7797435]
[142]
Nogawa T, Ogita N, Futamura Y, Negishi S, Watanabe N, Osada H. Trachyspic acid 19-butyl ester, a new inhibitor of Plk1 polo box domain-dependent recognition from uncharacterized fungus RKGS-F2684. J Antibiot (Tokyo) 2017; 70(5): 705-7.
[http://dx.doi.org/10.1038/ja.2016.167] [PMID: 28096547]
[143]
Hamaguchi T, Sudo T, Osada H. RK-682, a potent inhibitor of tyrosine phosphatase, arrested the mammalian cell cycle progression at G1phase. FEBS Lett 1995; 372(1): 54-8.
[http://dx.doi.org/10.1016/0014-5793(95)00953-7] [PMID: 7556642]
[144]
Ishida K, Teruya T, Simizu S, Osada H. Exploitation of heparanase inhibitors from microbial metabolites using an efficient visual screening system. J Antibiot (Tokyo) 2004; 57(2): 136-42.
[http://dx.doi.org/10.7164/antibiotics.57.136] [PMID: 15112962]
[145]
Ishida K, Hirai G, Murakami K, et al. Structure-based design of a selective heparanase inhibitor as an antimetastatic agent. Mol Cancer Ther 2004; 3(9): 1069-77.
[PMID: 15367701]
[146]
Woll PJ, Ranson M, Margison J, et al. Suramin for breast and prostate cancer: a pilot study of intermittent short infusions without adaptive control. Ann Oncol 1994; 5(7): 597-600.
[http://dx.doi.org/10.1093/oxfordjournals.annonc.a058930] [PMID: 7993834]
[147]
Firsching A, Nickel P, Mora P, Allolio B. Antiproliferative and angiostatic activity of suramin analogues. Cancer Res 1995; 55(21): 4957-61.
[PMID: 7585536]
[148]
Marchetti D, Reiland J, Erwin B, Roy M. Inhibition of heparanase activity and heparanase-induced angiogenesis by suramin analogues. Int J Cancer 2003; 104(2): 167-74.
[http://dx.doi.org/10.1002/ijc.10930] [PMID: 12569571]
[149]
Nadir Y, Vlodavsky I, Brenner B. Heparanase, tissue factor, and cancer. Semin Thromb Hemost 2008; 34(2): 187-94.
[http://dx.doi.org/10.1055/s-2008-1079259] [PMID: 18645924]
[150]
Tayel A, Abd El Galil KH, Ebrahim MA, Ibrahim AS, El-Gayar AM, Al-Gayyar MM. Suramin inhibits hepatic tissue damage in hepatocellular carcinoma through deactivation of heparanase enzyme. Eur J Pharmacol 2014; 728: 151-60.
[http://dx.doi.org/10.1016/j.ejphar.2014.02.001] [PMID: 24530413]
[151]
Li H, Li H, Qu H, et al. Suramin inhibits cell proliferation in ovarian and cervical cancer by downregulating heparanase expression. Cancer Cell Int 2015; 15: 52.
[http://dx.doi.org/10.1186/s12935-015-0196-y] [PMID: 26052253]
[152]
Berg A, Berg T. A small-molecule screen identifies the antitrypanosomal agent suramin and analogues NF023 and NF449 as inhibitors of STAT5a/b. Bioorg Med Chem Lett 2017; 27(15): 3349-52.
[http://dx.doi.org/10.1016/j.bmcl.2017.06.012] [PMID: 28624143]
[153]
Villalona-Calero MA, Otterson GA, Wientjes MG, et al. Noncytotoxic suramin as a chemosensitizer in patients with advanced non-small-cell lung cancer: a phase II study. Ann Oncol 2008; 19(11): 1903-9.
[http://dx.doi.org/10.1093/annonc/mdn412] [PMID: 18632723]
[154]
Miao HQ, Ornitz DM, Aingorn E, Ben-Sasson SA, Vlodavsky I. Modulation of fibroblast growth factor-2 receptor binding, dimerization, signaling, and angiogenic activity by a synthetic heparin-mimicking polyanionic compound. J Clin Invest 1997; 99(7): 1565-75.
[http://dx.doi.org/10.1172/JCI119319] [PMID: 9120000]
[155]
Benezra M, Ishai-Michaeli R, Ben-Sasson SA, Vlodavsky I. Structure-activity relationships of heparin-mimicking compounds in induction of bFGF release from extracellular matrix and inhibition of smooth muscle cell proliferation and heparanase activity. J Cell Physiol 2002; 192(3): 276-85.
[http://dx.doi.org/10.1002/jcp.10136] [PMID: 12124773]
[156]
Courtney SM, Hay PA, Buck RT, et al. Furanyl-1,3-thiazol-2-yl and benzoxazol-5-yl acetic acid derivatives: novel classes of heparanase inhibitor. Bioorg Med Chem Lett 2005; 15(9): 2295-9.
[http://dx.doi.org/10.1016/j.bmcl.2005.03.014] [PMID: 15837312]
[157]
Qu H, Hu B, Wang C, Tao J, Zhang Y, Cui J. Effect of 1,3-O,N spiroheterocyclic inhibitors of heparanase on the growth of HeLa cells. Zhonghua Fu Chan Ke Za Zhi 2015; 50(7): 529-36.
[PMID: 26311644]
[158]
Song Y, Hu B, Qu H, et al. Novel 1, 3-N, O-Spiroheterocyclic compounds inhibit heparanase activity and enhance nedaplatin-induced cytotoxicity in cervical cancer cells. Oncotarget 2016; 7(24): 36154-67.
[http://dx.doi.org/10.18632/oncotarget.8959] [PMID: 27166252]
[159]
Basappa MS, Murugan S, Kavitha CV, et al. A small oxazine compound as an anti-tumor agent: a novel pyranoside mimetic that binds to VEGF, HB-EGF, and TNF-α. Cancer Lett 2010; 297(2): 231-43.
[http://dx.doi.org/10.1016/j.canlet.2010.05.016] [PMID: 20831981]
[160]
Gozalbes R, Mosulén S, Ortí L, et al. Hit identification of novel heparanase inhibitors by structure- and ligand-based approaches. Bioorg Med Chem 2013; 21(7): 1944-51.
[http://dx.doi.org/10.1016/j.bmc.2013.01.033] [PMID: 23415087]
[161]
Fu K, Bai Z, Chen L, et al. Antitumor activity and structure-activity relationship of heparanase inhibitors: Recent advances. Eur J Med Chem 2020; 193112221
[http://dx.doi.org/10.1016/j.ejmech.2020.112221] [PMID: 32222663]
[162]
Wang T, Yin H, Wang W, Wang M. Preparation, characterization and in vitro anti-metastasis activity of glucan derivatives. Carbohydr Polym 2012; 87: 1913-8.
[http://dx.doi.org/10.1016/j.carbpol.2011.09.083]
[163]
Pan W, Miao HQ, Xu YJ, et al. 1-[4-(1H-Benzoimidazol-2-yl)-phenyl]-3-[4-(1H-benzoimidazol-2-yl)-phenyl]-urea derivatives as small molecule heparanase inhibitors. Bioorg Med Chem Lett 2006; 16(2): 409-12.
[http://dx.doi.org/10.1016/j.bmcl.2005.09.069] [PMID: 16246560]
[164]
Courtney SM, Hay PA, Buck RT, et al. 2,3-Dihydro-1,3-dioxo-1H-isoindole-5-carboxylic acid derivatives: a novel class of small molecule heparanase inhibitors. Bioorg Med Chem Lett 2004; 14(12): 3269-73.
[http://dx.doi.org/10.1016/j.bmcl.2004.03.086] [PMID: 15149688]
[165]
Xu YJ, Miao HQ, Pan W, et al. -(4-[4-(1H-Benzoimidazol-2-yl)-arylamino]-methyl-phenyl)-benzamide derivatives as small molecule heparanase inhibitors. Bioorg Med Chem Lett 2006; 16: 404-8.
[http://dx.doi.org/10.1016/j.bmcl.2005.09.070] [PMID: 16246551]
[166]
Madia VN, Messore A, Pescatori L, et al. Novel benzazole derivatives endowed with potent antiheparanase activity. J Med Chem 2018; 61(15): 6918-36.
[http://dx.doi.org/10.1021/acs.jmedchem.8b00908] [PMID: 30010344]
[167]
Baburajeev CP, Mohan CD, Rangappa S, et al. Identification of novel class of triazolo-thiadiazoles as potent inhibitors of human heparanase and their anticancer activity. BMC Cancer 2017; 17(1): 235.
[http://dx.doi.org/10.1186/s12885-017-3214-8] [PMID: 28359266]
[168]
Sola F, Farao M, Ciomei M, Pastori A, Mongelli N, Grandi M. FCE 27266, a sulfonic distamycin derivative, inhibits experimental and spontaneous lung and liver metastasis. Invasion Metastasis 1995; 15(5-6): 222-31.
[PMID: 8765197]
[169]
Manetti F, Cappello V, Botta M, et al. Synthesis and binding mode of heterocyclic analogues of suramin inhibiting the human basic fibroblast growth factor. Bioorg Med Chem 1998; 6(7): 947-58.
[http://dx.doi.org/10.1016/S0968-0896(98)00052-2] [PMID: 9730230]
[170]
Rondanin R, Fochi S, Baruchello R, et al. Arylamidonaphtalene sulfonate compounds as a novel class of heparanase inhibitors. Bioorg Med Chem Lett 2017; 27(18): 4421-5.
[http://dx.doi.org/10.1016/j.bmcl.2017.08.013] [PMID: 28811133]
[171]
Thun MJ, Henley SJ, Patrono C. Nonsteroidal anti-inflammatory drugs as anticancer agents: mechanistic, pharmacologic, and clinical issues. J Natl Cancer Inst 2002; 94(4): 252-66.
[http://dx.doi.org/10.1093/jnci/94.4.252] [PMID: 11854387]
[172]
Kumar D, Rahman H, Tyagi E, et al. Aspirin suppresses PGE2 and activates AMP kinase to inhibit melanoma cell motility, pigmentation, and selective tumor growth in vivo. Cancer Prev Res (Phila) 2018; 11(10): 629-42.
[http://dx.doi.org/10.1158/1940-6207.CAPR-18-0087] [PMID: 30021726]
[173]
Ruder EH, Laiyemo AO, Graubard BI, Hollenbeck AR, Schatzkin A, Cross AJ. Non-steroidal anti-inflammatory drugs and colorectal cancer risk in a large, prospective cohort. Am J Gastroenterol 2011; 106(7): 1340-50.
[http://dx.doi.org/10.1038/ajg.2011.38] [PMID: 21407185]
[174]
Rothwell PM, Wilson M, Price JF, Belch JF, Meade TW, Mehta Z. Effect of daily aspirin on risk of cancer metastasis: a study of incident cancers during randomised controlled trials. Lancet 2012; 379(9826): 1591-601.
[http://dx.doi.org/10.1016/S0140-6736(12)60209-8] [PMID: 22440947]
[175]
Patrignani P, Patrono C. Aspirin and cancer. J Am Coll Cardiol 2016; 68(9): 967-76.
[http://dx.doi.org/10.1016/j.jacc.2016.05.083] [PMID: 27561771]
[176]
Dai X, Yan J, Fu X, et al. Aspirin inhibits cancer metastasis and angiogenesis via targeting heparanase. Clin Cancer Res 2017; 23(20): 6267-78.
[http://dx.doi.org/10.1158/1078-0432.CCR-17-0242] [PMID: 28710312]
[177]
Algra AM, Rothwell PM. Effects of regular aspirin on long-term cancer incidence and metastasis: a systematic comparison of evidence from observational studies versus randomised trials. Lancet Oncol 2012; 13(5): 518-27.
[http://dx.doi.org/10.1016/S1470-2045(12)70112-2] [PMID: 22440112]
[178]
Allen KA, Brown RL, Norris G, Tyler PC, Watt DK, Zubkova OV. Syntheses of novel azasugar-containing mimics of heparan sulfate fragments as potential heparanase inhibitors. Carbohydr Res 2010; 345(13): 1831-41.
[http://dx.doi.org/10.1016/j.carres.2010.05.032] [PMID: 20630499]
[179]
Guglielmelli T, Bringhen S, Palumbo A. Update on the use of defibrotide. Expert Opin Biol Ther 2012; 12(3): 353-61.
[http://dx.doi.org/10.1517/14712598.2012.657623] [PMID: 22283742]
[180]
Mitsiades CS, Rouleau C, Echart C, et al. Preclinical studies in support of defibrotide for the treatment of multiple myeloma and other neoplasias. Clin Cancer Res 2009; 15(4): 1210-21.
[http://dx.doi.org/10.1158/1078-0432.CCR-08-1270] [PMID: 19228727]
[181]
Zhou G, Wilson G, Hebbard L, et al. Aptamers: A promising chemical antibody for cancer therapy. Oncotarget 2016; 7(12): 13446-63.
[http://dx.doi.org/10.18632/oncotarget.7178] [PMID: 26863567]
[182]
Mongelard F, Bouvet P. AS-1411, a guanosine-rich oligonucleotide aptamer targeting nucleolin for the potential treatment of cancer, including acute myeloid leukemia. Curr Opin Mol Ther 2010; 12(1): 107-14.
[PMID: 20140822]
[183]
Simmons SC, McKenzie EA, Harris LK, et al. Development of novel single-stranded nucleic acid aptamers against the pro-angiogenic and metastatic enzyme heparanase (HPSE1). PLoS One 2012; 7(6)e37938
[http://dx.doi.org/10.1371/journal.pone.0037938] [PMID: 22719856]
[184]
Simmons SC, Jämsä H, Silva D, et al. Anti-heparanase aptamers as potential diagnostic and therapeutic agents for oral cancer. PLoS One 2014; 9(10)e96846
[http://dx.doi.org/10.1371/journal.pone.0096846] [PMID: 25295847]
[185]
Väyrynen O, Piippo M, Jämsä H, et al. Effects of ionizing radiation and HPSE1 inhibition on the invasion of oral tongue carcinoma cells on human extracellular matrices in vitro. Exp Cell Res 2018; 371(1): 151-61.
[http://dx.doi.org/10.1016/j.yexcr.2018.08.005] [PMID: 30086306]
[186]
Maimaitiyiming Y, Hong F, Yang C, Naranmandura H. Novel insights into the role of aptamers in the fight against cancer. J Cancer Res Clin Oncol 2019; 145(4): 797-810.
[http://dx.doi.org/10.1007/s00432-019-02882-7] [PMID: 30830295]
[187]
Weissmann M, Arvatz G, Horowitz N, et al. Heparanase-neutralizing antibodies attenuate lymphoma tumor growth and metastasis. Proc Natl Acad Sci USA 2016; 113(3): 704-9.
[http://dx.doi.org/10.1073/pnas.1519453113] [PMID: 26729870]
[188]
Barash U, Arvatz G, Farfara R, et al. Clinical significance of heparanase splice variant (t5) in renal cell carcinoma: evaluation by a novel t5-specific monoclonal antibody. PLoS One 2012; 7(12)e51494
[http://dx.doi.org/10.1371/journal.pone.0051494] [PMID: 23251556]
[189]
Lillelund VH, Jensen HH, Liang X, Bols M. Recent developments of transition-state analogue glycosidase inhibitors of non-natural product origin. Chem Rev 2002; 102(2): 515-53.
[http://dx.doi.org/10.1021/cr000433k] [PMID: 11841253]
[190]
Nishimura Y. Gem-diamine 1-N-iminosugars as versatile glycomimetics: synthesis, biological activity and therapeutic potential. J Antibiot (Tokyo) 2009; 62(8): 407-23.
[http://dx.doi.org/10.1038/ja.2009.53] [PMID: 19575039]
[191]
Sue M, Higashi N, Shida H, et al. An iminosugar-based heparanase inhibitor heparastatin (SF4) suppresses infiltration of neutrophils and monocytes into inflamed dorsal air pouches. Int Immunopharmacol 2016; 35: 15-21.
[http://dx.doi.org/10.1016/j.intimp.2016.03.017] [PMID: 27015605]
[193]
Koganti R, Suryawanshi R, Shukla D. Heparanase, cell signaling, and viral infections. Cell Mol Life Sci 2020; 77(24): 5059-77.
[http://dx.doi.org/10.1007/s00018-020-03559-y] [PMID: 32462405]

Rights & Permissions Print Export Cite as
© 2022 Bentham Science Publishers | Privacy Policy