Glycosaminoglycans in cancer treatment

Thrombosis Research

Volumn 133, Issue SUPPL. 2, 2014, Pages

  Belting, Mattias ^a,b  

^a LUND UNIVERSITY   (Sweden)

^b Section of Oncology   (Sweden)

Author keywords

Cancer; Coagulation; Heparan sulfate; Heparin; Proteoglycan

Indexed keywords

BIOLOGICAL MARKER; CARBOPLATIN; CISPLATIN; COUMARIN; DECORIN; ETOPOSIDE; FIBROBLAST GROWTH FACTOR 2; GLYCOSAMINOGLYCAN; HEPARIN; LOW MOLECULAR WEIGHT HEPARIN; MESSENGER RNA; MICRORNA; MUPARFOSTAT; PROTEINASE ACTIVATED RECEPTOR 2; PROTEOGLYCAN; SOMATOMEDIN C RECEPTOR; THROMBOPLASTIN; HEPARAN SULFATE;

ANGIOGENESIS; ANTICOAGULATION; ARTICLE; BLOOD CLOTTING; CANCER CELL; CANCER COMBINATION CHEMOTHERAPY; CANCER MORTALITY; CANCER PROGNOSIS; CANCER SURVIVAL; CANCER THERAPY; COLORECTAL CANCER; DEEP VEIN THROMBOSIS; DRUG EFFICACY; HUMAN; LIFE EXPECTANCY; LIVER CELL CARCINOMA; LUNG CANCER; LUNG SMALL CELL CANCER; META ANALYSIS (TOPIC); METASTASIS; OVERALL SURVIVAL; PANCREAS CANCER; PERSONALIZED MEDICINE; PHASE 2 CLINICAL TRIAL (TOPIC); PHENOTYPE; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; PROTEIN TARGETING; RANDOMIZED CONTROLLED TRIAL (TOPIC); STROMA CELL; SURVIVAL RATE; THROMBOEMBOLISM; TUMOR INVASION; TUMOR MICROENVIRONMENT; VENOUS THROMBOEMBOLISM; DISEASE COURSE; METABOLISM; NEOPLASMS; PHYSIOLOGY;

BIOLOGICAL MARKERS; BLOOD COAGULATION; DISEASE PROGRESSION; GLYCOSAMINOGLYCANS; HEPARITIN SULFATE; HUMANS; NEOPLASMS;

EID: 84901399018     PISSN: 00493848     EISSN: 18792472     Source Type: Journal    
DOI: 10.1016/S0049-3848(14)50016-3     Document Type: Article

References (79)

1. D. Hanahan, and R.A. Weinberg Hallmarks of cancer: The next generation Cell 144 2011 646 674
2. H. Qazi, R. Palomino, Z.D. Shi, L.L. Munn, and J.M. Tarbell Cancer cell glycocalyx [30 mediates mechanotransduction and flow-regulated invasion Integr Biol (Camb) 5 2013 1334 1343
3. J. Pouyssegur, F. Dayan, and N.M. Mazure Hypoxia signalling in cancer and approaches to enforce tumour regression Nature 441 2006 437 443 (Pubitemid 44050138)
4. M. Belting, J. Ahamed, and W. Ruf Signalling of the tissue factor coagulation pathway in angiogenesis and cancer Arterioscler Thromb Vasc Biol 25 2005 1545 1550 (Pubitemid 41098920)
5. R.D. Sanderson Heparan sulfate proteoglycans in invasion and metastasis Semin Cell Dev Biol 12 2001 89 98
6. M. Belting Heparan sulfate proteoglycan as a plasma membrane carrier Trends Biochem Sci 28 2003 145 151 (Pubitemid 36293852)
7. M.M. Fuster, and J.D. Esko The sweet and sour of cancer: glycans as novel therapeutic targets Nat Rev Cancer 5 2005 526 542 (Pubitemid 40942829)
8. R.V. Iozzo, and R.D. Sanderson Proteoglycans in cancer biology, tumour microenvironment and angiogenesis J Cell Mol Med 15 2011 1013 1031
9. U. Lindahl, and L. Kjellén Pathophysiology of heparan sulphate: many diseases, few drugs J Intern Med 273 2013 555 571
10. A. Ori, M.C. Wilkinson, and D.G. Fernig A systems biology approach for the investigation of the heparin/heparan sulfate interactome J Biol Chem 286 2011 19892 19904
11. R.V. Iozzo, J.J. Zoeller, and A. Nystrom Basement membrane proteoglycans: modulators Par Excellence of cancer growth and angiogenesis Mol Cells 27 2009 503 513
12. T. Manon-Jensen, Y. Itoh, and J.R. Couchman Proteoglycans in health and disease: the multiple roles of syndecan shedding Febs J 277 2010 3876 3889
13. L.A. Fransson, M. Belting, F. Cheng, M. Jonsson, K. Mani, and S. Sandgren Novel aspects of glypican glycobiology Cell Mol Life Sci 61 2004 1016 1024 (Pubitemid 38656128)
14. E.J. Nam, and P.W. Park Shedding of cell membrane-bound proteoglycans Methods Mol Biol 836 2012 291 305
15. I. Vlodavsky, P. Beckhove, I. Lerner, C. Pisano, A. Meirovitz, N. Ilan, and M. Elkin Significance of heparanase in cancer and inflammation Cancer Microenviron 5 2012 115 132
16. M. Morimoto-Tomita, K. Uchimura, Z. Werb, S. Hemmerich, and S.D. Rosen Cloning and characterization of two extracellular heparin-degrading endosulfatases in mice and humans J Biol Chem 277 2002 49175 49185 (Pubitemid 36014346)
17. J. Folkman, R. Langer, R.J. Linhardt, C. Haudenschild, and S. Taylor Angiogenesis inhibition and tumor regression caused by heparin or a heparin fragment in the presence of cortisone Science 221 1983 719 725 (Pubitemid 13030626)
18. M.M. Fuster, L. Wang, J. Castagnola, L. Sikora, K. Reddi, and P.H. Lee et al. Genetic alteration of endothelial heparan sulfate selectively inhibits tumor angiogenesis J Cell Biol 177 2007 539 549 (Pubitemid 46718281)
19. J. Li, N.W. Shworak, and M. Simons Increased responsiveness of hypoxic endothelial cells to FGF2 is mediated by HIF-1alpha-dependent regulation of enzymes involved in synthesis of heparan sulfate FGF2-binding sites J Cell Sci 115 2002 1951 1959 (Pubitemid 34567256)
20. C. Ruhrberg, H. Gerhardt, M. Golding, R. Watson, S. Ioannidou, and H. Fujisawa et al. Spatially restricted patterning cues provided by heparin-binding VEGF-A control blood vessel branching morphogenesis Genes Dev 16 2002 2684 2698
21. P. Lindblom, H. Gerhardt, S. Liebner, A. Abramsson, M. Enge, and M. Hellstrom et al. Endothelial PDGF-B retention is required for proper investment of pericytes in the microvessel wall Genes Dev 17 2003 1835 1840 (Pubitemid 36944561)
22. Z. Kasza, P. Fredlund Fuchs, C. Tamm, A.S. Eriksson, and P. O'Callaghan et al. MicroRNA-24 suppression of N-deacetylase/N-sulfotransferase-1 (NDST1) reduces endothelial cell responsiveness to vascular endothelial growth factor A (VEGFA) J Biol Chem 288 2013 25956 25963
23. C. Ferreras, G. Rushton, C.L. Cole, M. Babur, B.A. Telfer, and T.H. Van Kuppevelt et al. Endothelial heparan sulfate 6-o-sulfation levels regulate angiogenic responses of endothelial cells to fibroblast growth factor 2 and vascular endothelial growth factor J Biol Chem 287 2012 36132 36146
24. B. Gorsi, F. Liu, X. Ma, T.J. Chico, A. Shrinivasan, and K.L. Kramer et al. The heparan sulfate editing enzyme Sulf1 plays a novel role in zebrafish VegfA mediated arterial venous identity Angiogenesis 17 2014 77 91
25. D. Bonneh-Barkay, M. Shlissel, B. Berman, E. Shaoul, A. Admon, and I. Vlodavsky et al. Identification of glypican as a dual modulator of the biological activity of fibroblast growth factors J Biol Chem 272 1997 12415 12421 (Pubitemid 27203329)
26. D. Qiao, K. Meyer, C. Mundhenke, S.A. Drew, and A. Friedl Heparan sulfate proteoglycans as regulators of fibroblast growth factor-2 signaling in brain endothelial cells. Specific role for glypican-1 in glioma angiogenesis J Biol Chem 278 2003 16045 16053 (Pubitemid 36799725)
27. S. Gengrinovitch, B. Berman, G. David, L. Witte, G. Neufeld, and D. Ron Glypican-1 is a VEGF165 binding proteoglycan that acts as an extracellular chaperone for VEGF165 J Biol Chem 274 1999 10816 10822
28. S.A. Karumanchi, V. Jha, R. Ramchandran, A. Karihaloo, L. Tsiokas, and B. Chan et al. Cell surface glypicans are low-affinity endostatin receptors Mol Cell 7 2001 811 822 (Pubitemid 32436441)
29. F. Corti, F. Finetti, M. Ziche, and M. Simons The syndecan-4/protein kinase Cα pathway mediates prostaglandin E2-induced extracellular regulated kinase (ERK) activation in endothelial cells and angiogenesis in vivo J Biol Chem 288 2013 12712 12721
30. D.M. Beauvais, and A.C. Rapraeger Syndecan-1 couples the insulin-like growth factor-1 receptor to inside-out integrin activation J Cell Sci 123 2010 3796 3807
31. D.M. Beauvais, B.J. Ell, A.R. McWhorter, and A.C. Rapraeger Syndecan-1 regulates alphavbeta3 and alphavbeta5 integrin activation during angiogenesis and is blocked by synstatin, a novel peptide inhibitor J Exp Med 206 2009 691 705
32. A. Purushothaman, T. Uyama, F. Kobayashi, S. Yamada, K. Sugahara, A.C. Rapraeger, and R.D. Sanderson Heparanase-enhanced shedding of syndecan-1 by myeloma cells promotes endothelial invasion and angiogenesis Blood 115 2010 2449 2457
33. G. Su, S.A. Blaine, D. Qiao, and A. Friedl Shedding of syndecan 1 by stromal fibroblasts stimulates human breast cancer cell proliferation via FGF2 activation J Biol Chem 282 2007 14906 14915 (Pubitemid 47093352)
34. M. Elkin, N. Ilan, R. Ishai-Michaeli, Y. Friedmann, O. Papo, I. Pecker, and I. Vlodavsky Heparanase as mediator of angiogenesis: mode of action Faseb J 15 2001 1661 1663
35. H.C. Christianson, T.H. Van Kuppevelt, and M. Belting ScFv anti-heparan sulfate antibodies unexpectedly activate endothelial and cancer cells through p38 MAPK: implications for antibody-based targeting of heparan sulfate proteoglycans in cancer PLoS One 7 2012 e49092
36. A. Wittrup, S.H. Zhang, G.B. ten Dam, T.H. Van Kuppevelt, P. Bengtson, and M. Johansson et al. ScFv antibody-induced translocation of cell-surface heparan sulfate proteoglycan to endocytic vesicles: evidence for heparan sulfate epitope specificity and role of both syndecan and glypican J Biol Chem 284 2009 32959 32967
37. E. Hsia, T.P. Richardson, and M.A. Nugent Nuclear localization of basic fibroblast growth factor is mediated by heparan sulfate proteoglycans through protein kinase C signaling J Cell Biochem 88 2003 1214 1225 (Pubitemid 36397459)
38. Elfenbein A, Lanahan A, Zhou TX, Yamasaki A, Tkachenko E, Matsuda M, Simons M. Syndecan 4 regulates FGFR1 signaling in endothelial cells by directing macropinocytosis. Sci Signal 2012:5:ra36.
39. J.W. Blom, C.J. Doggen, S. Osanto, and F.R. Rosendaal Malignancies, prothrombotic mutations, and the risk of venous thrombosis Jama 293 2005 715 722 (Pubitemid 40216041)
40. J. Rak, J.L. Yu, J. Luyendyk, and N. Mackman Oncogenes, trousseau syndrome, and cancer-related changes in the coagulome of mice and humans Cancer Res 66 2006 10643 10646 (Pubitemid 44876956)
41. K.J. Svensson, P. Kucharzewska, H.C. Christianson, S. Sköld, T. Löfstedt, and M.C. Johansson et al. Hypoxia triggers a proangiogenic pathway involving cancer cell microvesicles and PAR-2-mediated heparin-binding EGF signaling in endothelial cells Proceedings of the National Academy of Sciences USA 108 2011 13147 13152
42. L. Rydén, D. Grabau, F. Schaffner, P.E. Jönsson, W. Ruf, and M. Belting Evidence for tissue factor phosphorylation and its correlation with protease-activated receptor expression and the prognosis of primary breast cancer Int J Cancer 126 2010 2330 2340
43. S. Koizume, M.S. Jin, E. Miyagi, F. Hirahara, Y. Nakamura, and J.H. Piao et al. Activation of cancer cell migration and invasion by ectopic synthesis of coagulation factor VII Cancer Res 66 2006 9453 9460 (Pubitemid 44623642)
44. B.F. Liebersbach, and R.D. Sanderson Expression of syndecan 1 inhibits cell invasion into type I collagen J Biol Chem 269 1994 20013 20019 (Pubitemid 24250921)
45. M. Kato, S. Saunders, H. Nguyen, and M. Bernfield Loss of cell surface syndecan-1 causes epithelia to transform into anchorage-independent mesenchyme-like cells Mol Biol Cell 6 1995 559 576
46. Y.B. Khotskaya, Y. Dai, J.P. Ritchie, V. MacLeod, Y. Yang, K. Zinn, and R.D. Sanderson Syndecan-1 is required for robust growth, vascularization, and metastasis of myeloma tumors in vivo J Biol Chem 284 2009 26085 26095
47. T. Neill, L. Schaefer, and R.V. Iozzo Decorin: A guardian from the matrix Am J Pathol 181 2012 380 387
48. Y. Yamaguchi, D.M. Mann, and E. Ruoslahti Negative regulation of transforming growth factor-beta by the proteoglycan decorin Nature 346 1990 281 284
49. Y. Wegrowski, and F.X. Maquart Chondroitin sulfate proteoglycans in tumor progression Adv Pharmacol 53 2006 297 321
50. S. Yamada, and K. Sugahara Potential therapeutic application of chondroitin sulfate/dermatan sulfate Curr Drug Discov Technol 5 2008 289 301
51. K.J. Svensson, H.C. Christianson, P. Kucharzewska, V. Fagerström, L. Lundstedt, and S. Borgquist et al. Chondroitin sulfate expression predicts poor outcome in breast cancer Int J Oncol 39 2011 1421 1428
52. C. Ricciardelli, K. Mayne, P.J. Sykes, W.A. Raymond, K. McCaul, and V.R. Marshall et al. Elevated stromal chondroitin sulfate glycosaminoglycan predicts progression in early-stage prostate cancer Clin Cancer Res 3 1997 983 992 (Pubitemid 27252948)
53. C. Ricciardelli, A.J. Sakko, M.P. Ween, D.L. Russell, and D.J. Horsfall The biological role and regulation of versican levels in cancer Cancer Metastasis Rev 28 2009 233 245
54. I.J. Edwards Proteoglycans in prostate cancer Nat Rev Urol 9 2012 196 206
55. E.M. Denholm, Y.Q. Lin, and P.J. Silver Anti-tumor activities of chondroitinase AC and chondroitinase B: inhibition of angiogenesis, proliferation and invasion Eur J Pharmacol 416 2001 213 221 (Pubitemid 32274248)
56. F. Li, G.B. Ten Dam, S. Murugan, S. Yamada, T. Hashiguchi, and S. Mizumoto et al. Involvement of highly sulfated chondroitin sulfate in the metastasis of the Lewis lung carcinoma cells J Biol Chem 283 2008 34294 34304
57. Murugan S. Basappa, K.N. Sugahara, C.M. Lee, G.B. ten Dam, and T.H. Van Kuppevelt Involvement of chondroitin sulfate E in the liver tumor focal formation of murine osteosarcoma cells Glycobiology 19 2009 735 742
58. M.A. Thelin, K.J. Svensson, X. Shi, M. Bagher, J. Axelsson, and A. Isinger-Ekstrand et al. Dermatan sulfate is involved in the tumorigenic properties of esophagus squamous cell carcinoma Cancer Res 72 2012 1943 1952
59. S.A. Mousa, and L. Petersen Anti-cancer properties of low molecular-weight heparin: preclinical evidence Thromb Haemost 102 2009 258 267
60. K.D. Johnstone, T. Karoli, L. Liu, K. Dredge, E. Copeman, and C.P. Li et al. Synthesis and biological evaluation of polysulfated oligosaccharide glycosides as inhibitors of angiogenesis and tumor growth J Med Chem 53 2010 1686 1699
61. K. Mani, M. Belting, U. Ellervik, N. Falk, G. Svensson, and S. Sandgren et al. Tumor attenuation by 2(6-hydroxynaphthyl)-beta-D-xylopyranoside requires priming of heparan sulfate and nuclear targeting of the products Glycobiology 14 2004 387 397 (Pubitemid 38750143)
62. K. Dredge, E. Hammond, P. Handley, T.J. Gonda, M.T. Smith, and C. Vincent et al. PG545, a dual heparanase and angiogenesis inhibitor, induces potent anti-tumour and antimetastatic efficacy in preclinical models Br J Cancer 104 2011 635 642
63. J.P. Ritchie, V.C. Ramani, Y. Ren, A. Naggi, G. Torri, and B. Casu et al. SST0001, a chemically modified heparin, inhibits myeloma growth and angiogenesis via disruption of the heparanase/syndecan-1 axis Clin Cancer Res 171 2011 382 393
64. K. Mani, S. Sandgren, J. Lilja, F. Cheng, K. Svensson, L. Persson, and M. Belting HIV-Tat protein transduction domain specifically attenuates growth of polyamine deprived tumor cells Mol Cancer Ther 6 2007 782 788 (Pubitemid 46332479)
65. M.M. Hossain, T. Hosono-Fukao, R. Tang, N. Sugaya, T.H. Van Kuppevelt, and G.J. Jenniskens et al. Direct detection of HSulf-1 and HSulf-2 activities on extracellular heparan sulfate and their inhibition by PI-88 Glycobiology 20 2010 175 186
66. C.J. Liu, P.H. Lee, D.Y. Lin, C.C. Wu, L.B. Jeng, and P.W. Lin et al. Heparanase inhibitor PI-88 as adjuvant therapy for hepatocellular carcinoma after curative resection: A randomized phase II trial for safety and optimal dosage J Hepatol 50 2009 958 968
67. T.H. Van Kuppevelt, M.A. Dennissen, W.J. Van Venrooij, R.M. Hoet, and J.H. Veerkamp Generation and application of type-specific anti-heparan sulfate antibodies using phage display technology. Further evidence for heparan sulfate heterogeneity in the kidney J Biol Chem 273 1998 12960 12966 (Pubitemid 28246857)
68. J.E. Welch, P. Bengtson, K. Svensson, A. Wittrup, G.J. Jenniskens, and G.B. Ten Dam et al. Single chain fragment anti-heparan sulfate antibody targets the polyamine transport system and attenuates polyamine-dependent cell proliferation Int J Oncol 32 2008 749 756 (Pubitemid 351780585)
69. L. Borsig, R. Wong, J. Feramisco, D.R. Nadeau, N.M. Varki, and A. Varki Heparin and cancer revisited: mechanistic connections involving platelets, P-selectin, carcinoma mucins, and tumor metastasis Proc Natl Acad Sci USA 98 2001 3352 3357 (Pubitemid 32220849)
70. G. Bendas, and L. Borsig Cancer cell adhesion and metastasis: selectins, integrins, and the inhibitory potential of heparins Int J Cell Biol 2012 2012 676731
71. M.K. Gould, A.D. Dembitzer, R.L. Doyle, T.J. Hastie, and A.M. Garber Low-molecular-weight heparins compared with unfractionated heparin for treatment of acute deep venous thrombosis. A meta-analysis of randomized, controlled trials Ann Intern Med 130 1999 800 809 (Pubitemid 29231148)
72. A. Lee, F.R. Rickles, J.A. Julian, M. Gent, R.I. Baker, and C. Bowden et al. Randomized Comparison of LMWH and Coumarin Derivatives on the Survival of Patients with Cancer and Venous Thromboembolism J Clin Oncol 23 2005 2123 2129 (Pubitemid 46218703)
73. C.P. Klerk, S.M. Smorenburg, H.M. Otten, A.W. Lensing, M.H. Prins, and F. Piovella et al. The Effect of LMWH on Survival in Patients With Advanced Malignancy J Clin Oncol 23 2005 2130 2135 (Pubitemid 46218704)
74. A.K. Kakkar, M.N. Levine, Z. Kadziola, N.R. Lemoine, V. Low, and H.K. Patel et al. Low molecular weight heparin, therapy with dalteparin, and survival in advanced cancer: the fragmin advanced malignancy outcome study (FAMOUS) J Clin Oncol 22 2004 1944 1948 (Pubitemid 41095187)
75. B. Lebeau, C. Chastang, J.M. Brechot, F. Capron, B. Dautzenberg, and C. Delaisements et al. Subcutaneous heparin treatment increases survival in small cell lung cancer. "Petites Cellules" Group Cancer 74 1994 38 45 (Pubitemid 24187607)
76. M. Altinbas, H.S. Coskun, O. Er, M. Ozkan, B. Eser, and A. Unal et al. A randomized clinical trial of combination chemotherapy with and without low-molecular-weight heparin in small cell lung cancer J Thromb Haemost 2 2004 1266 1271 (Pubitemid 40186120)
77. B. Lebeau, M. Baud, M.J. Masanes, M. Febvre, T. Mokhtari, and C. Chouaïd Optimization of Small-Cell Lung Cancer Chemotherapy with Heparin: A Comprehensive Retrospective Study of 239 Patients Treated in a Single Specialized Center Chemotherapy 57 2011 253 258
78. Parenteral anticoagulation in patients with cancer who have no therapeutic or prophylactic indication for anticoagulation (Review). The Cochrane Collaboration. 2011 John Wiley & Sons, Ltd.
79. J. Zhang, Y.L. Zhang, K.X. Ma, and J.M. Qu Efficacy and safety of adjunctive anticoagulation in patients with lung cancer without indication for anticoagulants: A systematic review and meta-analysis Thorax 68 2013 442 450