Heparan sulfate proteoglycans and heparin regulate melanoma cell functions

Biochimica et Biophysica Acta - General Subjects

Volumn 1840, Issue 8, 2014, Pages 2471-2481

  Nikitovic, D ^a   Mytilinaiou, M ^a   Berdiaki, Ai ^a   Karamanos, N K ^b   Tzanakakis, G N ^a  

^a UNIVERSITY OF CRETE   (Greece)

^b UNIVERSITY OF CRETE   (Greece)

Author keywords

Cell function; Heparan sulfate proteoglycan; Heparin; Melanoma

Indexed keywords

HEPARANASE; HEPARIN; LOW MOLECULAR WEIGHT HEPARIN; MELANOMA VACCINE; PROTEOHEPARAN SULFATE; RIBOZYME; SMALL INTERFERING RNA; SYNDECAN; TINZAPARIN;

ANTIANGIOGENIC ACTIVITY; ANTICOAGULATION; CANCER INHIBITION; CARCINOGENESIS; CELL ADHESION; CELL MIGRATION; CELLULAR DISTRIBUTION; COMPLEMENT CLASSICAL PATHWAY; EXTRACELLULAR MATRIX; GENE MUTATION; HUMAN; MALIGNANT TRANSFORMATION; MELANOMA; MELANOMA B16; MELANOMA CELL; METASTASIS INHIBITION; MOLECULARLY TARGETED THERAPY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; THROMBOEMBOLISM; TUMOR GROWTH; TUMOR INVASION; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION; VENOUS THROMBOEMBOLISM;

CELL FUNCTION; HEPARAN SULFATE PROTEOGLYCAN; HEPARIN; MELANOMA;

ANIMALS; DISEASE PROGRESSION; EXTRACELLULAR MATRIX; HEPARAN SULFATE PROTEOGLYCANS; HEPARIN; HUMANS; MELANOMA; SIGNAL TRANSDUCTION;

EID: 84903549150     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2014.01.031     Document Type: Review

References (182)

1. C.L. O'Bryant, and J.C. Poust Melanoma J.T. DiPiro, R.L. Talbert, G.C. Yee, Pharmacotherapy: A Pathophysiologic Approach eighth ed. 2011 McGraw-Hill Medical New York
2. J. Villanueva, and M. Herlyn Melanoma and the tumor microenvironment Curr. Oncol. Rep. 10 2008 439 446
3. R. Sawaya, B.L. Ligon, A.K. Bindal, R.K. Bindal, and K.R. Hess Surgical treatment of metastatic brain tumors J. Neurooncol. 27 1996 269 277
4. R. Soffietti, R. Ruda, and R. Mutani Management of brain metastases J. Neurol. 249 2002 1357 1369
5. A.J. Miller, and M.C. Mihm Jr. Melanoma N. Engl. J. Med. 355 2006 51 65
6. A. Jemal, R. Siegel, J. Xu, and E. Ward Cancer statistics, 2010 CA Cancer J. Clin. 60 2010 277 300
7. http://www.cdc.gov/cancer/skin/statistics/ United States Cancer Statistics: 1999-2009 Incidence and Mortality Web-based Report October 23 2013 Department of Health and Human Services, Centers for Disease Control and Prevention, and National Cancer Institute Atlanta (GA)
8. A.C. Geller, D.R. Miller, G.D. Annas, M.F. Demierre, B.A. Gilchrest, and H.K. Koh Melanoma incidence and mortality among US whites, 1969-1999 JAMA 288 2002 1719 1720
9. J.M. Kirkwood, M.H. Strawderman, M.S. Ernstoff, T.J. Smith, E.C. Borden, and R.H. Blum Interferon alfa-2b adjuvant therapy of high-risk resected cutaneous melanoma: the Eastern Cooperative Oncology Group Trial EST 1684 J. Clin. Oncol. 14 1996 7 17
10. B.F. Cole, R.D. Gelber, J.M. Kirkwood, A. Goldhirsch, E. Barylak, and E. Borden Quality-of-life-adjusted survival analysis of interferon alfa-2b adjuvant treatment of high-risk resected cutaneous melanoma: an Eastern Cooperative Oncology Group study J. Clin. Oncol. 14 1996 2666 2673
11. M.B. Atkins, J. Hsu, S. Lee, G.I. Cohen, L.E. Flaherty, J.A. Sosman, V.K. Sondak, and J.M. Kirkwood Phase III trial comparing concurrent biochemotherapy with cisplatin, vinblastine, dacarbazine, interleukin-2, and interferon alfa-2b with cisplatin, vinblastine, and dacarbazine alone in patients with metastatic malignant melanoma (E3695): a trial coordinated by the Eastern Cooperative Oncology Group J. Clin. Oncol. 26 2008 5748 5754
12. K.S. Peggs, and S.A. Quezada Ipilimumab: attenuation of an inhibitory immune checkpoint improves survival in metastatic melanoma Expert Rev. Anticancer Ther. 10 2010 1697 1701
13. M.B. Atkins The role of cytotoxic chemotherapeutic agents either alone or in combination with biological response modifiers J.K. Kirkwood, M. Dekker, Molecular Diagnosis, Prevention & Therapy of Melanoma 1997 Marcel Dekker New York 219 251
14. A.N. Houghton, S. Legha, and D.F. Bajorin Balch Houghton Milton Chemotherapy for metastatic melanoma 1992 J.B. Lippincott Company Philadelphia 498 508
15. K. van den Hurk, H.E. Niessen, J. Veeck, J.J. van den Oord, M.A. van Steensel, A. Zur Hausen, M. van Engeland, and V.J. Winnepenninckx Genetics and epigenetics of cutaneous malignant melanoma: a concert out of tune Biochim. Biophys. Acta 1826 2012 89 102
16. K. Dutton-Regester, and N.K. Hayward Whole genome and exome sequencing of melanoma: a step toward personalized targeted therapy Adv. Pharmacol. 65 2012 399 435
17. M. Herlyn, and K. Satyamoorthy Activated ras. Yet another player in melanoma? Am. J. Pathol. 149 1996 739 744
18. L.A. Fecher, R.K. Amaravadi, and K.T. Flaherty The MAPK pathway in melanoma Curr. Opin. Oncol. 20 2008 183 189
19. M. Cully, H. You, A.J. Levine, and T.W. Mak Beyond PTEN mutations: the PI3K pathway as an integrator of multiple inputs during tumorigenesis Nat. Rev. Cancer 6 2006 184 192
20. F. Meier, B. Schittek, S. Busch, C. Garbe, K. Smalley, K. Satyamoorthy, G. Li, and M. Herlyn The RAS/RAF/MEK/ERK and PI3K/AKT signaling pathways present molecular targets for the effective treatment of advanced melanoma Front. Biosci. 10 2005 2986 3001
21. H. Wu, V. Goel, and F.G. Haluska PTEN signaling pathways in melanoma Oncogene 22 2003 3113 3122
22. R.R. Braeuer, M. Zigler, G.J. Villares, A.S. Dobroff, and M. Bar-Eli Transcriptional control of melanoma metastasis: the importance of the tumor microenvironment Semin. Cancer Biol. 21 2011 83 88
23. J.A. Curtin, K. Busam, D. Pinkel, and B.C. Bastian Somatic activation of KIT in distinct subtypes of melanoma J. Clin. Oncol. 24 2006 4340 4346
24. D. Hubmacher, and S.S. Apte The biology of the extracellular matrix: novel insights Curr. Opin. Rheumatol. 25 2013 65 70
25. T. Bogenrieder, and M. Herlyn Cell-surface proteolysis, growth factor activation and intercellular communication in the progression of melanoma Crit. Rev. Oncol. Hematol. 44 2002 1 15
26. B. Leitinger Transmembrane collagen receptors Annu. Rev. Cell Dev. Biol. 27 2011 265 290
27. J.J. Doyle, E.E. Gerber, and H.C. Dietz Matrix-dependent perturbation of TGFbeta signaling and disease FEBS Lett. 586 2012 2003 2015
28. M. Bernfield, M. Gotte, P.W. Park, O. Reizes, M.L. Fitzgerald, J. Lincecum, and M. Zako Functions of cell surface heparan sulfate proteoglycans Annu. Rev. Biochem. 68 1999 729 777
29. N. Perrimon, and M. Bernfield Specificities of heparan sulphate proteoglycans in developmental processes Nature 404 2000 725 728
30. M.A. Skidmore, S.E. Guimond, T.R. Rudd, D.G. Fernig, J.E. Turnbull, and E.A. Yates The activities of heparan sulfate and its analogue heparin are dictated by biosynthesis, sequence, and conformation Connect. Tissue Res. 49 2008 140 144
31. J.D. Esko, and S.B. Selleck Order out of chaos: assembly of ligand binding sites in heparan sulfate Annu. Rev. Biochem. 71 2002 435 471
32. J.T. Gallagher, and A. Walker Molecular distinctions between heparan sulphate and heparin. Analysis of sulphation patterns indicates that heparan sulphate and heparin are separate families of N-sulphated polysaccharides Biochem. J. 230 1985 665 674
33. D.J. Carey Syndecans: multifunctional cell-surface co-receptors Biochem. J. 327 1997 1 16
34. C. Kirn-Safran, M.C. Farach-Carson, and D.D. Carson Multifunctionality of extracellular and cell surface heparan sulfate proteoglycans Cell. Mol. Life Sci. 66 2009 3421 3434
35. B. Sharma, M. Handler, I. Eichstetter, J.M. Whitelock, M.A. Nugent, and R.V. Iozzo Antisense targeting of perlecan blocks tumor growth and angiogenesis in vivo J. Clin. Invest. 102 1998 1599 1608
36. R. Adatia, A. Albini, S. Carlone, D. Giunciuglio, R. Benelli, L. Santi, and D.M. Noonan Suppression of invasive behavior of melanoma cells by stable expression of anti-sense perlecan cDNA Ann. Oncol. 8 1997 1257 1261
37. K. Elenius, and M. Jalkanen Function of the syndecans - a family of cell surface proteoglycans J. Cell Sci. 107 1994 2975 2982
38. J. Schlessinger, I. Lax, and M. Lemmon Regulation of growth factor activation by proteoglycans: what is the role of the low affinity receptors? Cell 83 1995 357 360
39. S. Tumova, A. Woods, and J.R. Couchman Heparan sulfate proteoglycans on the cell surface: versatile coordinators of cellular functions Int. J. Biochem. Cell Biol. 32 2000 269 288
40. H.H. Song, and J. Filmus The role of glypicans in mammalian development Biochim. Biophys. Acta 1573 2002 241 246
41. D.M. Beauvais, and A.C. Rapraeger Syndecans in tumor cell adhesion and signaling Reprod. Biol. Endocrinol. 2 2004 3 15
42. E. Tkachenko, J.M. Rhodes, and M. Simons Syndecans: new kids on the signaling block Circ. Res. 96 2005 488 500
43. J.J. Grootjans, P. Zimmermann, G. Reekmans, A. Smets, G. Degeest, J. Durr, and G. David Syntenin, a PDZ protein that binds syndecan cytoplasmic domains Proc. Natl. Acad. Sci. U. S. A. 94 1997 13683 13688
44. P. Zimmermann, and G. David The syndecans, tuners of transmembrane signaling FASEB J. 13 Suppl. 1999 S91 S100
45. R. Chakravarti, V. Sapountzi, and J.C. Adams Functional role of syndecan-1 cytoplasmic V region in lamellipodial spreading, actin bundling, and cell migration Mol. Biol. Cell 16 2005 3678 3691
46. C.M. Klass, J.R. Couchman, and A. Woods Control of extracellular matrix assembly by syndecan-2 proteoglycan J. Cell Sci. 113 2000 493 506
47. S.T. Lim, R.L. Longley, J.R. Couchman, and A. Woods Direct binding of syndecan-4 cytoplasmic domain to the catalytic domain of protein kinase C alpha (PKC alpha) increases focal adhesion localization of PKC alpha J. Biol. Chem. 278 2003 13795 13802
48. 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
49. F. Zong, E. Fthenou, F. Mundt, T. Szatmari, I. Kovalszky, L. Szilak, D. Brodin, G. Tzanakakis, A. Hjerpe, and K. Dobra Specific syndecan-1 domains regulate mesenchymal tumor cell adhesion, motility and migration PLoS One 6 2011 e14816 e14827
50. F. Granes, J.M. Urena, N. Rocamora, and S. Vilaro Ezrin links syndecan-2 to the cytoskeleton J. Cell Sci. 113 2000 1267 1276
51. F. Granes, R. Garcia, R.P. Casaroli-Marano, S. Castel, N. Rocamora, M. Reina, J.M. Urena, and S. Vilaro Syndecan-2 induces filopodia by active cdc42Hs Exp. Cell Res. 248 1999 439 456
52. H. Park, I. Han, H.J. Kwon, and E.S. Oh Focal adhesion kinase regulates syndecan-2-mediated tumorigenic activity of HT1080 fibrosarcoma cells Cancer Res. 65 2005 9899 9905
53. R.L. Longley, A. Woods, A. Fleetwood, G.J. Cowling, J.T. Gallagher, and J.R. Couchman Control of morphology, cytoskeleton and migration by syndecan-4 J. Cell Sci. 112 1999 3421 3431
54. D.M. Beauvais, and A.C. Rapraeger Syndecan-1-mediated cell spreading requires signaling by alphavbeta3 integrins in human breast carcinoma cells Exp. Cell Res. 286 2003 219 232
55. C.S. Lebakken, and A.C. Rapraeger Syndecan-1 mediates cell spreading in transfected human lymphoblastoid (Raji) cells J. Cell Biol. 132 1996 1209 1221
56. J. Yoneda, I. Saiki, Y. Igarashi, H. Kobayashi, H. Fujii, Y. Ishizaki, F. Kimizuka, I. Kato, and I. Azuma Role of the heparin-binding domain of chimeric peptides derived from fibronectin in cell spreading and motility Exp. Cell Res. 217 1995 169 179
57. J.R. Bishop, M. Schuksz, and J.D. Esko Heparan sulphate proteoglycans fine-tune mammalian physiology Nature 446 2007 1030 1037
58. N.K. Haass, K.S. Smalley, L. Li, and M. Herlyn Adhesion, migration and communication in melanocytes and melanoma Pigment Cell Res. 18 2005 150 159
59. G. Li, M. Fukunaga, and M. Herlyn Reversal of melanocytic malignancy by keratinocytes is an E-cadherin-mediated process overriding beta-catenin signaling Exp. Cell Res. 297 2004 142 151
60. J. Smolle, M. Fiebiger, R. Hofmann-Wellenhof, and H. Kerl Quantitative morphology of collagen fibers in cutaneous malignant melanoma and melanocytic nevus Am. J. Dermatopathol. 18 1996 358 363
61. D. Ruiter, T. Bogenrieder, D. Elder, and M. Herlyn Melanoma-stroma interactions: structural and functional aspects Lancet Oncol. 3 2002 35 43
62. G. Schaumburg-Lever, I. Lever, B. Fehrenbacher, H. Moller, B. Bischof, E. Kaiserling, C. Garbe, and G. Rassner Melanocytes in nevi and melanomas synthesize basement membrane and basement membrane-like material. An immunohistochemical and electron microscopic study including immunoelectron microscopy J. Cutan. Pathol. 27 2000 67 75
63. S.M. Albelda, S.A. Mette, D.E. Elder, R. Stewart, L. Damjanovich, M. Herlyn, and C.A. Buck Integrin distribution in malignant melanoma: association of the beta 3 subunit with tumor progression Cancer Res. 50 1990 6757 6764
64. P.C. Brooks, S. Stromblad, L.C. Sanders, T.L. von Schalscha, R.T. Aimes, W.G. Stetler-Stevenson, J.P. Quigley, and D.A. Cheresh Localization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin alpha v beta 3 Cell 85 1996 683 693
65. E. Petitclerc, S. Stromblad, T.L. von Schalscha, F. Mitjans, J. Piulats, A.M. Montgomery, D.A. Cheresh, and P.C. Brooks Integrin alpha(v)beta3 promotes M21 melanoma growth in human skin by regulating tumor cell survival Cancer Res. 59 1999 2724 2730
66. S. Ilmonen, T. Jahkola, J.P. Turunen, T. Muhonen, and S. Asko-Seljavaara Tenascin-C in primary malignant melanoma of the skin Histopathology 45 2004 405 411
67. F. Ledda, A.I. Bravo, S. Adris, L. Bover, J. Mordoh, and O.L. Podhajcer The expression of the secreted protein acidic and rich in cysteine (SPARC) is associated with the neoplastic progression of human melanoma J. Invest. Dermatol. 108 1997 210 214
68. P.G. Natali, M.R. Nicotra, F. Di Filippo, and A. Bigotti Expression of fibronectin, fibronectin isoforms and integrin receptors in melanocytic lesions Br. J. Cancer 71 1995 1243 1247
69. C. Pyke, J. Romer, P. Kallunki, L.R. Lund, E. Ralfkiaer, K. Dano, and K. Tryggvason The gamma 2 chain of kalinin/laminin 5 is preferentially expressed in invading malignant cells in human cancers Am. J. Pathol. 145 1994 782 791
70. M. Herlyn, M. Padarathsingh, L. Chin, M. Hendrix, D. Becker, M. Nelson, Y. DeClerck, J. McCarthy, and S. Mohla New approaches to the biology of melanoma: a workshop of the National Institutes of Health Pathology B Study Section Am. J. Pathol. 161 2002 1949 1957
71. J. Reiland, R.D. Sanderson, M. Waguespack, S.A. Barker, R. Long, D.D. Carson, and D. Marchetti Heparanase degrades syndecan-1 and perlecan heparan sulfate: functional implications for tumor cell invasion J. Biol. Chem. 279 2004 8047 8055
72. K. Raman, and B. Kuberan Chemical tumor biology of heparan sulfate proteoglycans Curr. Chem. Biol. 4 2010 20 31
73. Y. Dai, Y. Yang, V. MacLeod, X. Yue, A.C. Rapraeger, Z. Shriver, G. Venkataraman, R. Sasisekharan, and R.D. Sanderson HSulf-1 and HSulf-2 are potent inhibitors of myeloma tumor growth in vivo J. Biol. Chem. 280 2005 40066 40073
74. M.P. O'Connell, and A.T. Weeraratna A spoonful of sugar makes the melanoma go: the role of heparan sulfate proteoglycans in melanoma metastasis Pigment Cell Melanoma Res. 24 2011 1133 1147
75. C. Bret, J. Moreaux, J.F. Schved, D. Hose, and B. Klein SULFs in human neoplasia: implication as progression and prognosis factors J. Transl. Med. 9 2011 72 81
76. 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 2011 115 132
77. M. Nakajima, T. Irimura, and G.L. Nicolson Heparanases and tumor metastasis J. Cell. Biochem. 36 1988 157 167
78. Y. Chen, Y. Chen, L. Huang, and J. Yu Evaluation of heparanase and matrix metalloproteinase-9 in patients with cutaneous malignant melanoma J. Dermatol. 39 2012 339 343
79. X. Wang, W. Wen, H. Wu, Y. Chen, G. Ren, and W. Guo Heparanase expression correlates with poor survival in oral mucosal melanoma Med. Oncol. 30 2013 633 639
80. M. Roy, J. Reiland, B.P. Murry, V. Chouljenko, K.G. Kousoulas, and D. Marchetti Antisense-mediated suppression of heparanase gene inhibits melanoma cell invasion Neoplasia 7 2005 253 262
81. M.D. Hulett, C. Freeman, B.J. Hamdorf, R.T. Baker, M.J. Harris, and C.R. Parish Cloning of mammalian heparanase, an important enzyme in tumor invasion and metastasis Nat. Med. 5 1999 803 809
82. I. Vlodavsky, Y. Friedmann, M. Elkin, H. Aingorn, R. Atzmon, R. Ishai-Michaeli, M. Bitan, O. Pappo, T. Peretz, I. Michal, L. Spector, and I. Pecker Mammalian heparanase: gene cloning, expression and function in tumor progression and metastasis Nat. Med. 5 1999 793 802
83. V. Vreys, and G. David Mammalian heparanase: what is the message? J. Cell. Mol. Med. 11 2007 427 452
84. Q. Luan, J. Sun, C. Li, G. Zhang, Y. Lv, G. Wang, C. Li, C. Ma, and T. Gao Mutual enhancement between heparanase and vascular endothelial growth factor: a novel mechanism for melanoma progression Cancer Lett. 308 2011 100 111
85. M. Roy, and D. Marchetti Cell surface heparan sulfate released by heparanase promotes melanoma cell migration and angiogenesis J. Cell. Biochem. 106 2009 200 209
86. B. Cornelissen, R. Oltenfreiter, V. Kersemans, L. Staelens, F. Frankenne, J.M. Foidart, and G. Slegers In vitro and in vivo evaluation of [123I]-VEGF165 as a potential tumor marker Nucl. Med. Biol. 32 2005 431-416
87. T. Irimura, M. Nakajima, and G.L. Nicolson Chemically modified heparins as inhibitors of heparan sulfate specific endo-beta-glucuronidase (heparanase) of metastatic melanoma cells Biochemistry 25 1986 5322 5328
88. J. Reiland, D. Kempf, M. Roy, Y. Denkins, and D. Marchetti FGF2 binding, signaling, and angiogenesis are modulated by heparanase in metastatic melanoma cells Neoplasia 8 2006 596 606
89. P. Pinon, and B. Wehrle-Haller Integrins: versatile receptors controlling melanocyte adhesion, migration and proliferation Pigment Cell Melanoma Res. 24 2011 282 294
90. S. Kuphal, R. Bauer, and A.K. Bosserhoff Integrin signaling in malignant melanoma Cancer Metastasis Rev. 24 2005 195 222
91. Z. Mostafavi-Pour, J.A. Askari, S.J. Parkinson, P.J. Parker, T.T. Ng, and M.J. Humphries Integrin-specific signaling pathways controlling focal adhesion formation and cell migration J. Cell Biol. 161 2003 155 167
92. S.M. Oba-Shinjo, M. Correa, T.I. Ricca, F. Molognoni, M.A. Pinhal, I.A. Neves, S.K. Marie, L.O. Sampaio, H.B. Nader, R. Chammas, and M.G. Jasiulionis Melanocyte transformation associated with substrate adhesion impediment Neoplasia 8 2006 231 241
93. J.B. McCarthy, and L.T. Furcht Laminin and fibronectin promote the haptotactic migration of B16 mouse melanoma cells in vitro J. Cell Biol. 98 1984 1474 1480
94. R. Pankov, and K.M. Yamada Fibronectin at a glance J. Cell Sci. 115 2002 3861 3863
95. C. Gaggioli, M. Deckert, G. Robert, P. Abbe, M. Batoz, M.U. Ehrengruber, J.P. Ortonne, R. Ballotti, and S. Tartare-Deckert HGF induces fibronectin matrix synthesis in melanoma cells through MAP kinase-dependent signaling pathway and induction of Egr-1 Oncogene 24 2005 1423 1433
96. A. Woods, and J.R. Couchman Syndecan 4 heparan sulfate proteoglycan is a selectively enriched and widespread focal adhesion component Mol. Biol. Cell 5 1994 183 192
97. A. Woods, and J.R. Couchman Syndecan-4 and focal adhesion function Curr. Opin. Cell Biol. 13 2001 578 583
98. J. Timar, L. Meszaros, A. Ladanyi, L.G. Puskas, and E. Raso Melanoma genomics reveals signatures of sensitivity to bio- and targeted therapies Cell. Immunol. 244 2006 154 157
99. J.V. Moyano, A. Maqueda, J.P. Albar, and A. Garcia-Pardo A synthetic peptide from the heparin-binding domain III (repeats III4-5) of fibronectin promotes stress-fibre and focal-adhesion formation in melanoma cells Biochem. J. 371 2003 565 571
100. G. Chalkiadaki, D. Nikitovic, A. Berdiaki, M. Sifaki, K. Krasagakis, P. Katonis, N.K. Karamanos, and G.N. Tzanakakis Fibroblast growth factor-2 modulates melanoma adhesion and migration through a syndecan-4-dependent mechanism Int. J. Biochem. Cell Biol. 41 2009 1323 1331
101. V.P. Terranova, L.A. Liotta, R.G. Russo, and G.R. Martin Role of laminin in the attachment and metastasis of murine tumor cells Cancer Res. 42 1982 2265 2269
102. M.P. Hoffman, J.A. Engbring, P.K. Nielsen, J. Vargas, Z. Steinberg, A.J. Karmand, M. Nomizu, Y. Yamada, and H.K. Kleinman Cell type-specific differences in glycosaminoglycans modulate the biological activity of a heparin-binding peptide (RKRLQVQLSIRT) from the G domain of the laminin alpha1 chain J. Biol. Chem. 276 2001 22077 22085
103. B. Felding-Habermann, B.M. Mueller, C.A. Romerdahl, and D.A. Cheresh Involvement of integrin alpha V gene expression in human melanoma tumorigenicity J. Clin. Invest. 89 1992 2018 2022
104. A.M. Montgomery, R.A. Reisfeld, and D.A. Cheresh Integrin alpha v beta 3 rescues melanoma cells from apoptosis in three-dimensional dermal collagen Proc. Natl. Acad. Sci. U. S. A. 91 1994 8856 8860
105. A.L. Labrousse, C. Ntayi, W. Hornebeck, and P. Bernard Stromal reaction in cutaneous melanoma Crit. Rev. Oncol. Hematol. 49 2004 269 275
106. M. Simons, and A. Horowitz Syndecan-4-mediated signalling Cell. Signal. 13 2001 855 862
107. A. Yoneda, and J.R. Couchman Regulation of cytoskeletal organization by syndecan transmembrane proteoglycans Matrix Biol. 22 2003 25 33
108. P.C. Baciu, and P.F. Goetinck Protein kinase C regulates the recruitment of syndecan-4 into focal contacts Mol. Biol. Cell 6 1995 1503 1513
109. E.S. Oh, A. Woods, and J.R. Couchman Syndecan-4 proteoglycan regulates the distribution and activity of protein kinase C J. Biol. Chem. 272 1997 8133 8136
110. E.S. Oh, A. Woods, and J.R. Couchman Multimerization of the cytoplasmic domain of syndecan-4 is required for its ability to activate protein kinase C J. Biol. Chem. 272 1997 11805 11811
111. K.S. Midwood, Y. Mao, H.C. Hsia, L.V. Valenick, and J.E. Schwarzbauer Modulation of cell-fibronectin matrix interactions during tissue repair J. Investig. Dermatol. Symp. Proc. 11 2006 73 78
112. W. Huang, R. Chiquet-Ehrismann, J.V. Moyano, A. Garcia-Pardo, and G. Orend Interference of tenascin-C with syndecan-4 binding to fibronectin blocks cell adhesion and stimulates tumor cell proliferation Cancer Res. 61 2001 8586 8594
113. F. Meier, U. Caroli, K. Satyamoorthy, B. Schittek, J. Bauer, C. Berking, H. Moller, E. Maczey, G. Rassner, M. Herlyn, and C. Garbe Fibroblast growth factor-2 but not Mel-CAM and/or beta3 integrin promotes progression of melanocytes to melanoma Exp. Dermatol. 12 2003 296 306
114. E. Lazar-Molnar, H. Hegyesi, S. Toth, and A. Falus Autocrine and paracrine regulation by cytokines and growth factors in melanoma Cytokine 12 2000 547 554
115. D.T. Yamanishi, M.J. Graham, R.Z. Florkiewicz, J.A. Buckmeier, and F.L. Meyskens Jr. Differences in basic fibroblast growth factor RNA and protein levels in human primary melanocytes and metastatic melanoma cells Cancer Res. 52 1992 5024 5029
116. L.D. Ridgway, M.D. Wetzel, and D. Marchetti Modulation of GEF-H1 induced signaling by heparanase in brain metastatic melanoma cells J. Cell. Biochem. 111 2010 1299 1309
117. R. Gangemi, V. Mirisola, G. Barisione, M. Fabbi, A. Brizzolara, F. Lanza, C. Mosci, S. Salvi, M. Gualco, M. Truini, G. Angelini, S. Boccardo, M. Cilli, I. Airoldi, P. Queirolo, M.J. Jager, A. Daga, U. Pfeffer, and S. Ferrini Mda-9/syntenin is expressed in uveal melanoma and correlates with metastatic progression PLoS One 7 2012 e29989 e30002
118. J.M. Beekman, and P.J. Coffer The ins and outs of syntenin, a multifunctional intracellular adaptor protein J. Cell Sci. 121 2008 1349 1355
119. J.H. Lee, H. Park, H. Chung, S. Choi, Y. Kim, H. Yoo, T.Y. Kim, H.J. Hann, I. Seong, J. Kim, K.G. Kang, I.O. Han, and E.S. Oh Syndecan-2 regulates the migratory potential of melanoma cells J. Biol. Chem. 284 2009 27167 27175
120. E. Baljinnyam, K. Iwatsubo, R. Kurotani, X. Wang, C. Ulucan, M. Iwatsubo, D. Lagunoff, and Y. Ishikawa Epac increases melanoma cell migration by a heparan sulfate-related mechanism Am. J. Physiol. Cell Physiol. 297 2009 C802 C813
121. H. Chung, J.H. Lee, D. Jeong, I.O. Han, and E.S. Oh Melanocortin 1 receptor regulates melanoma cell migration by controlling syndecan-2 expression J. Biol. Chem. 287 2012 19326 19335
122. T. Aikawa, C.A. Whipple, M.E. Lopez, J. Gunn, A. Young, A.D. Lander, and M. Korc Glypican-1 modulates the angiogenic and metastatic potential of human and mouse cancer cells J. Clin. Invest. 118 2008 89 99
123. T. Nakatsura, T. Kageshita, S. Ito, K. Wakamatsu, M. Monji, Y. Ikuta, S. Senju, T. Ono, and Y. Nishimura Identification of glypican-3 as a novel tumor marker for melanoma Clin. Cancer Res. 10 2004 6612 6621
124. D. Kandil, G. Leiman, M. Allegretta, and M. Evans Glypican-3 protein expression in primary and metastatic melanoma: a combined immunohistochemistry and immunocytochemistry study Cancer 117 2009 271 278
125. Y. Nishimura, T. Nakatsura, and S. Senju Usefulness of a novel oncofetal antigen, glypican-3, for diagnosis and immunotherapy of hepatocellular carcinoma Nihon Rinsho Meneki Gakkai Kaishi 31 2008 383 391
126. T. Nakatsura, and Y. Nishimura Usefulness of the novel oncofetal antigen glypican-3 for diagnosis of hepatocellular carcinoma and melanoma BioDrugs 19 2005 71 77
127. D. Naor, S. Nedvetzki, I. Golan, L. Melnik, and Y. Faitelson CD44 in cancer Crit. Rev. Clin. Lab. Sci. 39 2002 527 579
128. D. Naor, R.V. Sionov, and D. Ish-Shalom CD44: structure, function, and association with the malignant process Adv. Cancer Res. 71 1997 241 319
129. R. Marhaba, and M. Zoller CD44 in cancer progression: adhesion, migration and growth regulation J. Mol. Histol. 35 2004 211 231
130. L.Y. Bourguignon CD44-mediated oncogenic signaling and cytoskeleton activation during mammary tumor progression J. Mammary Gland Biol. Neoplasia 6 2001 287 297
131. J. Cichy, P. Kulig, and E. Pure Regulation of the release and function of tumor cell-derived soluble CD44 Biochim. Biophys. Acta 1745 2005 59 64
132. M. Heenen, and M. Laporte Molecular markers associated to prognosis of melanoma Ann. Dermatol. Venereol. 130 2003 1025 1031
133. J.M. Karjalainen, R.H. Tammi, M.I. Tammi, M.J. Eskelinen, U.M. Agren, J.J. Parkkinen, E.M. Alhava, and V.M. Kosma Reduced level of CD44 and hyaluronan associated with unfavorable prognosis in clinical stage I cutaneous melanoma Am. J. Pathol. 157 2000 957 965
134. M. Edward Integrins and other adhesion molecules involved in melanocytic tumor progression Curr. Opin. Oncol. 7 1995 185 191
135. Y. Guo, J. Ma, J. Wang, X. Che, J. Narula, M. Bigby, M. Wu, and M.S. Sy Inhibition of human melanoma growth and metastasis in vivo by anti-CD44 monoclonal antibody Cancer Res. 54 1994 1561 1565
136. I.R. Cohen, A.D. Murdoch, M.F. Naso, D. Marchetti, D. Berd, and R.V. Iozzo Abnormal expression of perlecan proteoglycan in metastatic melanomas Cancer Res. 54 1994 5771 5774
137. A.S. Mansfield, and S.N. Markovic Inhibition of angiogenesis for the treatment of metastatic melanoma Curr. Oncol. Rep. 15 2013 492 499
138. C. Lugassy, and R.L. Barnhill Angiotropic melanoma and extravascular migratory metastasis: a review Adv. Anat. Pathol. 14 2007 195 201
139. R.D. Sanderson, Y. Yang, T. Kelly, V. MacLeod, Y. Dai, and A. Theus Enzymatic remodeling of heparan sulfate proteoglycans within the tumor microenvironment: growth regulation and the prospect of new cancer therapies J. Cell. Biochem. 96 2005 897 905
140. D. Dewing, M. Emmett, and R. Pritchard Jones The roles of angiogenesis in malignant melanoma: trends in basic science research over the last 100 years ISRN Oncol. 2012 2012 546927 546934
141. G.H. Mahabeleshwar, and T.V. Byzova Angiogenesis in melanoma Semin. Oncol. 34 2007 555 565
142. C.J. Powers, S.W. McLeskey, and A. Wellstein Fibroblast growth factors, their receptors and signaling Endocr. Relat. Cancer 7 2000 165 197
143. T. Kaji, C. Yamamoto, M. Oh-i, Y. Fujiwara, Y. Yamazaki, T. Morita, A.H. Plaas, and T.N. Wight The vascular endothelial growth factor VEGF165 induces perlecan synthesis via VEGF receptor-2 in cultured human brain microvascular endothelial cells Biochim. Biophys. Acta 1760 2006 1465 1474
144. B. Boilly, A.S. Vercoutter-Edouart, H. Hondermarck, V. Nurcombe, and X. Le Bourhis FGF signals for cell proliferation and migration through different pathways Cytokine Growth Factor Rev. 11 2000 295 302
145. I. Hunger-Glaser, R.S. Fan, E. Perez-Salazar, and E. Rozengurt PDGF and FGF induce focal adhesion kinase (FAK) phosphorylation at Ser-910: dissociation from Tyr-397 phosphorylation and requirement for ERK activation J. Cell. Physiol. 200 2004 213 222
146. P. Orecchia, R. Conte, E. Balza, A. Petretto, P. Mauri, M.C. Mingari, and B. Carnemolla A novel human anti-syndecan-1 antibody inhibits vascular maturation and tumour growth in melanoma Eur. J. Cancer 49 2013 2022 2033
147. D. Aviezer, D. Hecht, M. Safran, M. Eisinger, G. David, and A. Yayon Perlecan, basal lamina proteoglycan, promotes basic fibroblast growth factor-receptor binding, mitogenesis, and angiogenesis Cell 79 1994 1005 1013
148. H.B. Nader, S.F. Chavante, E.A. dos-Santos, T.W. Oliveira, J.F. de-Paiva, S.M. Jeronimo, G.F. Medeiros, L.R. de-Abreu, E.L. Leite, J.F. de-Sousa-Filho, R.A. Castro, L. Toma, I.L. Tersariol, M.A. Porcionatto, and C.P. Dietrich Heparan sulfates and heparins: similar compounds performing the same functions in vertebrates and invertebrates? Braz. J. Med. Biol. Res. 32 1999 529 538
149. T. Gottwald, S. Coerper, M. Schaffer, G. Koveker, and R.H. Stead The mast cell-nerve axis in wound healing: a hypothesis Wound Repair Regen. 6 1998 8 20
150. Z. Shriver, I. Capila, G. Venkataraman, and R. Sasisekharan Heparin and heparan sulfate: analyzing structure and microheterogeneity Handb. Exp. Pharmacol. 207 2012 159 176
151. U. Lindahl, M. Kusche-Gullberg, and L. Kjellen Regulated diversity of heparan sulfate J. Biol. Chem. 273 1998 24979 24982
152. A. Canales, J. Angulo, R. Ojeda, M. Bruix, R. Fayos, R. Lozano, G. Gimenez-Gallego, M. Martin-Lomas, P.M. Nieto, and J. Jimenez-Barbero Conformational flexibility of a synthetic glycosylaminoglycan bound to a fibroblast growth factor. FGF-1 recognizes both the (1)C(4) and (2)S(O) conformations of a bioactive heparin-like hexasaccharide J. Am. Chem. Soc. 127 2005 5778 5779
153. M. Schlesinger, P. Schmitz, R. Zeisig, A. Naggi, G. Torri, B. Casu, and G. Bendas The inhibition of the integrin VLA-4 in MV3 melanoma cell binding by non-anticoagulant heparin derivatives Thromb. Res. 129 2012 603 610
154. H. Liu, Z. Zhang, and R.J. Linhardt Lessons learned from the contamination of heparin Nat. Prod. Rep. 26 2009 313 321
155. V. Toschi, and M. Lettino Fondaparinux: pharmacology and clinical experience in cardiovascular medicine Mini Rev. Med. Chem. 7 2007 383 387
156. T.W. Barrowcliffe Low molecular weight heparin(s) Br. J. Haematol. 90 1995 1 7
157. J. Hirsh, K.A. Bauer, M.B. Donati, M. Gould, M.M. Samama, and J.I. Weitz Parenteral anticoagulants: American College of Chest Physicians Evidence-Based Clinical Practice Guidelines (8th Edition) Chest 133 2008 141S 159S
158. D. Wardrop, and D. Keeling The story of the discovery of heparin and warfarin Br. J. Haematol. 141 2008 757 763
159. S.J. Barsam, R. Patel, and R. Arya Anticoagulation for prevention and treatment of cancer-related venous thromboembolism Br. J. Haematol. 161 2013 764 777
160. M. Monreal Bosch, A. Vignoli, R. Lecumberri Villamediana, and P. Prandoni Bemiparin in oncology Drugs 70 2010 35 42
161. M. Samoszuk, E. Kanakubo, and J.K. Chan Degranulating mast cells in fibrotic regions of human tumors and evidence that mast cell heparin interferes with the growth of tumor cells through a mechanism involving fibroblasts BMC Cancer 5 2005 121 131
162. D. Alonso, G. Bertolesi, E. Farias, A. Eijan, E. Joffe, and L. Decidre Antimetastatic effects associated with anticoagulant properties of heparin and chemically modified heparin species in a mouse mammary tumor model Oncol. Rep. 3 1996 219 222
163. H. Engelberg Actions of heparin that may affect the malignant process Cancer 85 1999 257 272
164. D. Nikitovic, M. Assouti, M. Sifaki, P. Katonis, K. Krasagakis, N.K. Karamanos, and G.N. Tzanakakis Chondroitin sulfate and heparan sulfate-containing proteoglycans are both partners and targets of basic fibroblast growth factor-mediated proliferation in human metastatic melanoma cell lines Int. J. Biochem. Cell Biol. 40 2008 72 83
165. D.Y. Lee, S.W. Lee, S.K. Kim, M. Lee, H.W. Chang, H.T. Moon, Y. Byun, and S.Y. Kim Antiangiogenic activity of orally absorbable heparin derivative in different types of cancer cells Pharm. Res. 26 2009 2667 2676
166. I. Kenessey, E. Simon, K. Futosi, B. Bereczky, A. Kiss, F. Erdodi, J.T. Gallagher, J. Timar, and J. Tovari Antimigratory and antimetastatic effect of heparin-derived 4-18 unit oligosaccharides in a preclinical human melanoma metastasis model Thromb. Haemost. 102 2009 1265 1273
167. B. Bereczky, R. Gilly, E. Raso, A. Vago, J. Timar, and J. Tovari Selective antimetastatic effect of heparins in preclinical human melanoma models is based on inhibition of migration and microvascular arrest Clin. Exp. Metastasis 22 2005 69 76
168. M. Schlesinger, D. Simonis, P. Schmitz, J. Fritzsche, and G. Bendas Binding between heparin and the integrin VLA-4 Thromb. Haemost. 102 2009 816 822
169. P. Schmitz, U. Gerber, N. Schutze, E. Jungel, R. Blaheta, A. Naggi, G. Torri, and G. Bendas Cyr61 is a target for heparin in reducing MV3 melanoma cell adhesion and migration via the integrin VLA-4 Thromb. Haemost. 110 2013 1046 1054
170. M. Wei, Y. Gao, M. Tian, N. Li, S. Hao, and X. Zeng Selectively desulfated heparin inhibits P-selectin-mediated adhesion of human melanoma cells Cancer Lett. 229 2005 123 126
171. G. Chalkiadaki, D. Nikitovic, A. Berdiaki, P. Katonis, N.K. Karamanos, and G.N. Tzanakakis Heparin plays a key regulatory role via a p53/FAK-dependent signaling in melanoma cell adhesion and migration IUBMB Life 63 2011 109 119
172. G. Chalkiadaki, D. Nikitovic, P. Katonis, A. Berdiaki, A. Tsatsakis, I. Kotsikogianni, N.K. Karamanos, and G.N. Tzanakakis Low molecular weight heparin inhibits melanoma cell adhesion and migration through a PKCa/JNK signaling pathway inducing actin cytoskeleton changes Cancer Lett. 312 2011 235 244
173. S.A. Mousa, R. Linhardt, J.L. Francis, and A. Amirkhosravi
174. A. Amirkhosravi, S.A. Mousa, M. Amaya, and J.L. Francis Antimetastatic effect of tinzaparin, a low-molecular-weight heparin J. Thromb. Haemost. 1 2003 1972 1976
175. T. Sciumbata, P. Caretto, P. Pirovano, P. Pozzi, P. Cremonesi, G. Galimberti, F. Leoni, and F. Marcucci Treatment with modified heparins inhibits experimental metastasis formation and leads, in some animals, to long-term survival Invasion Metastasis 16 1996 132 143
176. S.M. Plum, J.W. Holaday, A. Ruiz, J.W. Madsen, W.E. Fogler, and A.H. Fortier Administration of a liposomal FGF-2 peptide vaccine leads to abrogation of FGF-2-mediated angiogenesis and tumor development Vaccine 19 2000 1294 1303
177. G. Neufeld, T. Cohen, S. Gengrinovitch, and Z. Poltorak Vascular endothelial growth factor (VEGF) and its receptors FASEB J. 13 1999 9 22
178. M.E. Bromberg, R. Sundaram, R.J. Homer, A. Garen, and W.H. Konigsberg Role of tissue factor in metastasis: functions of the cytoplasmic and extracellular domains of the molecule Thromb. Haemost. 82 1999 88 92
179. D.Y. Lee, K. Park, S.K. Kim, R.W. Park, I.C. Kwon, S.Y. Kim, and Y. Byun Antimetastatic effect of an orally active heparin derivative on experimentally induced metastasis Clin. Cancer Res. 14 2008 2841 2849
180. H. Zhou, S. Roy, E. Cochran, R. Zouaoui, C.L. Chu, J. Duffner, G. Zhao, S. Smith, Z. Galcheva-Gargova, J. Karlgren, N. Dussault, R.Y. Kwan, E. Moy, M. Barnes, A. Long, C. Honan, Y.W. Qi, Z. Shriver, T. Ganguly, B. Schultes, G. Venkataraman, and T.K. Kishimoto M402, a novel heparan sulfate mimetic, targets multiple pathways implicated in tumor progression and metastasis PLoS One 6 2011 e21106 e21117
181. E. Edovitsky, M. Elkin, E. Zcharia, T. Peretz, and I. Vlodavsky Heparanase gene silencing, tumor invasiveness, angiogenesis, and metastasis J. Natl. Cancer Inst. 96 2004 1219 1230
182. X.Y. Liu, Q.S. Tang, H.C. Chen, X.L. Jiang, and H. Fang Lentiviral miR30-based RNA interference against heparanase suppresses melanoma metastasis with lower liver and lung toxicity Int. J. Biol. Sci. 9 2013 564 577