Low molecular weight heparin inhibits melanoma cell adhesion and migration through a PKCa/JNK signaling pathway inducing actin cytoskeleton changes

Cancer Letters

Volumn 312, Issue 2, 2011, Pages 235-244

  Chalkiadaki, Georgia ^a   Nikitovic, Dragana ^a   Katonis, Pavlos ^b   Berdiaki, Aikaterini ^a   Tsatsakis, Aristidis ^a   Kotsikogianni, Ioanna ^c   Karamanos, Nikos K ^d   Tzanakakis, George N ^a  

^a UNIVERSITY OF CRETE   (Greece)

^b UNIVERSITY HOSPITAL OF HERAKLION   (Greece)

^c UNIVERSITY GENERAL HOSPITAL OF PATRAS   (Greece)

^d UNIVERSITY OF PATRAS   (Greece)

Author keywords

Cell signaling; JNK; Low molecular weight heparin; Melanoma cell adhesion; Migration; PKC alpha

Indexed keywords

ACTIN; ENOXAPARIN; FIBRONECTIN; PROTEIN KINASE C ALPHA; STRESS ACTIVATED PROTEIN KINASE;

ARTICLE; CELL ADHESION; CELL MIGRATION; CELL MOTILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOPLASM; CYTOSKELETON; DOWN REGULATION; DRUG MECHANISM; DRUG TARGETING; ENZYME ACTIVATION; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; MELANOMA CELL; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; STRESS FIBER;

ACTINS; BASE SEQUENCE; CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYTOSKELETON; DNA PRIMERS; ENZYME ACTIVATION; HEPARIN, LOW-MOLECULAR-WEIGHT; HUMANS; MAP KINASE KINASE 4; MELANOMA; SIGNAL TRANSDUCTION;

EID: 80053934330     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2011.08.016     Document Type: Article

References (49)

1. Linhardt R.J. 2003 Claude S. Hudson Award address in carbohydrate chemistry. Heparin: structure and activity. J. Med. Chem. 2003, 46(13):2551-2564.
2. Malavaki C.J., Theocharis A.D., Lamari F.N., Kanakis I., Tsegenidis T., Tzanakakis G.N., Karamanos N.K. Heparan sulfate: biological significance, tools for biochemical analysis and structural characterization. Biomed. Chromatogr. 2011, 25(1-2):11-20.
3. Borsig L. Antimetastatic activities of heparins and modified heparins. Experimental evidence. Thromb. Res. 2011, 125(Suppl 2):S66-S71.
4. Smorenburg S.M., Van Noorden C.J. The complex effects of heparins on cancer progression and metastasis in experimental studies. Pharmacol. Rev. 2001, 53(1):93-105.
5. Maraveyas A., Johnson M.J., Xiao Y.P., Noble S. Malignant melanoma as a target malignancy for the study of the anti-metastatic properties of the heparins. Cancer Metastasis Rev. 2010, 29(4):777-784.
6. Varki N.M., Varki A. Heparin inhibition of selectin-mediated interactions during the hematogenous phase of carcinoma metastasis: rationale for clinical studies in humans. Semin. Thromb. Hemost. 2002, 28(1):53-66.
7. Engelberg H. Actions of heparin that may affect the malignant process. Cancer 1999, 85(2):257-272.
8. Folkman J., Shing Y. Control of angiogenesis by heparin and other sulfated polysaccharides. Adv. Exp. Med. Biol. 1992, 313:355-364.
9. Vlodavsky I., Friedmann Y. Molecular properties and involvement of heparanase in cancer metastasis and angiogenesis. J. Clin. Invest. 2001, 108(3):341-347.
10. Tyagi S.C., Kumar S., Katwa L. Differential regulation of extracellular matrix metalloproteinase and tissue inhibitor by heparin and cholesterol in fibroblast cells. J. Mol. Cell. Cardiol. 1997, 29(1):391-404.
11. Chalkiadaki G., Nikitovic D., Berdiaki A., Katonis P., Karamanos N.K., Tzanakakis G.N. Heparin plays a key regulatory role via a p53/FAK-dependent signaling in melanoma cell adhesion and migration. IUBMB Life 2011, 63(2):109-119.
12. Young E., Venner T., Ribau J., Shaughnessy S., Hirsh J., Podor T.J. The binding of unfractionated heparin and low molecular weight heparin to thrombin-activated human endothelial cells. Thromb. Res. 1999, 96(5):373-381.
13. Norrby K. Low-molecular-weight heparins and angiogenesis. Apmis 2006, 114(2):79-102.
14. Liao S.K., Dent P.B., McCulloch P.B. Characterization of human maligant melanoma cell lines. I. Morphology and growth characteristics in culture. J. Natl Cancer Inst. 1975, 54(5):1037-1044.
15. Chalkiadaki G., Nikitovic D., Berdiaki A., Sifaki M., Krasagakis K., Katonis P., Karamanos N.K., Tzanakakis G.N. Fibroblast growth factor-2 modulates melanoma adhesion and migration through a syndecan-4-dependent mechanism. Int. J. Biochem. Cell Biol. 2009, 41(6):1323-1331.
16. Papakonstanti E.A., Ridley A.J., Vanhaesebroeck B. The p110delta isoform of PI 3-kinase negatively controls RhoA and PTEN. EMBO J. 2007, 26(13):3050-3061.
17. Hendrix M.J., Seftor E.A., Hess A.R., Seftor R.E. Molecular plasticity of human melanoma cells. Oncogene 2003, 22(20):3070-3075.
18. Keum E., Kim Y., Kim J., Kwon S., Lim Y., Han I., Oh E.S. Syndecan-4 regulates localization, activity and stability of protein kinase C-alpha. Biochem. J. 2004, 378(Pt 3):1007-1014.
19. Levy-Adam F., Feld S., Suss-Toby E., Vlodavsky I., Ilan N. Heparanase facilitates cell adhesion and spreading by clustering of cell surface heparan sulfate proteoglycans. PLoS One 2008, 3(6):e2319.
20. Xu X., Dai Y. Heparin: an intervenor in cell communication. J. Cell. Mol. Med. 2011, 14(1-2):175-180.
21. Newton A.C. Protein kinase C: structural and spatial regulation by phosphorylation, cofactors, and macromolecular interactions. Chem. Rev. 2001, 101(8):2353-2364.
22. Woods A., Couchman J.R. Protein kinase C involvement in focal adhesion formation. J. Cell Sci. 1992, 101(Pt 2):277-290.
23. Geiger T., Geiger B. Towards elucidation of functional molecular signatures of the adhesive-migratory phenotype of malignant cells. Semin. Cancer Biol. 2011, 20(3):146-152.
24. Huang C., Jacobson K., Schaller M.D. MAP kinases and cell migration. J. Cell Sci. 2004, 117(Pt 20):4619-4628.
25. Fecher L.A., Amaravadi R.K., Flaherty K.T. The MAPK pathway in melanoma. Curr. Opin. Oncol. 2008, 20(2):183-189.
26. Lin C.W., Shen S.C., Chien C.C., Yang L.Y., Shia L.T., Chen Y.C. 12-O-tetradecanoylphorbol-13-acetate-induced invasion/migration of glioblastoma cells through activating PKCalpha/ERK/NF-kappaB-dependent MMP-9 expression. J. Cell. Physiol. 2010, 225(2):472-481.
27. Nomura N., Nomura M., Takahira M., Sugiyama K. Phorbol 12-myristate 13-acetate-activated protein kinase C increased migratory activity of subconjunctival fibroblasts via stress-activated protein kinase pathways. Mol. Vis. 2007, 13:2320-2327.
28. Barr R.K., Bogoyevitch M.A. The c-Jun N-terminal protein kinase family of mitogen-activated protein kinases (JNK MAPKs). Int. J. Biochem. Cell Biol. 2001, 33(11):1047-1063.
29. Lu M.K., Shih Y.W., Chang Chien T.T., Fang L.H., Huang H.C., Chen P.S. alpha-Solanine inhibits human melanoma cell migration and invasion by reducing matrix metalloproteinase-2/9 activities. Biol. Pharm. Bull. 2010, 33(10):1685-1691.
30. Huang C., Jacobson K., Schaller M.D. A role for JNK-paxillin signaling in cell migration. Cell Cycle 2004, 3(1):4-6.
31. Murthy K.S., Grider J.R., Makhlouf G.M. Receptor-coupled G proteins mediate contraction and Ca++ mobilization in isolated intestinal muscle cells. J. Pharmacol. Exp. Ther. 1992, 260(1):90-97.
32. Tanabe T., Otani H., Mishima K., Ogawa R., Inagaki C. Mechanisms of oxyradical production in substance P stimulated rheumatoid synovial cells. Rheumatol. Int. 1996, 16(4):159-167.
33. Martelli A.M., Sang N., Borgatti P., Capitani S., Neri L.M. Multiple biological responses activated by nuclear protein kinase C. J. Cell. Biochem. 1999, 74(4):499-521.
34. Aoyagi K., Kuzure Y., Shahrzad S., Hirayama A., Nagase S., Ueda A. Inhibition by heparin of protein kinase C activation and hydroxyl radical generation in puromycin aminonucleoside treated isolated rat hepatocytes. Mol. Cell. Biochem. 2003, 244(1-2):3-9.
35. Burridge K., Fath K., Kelly T., Nuckolls G., Turner C. Focal adhesions: transmembrane junctions between the extracellular matrix and the cytoskeleton. Annu. Rev. Cell Biol. 1988, 4:487-525.
36. Jockusch B.M., Bubeck P., Giehl K., Kroemker M., Moschner J., Rothkegel M., Rudiger M., Schluter K., Stanke G., Winkler J. The molecular architecture of focal adhesions. Annu. Rev. Cell Dev. Biol. 1995, 11:379-416.
37. Berrier A.L., Yamada K.M. Cell-matrix adhesion. J. Cell. Physiol. 2007, 213(3):565-573.
38. Larsson C. Protein kinase C and the regulation of the actin cytoskeleton. Cell. Signal. 2006, 18(3):276-284.
39. Cheng C.Y., Hsieh H.L., Sun C.C., Lin C.C., Luo S.F., Yang C.M. IL-1 beta induces urokinase-plasminogen activator expression and cell migration through PKC alpha, JNK1/2, and NF-kappaB in A549 cells. J. Cell. Physiol. 2009, 219(1):183-193.
40. Huang C., Rajfur Z., Borchers C., Schaller M.D., Jacobson K. JNK phosphorylates paxillin and regulates cell migration. Nature 2003, 424(6945):219-223.
41. Karin M., Gallagher E. From JNK to pay dirt: jun kinases, their biochemistry, physiology and clinical importance. IUBMB Life 2005, 57(4-5):283-295.
42. Kuriyama S., Mayor R. A role for Syndecan-4 in neural induction involving ERK- and PKC-dependent pathways. Development 2009, 136(4):575-584.
43. Becker R.C. Optimizing heparin compounds: a working construct for future antithrombotic drug development. J. Thromb. Thrombolysis 2004, 18(1):55-58.
44. Harris E.N., Baggenstoss B.A., Weigel P.H. Rat and human HARE/stabilin-2 are clearance receptors for high- and low-molecular-weight heparins. Am. J. Physiol. Gastrointest. Liver Physiol. 2009, 296(6):G1191-1199.
45. Saltissi D., Morgan C., Westhuyzen J., Healy H. Comparison of low-molecular-weight heparin (enoxaparin sodium) and standard unfractionated heparin for haemodialysis anticoagulation. Nephrol. Dial. Transplant. 1999, 14(11):2698-2703.
46. Salzman E.W., Rosenberg R.D., Smith M.H., Lindon J.N., Favreau L. Effect of heparin and heparin fractions on platelet aggregation. J. Clin. Invest. 1980, 65(1):64-73.
47. Teraoka J., Matsui N., Nakagawa S., Takeuchi J. The role of heparin in the changes of lipid patterns during a single hemodialysis. Clin. Nephrol. 1982, 17(2):96-99.
48. Kelton J.G. Heparin-induced thrombocytopenia. Haemostasis 1986, 16(2):173-186.
49. Street A.M. Hunter's syndrome with an endogenous anticoagulant. Am. J. Hematol. 1996, 53(4):277.