Thrombosis Research
Volume 125, Issue 3 , Pages 235-238 , March 2010

Prophylactic plasma levels of the low molecular weight heparin nadroparin does not affect colon cancer tumor development in mouse liver

  • Clara P.W. Klerk

      Affiliations

    • Department of Cell Biology and Histology, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
    • Department of Medical Oncology, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
    • Department of Vascular Medicine, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
  • ,
  • Tatjana M.H. Niers

      Affiliations

    • Department of Medical Oncology, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
    • Center for Experimental and Molecular Medicine, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
  • ,
  • Lois W. Brüggemann

      Affiliations

    • Center for Experimental and Molecular Medicine, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
  • ,
  • Susanne M. Smorenburg

      Affiliations

    • Department of Cell Biology and Histology, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
    • Department of Vascular Medicine, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
  • ,
  • Dick J. Richel

      Affiliations

    • Department of Medical Oncology, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
  • ,
  • C. Arnold Spek

      Affiliations

    • Center for Experimental and Molecular Medicine, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
  • ,
  • Cornelis J.F. Van Noorden

      Affiliations

    • Department of Cell Biology and Histology, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
    • Corresponding Author InformationCorresponding author. Department of Cell Biology and Histology, Academic Medical Center, Meibergdreef 15, 1105 AZ Amsterdam, The Netherlands. Tel.: +31 20 566 4970/4966; fax: +31 20 697 4156.

Received 23 October 2008 ,Revised 16 February 2009 ,Accepted 3 March 2009.

References 

  1. Kakkar AK, Levine MN, Kadziola Z, Lemoine NR, Low V, Patel HK, et al. Low molecular weight heparin, therapy with dalteparin, and survival in advanced cancer: the fragmin advanced malignancy outcome study (FAMOUS). J Clin Oncol. 2004;22:1944–1948
  2. Klerk CP, Smorenburg SM, Otten HM, Lensing AW, Prins MH, Piovella F, et al. The effect of low molecular weight heparin on survival in patients with advanced malignancy. J Clin Oncol. 2005;23:2130–2135
  3. Lee AY, Levine MN, Baker RI, Bowden C, Kakkar AK, Prins M, et al. Low-molecular-weight heparin versus a coumarin for the prevention of recurrent venous thromboembolism in patients with cancer. N Engl J Med. 2003;349:146–153
  4. Smorenburg SM, Van Noorden CJF. The complex effects of heparins on cancer progression and metastasis in experimental studies. Pharmacol Rev. 2001;53:93–105
  5. Niers TM, Klerk CP, Dinisio M, Van Noorden CJ, Buller HR, Reitsma PH, et al. Mechanisms of heparin induced anti-cancer activity in experimental cancer models. Crit Rev Oncol Hematol. 2007;61:195–207
  6. Zacharski LR, Ornstein DL. Heparin and cancer. Thromb Haemost. 1998;80:10–23
  7. Palumbo JS, Degen JL. Mechanisms linking tumor cell-associated procoagulant function to tumor metastasis. Thromb Res. 2007;120(Suppl 2):S22–S28
  8. Vlodavsky I, Ilan N, Nadir Y, Brenner B, Katz BZ, Naggi A, et al. Heparanase, heparin and the coagulation system in cancer progression. Thromb Res. 2007;120(Suppl 2):S112–S120
  9. Stevenson JL, Varki A, Borsig L. Heparin attenuates metastasis mainly due to inhibition of P- and L-selectin, but non-anticoagulant heparins can have additional effects. Thromb Res. 2007;120(Suppl 2):S107–S111
  10. Borsig L, Wong R, Feramisco J, Nadeau DR, Varki NM, Varki A. Heparin and cancer revisited: mechanistic connections involving platelets, P-selectin, carcinoma mucins, and tumor metastasis. Proc Natl Acad Sci U S A. 2001;98:3352–3357
  11. Borsig L, Wong R, Hynes RO, Varki NM, Varki A. Synergistic effects of L- and P-selectin in facilitating tumor metastasis can involve non-mucin ligands and implicate leukocytes as enhancers of metastasis. Proc Natl Acad Sci U S A. 2002;99:2193–2198
  12. Ludwig RJ, Alban S, Bistrian R, Boehncke1 WH, Kaufmann R, Henschler R, et al. The ability of different forms of heparins to suppress P-selectin function in vitro correlates to their inhibitory capacity on bloodborne metastasis in vivo. Thromb Haemost. 2006;95:535–540
  13. Hostettler N, Naggi A, Torri G, Ishai-Michaeli R, Casu B, Vlodavsky I, et al. P-selectin- and heparanase-dependent antimetastatic activity of non-anticoagulant heparins. FASEB J. 2007;21:3562–3572
  14. Hembrough TA, Swartz GM, Papathanassiu A, Vlasuk GP, Rote WE, Green SJ, et al. Tissue factor/factor VIIa inhibitors block angiogenesis and tumor growth through a nonhemostatic mechanism. Cancer Res. 2003;63:2997–3000
  15. Banke IJ, Arlt MJ, Mueller MM, Sperl S, Stemberger A, Sturzebecher J, et al. Effective inhibition of experimental metastasis and prolongation of survival in mice by a potent factor Xa-specific synthetic serine protease inhibitor with weak anticoagulant activity. Thromb Haemost. 2005;94:1084–1093
  16. Hu L, Lee M, Campbell W, Perez-Soler R, Karpatkin S. Role of endogenous thrombin in tumor implantation, seeding, and spontaneous metastasis. Blood. 2004;104:2746–2751
  17. Palumbo JS, Kombrinck KW, Drew AF, Grimes TS, Kiser JH, Degen JL, et al. Fibrinogen is an important determinant of the metastatic potential of circulating tumor cells. Blood. 2000;96:3302–3309
  18. Broze GJ. Tissue factor pathway inhibitor and the revised theory of coagulation. Annu Rev Med. 1995;46:103–112
  19. Brüggemann LW, Versteeg HH, Niers TM, Reitsma PH, Spek CA. Experimental melanoma metastasis in lungs of mice with congenital coagulation disorders. J Cell Mol Med. 2008;12(6B):2622–2627
  20. Klerk CP, Smorenburg SM, Spek CA, Van Noorden CJ. Colon cancer metastasis in mouse liver is not affected by hypercoagulability due to Factor V Leiden mutation. J Cell Mol Med. 2007;11:561–568
  21. Piscatelli JJ, Cohen SA, Berenson CS, Lance P. Determinants of differential liver-colonizing potential of variants of the MCA-38 murine colon cancer cell line. Clin Exp Metast. 1995;13:141–150
  22. Griffini P, Fehres O, Klieverik L, Vogels IM, Tigchelaar W, Smorenburg SM, et al. Dietary omega-3 polyunsaturated fatty acids promote colon carcinoma metastasis in rat liver. Cancer Res. 1998;58:3312–3319
  23. Ten Cate H, Lamping RJ, Henny CP, Prins A, Ten Cate JW. Automated amidolytic method for determining heparin, a heparinoid, and a low-Mr heparin fragment, based on their anti-Xa activity. Clin Chem. 1984;30:860–864
  24. Collen A, Smorenburg SM, Peters E, Lupu F, Koolwijk P, Van Noorden C, et al. Unfractionated and low molecular weight heparin affect fibrin structure and angiogenesis in vitro. Cancer Res. 2000;60:6196–6200
  25. Fonsatti E, Sigalotti L, Arslan P, Altomonte M, Maio M. Emerging role of endoglin (CD105) as a marker of angiogenesis with clinical potential in human malignancies. Curr Cancer Drug Targets. 2003;3:427–432
  26. Fonsatti E, Maio M. Highlights on endoglin (CD105): from basic findings towards clinical applications in human cancer. J Transl Med. 2004;2:18
  27. Murray JC, Smith KA, Lauk S. Vascular markers for murine tumours. Radiother Oncol. 1989;16:221–234
  28. Shoobridge MP. A new principle in polychrome staining: a system of automated staining, complementary to hematoxylin and eosin, and usable as a research tool. Stain Technol. 1983;58:245–258
  29. Van Noorden CJ, Jonges GN. Quantification of the histochemical reaction for alkaline phosphatase activity using the indoxyl-tetranitro BT method. Histochem J. 1987;19:94–102
  30. Altinbas M, Coskun HS, Er O, Ozkan M, Eser B, Unal A, et al. A randomized clinical trial of combination chemotherapy with and without low-molecular-weight heparin in small cell lung cancer. J Thromb Haemost. 2004;2:1266–1271
  31. Smorenburg SM, Vink R, te Lintelo M, Tigchelaar W, Maas A, Büller HR, et al. In vivo treatment of rats with unfractionated heparin (UFH) or low molecular weight heparin (LMWH) does not affect experimentally induced colon carcinoma metastasis. Clin Exp Metast. 1999;17:451–456
  32. Nagawa H, Paris P, Chauffert B, Martin F. Treatment of experimental liver metastases in the rat by continuous intraportal infusion of 5-fluorouracil and heparin: a pilot study. Anticancer Drugs. 1990;1:149–156
  33. Mook ORF, Van Marle J, Vreeling-Sindelárová H, Jonges R, Frederiks WM, Van Noorden CJF. Visualization of early events in tumor formation of eGFP-transfected rat colon cancer cells in liver. Hepatology. 2003;38:295–304
  34. Mook ORF, Van Marle J, Jonges R, Vreeling-Sindelárová H, Frederiks WM, Van Noorden CJF. Interactions between colon cancer cells and hepatocytes in rats in relation to metastasis. J Cell Mol Med. 2008;12:2052–2061

PII: S0049-3848(09)00127-3

doi: 10.1016/j.thromres.2009.03.005

Thrombosis Research
Volume 125, Issue 3 , Pages 235-238 , March 2010