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PMID: 21258396 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Review

Contribution of platelets to tumour metastasis.

Nature reviews. Cancer ·Vol. 11 ·No. 2 ·2011-02-00 ·Pages 123-34

Gay LJ, Felding-Habermann B

Abstract

Extensive experimental evidence shows that platelets support tumour metastasis. The activation of platelets and the coagulation system have a crucial role in the progression of cancer. Within the circulatory system, platelets guard tumour cells from immune elimination and promote their arrest at the endothelium, supporting the establishment of secondary lesions. These contributions of platelets to tumour cell survival and spread suggest platelets as a new avenue for therapy.

MeSH Terms
Biomarkers, Tumor/metabolism Blood Platelets/pathology Capillary Permeability Cell Survival Humans Neoplasm Metastasis/physiopathology,prevention & control Neoplastic Cells, Circulating Neovascularization, Pathologic Platelet Activation Platelet Aggregation Inhibitors
Chemicals
Biomarkers, Tumor Platelet Aggregation Inhibitors
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Gay Laurie J
Department of Molecular and Experimental Medicine, The Scripps Research Institute, La Jolla, CA 92037, USA.
Felding-Habermann Brunhilde
References (168)
168 references, click to expand
  1. Increased metastatic potential of tumor cells in von Willebrand factor-deficient mice.
    J Thromb Haemost. 2006 Mar;4(3):519-26 PMID: 16405520
  2. The value of preoperative platelet count in the prediction of cervical involvement and poor prognostic variables in patients with endometrial carcinoma.
    Gynecol Oncol. 2006 Dec;103(3):902-5 PMID: 16828847
  3. Distinct selectin ligands on colon carcinoma mucins can mediate pathological interactions among platelets, leukocytes, and endothelium.
    Am J Pathol. 1999 Aug;155(2):461-72 PMID: 10433939
  4. Role of adhesive proteins in platelet tumor interaction in vitro and metastasis formation in vivo.
    J Clin Invest. 1988 Apr;81(4):1012-9 PMID: 3280598
  5. Regulation of cerebromicrovascular permeability by lysophosphatidic acid.
    Microcirculation. 2010 Jan;17(1):39-46 PMID: 20141599
  6. Cancer, clots and consensus: new understanding of an old problem.
    J Clin Oncol. 2009 Oct 10;27(29):4821-6 PMID: 19752337
  7. American Society of Clinical Oncology guideline: recommendations for venous thromboembolism prophylaxis and treatment in patients with cancer.
    J Clin Oncol. 2007 Dec 1;25(34):5490-505 PMID: 17968019
  8. CD63 is a component of Weibel-Palade bodies of human endothelial cells.
    Blood. 1993 Aug 15;82(4):1184-91 PMID: 8353283
  9. Inflammation and melanoma growth and metastasis: the role of platelet-activating factor (PAF) and its receptor.
    Cancer Metastasis Rev. 2007 Dec;26(3-4):359-71 PMID: 17721743
  10. Platelets, petechiae, and preservation of the vascular wall.
    N Engl J Med. 2008 Sep 18;359(12):1261-70 PMID: 18799560
  11. The bidirectional relationship of cancer and hemostasis and the potential role of anticoagulant therapy in moderating thrombosis and cancer spread.
    Semin Thromb Hemost. 2009 Oct;35(7):644-53 PMID: 20013531
  12. Platelet-derived transforming growth factor-beta down-regulates NKG2D thereby inhibiting natural killer cell antitumor reactivity.
    Cancer Res. 2009 Oct 1;69(19):7775-83 PMID: 19738039
  13. Tumor cell-associated tissue factor and circulating hemostatic factors cooperate to increase metastatic potential through natural killer cell-dependent and-independent mechanisms.
    Blood. 2007 Jul 1;110(1):133-41 PMID: 17371949
  14. Platelet functions and clinical effects in acute myelogenous leukemia.
    Thromb Haemost. 2008 Jan;99(1):27-37 PMID: 18217131
  15. The role of tissue factor pathway inhibitor in tumor growth and metastasis.
    Semin Thromb Hemost. 2007 Oct;33(7):643-52 PMID: 18000790
  16. TGFbeta signalling: a complex web in cancer progression.
    Nat Rev Cancer. 2010 Jun;10(6):415-24 PMID: 20495575
  17. Tissue factor and PAR signaling in tumor progression.
    Thromb Res. 2007;120 Suppl 2:S7-12 PMID: 18023716
  18. Targeting activated integrin alphavbeta3 with patient-derived antibodies impacts late-stage multiorgan metastasis.
    Clin Exp Metastasis. 2010 Apr;27(4):217-31 PMID: 20225083
  19. Enhancing effect of platelet-derived microvesicles on the invasive potential of breast cancer cells.
    Transfusion. 2006 Jul;46(7):1199-209 PMID: 16836568
  20. Platelets and cancer metastasis: more than an epiphenomenon.
    Semin Thromb Hemost. 1992;18(4):392-415 PMID: 1470927
  21. Chemical modulators of sphingosine-1-phosphate receptors as barrier-oriented therapeutic molecules.
    Nat Rev Drug Discov. 2009 Apr;8(4):297-307 PMID: 19300460
  22. Platelet-associated PF-4 as a biomarker of early tumor growth.
    Blood. 2008 Feb 1;111(3):1201-7 PMID: 17914028
  23. Defective platelet activation in G alpha(q)-deficient mice.
    Nature. 1997 Sep 11;389(6647):183-6 PMID: 9296496
  24. Roles of integrin activation in eosinophil function and the eosinophilic inflammation of asthma.
    J Leukoc Biol. 2008 Jan;83(1):1-12 PMID: 17906117
  25. Inhibition of murine melanoma experimental metastasis by recombinant desulfatohirudin, a highly specific thrombin inhibitor.
    Cancer Res. 1991 Sep 1;51(17):4549-56 PMID: 1873799
  26. Platelet and osteoclast beta3 integrins are critical for bone metastasis.
    Proc Natl Acad Sci U S A. 2003 Nov 25;100(24):14205-10 PMID: 14612570
  27. Platelets: guardians of tumor vasculature.
    Cancer Res. 2009 Jul 15;69(14):5623-6 PMID: 19584268
  28. Prognostic value of thrombocytosis in renal cell carcinoma.
    J Urol. 2006 Mar;175(3 Pt 1):859-63 PMID: 16469566
  29. Platelets and metastasis revisited: a novel fatty link.
    J Clin Invest. 2004 Dec;114(12):1691-3 PMID: 15599391
  30. Absence of host plasminogen activator inhibitor 1 prevents cancer invasion and vascularization.
    Nat Med. 1998 Aug;4(8):923-8 PMID: 9701244
  31. Validation of an anti-sphingosine-1-phosphate antibody as a potential therapeutic in reducing growth, invasion, and angiogenesis in multiple tumor lineages.
    Cancer Cell. 2006 Mar;9(3):225-38 PMID: 16530706
  32. Integrin activation controls metastasis in human breast cancer.
    Proc Natl Acad Sci U S A. 2001 Feb 13;98(4):1853-8 PMID: 11172040
  33. Critical role for TrkB kinase function in anoikis suppression, tumorigenesis, and metastasis.
    Cancer Res. 2007 Jul 1;67(13):6221-9 PMID: 17616679
  34. Platelet-endothelial interaction in tumor angiogenesis and microcirculation.
    Blood. 2003 Mar 1;101(5):1970-6 PMID: 12584142
  35. Preoperative thrombocytosis predicts poor survival in patients with glioblastoma.
    Neuro Oncol. 2007 Jul;9(3):335-42 PMID: 17504931
  36. Thrombin induces tumor growth, metastasis, and angiogenesis: Evidence for a thrombin-regulated dormant tumor phenotype.
    Cancer Cell. 2006 Nov;10(5):355-62 PMID: 17097558
  37. Fibrinogen is an important determinant of the metastatic potential of circulating tumor cells.
    Blood. 2000 Nov 15;96(10):3302-9 PMID: 11071621
  38. Platelets take up the monoclonal antibody bevacizumab.
    Clin Cancer Res. 2007 Sep 15;13(18 Pt 1):5341-7 PMID: 17855648
  39. Electron microscopic observations on formation of pulmonary metastases.
    J Surg Res. 1975 Feb;18(2):137-61 PMID: 166253
  40. The importance of 5-HT for tumor cell lodgement in the liver.
    Int J Cancer. 1984 Apr 15;33(4):519-23 PMID: 6368410
  41. RANTES, a monocyte and T lymphocyte chemotactic cytokine releases histamine from human basophils.
    J Immunol. 1992 Jul 15;149(2):636-42 PMID: 1378073
  42. Matrix metalloproteinases and tumor metastasis.
    Cancer Metastasis Rev. 2006 Mar;25(1):9-34 PMID: 16680569
  43. 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 Feb 19;99(4):2193-8 PMID: 11854515
  44. Neutrophil recruitment under shear flow: it's all about endothelial cell rings and gaps.
    Microcirculation. 2009 Jan;16(1):43-57 PMID: 18720226
  45. Platelet-derived thrombospondin-1 is a critical negative regulator and potential biomarker of angiogenesis.
    Blood. 2010 Jun 3;115(22):4605-13 PMID: 20086246
  46. Historical review: megakaryopoiesis and thrombopoiesis.
    Blood. 2008 Feb 1;111(3):981-6 PMID: 18223171
  47. Role of alpha4beta1 integrins in chemokine-induced monocyte arrest under conditions of shear stress.
    Microcirculation. 2009 Jan;16(1):17-30 PMID: 18979279
  48. Blockade of a chemokine, CCL2, reduces chronic colitis-associated carcinogenesis in mice.
    Cancer Res. 2009 Oct 1;69(19):7884-92 PMID: 19773434
  49. Cancer cells in transit: the vascular interactions of tumor cells.
    Annu Rev Biomed Eng. 2009;11:177-202 PMID: 19413512
  50. The dual role of CD44 as a functional P-selectin ligand and fibrin receptor in colon carcinoma cell adhesion.
    Am J Physiol Cell Physiol. 2008 Apr;294(4):C907-16 PMID: 18234849
  51. Mechanisms linking tumor cell-associated procoagulant function to tumor metastasis.
    Thromb Res. 2007;120 Suppl 2:S22-8 PMID: 18023710
  52. Selectin-mediated activation of endothelial cells induces expression of CCL5 and promotes metastasis through recruitment of monocytes.
    Blood. 2009 Nov 12;114(20):4583-91 PMID: 19779041
  53. Coagulation facilitates tumor cell spreading in the pulmonary vasculature during early metastatic colony formation.
    Cancer Res. 2004 Dec 1;64(23):8613-9 PMID: 15574768
  54. Platelet glycoprotein VI facilitates experimental lung metastasis in syngenic mouse models.
    J Thromb Haemost. 2009 Oct;7(10):1713-7 PMID: 19624454
  55. Interaction of cancer cells with platelets mediated by Necl-5/poliovirus receptor enhances cancer cell metastasis to the lungs.
    Oncogene. 2008 Jan 10;27(3):264-73 PMID: 17637752
  56. Tissue factor activity is increased in a combined platelet and microparticle sample from cancer patients.
    Thromb Res. 2008;122(5):604-9 PMID: 18262600
  57. Impact of pretreatment thrombocytosis on survival in primary breast cancer.
    Thromb Haemost. 2003 Jun;89(6):1098-106 PMID: 12783124
  58. Platelet functions beyond hemostasis.
    J Thromb Haemost. 2009 Nov;7(11):1759-66 PMID: 19691483
  59. Constitutive production and thrombin-induced release of vascular endothelial growth factor by human megakaryocytes and platelets.
    Proc Natl Acad Sci U S A. 1997 Jan 21;94(2):663-8 PMID: 9012841
  60. Platelet-derived microparticles promote invasiveness of prostate cancer cells via upregulation of MMP-2 production.
    Int J Cancer. 2009 Apr 15;124(8):1773-7 PMID: 19101987
  61. Integrin structure, allostery, and bidirectional signaling.
    Annu Rev Cell Dev Biol. 2005;21:381-410 PMID: 16212500
  62. Assessing risk of venous thromboembolism in the patient with cancer.
    J Clin Oncol. 2009 Oct 10;27(29):4839-47 PMID: 19720906
  63. Cytokine-mediated deployment of SDF-1 induces revascularization through recruitment of CXCR4+ hemangiocytes.
    Nat Med. 2006 May;12(5):557-67 PMID: 16648859
  64. The final steps of integrin activation: the end game.
    Nat Rev Mol Cell Biol. 2010 Apr;11(4):288-300 PMID: 20308986
  65. Platelet--cancer interactions: mechanisms and pharmacology of tumour cell-induced platelet aggregation.
    Br J Pharmacol. 2004 Dec;143(7):819-26 PMID: 15492016
  66. Immobilized platelets support human colon carcinoma cell tethering, rolling, and firm adhesion under dynamic flow conditions.
    Blood. 2000 Sep 1;96(5):1789-97 PMID: 10961878
  67. Activation of tumor cell integrin alphavbeta3 controls angiogenesis and metastatic growth in the brain.
    Proc Natl Acad Sci U S A. 2009 Jun 30;106(26):10666-71 PMID: 19541645
  68. Trousseau's syndrome: multiple definitions and multiple mechanisms.
    Blood. 2007 Sep 15;110(6):1723-9 PMID: 17496204
  69. Role of beta3 integrins in melanoma cell adhesion to activated platelets under flow.
    J Biol Chem. 1996 Mar 8;271(10):5892-900 PMID: 8621462
  70. Angiogenesis is regulated by a novel mechanism: pro- and antiangiogenic proteins are organized into separate platelet alpha granules and differentially released.
    Blood. 2008 Feb 1;111(3):1227-33 PMID: 17962514
  71. Aspirin, salicylates, and cancer.
    Lancet. 2009 Apr 11;373(9671):1301-9 PMID: 19328542
  72. Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer.
    Int J Cancer. 2005 Feb 20;113(5):752-60 PMID: 15499615
  73. Microparticle-associated tissue factor activity: a link between cancer and thrombosis?
    J Thromb Haemost. 2007 Mar;5(3):520-7 PMID: 17166244
  74. Cancer cell-derived microparticles bearing P-selectin glycoprotein ligand 1 accelerate thrombus formation in vivo.
    J Exp Med. 2009 Aug 31;206(9):1913-27 PMID: 19667060
  75. Platelet-derived lysophosphatidic acid supports the progression of osteolytic bone metastases in breast cancer.
    J Clin Invest. 2004 Dec;114(12):1714-25 PMID: 15599396
  76. Formation of procoagulant microparticles and properties.
    Thromb Res. 2010 Apr;125 Suppl 1:S46-8 PMID: 20153515
  77. Platelet and coagulation activation with vascular endothelial growth factor generation in soft tissue sarcomas.
    Clin Cancer Res. 2000 Jan;6(1):166-71 PMID: 10656446
  78. Recent advances in understanding serotonin regulation of cardiovascular function.
    Trends Mol Med. 2004 May;10(5):232-8 PMID: 15121050
  79. Combinatorial antibody libraries from cancer patients yield ligand-mimetic Arg-Gly-Asp-containing immunoglobulins that inhibit breast cancer metastasis.
    Proc Natl Acad Sci U S A. 2004 Dec 7;101(49):17210-5 PMID: 15563590
  80. P-selectin deficiency attenuates tumor growth and metastasis.
    Proc Natl Acad Sci U S A. 1998 Aug 4;95(16):9325-30 PMID: 9689079
  81. Mechanisms linking tumor cell-associated procoagulant function to tumor dissemination.
    Semin Thromb Hemost. 2008 Mar;34(2):154-60 PMID: 18645920
  82. Platelet activation and atherothrombosis.
    N Engl J Med. 2007 Dec 13;357(24):2482-94 PMID: 18077812
  83. The role of platelet activation in tumor metastasis.
    Expert Rev Anticancer Ther. 2008 Aug;8(8):1247-55 PMID: 18699763
  84. Platelet microparticles: a potential predictive factor of survival in hormone-refractory prostate cancer patients treated with docetaxel-based chemotherapy.
    Eur Urol. 2009 Sep;56(3):479-84 PMID: 18585841
  85. Sequence of events in experimental metastases of Walker 256 tumor: light, immunofluorescent, and electron microscopic observations.
    J Natl Cancer Inst. 1971 Mar;46(3):493-504 PMID: 4100699
  86. Platelet-derived microparticles and coagulation activation in breast cancer patients.
    Thromb Haemost. 2008 Oct;100(4):663-9 PMID: 18841290
  87. Platelets and angiogenesis in malignancy.
    Semin Thromb Hemost. 2004 Feb;30(1):95-108 PMID: 15034801
  88. Integrin modulation and signaling in leukocyte adhesion and migration.
    Immunol Rev. 2007 Aug;218:126-34 PMID: 17624949
  89. Inhibition of tumor cell-induced platelet aggregation and lung metastasis by the oral GpIIb/IIIa antagonist XV454.
    Thromb Haemost. 2003 Sep;90(3):549-54 PMID: 12958625
  90. Malignancy, thrombosis and Trousseau: the case for an eponym.
    J Thromb Haemost. 2003 Dec;1(12):2463-5 PMID: 14675077
  91. Microenvironmental regulation of metastasis.
    Nat Rev Cancer. 2009 Apr;9(4):239-52 PMID: 19279573
  92. Platelet activation and platelet lipid composition in pulmonary cancer.
    Prostaglandins Leukot Essent Fatty Acids. 1995 Jul;53(1):65-8 PMID: 7675825
  93. Characterization of the proteins released from activated platelets leads to localization of novel platelet proteins in human atherosclerotic lesions.
    Blood. 2004 Mar 15;103(6):2096-104 PMID: 14630798
  94. Oncogenic and angiogenic growth factors accumulate during routine storage of apheresis platelet concentrates.
    Clin Cancer Res. 2008 Jun 15;14(12):3942-7 PMID: 18559616
  95. Spontaneous hematogenous and lymphatic metastasis, but not primary tumor growth or angiogenesis, is diminished in fibrinogen-deficient mice.
    Cancer Res. 2002 Dec 1;62(23):6966-72 PMID: 12460914
  96. Paraneoplastic syndromes: an approach to diagnosis and treatment.
    Mayo Clin Proc. 2010 Sep;85(9):838-54 PMID: 20810794
  97. Involvement of platelet membrane glycoprotein Ib and glycoprotein IIb/IIIa complex in thrombin-dependent and -independent platelet aggregations induced by tumor cells.
    Cancer Res. 1989 Feb 1;49(3):537-41 PMID: 2910473
  98. Deadly allies: the fatal interplay between platelets and metastasizing cancer cells.
    Blood. 2010 Apr 29;115(17):3427-36 PMID: 20194899
  99. Role of sphingosine-1 phosphate in the enhancement of endothelial barrier integrity by platelet-released products.
    Am J Physiol Lung Cell Mol Physiol. 2003 Jul;285(1):L258-67 PMID: 12626332
  100. Functional CXCR4-expressing microparticles and SDF-1 correlate with circulating acute myelogenous leukemia cells.
    Cancer Res. 2006 Nov 15;66(22):11013-20 PMID: 17108140
  101. A direct test of potential roles for beta3 and beta5 integrins in growth and metastasis of murine mammary carcinomas.
    Cancer Res. 2005 Nov 15;65(22):10324-9 PMID: 16288021
  102. Pancreatic cancer and thromboembolic disease.
    Lancet Oncol. 2004 Nov;5(11):655-63 PMID: 15522652
  103. Platelet-derived microparticles stimulate proliferation, survival, adhesion, and chemotaxis of hematopoietic cells.
    Exp Hematol. 2002 May;30(5):450-9 PMID: 12031651
  104. Tumor-stromal crosstalk in invasion of oral squamous cell carcinoma: a pivotal role of CCL7.
    Int J Cancer. 2010 Jul 15;127(2):332-44 PMID: 19937793
  105. Sphingosine 1-phosphate as a major bioactive lysophospholipid that is released from platelets and interacts with endothelial cells.
    Blood. 2000 Nov 15;96(10):3431-8 PMID: 11071638
  106. Plasma fibronectin promotes lung metastasis by contributions to fibrin clots and tumor cell invasion.
    Cancer Res. 2010 Jun 1;70(11):4327-34 PMID: 20501851
  107. Antimetastatic effects associated with platelet reduction.
    Proc Natl Acad Sci U S A. 1968 Sep;61(1):46-52 PMID: 5246932
  108. Expression of tissue factor by melanoma cells promotes efficient hematogenous metastasis.
    Proc Natl Acad Sci U S A. 1992 Dec 15;89(24):11832-6 PMID: 1465406
  109. Platelets as immune cells: bridging inflammation and cardiovascular disease.
    Circ Res. 2007 Jan 5;100(1):27-40 PMID: 17204662
  110. Histamine receptors and cancer pharmacology.
    Br J Pharmacol. 2010 Oct;161(4):755-67 PMID: 20636392
  111. Adhesion mechanisms in platelet function.
    Circ Res. 2007 Jun 22;100(12):1673-85 PMID: 17585075
  112. Tissue factor in cancer progression and angiogenesis.
    Thromb Res. 2010 Apr;125 Suppl 2:S36-8 PMID: 20434002
  113. Metastasis: from dissemination to organ-specific colonization.
    Nat Rev Cancer. 2009 Apr;9(4):274-84 PMID: 19308067
  114. Involvement of platelets in tumour angiogenesis?
    Lancet. 1998 Nov 28;352(9142):1775-7 PMID: 9848370
  115. Clinical significance of platelet count in patients with renal cell carcinoma.
    Urol Int. 2007;79(2):111-6 PMID: 17851278
  116. Microvesicles: mediators of extracellular communication during cancer progression.
    J Cell Sci. 2010 May 15;123(Pt 10):1603-11 PMID: 20445011
  117. Enhanced endothelial cell retraction mediated by 12(S)-HETE: a proposed mechanism for the role of platelets in tumor cell metastasis.
    Exp Cell Res. 1994 Jan;210(1):1-9 PMID: 8269984
  118. Targeting tumor cell-platelet interaction in breast cancer metastasis.
    Pathophysiol Haemost Thromb. 2003;33 Suppl 1:56-8 PMID: 12955006
  119. Protease-activated receptor (PAR) 2, but not PAR1, signaling promotes the development of mammary adenocarcinoma in polyoma middle T mice.
    Cancer Res. 2008 Sep 1;68(17):7219-27 PMID: 18757438
  120. Potential role of platelets in the pathogenesis of tumor metastasis.
    Blood. 1984 Jan;63(1):55-63 PMID: 6360248
  121. Tumor angiogenesis: therapeutic implications.
    N Engl J Med. 1971 Nov 18;285(21):1182-6 PMID: 4938153
  122. The role of calcium channels and serotonin (5-HT2) receptors for tumour cell lodgement in the liver.
    Clin Exp Metastasis. 1989 Mar-Apr;7(2):169-74 PMID: 2537694
  123. Platelets and platelet adhesion support angiogenesis while preventing excessive hemorrhage.
    Proc Natl Acad Sci U S A. 2006 Jan 24;103(4):855-60 PMID: 16418262
  124. Integrins in cancer: biological implications and therapeutic opportunities.
    Nat Rev Cancer. 2010 Jan;10(1):9-22 PMID: 20029421
  125. Platelets and fibrin(ogen) increase metastatic potential by impeding natural killer cell-mediated elimination of tumor cells.
    Blood. 2005 Jan 1;105(1):178-85 PMID: 15367435
  126. LPA and S1P increase corneal epithelial and endothelial cell transcellular resistance.
    Invest Ophthalmol Vis Sci. 2005 Jun;46(6):1927-33 PMID: 15914605
  127. Platelets actively sequester angiogenesis regulators.
    Blood. 2009 Mar 19;113(12):2835-42 PMID: 19036702
  128. Arrest and extravasation of B16 amelanotic melanoma in murine lungs. A light and electron microscopic study.
    Lab Invest. 1985 Oct;53(4):470-8 PMID: 4046557
  129. CXC chemokines in cancer angiogenesis and metastases.
    Adv Cancer Res. 2010;106:91-111 PMID: 20399957
  130. Increased preoperative platelet count is associated with decreased survival after resection for adenocarcinoma of the pancreas.
    Am J Surg. 2005 Mar;189(3):278-82 PMID: 15792750
  131. Activated integrin alphavbeta3 cooperates with metalloproteinase MMP-9 in regulating migration of metastatic breast cancer cells.
    Proc Natl Acad Sci U S A. 2003 Aug 5;100(16):9482-7 PMID: 12874388
  132. Inhibition of platelet GPIb alpha and promotion of melanoma metastasis.
    J Invest Dermatol. 2010 Feb;130(2):576-86 PMID: 19727118
  133. Tissue factor-positive microparticles: cellular origin and association with coagulation activation in patients with colorectal cancer.
    Thromb Haemost. 2007 Jan;97(1):119-23 PMID: 17200778
  134. Extrinsic-pathway activation in cancer with high factor VIIa and tissue factor.
    Lancet. 1995 Oct 14;346(8981):1004-5 PMID: 7475548
  135. The platelet count in carcinoma of the lung and colon.
    Thromb Haemost. 1990 Dec 28;64(4):501-5 PMID: 1964750
  136. Tumor-secreted vascular permeability factor increases cytosolic Ca2+ and von Willebrand factor release in human endothelial cells.
    Am J Pathol. 1991 Jan;138(1):213-21 PMID: 1987767
  137. Mechanisms and consequences of neutrophil interaction with the endothelium.
    Am J Pathol. 2008 Jan;172(1):1-7 PMID: 18079440
  138. Triggers, targets and treatments for thrombosis.
    Nature. 2008 Feb 21;451(7181):914-8 PMID: 18288180
  139. Thrombin stimulates tumor-platelet adhesion in vitro and metastasis in vivo.
    J Clin Invest. 1991 Jan;87(1):229-36 PMID: 1845869
  140. Tumor metastasis: mechanistic insights and clinical challenges.
    Nat Med. 2006 Aug;12(8):895-904 PMID: 16892035
  141. Selectins promote tumor metastasis.
    Semin Cancer Biol. 2010 Jun;20(3):169-77 PMID: 20452433
  142. Inhibition of metastasis in a murine 4T1 breast cancer model by liposomes preventing tumor cell-platelet interactions.
    Clin Exp Metastasis. 2010;27(1):25-34 PMID: 19916050
  143. Dissemination and growth of cancer cells in metastatic sites.
    Nat Rev Cancer. 2002 Aug;2(8):563-72 PMID: 12154349
  144. Platelet glycoprotein Ib alpha supports experimental lung metastasis.
    Proc Natl Acad Sci U S A. 2007 May 22;104(21):9024-8 PMID: 17494758
  145. Inhibition of platelet function: does it offer a chance of better cancer progression control?
    Semin Thromb Hemost. 2007 Oct;33(7):712-21 PMID: 18000800
  146. Proteinase-activated receptors 1 and 4 counter-regulate endostatin and VEGF release from human platelets.
    Proc Natl Acad Sci U S A. 2005 Jan 4;102(1):216-20 PMID: 15615851
  147. Role of von Willebrand factor in tumor metastasis.
    Thromb Res. 2007;120 Suppl 2:S64-70 PMID: 18023715
  148. Contrasting actions of selective inhibitors of angiopoietin-1 and angiopoietin-2 on the normalization of tumor blood vessels.
    Am J Pathol. 2009 Nov;175(5):2159-70 PMID: 19815705
  149. Membrane microvesicles: macromessengers in cancer disease and progression.
    Thromb Res. 2010 Apr;125 Suppl 2:S84-8 PMID: 20434014
  150. Therapeutic expression of the platelet-specific integrin, alphaIIbbeta3, in a murine model for Glanzmann thrombasthenia.
    Blood. 2005 Oct 15;106(8):2671-9 PMID: 15972454
  151. Heparin and cancer revisited: mechanistic connections involving platelets, P-selectin, carcinoma mucins, and tumor metastasis.
    Proc Natl Acad Sci U S A. 2001 Mar 13;98(6):3352-7 PMID: 11248082
  152. The dual role of thymidine phosphorylase in cancer development and chemotherapy.
    Med Res Rev. 2009 Nov;29(6):903-53 PMID: 19434693
  153. Platelets, protease-activated receptors, and fibrinogen in hematogenous metastasis.
    Blood. 2004 Jul 15;104(2):397-401 PMID: 15031212
  154. Lysis of tumor cells by natural killer cells in mice is impeded by platelets.
    Cancer Res. 1999 Mar 15;59(6):1295-300 PMID: 10096562
  155. Role of thrombin signalling in platelets in haemostasis and thrombosis.
    Nature. 2001 Sep 6;413(6851):74-8 PMID: 11544528
  156. Role of endogenous thrombin in tumor implantation, seeding, and spontaneous metastasis.
    Blood. 2004 Nov 1;104(9):2746-51 PMID: 15265791
  157. Thrombin generation and the pathogenesis of cancer.
    Semin Thromb Hemost. 2006 Apr;32 Suppl 1:61-8 PMID: 16673267
  158. Endothelial P-selectin as a target of heparin action in experimental melanoma lung metastasis.
    Cancer Res. 2004 Apr 15;64(8):2743-50 PMID: 15087389
  159. The metastatic niche: adapting the foreign soil.
    Nat Rev Cancer. 2009 Apr;9(4):285-93 PMID: 19308068
  160. Elevated levels of circulating platelet microparticles, VEGF, IL-6 and RANTES in patients with gastric cancer: possible role of a metastasis predictor.
    Eur J Cancer. 2003 Jan;39(2):184-91 PMID: 12509950
  161. Innate immune cells induce hemorrhage in tumors during thrombocytopenia.
    Am J Pathol. 2009 Oct;175(4):1699-708 PMID: 19729481
  162. Platelet granule secretion continuously prevents intratumor hemorrhage.
    Cancer Res. 2008 Aug 15;68(16):6851-8 PMID: 18701510
  163. Anti-cancer properties of low-molecular-weight heparin: preclinical evidence.
    Thromb Haemost. 2009 Aug;102(2):258-67 PMID: 19652876
  164. Cancer metastasis: building a framework.
    Cell. 2006 Nov 17;127(4):679-95 PMID: 17110329
  165. Increased soluble P-selectin in patients with haematological and breast cancer: a comparison with fibrinogen, plasminogen activator inhibitor and von Willebrand factor.
    Blood Coagul Fibrinolysis. 2001 Jan;12(1):43-50 PMID: 11229826
  166. Cancer cell expression of autotaxin controls bone metastasis formation in mouse through lysophosphatidic acid-dependent activation of osteoclasts.
    PLoS One. 2010 Mar 17;5(3):e9741 PMID: 20305819
  167. Twist is required for thrombin-induced tumor angiogenesis and growth.
    Cancer Res. 2008 Jun 1;68(11):4296-302 PMID: 18519689
  168. Nucleotide-binding domain of phosphoglycerate kinase 1 reduces tumor growth by suppressing COX-2 expression.
    Cancer Sci. 2010 Nov;101(11):2411-6 PMID: 20731664
Article Info
Journal
Nature reviews. Cancer
Abbr.
Nat Rev Cancer
ISSN
1474-1768
DOI
10.1038/nrc3004
Published
2011-02-00
Pages
123-34
Language
English
Region
England
NLM ID
101124168
PMCID
PMC6894505
Subset
IM
Grants
NCI NIH HHS · R01 CA112287 · United States
NCRR NIH HHS · 5TL1RR025772-03 · United States
NCI NIH HHS · CA 112287 · United States
Corrections
CommentIn
PMID: 21863051
External Links
PubMed source DOI: 10.1038/nrc3004 PMC Full Text View journal details
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