Home LiteratureArticle Details
PMID: 1423821 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S. Review

Platelets and cancer metastasis: a causal relationship?

Cancer metastasis reviews ·Vol. 11 ·No. 3-4 ·1992-11-00 ·Pages 325-51

Honn KV, Tang DG, Crissman JD

Abstract

Cancer metastasis is a highly coordinated and dynamic multistep process in which cancer cells undergo extensive interactions with various host cells before they establish a secondary metastatic colony. Ample morphological studies have documented the close association of circulating tumor cells with host platelets. Several lines of evidence provide strong support for the concept that tumor cell-platelet interactions (i.e., TCIPA) significantly contribute to hematogenous metastasis. Clinically, cancer patients with advanced diseases are characterized by a variety of thromboembolic disorders including thrombocytosis. Pharmacologically, various anti-platelet agents/anticoagulants have demonstrated potent inhibitory effects on tumor cell-platelet interactions as well as spontaneous or experimental metastasis. Experimentally, interference with many of the intermediate steps of tumor cell-platelet interactions has resulted in diminished platelet aggregation induced by tumor cells and blocked cancer metastasis. Platelet interaction with tumor cells is a sequential process which involves two general types of mediators, i.e., membrane-bound molecules (adhesion molecules) and soluble release products. alpha IIb beta 3 integrin receptors present on both platelets as well as on tumor cells and 12(S)-HETE, a 12-lipoxygenase metabolite of arachidonic acid, are prototypical examples of each category. Mechanistically, platelets may contribute to metastasis by: (1) stabilizing tumor cell arrest in the vasculature, (2) stimulating tumor cell proliferation, (3) promoting tumor cells extravasation by potentiating tumor cell-induced endothelial cell retraction, and (4) enhancing tumor cell interaction with the extracellular matrix.

MeSH Terms
Animals Blood Platelets/physiology Cell Communication/physiology Humans Neoplasm Metastasis/physiopathology Platelet Aggregation/physiology
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Honn K V
Department of Radiation Oncology, Wayne State University, Detroit, MI 48202.
Tang D G
Crissman J D
References (159)
159 references, click to expand
  1. 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
  2. Correlation between spontaneous metastatic potential, platelet-aggregating activity of cell surface extracts, and cell surface sialylation in 10 metastatic-variant derivatives of a rat renal sarcoma cell line.
    Proc Natl Acad Sci U S A. 1980 Jul;77(7):4336-9 PMID: 6933486
  3. Platelet-aggregating activities of metastasizing tumor cells. V. In situ roles of platelets in hematogenous metastases.
    Invasion Metastasis. 1986;6(4):209-24 PMID: 3759361
  4. Platelet enhancement of tumor cell adhesion to subendothelial matrix: role of platelet cytoskeleton and platelet membrane.
    J Natl Cancer Inst. 1987 Nov;79(5):1077-90 PMID: 3479634
  5. Influence of tumor-derived interleukin 1 on melanoma-endothelial cell interactions in vitro.
    Cancer Res. 1991 Sep 15;51(18):4768-75 PMID: 1680022
  6. Inhibition by prostacyclin of the tumor cell-induced platelet release reaction and platelet aggregation.
    J Natl Cancer Inst. 1987 May;78(5):961-9 PMID: 3553692
  7. Endothelial cell-associated platelet-activating factor: a novel mechanism for signaling intercellular adhesion.
    J Cell Biol. 1990 Feb;110(2):529-40 PMID: 2153685
  8. Presence of cytoadhesins (IIb-IIIa-like glycoproteins) on human metastatic melanomas but not on benign melanocytes.
    Am J Clin Pathol. 1989 Oct;92(4):495-9 PMID: 2801613
  9. Arachidonic acid metabolism of cytosolic fractions of Lewis lung carcinoma cells.
    Adv Prostaglandin Thromboxane Leukot Res. 1991;21B:895-900 PMID: 1825434
  10. CD62 and endothelial cell-leukocyte adhesion molecule 1 (ELAM-1) recognize the same carbohydrate ligand, sialyl-Lewis x.
    Proc Natl Acad Sci U S A. 1991 Jul 15;88(14):6224-8 PMID: 1712483
  11. Investigation of the biological effects of anti-cell adhesive synthetic peptides that inhibit experimental metastasis of B16-F10 murine melanoma cells.
    J Clin Invest. 1988 Mar;81(3):782-90 PMID: 3343338
  12. Granule membrane protein 140 (GMP140) binds to carcinomas and carcinoma-derived cell lines.
    Proc Natl Acad Sci U S A. 1992 Mar 15;89(6):2292-6 PMID: 1372439
  13. Increased expression of alpha IIb beta 3 integrin in subpopulations of murine melanoma cells with high lung-colonizing ability.
    Int J Cancer. 1992 May 28;51(3):445-51 PMID: 1375589
  14. Laminin receptor on platelets is the integrin VLA-6.
    Nature. 1988 Dec 1;336(6198):487-9 PMID: 2973567
  15. Inhibition of in vitro tumor cell invasion by Arg-Gly-Asp-containing synthetic peptides.
    J Cell Biol. 1988 Mar;106(3):925-30 PMID: 2450101
  16. Thrombin immobilized to extracellular matrix is a potent mitogen for vascular smooth muscle cells: nonenzymatic mode of action.
    Cell Regul. 1990 May;1(6):453-63 PMID: 1963793
  17. Expression of a Mr 41,000 glycoprotein associated with thrombin-independent platelet aggregation in high metastatic variants of murine B16 melanoma.
    Cancer Res. 1990 Oct 15;50(20):6657-62 PMID: 2208129
  18. Platelets and cancer metastasis: more than an epiphenomenon.
    Semin Thromb Hemost. 1992;18(4):392-415 PMID: 1470927
  19. Oxygen radicals induce human endothelial cells to express GMP-140 and bind neutrophils.
    J Cell Biol. 1991 Feb;112(4):749-59 PMID: 1704376
  20. The lipoxygenase metabolite 12(S)-HETE promotes alpha IIb beta 3 integrin-mediated tumor-cell spreading on fibronectin.
    Int J Cancer. 1992 Oct 21;52(4):594-603 PMID: 1399143
  21. 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
  22. Characterization of the platelet-aggregating activity of cancer cells with different metastatic potential.
    Int J Cancer. 1986 Aug 15;38(2):237-44 PMID: 3733262
  23. Human carcinoma cells express receptors for distinct domains of thrombospondin.
    Cancer Res. 1991 Mar 15;51(6):1645-50 PMID: 1705477
  24. Metastatic potential of colon carcinoma. Expression of ABO/Lewis-related antigens.
    Arch Surg. 1990 Feb;125(2):206-9 PMID: 2302060
  25. Suppression of experimental lung colonization of a metastatic variant of murine colon adenocarcinoma 26 by a monoclonal antibody 8F11 inhibiting tumor cell-induced platelet aggregation.
    Cancer Res. 1991 Feb 1;51(3):921-5 PMID: 1988132
  26. The human fibroblast class II extracellular matrix receptor mediates platelet adhesion to collagen and is identical to the platelet glycoprotein Ia-IIa complex.
    J Biol Chem. 1988 Apr 5;263(10):4516-9 PMID: 2832397
  27. Tumor cell-platelet-endothelial cell interactions and prostaglandin metabolism.
    Adv Prostaglandin Thromboxane Leukot Res. 1987;17B:981-5 PMID: 2960216
  28. Tumor-induced platelet aggregation and growth promoting factors as determinants for successful tumor metastasis.
    Clin Exp Metastasis. 1986 Jan-Mar;4(1):25-33 PMID: 3698366
  29. Characterization of platelet aggregation induced by the human melanoma cell line HMV-I: roles of heparin, plasma adhesive proteins, and tumor cell membrane proteins.
    Cancer Res. 1991 Feb 15;51(4):1286-93 PMID: 1847662
  30. Platelet-melanoma cell interaction is mediated by the glycoprotein IIb-IIIa complex.
    Blood. 1989 Aug 1;74(2):658-63 PMID: 2752140
  31. Signal transduction by integrins: increased protein tyrosine phosphorylation caused by clustering of beta 1 integrins.
    Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8392-6 PMID: 1717976
  32. Prostacyclin, thromboxanes, and hematogenous metastasis.
    Adv Prostaglandin Thromboxane Leukot Res. 1983;12:313-8 PMID: 6221609
  33. Platelet-aggregating activities of metastasizing tumor cells. IV. Effects of cell surface modification on thrombin generation, platelet aggregation and subsequent lung colonization.
    Invasion Metastasis. 1986;6(1):58-68 PMID: 3941029
  34. The importance of 5-HT for tumor cell lodgement in the liver.
    Int J Cancer. 1984 Apr 15;33(4):519-23 PMID: 6368410
  35. Disintegrins: a family of integrin inhibitory proteins from viper venoms.
    Proc Soc Exp Biol Med. 1990 Nov;195(2):168-71 PMID: 2236100
  36. Inhibition of tumor cell-induced platelet aggregation and experimental tumor metastasis by the synthetic Gly-Arg-Gly-Asp-Ser peptide.
    J Natl Cancer Inst. 1988 Nov 16;80(18):1461-6 PMID: 3184195
  37. The membrane skeleton--a distinct structure that regulates the function of cells.
    Bioessays. 1988 Jan;8(1):14-8 PMID: 3284521
  38. Inhibition of tumor cell induced platelet aggregation by prostacyclin and carbacyclin: an ultrastructural study.
    Invasion Metastasis. 1987;7(2):109-28 PMID: 3294727
  39. Loss of metastatic and primary tumor factor X activator capabilities by Lewis lung carcinoma cells cultured in vitamin K-dependent protein deficient serum.
    Cancer Res. 1988 Nov 15;48(22):6504-9 PMID: 3180067
  40. Prostacyclin and thromboxanes. Implications for their role in tumor cell metastasis.
    Biochem Pharmacol. 1983 Jan 1;32(1):1-11 PMID: 6338880
  41. Enhanced tumor cell adhesion to the subendothelial matrix resulting from 12(S)-HETE-induced endothelial cell retraction.
    FASEB J. 1989 Sep;3(11):2285-93 PMID: 2673900
  42. Early presence of activated ('exhausted') platelets in malignant tumors (breast adenocarcinoma and malignant melanoma).
    Eur J Cancer Clin Oncol. 1989 Oct;25(10):1413-7 PMID: 2531669
  43. Inhibition of human tumor cell induced platelet aggregation by antibodies to platelet glycoproteins Ib and IIb/IIIa.
    Proc Soc Exp Biol Med. 1987 Dec;186(3):378-83 PMID: 3423021
  44. Plasma-dependent and -independent mechanisms of platelet aggregation induced by human tumour cell lines.
    Thromb Res. 1987 Jun 1;46(5):715-26 PMID: 3629545
  45. Platelet membrane glycoproteins: functions in cellular interactions.
    Annu Rev Cell Biol. 1990;6:329-57 PMID: 2275816
  46. Stimulation of the growth of metastatic clones of mouse colon adenocarcinoma 26 in vitro by platelet-derived growth factor.
    Jpn J Cancer Res. 1989 Feb;80(2):136-40 PMID: 2542203
  47. Interactions of cancer cells with the microvasculature during metastasis.
    FASEB J. 1988 Jan;2(1):12-21 PMID: 3275560
  48. Tumor-cell-platelet aggregation does not correlate with metastatic potential of rat 13762NF mammary adenocarcinoma tumor cell clones.
    Int J Cancer. 1984 Jul 15;34(1):101-5 PMID: 6746111
  49. Is there a role for the tumor cell integrin alpha IIb beta 3 and cytoskeleton in tumor cell-platelet interaction?
    Clin Exp Metastasis. 1992 Mar;10(2):125-37 PMID: 1371433
  50. Effects of prostacyclin on tumor cell-induced platelet aggregation.
    Cancer Res. 1984 Feb;44(2):450-6 PMID: 6362850
  51. Rapid neutrophil adhesion to activated endothelium mediated by GMP-140.
    Nature. 1990 Feb 22;343(6260):757-60 PMID: 1689464
  52. Functional role of platelets in experimental metastasis studied with cloned murine fibrosarcoma cell variants.
    Cancer Res. 1988 Mar 15;48(6):1460-4 PMID: 3345518
  53. Biochemical characterization of PECAM-1 (CD31 antigen) on human platelets.
    Thromb Haemost. 1991 Dec 2;66(6):700-7 PMID: 1796415
  54. Interaction of fibrinogen with murine melanoma cells: covalent association with cell membranes and protection against recognition by lymphokine-activated killer cells.
    Cancer Res. 1990 Dec 15;50(24):8010-6 PMID: 2253243
  55. A new in vitro model for investigation of tumor cell-platelet-endothelial cell interactions and concomitant eicosanoid biosynthesis.
    Cancer Res. 1987 May 1;47(9):2425-32 PMID: 3552214
  56. Integrins: a family of cell surface receptors.
    Cell. 1987 Feb 27;48(4):549-54 PMID: 3028640
  57. Morphological study of the interaction of intravascular tumor cells with endothelial cells and subendothelial matrix.
    Cancer Res. 1988 Jul 15;48(14):4065-72 PMID: 3383198
  58. Cell adhesion, spreading, and motility of GM3-expressing cells based on glycolipid-glycolipid interaction.
    J Biol Chem. 1991 Sep 15;266(26):17552-8 PMID: 1894638
  59. A synthetic peptide from fibronectin inhibits experimental metastasis of murine melanoma cells.
    Science. 1986 Jul 25;233(4762):467-70 PMID: 3726541
  60. Endothelialization of embolized tumor cells during metastasis formation.
    Clin Exp Metastasis. 1988 Jan-Feb;6(1):73-89 PMID: 3335082
  61. Hemostasis following inoculation and during spreading of colon carcinoma in the rat.
    Cancer Res. 1986 Nov;46(11):5662-6 PMID: 3756913
  62. Recombinant E-selectin-protein mediates tumor cell adhesion via sialyl-Le(a) and sialyl-Le(x).
    Biochem Biophys Res Commun. 1992 Feb 14;182(3):1376-82 PMID: 1371681
  63. Alpha IIb beta 3 integrin expression and function in subpopulations of murine tumors.
    Exp Cell Res. 1992 Jul;201(1):23-32 PMID: 1377132
  64. Biological activities of peptides and peptide analogues derived from common sequences present in thrombospondin, properdin, and malarial proteins.
    J Cell Biol. 1992 Jan;116(1):209-17 PMID: 1730745
  65. Mechanisms of the antimetastatic activity of stable prostacyclin analogues: modulation of host immunocompetence.
    Adv Prostaglandin Thromboxane Leukot Res. 1991;21B:917-20 PMID: 1705087
  66. The role of GTP-binding proteins in platelet activation.
    Thromb Haemost. 1991 Oct 1;66(4):393-9 PMID: 1665593
  67. Role of IIb-IIIa-like glycoproteins in cell-substratum adhesion of human melanoma cells.
    J Cell Physiol. 1988 Sep;136(3):471-8 PMID: 3170644
  68. Integrins as mechanochemical transducers.
    Curr Opin Cell Biol. 1991 Oct;3(5):841-8 PMID: 1931084
  69. Decreased stabilization of prostacyclin activity in patients with bone tumors.
    Cancer Res. 1984 Jul;44(7):3132-4 PMID: 6373003
  70. How do cells sense and respond to adhesive contacts? Diffusion-trapping of laterally mobile membrane proteins at maturing adhesions may initiate signals leading to local cytoskeletal assembly response and lamella formation.
    J Cell Sci. 1992 Feb;101 ( Pt 2):255-66 PMID: 1629243
  71. Bidirectional control of membrane expression and/or activation of the tumor cell IRGpIIb/IIIa receptor and tumor cell adhesion by lipoxygenase products of arachidonic acid and linoleic acid.
    Cancer Res. 1989 Feb 15;49(4):1029-37 PMID: 2492204
  72. Separation of high and low metastatic subpopulations from solid tumors by centrifugal elutriation.
    Proc Soc Exp Biol Med. 1988 Feb;187(2):250-5 PMID: 2829227
  73. 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
  74. Inhibition of tumor cell metastasis by modulation of the vascular prostacyclin/thromboxane A2 system.
    Clin Exp Metastasis. 1983 Apr-Jun;1(2):103-14 PMID: 6242706
  75. Lipoxygenase products regulate IRGpIIb/IIIa receptor mediated adhesion of tumor cells to endothelial cells, subendothelial matrix and fibronectin.
    Proc Soc Exp Biol Med. 1988 Oct;189(1):130-5 PMID: 3141931
  76. Selectin GMP-140 (CD62; PADGEM) binds to sialosyl-Le(a) and sialosyl-Le(x), and sulfated glycans modulate this binding.
    Biochem Biophys Res Commun. 1991 Dec 31;181(3):1223-30 PMID: 1722400
  77. Role of tumor cytoskeleton and membrane glycoprotein IRGpIIb/IIIa in platelet adhesion to tumor cell membrane and tumor cell-induced platelet aggregation.
    Cancer Res. 1988 Jul 1;48(13):3787-800 PMID: 2837325
  78. Analysis of integrin mRNA in human and rodent tumor cells.
    Biochem Biophys Res Commun. 1991 Apr 15;176(1):108-13 PMID: 1708240
  79. Protein kinase C and cyclic AMP regulate reversible exposure of binding sites for fibrinogen on the glycoprotein IIB-IIIA complex of human platelets.
    Biochem J. 1991 Jan 1;273(Pt 1):115-20 PMID: 1846526
  80. Identification of a platelet-aggregating factor of murine colon adenocarcinoma 26: Mr 44,000 membrane protein as determined by monoclonal antibodies.
    Cancer Res. 1988 Nov 15;48(22):6411-6 PMID: 3180058
  81. Human colorectal adenocarcinoma cells: differential nitric oxide synthesis determines their ability to aggregate platelets.
    Cancer Res. 1991 Nov 15;51(22):6073-8 PMID: 1718593
  82. Role of the alpha v beta 3 integrin in human melanoma cell invasion.
    Proc Natl Acad Sci U S A. 1992 Mar 1;89(5):1557-61 PMID: 1371877
  83. Recognition by ELAM-1 of the sialyl-Lex determinant on myeloid and tumor cells.
    Science. 1990 Nov 23;250(4984):1132-5 PMID: 1701275
  84. 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
  85. The structure and function of platelet integrins.
    Curr Opin Cell Biol. 1989 Oct;1(5):947-52 PMID: 2483335
  86. New families of adhesion molecules play a vital role in platelet functions.
    Immunol Today. 1990 Jul;11(7):225-7 PMID: 2201305
  87. Isolation and characterization of cancer procoagulant: a cysteine proteinase from malignant tissue.
    Biochemistry. 1985 Sep 24;24(20):5558-67 PMID: 3935163
  88. Thrombospondin binds to the surface of human osteosarcoma cells and mediates platelet-osteosarcoma cell interaction.
    Cancer Res. 1991 May 15;51(10):2621-7 PMID: 1708697
  89. Carbohydrate ligands for endothelial-leukocyte adhesion molecule 1.
    Proc Natl Acad Sci U S A. 1991 Feb 15;88(4):1138-42 PMID: 1705026
  90. Identification of glycoprotein IV (CD36) as a primary receptor for platelet-collagen adhesion.
    J Biol Chem. 1989 May 5;264(13):7576-83 PMID: 2468670
  91. Antimetastatic effects of synthetic polypeptides containing repeated structures of the cell adhesive Arg-Gly-Asp (RGD) and Tyr-Ile-Gly-Ser-Arg (YIGSR) sequences.
    Br J Cancer. 1989 Nov;60(5):722-8 PMID: 2803948
  92. Ligands "activate" integrin alpha IIb beta 3 (platelet GPIIb-IIIa).
    Cell. 1991 May 3;65(3):409-16 PMID: 2018974
  93. Antimetastatic effects associated with platelet reduction.
    Proc Natl Acad Sci U S A. 1968 Sep;61(1):46-52 PMID: 5246932
  94. PECAM-1 (CD31) cloning and relation to adhesion molecules of the immunoglobulin gene superfamily.
    Science. 1990 Mar 9;247(4947):1219-22 PMID: 1690453
  95. Thrombospondin, a potentiator of tumor cell metastasis.
    Cancer Res. 1987 Aug 1;47(15):4130-3 PMID: 3607754
  96. Contact and adhesive specificities in the associations, migrations, and targeting of cells and axons.
    Cell. 1992 Jan 24;68(2):303-22 PMID: 1733501
  97. Binding of human factors X and Xa to HepG2 and J82 human tumor cell lines. Evidence that factor Xa binds to tumor cells independent of factor Va.
    J Biol Chem. 1990 Jun 5;265(16):9105-13 PMID: 2160956
  98. Downregulation of GMP-140 (CD62 or PADGEM) expression on platelets by N,N-dimethyl and N,N,N-trimethyl derivatives of sphingosine.
    Biochemistry. 1991 Dec 17;30(50):11682-6 PMID: 1721534
  99. Potentiation and inhibition of tumor cell invasion by host cells and mediators.
    Invasion Metastasis. 1989;9(2):134-48 PMID: 2708005
  100. Thromboxane production by platelets during tumor cell-induced platelet activation.
    Invasion Metastasis. 1991;11(2):102-9 PMID: 1917383
  101. Increased expression of sialyl-dimeric LeX antigen in liver metastases of human colorectal carcinoma.
    Cancer Res. 1989 Dec 15;49(24 Pt 1):6883-8 PMID: 2573422
  102. Thromboxanes and prostacyclin: positive and negative modulators of tumor growth.
    Biochem Biophys Res Commun. 1981 Oct 30;102(4):1122-9 PMID: 6274330
  103. New directions in cancer therapy based on aberrant expression of glycosphingolipids: anti-adhesion and ortho-signaling therapy.
    Cancer Cells. 1991 Dec;3(12):461-70 PMID: 1820092
  104. Sialyltransferase activity and hepatic tumor growth in a nude mouse model of colorectal cancer metastases.
    Cancer Res. 1992 Apr 1;52(7):1775-9 PMID: 1312899
  105. The inhibition of platelet aggregation of metastatic H-ras-transformed 10T1/2 fibroblasts with castanospermine, an N-linked glycoprotein processing inhibitor.
    Cancer Lett. 1991 Dec 1;60(3):185-91 PMID: 1756507
  106. The role of platelet cyclooxygenase and lipoxygenase pathways in tumor cell induced platelet aggregation.
    Biochem Biophys Res Commun. 1987 May 29;145(1):384-9 PMID: 3109414
  107. Purification and characterization of platelet aggregating activity from tumor cells: copurification with procoagulant activity.
    Thromb Res. 1985 Jan 15;37(2):309-26 PMID: 3975874
  108. Tumor-cell-induced platelet aggregation is a glycoprotein-dependent and lipoxygenase-associated process.
    Int J Cancer. 1987 Jun 15;39(6):760-3 PMID: 3034806
  109. Platelet fibronectin release induced by Walker 256 rat carcinoma tumor cells.
    Clin Exp Metastasis. 1985 Jul-Sep;3(3):209-20 PMID: 3902301
  110. The possible role of blood platelets in tumour growth and dissemination.
    Haematologica. 1986 May-Jun;71(3):245-55 PMID: 3093331
  111. Activation-independent exposure of the GPIIb-IIIa fibrinogen receptor.
    Thromb Res. 1991 Aug 1;63(3):343-54 PMID: 1957276
  112. Human lung adenocarcinoma cell lines with different lung colonization potential (LCP), and a correlation between expression of sialosyl dimeric Le(x) (defined by MAb FH6) and LCP.
    Clin Exp Metastasis. 1991 May-Jun;9(3):245-57 PMID: 1676353
  113. 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
  114. Interactions between cancer cells and the microvasculature: a rate-regulator for metastasis.
    Clin Exp Metastasis. 1989 Mar-Apr;7(2):127-67 PMID: 2465861
  115. Selectins: novel receptors that mediate leukocyte adhesion during inflammation.
    Thromb Haemost. 1991 Mar 4;65(3):223-8 PMID: 1710835
  116. New perspectives in cell adhesion: RGD and integrins.
    Science. 1987 Oct 23;238(4826):491-7 PMID: 2821619
  117. Role of platelet membrane in enhancement of tumor cell adhesion to endothelial cell extracellular matrix.
    Cancer Res. 1987 Dec 15;47(24 Pt 1):6751-62 PMID: 2824041
  118. Acquisition of metastatic ability in hybridomas between two low metastatic clones of murine colon adenocarcinoma 26 defective in either platelet-aggregating activity or in vivo growth potential.
    Cancer Res. 1987 Aug 15;47(16):4396-401 PMID: 3607771
  119. Activation of platelet heparitinase by tumor cell-derived factors.
    Blood. 1991 Aug 1;78(3):789-96 PMID: 1859891
  120. Trigramin, an RGD-containing peptide from snake venom, inhibits cell-substratum adhesion of human melanoma cells.
    Exp Cell Res. 1988 Nov;179(1):42-9 PMID: 3049127
  121. Tumor cell-platelet interactions in vitro and their relationship to in vivo arrest of hematogenously circulating tumor cells.
    Clin Exp Metastasis. 1987 Jan-Mar;5(1):65-78 PMID: 3829498
  122. Lipoxygenase metabolites of arachidonic and linoleic acids modulate the adhesion of tumor cells to endothelium via regulation of protein kinase C.
    Cell Regul. 1991 Dec;2(12):1045-55 PMID: 1801923
  123. Thrombin stimulates tumor-platelet adhesion in vitro and metastasis in vivo.
    J Clin Invest. 1991 Jan;87(1):229-36 PMID: 1845869
  124. Pathogenesis of metastasis formation observed in vivo in the rabbit ear chamber.
    AMA Arch Pathol. 1958 Oct;66(4):550-68 PMID: 13582395
  125. ELAM-1 mediates cell adhesion by recognition of a carbohydrate ligand, sialyl-Lex.
    Science. 1990 Nov 23;250(4984):1130-2 PMID: 1701274
  126. Human rhabdosarcoma cell-induced aggregation of blood platelets.
    Cancer Res. 1989 Jan 1;49(1):16-9 PMID: 2491750
  127. Specific interaction between Lex and Lex determinants. A possible basis for cell recognition in preimplantation embryos and in embryonal carcinoma cells.
    J Biol Chem. 1989 Jun 5;264(16):9476-84 PMID: 2470757
  128. Ligand bridging mediates integrin alpha IIb beta 3 (platelet GPIIB-IIIA) dependent homotypic and heterotypic cell-cell interactions.
    J Clin Invest. 1991 Oct;88(4):1128-34 PMID: 1918367
  129. Inhibition of murine melanoma cell-matrix adhesion and experimental metastasis by albolabrin, an RGD-containing peptide isolated from the venom of Trimeresurus albolabris.
    Exp Cell Res. 1991 Sep;196(1):6-12 PMID: 1879472
  130. PMN adhesion and extravasation as a paradigm for tumor cell dissemination.
    Cancer Metastasis Rev. 1991 May;10(1):61-78 PMID: 1914073
  131. Chemotactic activity of bone and platelet-derived TGF-beta for bone-metastasizing rat Walker 256 carcinosarcoma cells.
    Invasion Metastasis. 1990;10(4):241-52 PMID: 2358328
  132. Binding of the snake venom-derived proteins applaggin and echistatin to the arginine-glycine-aspartic acid recognition site(s) on platelet glycoprotein IIb.IIIa complex inhibits receptor function.
    J Biol Chem. 1990 Jul 15;265(20):11766-72 PMID: 2365698
  133. The lack of correlation between experimental metastatic potential and platelet aggregating activity of B16 melanoma clones viewed in relation to tumor cell heterogeneity.
    Clin Exp Metastasis. 1987 Apr-Jun;5(2):125-33 PMID: 3594970
  134. Activation of platelet prostaglandin biosynthesis pathway during neoplastic cell-induced platelet aggregation.
    Thromb Res. 1984 Apr 15;34(2):147-57 PMID: 6729776
  135. Leukocyte-endothelial cell recognition: three (or more) steps to specificity and diversity.
    Cell. 1991 Dec 20;67(6):1033-6 PMID: 1760836
  136. Possible mechanism of inhibition of experimental pulmonary metastasis of mouse colon adenocarcinoma 26 sublines by a sialic acid: nucleoside conjugate.
    Cancer Res. 1988 Jul 1;48(13):3728-32 PMID: 3288333
  137. Occupancy of an adhesive glycoprotein receptor modulates expression of an antigenic site involved in cell adhesion.
    J Biol Chem. 1988 Sep 5;263(25):12397-402 PMID: 2457583
  138. Platelet contribution to the formation of metastatic foci: the role of cancer cell-induced platelet activation.
    Haemostasis. 1988;18(1):29-36 PMID: 3047021
  139. Multiple very late antigen (VLA) heterodimers on platelets. Evidence for distinct VLA-2, VLA-5 (fibronectin receptor), and VLA-6 structures.
    J Biol Chem. 1988 Jun 5;263(16):7660-5 PMID: 2967289
  140. An Arg-Gly-Asp sequence within thrombin promotes endothelial cell adhesion.
    J Cell Biol. 1991 Jan;112(2):335-44 PMID: 1988465
  141. Prostacyclin: a potent antimetastatic agent.
    Science. 1981 Jun 12;212(4500):1270-2 PMID: 7015512
  142. HLA-DR is a procoagulant.
    Biochem Biophys Res Commun. 1991 Jul 31;178(2):467-73 PMID: 1859406
  143. Cloning of GMP-140, a granule membrane protein of platelets and endothelium: sequence similarity to proteins involved in cell adhesion and inflammation.
    Cell. 1989 Mar 24;56(6):1033-44 PMID: 2466574
  144. Isolation and characterization of a platelet membrane protein related to the vitronectin receptor.
    J Biol Chem. 1989 Mar 5;264(7):3742-9 PMID: 2465293
  145. Inhibition of selectin-dependent tumor cell adhesion to endothelial cells and platelets by blocking O-glycosylation of these cells.
    Biochem Biophys Res Commun. 1992 Feb 14;182(3):1288-95 PMID: 1371678
  146. Effect of human tumor cells on platelet aggregation: potential relevance to pattern of metastasis.
    Cancer Res. 1987 Jun 15;47(12):3115-7 PMID: 3472652
  147. An inducible endothelial cell surface glycoprotein mediates melanoma adhesion.
    Science. 1989 Dec 8;246(4935):1303-6 PMID: 2588007
  148. Role of tumor cell glycoproteins immunologically related to glycoproteins Ib and IIb/IIIa in tumor cell-platelet and tumor cell-matrix interactions.
    FASEB J. 1988 May;2(8):2385-95 PMID: 2452113
  149. Platelet-derived interleukin 1 induces human endothelial adhesion molecule expression and cytokine production.
    J Exp Med. 1991 Oct 1;174(4):785-90 PMID: 1680957
  150. Synthetic RGDS-containing peptides of von Willebrand factor inhibit platelet adhesion to collagen.
    Thromb Haemost. 1990 Dec 28;64(4):589-93 PMID: 2084945
  151. Lipoxygenase regulation of membrane expression of tumor cell glycoproteins and subsequent metastasis.
    Adv Prostaglandin Thromboxane Leukot Res. 1989;19:439-43 PMID: 2526514
  152. PADGEM: an adhesion receptor for leukocytes on stimulated platelets and endothelial cells.
    Proc Soc Exp Biol Med. 1991 Nov;198(2):703-9 PMID: 1718006
  153. An in vivo study of the role of the tumor cell cytoskeleton in tumor cell-platelet-endothelial cell interactions.
    Cancer Res. 1990 Dec 1;50(23):7686-96 PMID: 2253213
  154. The lipoxygenase metabolite 12(S)-HETE induces a cytoskeleton-dependent increase in surface expression of integrin alpha IIb beta 3 on melanoma cells.
    Int J Cancer. 1991 Nov 11;49(5):774-86 PMID: 1937964
  155. Role of plasma, platelets, and endothelial cells in tumor metastasis.
    Cancer Metastasis Rev. 1984;3(2):99-114 PMID: 6386144
  156. The role of polymorphonuclear leukocytes (PMN) on the growth and metastatic potential of 13762NF mammary adenocarcinoma cells.
    Int J Cancer. 1988 Nov 15;42(5):748-59 PMID: 2846449
  157. Tumor cells are protected from NK-cell-mediated lysis by adhesion to endothelial cells.
    Int J Cancer. 1988 Jun 15;41(6):847-9 PMID: 3372060
  158. Inhibition of experimental pulmonary metastasis of mouse colon adenocarcinoma 26 sublines by a sialic acid:nucleoside conjugate having sialyltransferase inhibiting activity.
    Cancer Res. 1986 Feb;46(2):858-62 PMID: 3753583
  159. Affinity modulation of the alpha IIb beta 3 integrin (platelet GPIIb-IIIa) is an intrinsic property of the receptor.
    Cell Regul. 1990 Nov;1(12):883-93 PMID: 2100193
Article Info
Journal
Cancer metastasis reviews
Abbr.
Cancer Metastasis Rev
ISSN
0167-7659
DOI
10.1007/BF01307186
Published
1992-11-00
Pages
325-51
Language
English
Region
Netherlands
NLM ID
8605731
Subset
IM
Grants
NCI NIH HHS · CA 29997-10 · United States
NCI NIH HHS · CA 47115-05 · United States
External Links
PubMed source DOI: 10.1007/BF01307186 View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2