Thromb Haemost 1993; 69(05): 406-414
Schattauer GmbH Stuttgart
Fibrin and Cancer
Vincenzo Costantini
1
The Institute of Internal and Vascular Medicine, University of Perugia, Perugia, Italy
,
Leo R Zacharski
2
The Department of Medicine, Dartmouth Medical School, Hanover, New Hampshire; and
the Department of Veterans Affairs Medical and Regional Office Center, White River
Junction, Vermont, USA
› Author Affiliations
References
1
Trousseau A.
Phlegmasia alba dolens. Clin Med Hotel Dieu de Paris. London: New Sydenham Society;
1865 3. 94 2
Billroth T.
Lectures on Surgical Pathology and Therapeutics (translated from ed. 8). London: The
New Syndeham Society; 1878 3
Sack Jr GH,
Levin J,
Bell W.
Trousseau’s syndrome and other manifestations of chronic disseminated coagulopathy
in patients with neoplasms: Clinical, pathologic, and therapeutic features. Medicine
1977; 56: 1-27 4
Donati MB,
Poggi A,
Semeraro N.
Coagulation and malignancy. In: Recent Advances in Blood Coagulation (vol.3).
Poller L.
(ed) New York: Livingston; 1981: 375-391 5
Dvorak HF.
Tumors: Wounds that do not heal. N Engl J Med 1986; 315: 1650-1659 6
Rickles FR,
Edwards RL.
Activation of blood coagulation in patients with cancer: Trousseau’s syndrome revisited.
Blood 1983; 62: 14-31 7
Zacharski LR,
Henderson WG,
Rickles FR,
Forman WG,
Cornell CJ,
Harrower HW,
Johnson RO.
Rationale und experimental design for the VA Cooperative Study of anticoagulation
(warfarin) in the treatment of cancer. Cancer 1979; 44: 732-741 8
Zacharski LR,
Henderson WG,
Rickles FR,
Forman WG,
Van Eeckhout JP,
Cornell CJ,
Forcier RJ,
Martin JF.
Rationale and experimental design for the VA Cooperative Study of RA-233 in the treatment
of cancer. Am J Clin Oncol 1982; 5: 593-609 9
Zacharski LR,
Memoli VA,
Costantini V,
Wojtukiewicz MZ,
Ornstein DL.
Clotting factors in tumor tissue: Implications for cancer therapy. Blood Coag Fibrinolys
1990; 1: 71-78 10
Zacharski LR,
Costantini V,
Wojtukiewicz MZ,
Memoli VA,
Kudryk BJ.
Anticoagulants as cancer therapy. Semin Oncol 1990; 17: 217-227 11
Zacharski LR,
Wojtukiewicz MZ,
Costantini V,
Ornstein DL,
Memoli VA.
Pathways of coagulation/fibrinolysis activation in malignancy. Semin Hemostas Thromb
1992; 18: 104-116 12
O’Meara RAQ.
Coagulative properties of cancers. Irish J Med Sci 1958; 394: 474-479 13
Day ED,
Planinsek JA,
Pressman D.
Localization in vivo of radioiodinated anti-rat fibrin antibodies and radioiodinated
rat fibrinogen in the Murphy rat lymphosarcoma and in other transplantable rat tumors.
J Natl Cancer Inst 1959; 22: 413-426 14
Spar IL,
Bale WF,
Marrack D,
Dewey WC,
McCardle RJ,
Harper PV.
131 I-labeled antibodies to human fibrinogen: Diagnostic studies and therapeutic trials.
Cancer 1967; 20: 865-870 15
Laki K,
Yancey ST.
Fibrinogen and the tumor problem. In: Fibrinogen.
Laki K.
(ed) Marcel Dekker; New York: 1968: 359-367 16
Hiramoto R,
Yagi Y,
Pressman D.
Immunohistochemical studies of antibodies in anti-Murphy lymphosarcoma sera. Cancer
Res 1959; 19: 874-879 17
Hiramoto R,
Bernecky J,
Jurandowski J,
Pressman D.
Fibrin in human tumors. Cancer Res 1960; 20: 592-593 18
Bini A,
Mea-Tejada R,
Fenoglio Jr JJ,
Kudryk B,
Kaplan KL.
Immunohistochemical characterization of fibrin(ogen)-related antigens in human tissues
using monoclonal antibodies. Lab Invest 1989; 60: 814-821 19
Kudryk B,
Rohoza A,
Ahadi M,
Chin J,
Wiebe ME.
A monoclonal antibody with ability to distinguish between NH2 -terminal fragments derived from fibrinogen and fibrin. Mol Immunol 1983; 20: 1191-1200
20
Kudryk B,
Rohoza A,
Ahadi M,
Chin J,
Wiebe ME.
Specificity of a monoclonal antibody for the NH2-terminal region of fibrin. Mol Immunol
1984; 21: 89-94 21
Kudryk BJ,
Grossman ZD,
McAfee JG,
Rosebrough SE.
Monoclonal antibodies as probes for fibrin(ogen) proteolysis. In: Monoclonal Antibodies
in Immunoscintigraphy.
Chatal JF.
(ed) CRC Press; Boca Raton, FL: 1988: 365-398 22
Hui KY,
Haber E,
Matsueda GR.
Monoclonal antibodies to a synthetic fibrin-like peptide bind to human fibrin but
not fibrinogen. Science 1983; 222: 1129-1132 23
Harris NL,
Dvorak AM,
Smith J,
Dvorak HE.
Fibrin deposits in Hodgkin’s disease. Am J Pathol 1982; 108: 119-129 24
Zacharski LR,
Schned A,
Sorenson GD.
Occurrence of fibrin and tissue factor antigen in small cell carcinma of the lung.
Cancer Res 1983; 43: 3963-3968 25
Dvorak HF,
Dvorak AM,
Manseau EJ,
Wiberg L,
Churchill WH.
Fibrin-gel investment associated with line 1 and line 10 solid tumor growth, angiogenesis,
and fibroplasia in guinea pigs: Role of cellular immunity, myofibroblasts, microvascular
damage, and infarction in line 1 tumor regression. J Natl Cancer Inst 1979; 62: 1459-1472
26
Zacharski LR,
Memoli VA,
Rousseau SM.
Cancer-coagulation interaction in situ in renal cell carcinoma. Blood 1986; 68: 394-399
27
Rickles FR,
Hancock WW,
Edwards RL,
Zacharski LR.
Antimetastatic agents. I. The role of cellular procoagulants in the pathogenesis of
fibrin deposition in cancer and the use of anticoagulants and/or antiplatelet drugs
in cancer treatment. Semin Thromb Hemostas 1988; 14: 88-94 28
Costantini V,
Zacharski LR,
Memoli VA,
Kisiel W,
Kudryk BJ,
Rousseau SM,
Stump DC.
Fibrinogen deposition and macrophage-associated fibrin formation in malignant and
non-malignant lymphoid tissue. J Lab Clin Med 1992; 119: 124-131 29
Wojtukiewicz MZ,
Zacharski LR,
Memoli VA,
Kisiel W,
Kudryk BJ,
Rousseau SM,
Stump DC.
Abnormal regulation of coagulation/fibrinolysis in small cell carcinoma of the lung.
Cancer 1990; 65: 481-485 30
Wojtukiewicz MZ,
Zacharski LR,
Memoli VA,
Kisiel W,
Kudryk BJ,
Rousseau SM,
Stump DC.
Malignant melanoma: Interaction with coagulation and fibrinolysis pathways in situ.
Am J Clin Pathol 1990; 93: 516-521 31
Wojtukiewicz MZ,
Zacharski LR,
Memoli VA,
Moritz TE,
Kisiel W,
Kudryk BJ,
Rousseau SM,
Stump DC.
Fibrin formation on vessel walls in hyperplastic and malignant prostate tissue. Cancer
1991; 67: 1377-1383 32
Wojtukiewicz MZ,
Zacharski LR,
Memoli VA,
Kisiel W,
Kudryk BJ,
Rousseau SM,
Stump DC.
Fibrinogen-fibrin transformation in situ in renal cell carcinoma. Anticancer Res 1990;
10: 579-582 33
Brown LF,
Asch B,
Harvey VS,
Buchinski B,
Dvorak HF.
Fibrinogen influx and accumulation of cross-linked fibrin in mouse carcinomas. Cancer
Res 1988; 48: 1920-1925 34
Zacharski LR,
Donati MB.
Registry of clincial trials of antithrombotic drugs in cancer. Thromb Haemostas 1989;
61: 526-528 35
Zacharski LR,
Henderson WG,
Rickles FR,
Forman WB,
Cornell CJ,
Forcier RJ,
Headley E,
Kim S-H,
O-Dell R,
Tornyos K,
Kwaan HC.
Effect of sodium warfarin on survival in small cell carcinoma of the lung. J Am Med
Assoc 1981; 245: 831-835 36
Zacharski LR,
Henderson WG,
Rickles FR,
Forman WB,
Cornell CJ,
Forcier RJ,
Edwards RL,
Headley E,
Kim S-H,
O-Donnell JF,
O’Dell R,
Tornyos K.
Effect of warfarin anticoagulation on survival in carcinoma of the lung, colon, head
and neck, and prostate. Final report of the VA Cooperative Study 75. Cancer 1984;
53: 2046-2052 37
Chahinian AP,
Propert KJ,
Ware JH,
Zimmer B,
Perry MC,
Hirsh V,
Skarin A,
Kopel S,
Holland JF,
Comis RL,
Green MR.
A randomized trial of anticoagulation with warfarin and of alternating chemotherapy
in extensive small-cell lung cancer by the Cancer and Leukemia Group B. J Clin Oncol
1989; 7: 993-1002 38
Lebeau B,
Chastang CL,
Brechot JM.
Subcutaneous heparin treatment increases complete response rate and overall survival
in small cell lung cancer (SCLC). Lung Cancer 1991; (Suppl. 07) 129 39
Dvorak HF,
Senger DR,
Dvorak AM.
Fibrin as a component of the tumor stroma: original and biological significance. Cancer
Metast Rev 1983; 2: 41-73 40
Zacharski LR,
Dunwiddie C,
Nutt EM,
Hunt J,
Memoli VA.
Cellular localization of activated factor X by a Xa-specific probe. Thromb Heamostas
1991; 65: 545-548 41
Pineo GF,
Brain MC,
Gallus AS,
Hirsh J,
Hatton MWC,
Regoeczi E.
Tumors, mucus production, and hypercoagulability. Ann NY Acad Sci 1974; 230: 262-270
42
Wojtukiewicz MZ,
Zacharski LR,
Memoli VA,
Kisiel W,
Kudryk BJ,
Rousseau SM,
Stump DC.
Indirect activation of coagulation in colon cancer. Thromb Haemostas 1989; 62: 1062-1066
43
Adany R,
Szegedi A,
Nemes Z,
Muszbek L.
Extravasal fibrin stabilization by factor XIII in lymph nodes with Hodgkin’s disease.
Thromb Haemostas 1987; 58: 235 44
Ornstein D,
Zacharski LR,
Memoli VA,
Kisiel W,
Kudryk BJ,
Hunt J,
Rousseau SM,
Stumo DC.
Coexistent macrophage procoagulant and tumor cell plasminogen activator in adenocarcinoma
and squamous cell carcinoma of the lung. Cancer 1991; 68: 1061-1067 45
Mosesson MW.
Fibrinogen heterogeneity. Ann N Y Acad Sci 1983; 408: 164-179 46
Folk JE,
Finlayson JS.
The ε(γglutamyl) lysine crosslink and the catalytic role of transglutaminase. Adv
Protein Chem 1977; 31: 1-33 47
McDonagh J.
Plasma fibronectin: Structure and Function. Marcel Dekker. New York: 1985 48
Dvorak HF,
Dickersin GR,
Dvorak AM,
Manseau EJ,
Pyne K.
Human breast carcinoma: fibrin deposits and desmoplasia, inflammatory cell type and
distribution, microvasculature and infarction. J Natl Cancer Inst 1981; 67: 335-345
49
Zacharski LR,
Memoli VA,
Rousseau SM,
Kisiel W.
Coagulation-cancer interaction in situ in small cell carcinoma of the lung. Cancer
1987; 60: 2675-2681 50
Zacharski LR,
Memoli VA,
Rousseau SM.
Thrombin-specific sites of fibrinogen in small cell carcinoma of the lung. Cancer
1988; 62: 299-302 51
Costantini V,
Zacharski LR,
Memoli VA,
Kisiel W,
Kudryk BJ,
Hunt J,
Rousseau SM,
Stump DC.
Fibrinogen deposition without thrombin generation in primary human breast cancer tissue.
Cancer Res 1991; 51: 349-353 52
Wojtukiewicz MZ,
Zacharski LR,
Memoli VA,
Kisiel W,
Kudryk BJ,
Rousseau SM,
Stump DC.
Absence of components of coagulation and fibrinolysis pathways in situ in mesothelioma.
Thromb Res 1989; 55: 279-284 53
Costanini V,
Zacharski LR,
Memoli VA,
Kisiel W,
Kudryk BJ,
Hunt J,
Rousseau SM,
Stump DC.
Occurrence of components of fibrinolysis pathways in situ neoplastic and non-neoplastic
human breast tissue. Cancer Res 1991; 51: 354-358 54
Donati MB,
Gambarcorti-Passerini C,
Casali B.
et al. Cancer procoagulant in human tumor cells: evidence from melanoma patients.
Cancer Res 1986; 26: 6471-6474 55
Gordon SG.
Cancer cell procoagulants and their role in malignant disease. Semin Thromb Hemostas
1992; 18: 424-433 56
Adany R,
Kappelmayer J,
Berenyi E,
Szegeda A,
Fabian E,
Muszbek L.
Factors of the extrinsic pathway of blood coagulation in tumor associated macrophages.
Thromb Haemostas 1989; 62: 850-855 57
Adany R,
Memes Z,
Musbek L.
Characterization of factor XIII containing macrophages in lymph nodes with Hodgkin’s
disease. Br J Cancer 1987; 55: 421-426 58
Muszbek L,
Adany R.
Intratumoral fibrin stabilization. In: Eicosanoids, Lipid Peroxidation and Cancer.
Nigam SK,
McBrien DCH,
Slater TF.
(eds) Springer-Verlag; New York: 1988: 339-349 59
Grignani G,
Pacciarini L,
Ricetti MM,
Dionigi P,
Jemos V,
Zucchella M,
Fratino P.
Mechanisms of platelet activation by cultured human cancer cells and cells freshly
isolated from tumor tissues. Invasion Metastasis 1989; 9: 298-309 60
Eche N,
Sie P,
Jozan S,
Courriere P,
David JF.
Platelet aggregating and procoagulant activities of cultured human breast cancer cells
(FAM). Thromb Res 1986; 43: 121-127 61
Dvorak HF,
Senger DR,
Dvorak AM,
Harvey VS,
McDonagh J.
Regulation of extravascular coagulation by microvascular permeability. Science 1985;
227: 1059-1061 62
Senger DR,
Perruzzi CA,
Feder J,
Dvorak HF.
A highly conserved vascular permeability factor secreted by a variety of human and
rodent tumor cell lines. Cancer Res 1986; 46: 5629-5632 63
Senger DR,
Galli SJ,
Dvorak AM,
Perruzzi CA,
Harvey VS,
Dvorak HF.
Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites
fluid. Science 1983; 219: 983-985 64
Ogawa S,
Connolly D,
Olander JV,
Familetti PC,
Stern D,
Clauss M.
Vascular permeability factor (VPF): A tumor-derived polypeptide which induced endothelial
cell and monocyte procoagulant activity and promotes monocyte migration. Thromb Haemostas
1991; 65: 648 65
Donati MB,
Semeraro N.
Cancer cell procoagulants and their pharmacological modulation. Haemostasis 1984;
14: 422-429 66
van Dewater L,
Tracy PB,
Aronson D,
Mann KG,
Dvorak HF.
Tumor cell generation of thrombin via functional prothrombinase assembly. Cancer Res
1985; 45: 5521-5525 67
Sakai T,
Lund-Hansen T,
Paborsky L,
Pedersen AH,
Kisiel W.
Binding of human factors VII and VIIa to a human bladder carcinoma cell line (J82).
Implications for the initiation of the extrinsic pathway of blood coagulation. J Biol
Chem 1989; 264: 9980-9988 68
Sakai T,
Kisiel W.
Binding of human factors X and Xa to Hep G2 and J82 human tumor cell lines. Evidence
that factor Xa binds to tumor cells independent of factor Va. J Biol Chem 1990; 265:
9105-9113 69
Rickles FR,
Hancock WW,
Edwards RL,
Zacharski LR.
Antimetastatic agents. I. The role of cellular procoagulants in the pathogenesis of
fibrin deposition in cancer and the use of anticoagulants and/or antiplatelet drugs
in cancer treatment. Semin Thromb Hemostas 1988; 14: 88-94 70
Semeraro N,
De Lucia O,
Lattanzio A,
Montemurro P,
Giordano D,
Loizzi M,
Carpagnano F.
Procoagulant activity of human alveolar macrophages. Different expression in patients
with lung cancer. Int J Cancer 1986; 37: 525-529 71
Semeraro N,
Montemurro P,
Conese M,
Giordano D,
Stella M,
Restaino A,
Cagnazzo G,
Colucci M.
Procoagulant activity of mononuclear phagocytes from different anatomical sites in
gynecologic malignancies. Int J Cancer 1990; 45: 251-254 72
Cozzolino F,
Torcia M,
Miliani A,
Carossino AM,
Giordani R,
Cinotti S,
Filimberti E,
Saccardi R,
Bernabei P,
Guidi G,
DiGuglielmo R,
Pistoia V,
Ferrarini M,
Nawroth PP,
Stern D.
Potential role of interleukin-1 as the trigger for diffuse intravascular coagulation
in acute nonlymphocytic leukemia. Am J Med 1988; 84: 240-250 73
Clariss M,
Murray JC,
Vianna M,
de Waal R,
Thurston G,
Nawroth P,
Gerlach H,
Bach R,
Familletti PC,
Stern D.
A polyppetide factor produced by fibrosarcoma cells that induces endothelial tissue
factor and enhances the procoagulant response to tumor necrosis factor/cachectin.
J Biol Chem 1990; 265: 7078-7083 74
McGee MP,
Wallin R,
Wheeler FB,
Rothberger H.
Initiation of the extrensic pathway of coagulation by human and rabbit alveolar macrophages:
A kinetic study. Blood 1989; 74: 1583-1590 75
Lorenzet R,
Peri G,
Locati D,
Allavena P,
Colucci M,
Semeraro NS,
Mantovani A,
Donati MB.
Generation of procoagulant activity by mononuclear phagocytes: a possible mechanism
contributing to blood clotting activation within malignant tissues. Blood 1983; 62:
271-273 76
Edwards RL,
Rickles FR,
Cronlund M.
Abnormalities of blood coagulation in patients with cancer: mononuclear cell tissue
factor generation. J Lab Clin Med 1981; 98: 917-928 77
Morgan D,
Edwards RL,
Rickles FR.
Monocyte procoagulant activity as a peripheral marker of clotting activation in cancer
patients. Haemostasis 1988; 18: 55-65 78
Viero P,
Cortellazzo S,
Caserotto C,
Barbui T,
Colucci M,
Semeraro N.
Increased production of mononuclear cell procoagulant activity in Hodgkin’s disease.
Eur J Cancer Clin Oncol 1983; 19: 1539-1543 79
Osterud B,
Due Jr J.
Blood coagulation in patients with benign and malignant tumors before and after surgery:
special reference to thromboplastin generation in monocytes. Scand J Haematol 1984;
32: 258-264 80
Geczy CL,
Ryan J,
Walsh J,
Goldstein D.
Lymphokine-induced monocyte procoagulant activity is depressed in patients with advanced
malignancies. Int J Cancer 1986; 37: 677-682 81
Guarini A,
Acero R,
Alessio G,
Donati MB,
Semeraro N,
Mantovani A.
Procoagulant activity of macrophages associated with different murine neoplasms. Int
J Cancer 1984; 34: 581-586 82
Lando PA,
Edgington TS.
An innate host response to the neoplastic cell: syngeneic rat tumor cells can elicit
a rapid de novo lymphoid procoagulant response. J Immunol 1985; 125: 3587-3595 83
Sharma S,
Mehta SR,
Ford RJ.
Growth factor, viruses, and oncogenes in human lymphoid neoplasia. Lymphokine Res
1987; 6: 245-264 84
Strauchen JA,
Breakstone BA.
IL-2 receptor expression in human lymphoid lesions. Immunohistochemical study of 166
cases. Am J Pathol 1987; 126: 506-512 85
Mingari MC,
Gerosa F,
Carra G.
et al. Human interleukin-2 promotes proliferation of activated B cells via surface
receptors similar to those of activated T cells. Nature 1984; 312: 2641-2643 86
Cordingly FT,
Bianchi A,
Hoffbrand AV,
Reittie JE,
Heslop HE,
Vyakarnam A,
Turner M,
Meager A,
Brenner MK.
Tumour necrosis factor as an autocrine tumor growth factor for chronic B-cell malignancies.
Lancet 1988; 1: 969-971 87
Hahn T,
Kusminsky G,
Bassous L,
Barak Y,
Barrebi A.
Tumor necrosis factor in B chronic lymphocytic leukemia. Br J Haematol 1989; 71: 299
88
Bennicelli JL,
Elias J,
Kern J,
Guerry D.
Production of interleukin-1 activity by cultured human melanoma cells. Cancer Res
1989; 49: 930-935 89
Kock A,
Schwarz T,
Urbanski A,
Peng Z,
Vitterlein M,
Micksche M,
Ansel JC,
Kung HF,
Luger TA.
Expression and release of interleukin-1 by different human melanoma cell lines. J
Natl Cancer Inst 1989; 81: 36-42 90
Sato K,
Fujii Y,
Kakiuchi T,
Kasona K,
Imamura H,
Kondo Y,
Mano H,
O-Rabe T,
Asano S,
Takaku F.
Paraneoplastic syndrome of hypercalcemia and leukocytosis caused by squamous carcinoma
cells (T3M-1) producing parathyroid hormone-related protein, interleukin 1α, and granulocyte
colony-stimulating factor. Cancer Res 1989; 49: 4740-4746 91
Ciano PS,
Colvin RB,
Dvorak AM,
McDonagh J,
Dvorak HF.
Macrophage migration in fibrin gel matrices. Lab Invest 1986; 54: 62-70 92
Gorelik E,
Bere WW,
Herberman RB.
Role of NK cells in the antimetastatic effect of anticoagulant drugs. Int J Cancer
1984; 3: 87-94 93
Gorelik E.
Augmentation of the antimetastatic effect of anticoagulant drugs by immunostimulation
in mice. Cancer Res 1987; 47: 809-815 94
Gunji Y,
Gorelik E.
Role of fibrin coagulation in protection of murine tumor cells from destruction by
immune cells. Cancer Res 1988; 48: 5216-5221 95
Olander JV,
Bremer ME,
Marasa JC,
Feder J.
Fibrin-enhanced endothelial cell organization. J Cell Physiol 1985; 125: 1-9 96
Zetter BR,
Chen LB,
Buchanan JM.
Binding and internalization of thrombin by normal and transformed chick cells. Proc
Natl Acad Sci 1988; 74: 596-600 97
Fair DS,
Plow EF.
Specific association of thrombin-antithrombin complexes with a human hepatoma cell
line. Thromb Res 1986; 41: 67-78 98
Maruyama I,
Majerus PW.
The turnover of thrombin-thrombomodulin complex in cultured human umbilical vein endothelial
cells and A549 lung cancer cells: Endocytosis and degradation of thrombin. J Biol
Chem 1985; 260: 15,432-15,438 99
Tullis JL,
Honegger H,
Fleischaker O,
Hewitt L,
Kenney D,
Chao FC.
Thrombin inhibition by malignant and normal cells: A cell-bound antithrombin effect.
Cancer 1981; 48: 1177-1182 100
Carney DH,
Stiernberg J,
Fenton JW.
Initiation of proliferative events by human alpha thrombin. J Cell Biochem 1984; 26:
181-195 101
Paris S,
Pouyssegur J.
Growth factors, activate the Na+ /K+ antiporter in quiescent fibroblasts by increasing its affinity for intracellular
H+
. J Biol Chem 1984; 259: 10,989-10,994 102
Raben DM,
Cunningham DD.
Effects of EGF and thrombin on inositol-containing phospholipids of cultured fibroblasts:
Stimulation of phosphatidylinositol synthesis by thrombin but not EGF. J Cell Physiol
1985; 125: 582-590 103
Murayama T,
Ui M.
Receptor mediated inhibition of adenylate cyclase and stimulation of arachidonic acid
release in 3T3 fibroblasts: Selective susceptibility to islet-activating protein,
pertusis toxin. J Biol Chem 1985; 260: 7226-7233 104
Galdal KS,
Lyberg T,
Evensen SA,
Nilsen E,
Prydz H.
Thrombin induces thromboplastin synthesis in cultured vascular endothelial cells.
Thromb Haemostas 1985; 54: 373-376 105
van Obberghen-Schilling E,
Chambard JC,
Paris S,
L’Allemain G,
Pouyssegur J.
Alpha-thrombin-induced early mitogenic signalling events and Go to S-phase transition
of fibroblasts require continual external stimulation. EMBO J 1985; 4: 2927-2932 106
Bar-Shavit R,
Kahn AJ,
Mann KG,
Wilner GD.
Identification of a thrombin sequence with growth factor activity on macrophages.
Proc Natl Acad Sci USA 1986; 83: 976-980
