Fibrin formation and Fibrinolysis April, 23, 1985, London,

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PREFACE

This volume contains the proceedings of a workshop entitled

"Fibrinogen, fibrin formation and fibrinolysis" that was held on
April 2-3 1985 at Queen Elizabeth College, London. The workshop
was attended by approximately 100 basic and clinical researchers
and its aim was to encourage informal interchange of ideas about
the fibrinogen molecule, its involvement in normal haemostasis and
in pathology. Previous workshops have been held at Martinsried,
Leiden and Stockholm. Their proceedings have been published as
earlier volumes in a series of which this volume constitutes the
4th:

Fibrinogen - Recent Biochemical and Medical Aspects;

A. Henschen, H. Graeff and F. Lottspeich, editors. Vol.
W. de Gruyter, Berlin and New York, 1982.

Fibrinogen - Structure, Functional Aspects and Metabolism;

F. Haverkate, A. Henschen, W. Neiuwenhuizen and P.W. Straub,
editors. Vol. 2, W. de Gruyter, Berlin and New York, 1983.

Fibrinogen - Structural Variants and Interactions;

A. Henschen, B. Hessel, J. McDonagh and T. Saldeen, editors.
Vol. 3, W. de Gruyter, Berlin and New York, 1985.

The meeting at Queen Elizabeth College was judged a success by the

participants who found time in between a packed scientific pro-
gramme to mix informally in the pleasant environment of the College
Dr. Neville Marsh of the Department of Physiology, Queen Elizabeth
College, is warmly thanked by the Editors for arranging this aspect
of the meeting.

Finally, the Editors wish to thank Dr. Alan White of Ciba Geigy
Pharmaceuticals Division, Horsham for arranging financial support
that made the workshop possible.

London, München and Horsham, September 1985

D.A. Lane
A. Henschen
M.K. Jasani
CONTRIBUTORS

B e c k , E.A.
C e n t r a l H a e m a t o l o g y L a b o r a t o r y , I n s e l s p i t a l , CH-3010 Berne,
Switzerland

Bernadou, A.
Hôtel-Dieu, Paris, France

B e r t r a n d , 0.
L a b o r a t o i r e s C e n t r a u x d ' H é m a t o l o g i e et d e B i o c h e m i e , Hôtel-Dieu,
Paris, France

B l o b e l , H.
I n s t i t u t für B a k t e r i o l o g i e u n d I m m u n o l o g i e , J u s t u s L i e b i g -
U n i v e r s i t ä t , F r a n k f u r t e r S t r a s s e 107, 6300 G i e s s e n , F R G

B o d e , W.
Max-Planck-Institut für B i o c h e m i e , D - 8 0 3 3 M a r t i n s r i e d , FRG

B o n n e t , P.
Hôpital Lariboisière, Paris, France

B o u c h i e u x , C.
Hôtel-Dieu, Paris, France

Brommer, E.J.P.
G a u b i u s I n s t i t u t e , H e a l t h R e s e a r c h D i v i s i o n TNO, H e r e n s t r a a t 5d,
2313 AD L e i d e n , The N e t h e r l a n d s

C a e n , J.P.
Hôpital Lariboisière, Paris, France

Chhatwal, G.S.
I n s t i t u t für B a k t e r i o l o g i e und I m m u n o l o g i e , J u s t u s L i e b i g -
U n i v e r s i t ä t , F r a n k f u r t e r S t r a s s e 107, 6300 G i e s s e n , FRG

C o c c h e r i , S.
D e p a r t m e n t of A n g i o l o g y a n d B l o o d C o a g u l a t i o n , University
H o s p i t a l S. O r s o l a , 40138 B o l o g n a , Italy

C o l e l l a , S.
Istituo di R i c e r c h e F a r m a c o l o g i c h e M a r i o N e g r i , v i a E r i t r e a 62,
20157 M i l a n o , Italy

D e j a n a , E.
Istituo di R i c e r c h e F a r m a c o l o g i c h e M a r i o N e g r i , v i a E r i t r e a 62,
20157 M i l a n o , Italy

D e l v o s , U.
C l i n i c a l R e s e a r c h U n i t for B l o o d C o a g u l a t i o n and T h r o m b o s i s of
the M a x - P l a n c k - G e s e l l s c h a f t at the J u s t u s - L i e b i g - U n i v e r s i t y ,
Giessen, FRG

Desvignes, P.
Hôpital Lariboisiere, Paris, France
VIII

Douglas, J.T.
University Department of Medicine, Royal Infirmary, Glasgow,
G31 2ER, UK

Dunn, F.W.
Laboratoires Centraux d'Hématologie et de Biochemie, Hôtel-Dieu,
Paris, France

Eastham, R.
Frenchay Hospital, Bristol, BS16 1 LE, UK

Elwood, P.C.
MRC Epidemiology Unit, 4 Richmond Road, Cardiff CF2 3AS, UK

Engbers, J.
TNO Gaubius Institute for Cardiovascular Research, Herenstraat
5d, 2313 AD Leiden, The Netherlands
Errol, A.
Istituo di Richerche Farmacologiche Mario Negri, via Eritrea 62,
20157 Milano, Italy

Etherington, M.D.
Central Laboratory, St. Mary's Hospital, Portsmouth, P03 6AG, UK

Forbes, C.D.
University Department of Medicine, Royal Infirmary, Glasgow,
G31 2ER, UK

Fuhge, P.
Behringwerke AG, Marburg, FRG

Furlan, M.
Central Haematology Laboratory, Inselspital, CH-3010 Berne,
Switzerland

Gabrijelcic, D.
Max-Planck-Institut für Biochemie, D-8033 Martinsried, FRG

Gaffney, P.J.
National Institute for Biological Standards and Control, Holly
Hill, Hampstead, London, NW3 6RB, UK

Gilmour, R.A.
Frenchay Hospital, Bristol, BS16 1 LE, UK

Ginsberg, M.H.
Research Institute of Scripps Clinic, La Jolla, CA 92037, USA

Gollwitzer, R.

Max-Planck-Institut für Biochemie, D-8033 Martinsried, FRG

Graeff, H.

Frauenklinik der Technischen Universität, D-8000 München, FRG

Hafter, R.
Frauenklinik der Technischen Universität, D-8000 München, FRG
 IX

Handley, D.A.
Department of Medicine, College of Physicians and Surgeons,
Columbia University, New York, NY 10032, USA

Haverkate, F.
Gaubius Institute, Health Research Division TNO, Herenstraat 5d,
2313 AD Leiden, The Netherlands

Heimburger, N.
Behringwerke AG, Marburg, FRG

Henschen, A.
Max-Planck-Institute for Biochemistry, D-8033 Martinsried, FRG

Hugo, R. von
Frauenklinik der Technischen Universität, D-8000 München, FRG
Huijsmans, C.M.G.
TNO Gaubius Institute for Cardiovascular Research, Herenstraat
5d, 2313 AD Leiden, The Netherlands

Ireland, H.
Department of Haematology, Charing Cross and Westminster Medical
School, Hammersmith, London, W6 8RP, UK

Jasani, M.K.
Ciba Geigy Pharmaceuticals, Horsham, West Sussex, RH12 4AB, UK

Jayson, M.I.V.
Rheumatic Diseases Centre, University of Manchester, Hope
Hospital, Salford, UK
Kaudewitz, H.
Max-Planck-Institute for Biochemistry, D-8033 Martinsried, FRG

Keegan, A.
Rheumatic Diseases Centre, University of Manchester, Hope
Hospital, Salford, UK
Kehl, M.
Max-Planck-Institute for Biochemistry, D-8033 Martinsried, FGR

Keyser, J.
TNO Gaubius Institute for Cardiovascular Research, Herenstraat
5d, 2313 AD Leiden, The Netherlands
Knight, I.
Department of Haematology, Charing Cross and Westminster Medical
School, Hammersmith, London, W6 8RP, UK

Koopman, J.
Gaubius Institute, Health Research Division TNO, Herenstraat 5d,
2313 AD Leiden, The Netherlands

Koppert, P.W.
TNO Gaubius Institute for Cardiovascular Research, Herenstraat
5d, 2313 AD Leiden, The Netherlands
X

Kudryk, B.
Lindsley F. Kimball Research Institute, New York Blood Center,
New York, NY 10021, USA

Kulbe, G.E.
Max-Planck-Institut für Biochemie, D-8033 Martinsried, FRG

Lane, D.A.
Department of Haematology, Charing Cross and Westminster Medical
School, Hammersmith, London, W6 8RP, UK
Languino, L.R.
Istituo di Ricerche Farmacologiche Mario Negri, via Eritrea 62,
20157 Milano, Italy

Leeksma, O.C.
Central Laboratory of the Netherlands Red Cross Blood Transfusion
Service, Amsterdam, The Netherlands

Lijnen, H.R.
Center for Thrombosis and Vascular Research, University of
Leuven, Campus Gasthuisberg, Herestraat 49, B-3000 Leuven,
Belgium

Linke, R.P.
Institut für Immunologie der Universität München, D-8000 München,
FRG

Liu, C.Y.
Department of Medicine, College of Physicians and Surgeons,
Columbia University, New York, NY 1 0032, USA

Lowe, G.D.O.
University Department of Medicine, Royal Infirmary, Glasgow,
G31 2ER, UK

Maes, L.
Faculty of Medicine, VUB, Brussels, Belgium

Mantovani, A.
Istituo di Ricerche Farmacologiche Mario Negri, via Eritrea 62,
20157 Milano, Italy
Manucci, P.M.
Centro Angelo Bianchi Bonomi, 1-20122 Milano, Italy

Marguerie,
Inserm U G.
217, Centre d'Etude Nuclèaire, Grenoble, France

Meijer-Huizinga, F.M.
Central Laboratory of the Netherlands Red Cross Blood Trans-
fusion Service, Amsterdam, The Netherlands

Million, R.
Rheumatic Diseases Centre, University of Manchester, Hope
Hospital, Salford, UK
 XI

Mirshahi, M.
Laboratoires Centraux d'Hématologie et de Biochemie, Hôtel-Dieu,
Paris, France

Miyada, D.
Department of Pathology, College of Medicine, University of
California, Irvine, CA 92717, USA

Mourik, J.A. van

Central Laboratory of the Netherlands Red Cross Blood Trans-
fusion Service, Amsterdam, The Netherlands

Müller, E.
Max-Planck-Institute for Biochemistry, D-8033 Martinsried, FRG

Müller-Berghaus, G.
Clinical Research Unit for Blood Coagulation and Thrombosis of
the Max-Planck-Gesellschaft at the Justus-Liebig-University,
Giessen, FRG

Nieuwenhuizen, W.
TNO Gaubius Institute for Cardiovascular Research, Herenstraat
5d, 2313 AD Leiden, The Netherlands

O'Brien, J.R.

Central Laboratory, St. Mary's Hospital, Portsmouth, P03 6AG, UK

Palareti, G.
Department of Angiology and Blood Coagulation, University
Hospital S. Orsola, 40138 Bologna, Italy
Perry, M.J.
National Institute for Biological Standards and Control, Holly
Hill, Hampstead, London, NW3 6RB, UK

Perrot, J.Y.
Laboratoires Centraux d'Hématologie et de Biochemie, Hôtel-Dieu,
Paris, France

Peters, R.F.
Ciba Geigy Pharmaceuticals, Horsham, West Sussex, RH12 4AB, UK

Pirkle, H.
Department of Pathology, College of Medicine, University of
California, Irvine, CA 92717, USA
Plow, E.F.
Research Institute of Scripps Clinic, La Jolla, CA 92037, USA

Poggi, M.
Department of Angiology and Blood Coagulation, University
Hospital S. Orsola, 40138 Bologna, Italy
Pountain, G.
Rheumatic Diseases Centre, University of Manchester, Hope
Hospital, Salford, UK
XII

Preissner, K.T.
C l i n i c a l R e s e a r c h U n i t f o r B l o o d C o a g u l a t i o n a n d T h r o m b o s i s of
the M a x - P l a n c k - G e s e l l s c h a f t at the J u s t u s - L i e b i g U n i v e r s i t y ,
Giessen, FRG

P r y d z , H.
R e s e a r c h Institute for Internal M e d i c i n e , University of Oslo,
Rikshospitalet, Oslo, Norway

Rampling, M.W.
D e p a r t m e n t of P h y s i o l o g y a n d B i o p h y s i c s , St. Mary's Hospital
M e d i c a l S c h o o l , L o n d o n , W 2 "IPG, U K

R e b e r , P.
Central Haematology Laboratory, Inselspital, CH-3010 Berne,
Switzerland

R e d m a n , C.
L i n d s l e y F. K i m b a l l R e s e a r c h Institute, New York Blood Center,
N e w Y o r k , NY 10021, USA

Rötker, J.
C l i n i c a l R e s e a r c h U n i t for B l o o d C o a g u l a t i o n and T h r o m b o s i s ,
Max-Planck-Gesellschaft at the Justus-Liebig-University, Giessen,
FRG

R u p p , C.
Central Haematology Laboratory, Inselspital, CH-3010 Berne,
Switzerland

Samama, M.
Hôtel-Dieu, Paris, France

Scheefers-Borchel, U.
C l i n i c a l R e s e a r c h U n i t f o r B l o o d C o a g u l a t i o n a n d T h r o m b o s i s of
the Max-Planck-Gesellschaft at the Justus-Liebig-University,
Giessen, FRG

Schröck, R.

Frauenklinik der Technischen Universität, D-8000 München, FRG

S c h u b r i n g , C.
D e p a r t m e n t of O b s t e t r i c s and G y n a e c o l o g y , E v a n g e l i s c h e s
Krankenhaus, Giessen, FRG
S e l m a y r , E.
C l i n i c a l R e s e a r c h Unit for B l o o d C o a g u l a t i o n and T h r o m b o s i s ,
M a x - P l a n c k - G e s e l l s c h a f t at the J u s t u s - L i e b i g - U n i v e r s i t y ,
Giessen, FRG

S m i t h , E.
D e p a r t m e n t of C h e m i c a l P a t h o l o g y , U n i v e r s i t y of Aberdeen,
Foresterhill, Aberdeen, AB9 2ZD, UK

S o r i a , C.
Laboratoires Centraux d'Hématologie et de B i o c h e m i e , Hôpital
Lariboisière, Paris, France
 XIII

Soria, J.
Laboratoires Centraux d'Hématologie et de Biochemie, Hôtel-Dieu,
Paris, France

Southan, C.
Department of Haematology, Charing Cross and Westminster Medical
School, Hammersmith, London, W6 8RP, UK

Svenson, E.
Laboratoires Centraux d'Hématologie et de Biochemie, Hôtel-Dieu,
Paris, France

Sweetnam, P.M.
MRC Epidemiology Unit, 4 Richmond Road, Cardiff, CF2 3AS, UK

Talbot, M.D.

Ciba Geigy Pharmaceuticals, Horsham, West Sussex, RH12 4AB, UK

Takada, A.
Department of Physiology, Hamamatsu University, School of
Medicine, Hamamatsu-shi, Shizuoka 431-31, Japan
Takada, Y.
Department of Physiology, Hamamatsu University, School of
Medicine, Hamamatsu-shi, Shizuoka 431-31, Japan
Theodor, I.
Department of Pathology, College of Medicine, University of
California, Irvine, CA 92717, USA

Thiel, W.
Clinical Research Unit for Blood Coagulation and Thrombosis,
Max-Planck-Gesellschaft at the Justus-Liebig-University,
Giessen, FRG

Thomaidis, A.
Hôpital Lariboisière, Paris, France

Thompson, E.
Department of Haematology, Charing Cross and Westminster Medical
School, Hammersmith, London, W6 8RP, UK

Tomlinson, I.
Rheumatic Diseases Centre, University of Manchester, Hope
Hospital, Salford, UK

Tweed, M.F.
Ciba Geigy Pharmaceuticals, Horsham, West Sussex, RH12 4AB, UK

Vukasin, P.
Department of Pathology, College of Medicine, University of
California, Irvine, CA 92717, USA
Walker, J.E.
Department of Chemical Pathology, University of Aberdeen,
Foresterhill, Aberdeen, AB9 2ZD, UK
XIV

Wallen, P.
Department of Physiological Chemistry, University of Umea,
S-90187, Umea, Sweden

Weimar, B.
Clinical Research Unit for Blood Coagulation and Thrombosis of
the Max-Planck-Gesellschaft at the Justus-Liebig-University,
Giessen, FRG

Werf, W.G.C. van der

Gaubius Institute, Health Research Division TNO, Herenstraat 5d,
2313 AD Leiden, The Netherlands

Yarnell, J.W.G.
MRC Epidemiology Unit, 4 Richmond Road, Cardiff, CF2 3AS, UK

Yu, S.
Lindsley F. Kimball Research Institute, New York Blood Center,
New York, NY 10021, USA
CONTENTS

I. SYNTHESIS AND ASSEMBLY

A scheme for the intracellular assembly of human

fibrinogen
S. Yu, B. Kudryk and C. Redman 3

Evidence that platelet and plasma fibrinogen have

the same A-alpha chain gene product
C. Southan, I. Knight, H. Ireland and D.A. Lane 15

Fibrinopeptide A and the phosphorylation of

fibrinogen
O.C. Leeksma, F.M. Meijer-Huizinga and
J.A. van Mourik 23

II. STRUCTURE AND FUNCTION

Size and shape of the fibrinogen molecule:

crystalline forms of native and modified human
fibrinogen
R. Gollwitzer and W. Bode 35

The C-terminal polymerisation domain of fibrinogen

C. Southan, E. Thompson and D.A. Lane 47

y-Chain
E. crosslinking
Selmayr, of fibrin
W. Thiel and at DD-trans contact
G. Muller-Berghaus 55
Soluble fibrin contains fibrin polymers of
different molecular weight. Ultracentrifugation
studies at 37°C
K.T. Preissner, J. Rotker and G. Muller-Berghaus 61

Relationship of final thickness of fibrin fibers

to maximal rate of assembly and to fibrinopeptide B
release
H. Pirkle, P. Vukasin, I. Theodor and D. Miyada 69

III. CONGENITAL VARIANTS

Fibrinogen New York 1: The structural, functional,

and genetic defects and an hypothesis of the role of
fibrin in the regulation of coagulation and
fibrinolysis
C.Y. Liu, P. Wallen and D.A. Handley 79

Fibrinogen Pontoise - a genetically abnormal

fibrinogen with defective fibrin polymerisation but
normal fibrinopeptide release
H. Kaudewitz, A. Henschen, J. Soria and C. Soria 91
XVI

Fibrinogen Milano I: Abnormal fibrin polymerization

related to a carboxy-terrainal defect of the y-chain
(y-330 Asp Val)
P. Reber, M. Furlan, C. Rupp, M. Kehl, A. Henschen,
P.M. Manucci and E.A. Beck 97

Fibrinogen "Bergamo I" (Act 16 Arg •>• Cys ) :

Alternative methods for structure elucidation
P. Reber, M. Furlan and E.A. Beck 103

Screening small plasma samples by HPLC for

abnormalities of fibrinopeptide release
C. Southan and D.A. Lane 111

IV. FIBRIN(OGEN) AND FIBRINOLYSIS

On the role of fibrin in the fibrinolytic system

H.R. Lij nen 121

Isolation and characterisation of plasmic

degradation products of fibrinogen by high-performance
liquid chromatography
E. Miiller and A. Henschen 137

The acceleration of tissue-type plasminogen

activator (t-PA)-mediated activation of plasminogen by
fibrinogen cyanogen bromide fragments is species
specific
W. Nieuwenhuizen and J. Keyser 145

Role of fibrin polymerization in fibrinolysis:

Comparison between polymerisable and unpolymerisable
fibrins in the potentiating effect of plasminogen
activation by tissue-type plasminogen activator (tpA)
J. Soria, C. Soria, O. Bertrand, M. Mirshahi,
F.W. Dunn, E. Svenson, P. Desvignes, P. Bonnet,
M. Samama and J.P. Caen 153

Role of fibrin and its degradation products in the

activation of plasminogen by streptokinase and
urokinase
A. Takada and Y. Takada 159

V. INTERACTIONS WITH CELLS

The role of fibrinogen in platelet aggregation

G. Marguerie, M.H. Ginsberg and E.F. Plow 175

Platelet-associated fibrinogen: Conformational

change of fibrinogen induced by its adsorption to
platelet-surface
C. Soria, J. Soria, M. Mirshahi, C. Boucheix,
A. Thomaidis, A. Bernadou, M. Samama and J.P. Caen 185
 XVII

Migration of cultured endothelial cells in response

to fibrinogen
E. Dejana, L.R. Languino, S. Colella, A. Erroi,
A. Mantovani, G. Marguerie and L. Maes 193

Characteristics of the interactions of fibrinogen

and soluble fibrin with cultured endothelial cells
U. Delvos, K.T. Preissner and G. Milller-Berghaus 203

Mechanism of fibrin-induced disorganisation of

cultured human endothelial cells
B. Weimar, U. Delvos, C. Schubring and
G. Muller-Berghaus 211

The fibrinogen: red cell interaction and its

influence on blood rheology
M.W. Rampling 219

Haemorheologic effects of plasmin and thrombin-

induced fibrinogen derivatives: An in vitro study
G. Palareti, M. Poggi and S. Coccheri 229

Binding of human fibrinogen to streptococci and

its role in streptococcal pathogenicity
G.S. Chhatwal and H. Blobel 239

VI. ASSAYS TO FIBRIN(OGEN) FRAGMENTS AND THEIR USE

Discrimination between fibrin and fibrinogen by a

monoclonal antibody against a synthetic hexapeptide
representing the amino-terminus of the alpha-chain
of fibrin
U. Scheefers-Borchel, G. Muller-Berghaus, P. Fuhge
and N. Heimburger 253

A new enzyme immunoassay of fibrin(ogen) degradation

products in plasma using a monoclonal antibody
J. Koopman, F. Haverkate, P. Koppert, W. Nieuwenhuizen,
E.J.P. Brommer and W.G.C. van der Werf 261

Fibrin(ogen) degradation products. Determination

using a monoclonal anti D neo antibody. Advantages
in clinical investigation
M. Mirshahi, J. Soria, C. Soria, J.Y. Perrot,
A. Bernadou and C. Boucheix 271

A monoclonal antibody, specific for human

fibrinogen and fibrinopeptide A-containing fragments.
Its application in an enzyme-immunoassay for fibrino-
gen degradation products, suitable for use in plasma
P.W. Koppert, C.M.G. Huijsmans, F. Haverkate,
J. Engbers, E.J.P. Brommer and W. Nieuwenhuizen 279

A monoclonal antibody against the CNBr-peptide F-CB3

of the Aa-chain of human fibrinogen
R. Gollwitzer, G.E. Kulbe, D. Gabrijelcic and
R.P. Linke 297
XVIII

Clinical aspects of fibrin formation and fibrinolysis

measured with monoclonal antibodies against D-dimer
R. Hafter, R. Schröck, R. von Hugo and H. Graeff 303

Fibrinogen derivatives in acute stroke

J.T. Douglas, G.D.O. Lowe, C.D. Forbes, I. Knight,

D.A. Lane, M.J. Perry and P.J. Gaffney 313

VII. FIBRIN(OGEN) AND DISEASE PATHOLOGY

Triggering of the extrinsic blood coagulation system
H. Prydz 325

Extravascular fibrin formation and fibrinolysis in a

model of inflammation accompanying cellular
hypersensitivity
R.F. Peters, M.K. Jasani, M.F. Tweed, I. Knight and
D.A. Lane 337

Extra-vascular fibrin deposition in cellular hyper-

sensitivity - the role of T lymphocyte-macrophage
interactions
M.D. Talbot, R.F. Peters, M.F. Tweed and M.K. Jasani 347

Fibrinolytic studies in disorders of connective tissue

A. Keegan, M.I.V. Jayson, I. Tomlinson, R. Million
and G. Pountain 357

Soluble fibrin/fibrinogen related antigen in human

intima in relation to atherogenesis
E.B. Smith and J.E. Walker 363

Fibrinogen as a possible risk factor for IHD in the

Caerphilly study
J.W.G. Yarnell, P.M. Sweetnam, P.C. Elwood,
R. Eastham, R.A. Gilmour, J.R. O'Brien and

M.D. Etherington 371

VIII. APPENDIX: DATA ON FIBRINOGEN

Fibrinogen amino acid sequences
A. Henschen 381

AUTHOR INDEX 389

SUBJECT INDEX 391

I. SYNTHESIS AND ASSEMBLY