Table Of ContentBIOLOGY OF ENDOTHELIAL CELLS
DEVELOPMENTS IN CARDIOVASCULAR MEDICINE
Lancee cr, ed: Echocardiology. 1979. ISBN 90-247-2209-8.
Baan J, Arntzenius AC, Yellin EL, eds: Cardiac dynamics. 1980. ISBN 90-247-2212-8.
Thalen HJT, Meere CC, eds: Fundamentals of cardiac pacing. 1970. ISBN 90-247-2245-4.
Kulbertus HE, Wellens HJJ, eds: Sudden death. 1980. ISBN 90-247-2290-X.
Dreifus LS, Brest AN, eds: Clinical applications of cardiovascular drugs. 1980. ISBN 90-247-2295-0.
Spencer MP, Reid JM, eds: Cerebrovascular evaluation with Doppler ultrasound. 1981. ISBN 90-247-90-247-2348-1.
Zipes DP, Bailey JC, Elharrar V, eds: The slow inward current and cardiac arrhythmias. 1980. ISBN 90-247-2380-9.
Kesteloot H, Joossens JV, eds: Epidemiology of arteral blood pressure. 1980. ISBN 90-247-2386-8.
Wackers FJT, ed: Thallium - 201 and technetium-99m-pyrophosphate myocardial imaging in the coronary care unit. 1980.
ISBN 90-247-2396-5.
Maseri A, Marchesi C, Chierchia S, Trivella MG, eds: Coronary care units. 1981. ISBN 90-247-2456-2.
Morganroth J, Moore EN, Dreifus LS, Michelson EL, eds: The evaluation of new antiarrhythmic drugs. 1981. ISBN 90-247-2474-0.
Alboni P: Intraventricular conduction disturbances. 1981. ISBN 90-247-2483-X.
Rijsterborgh H, ed: Echocardiology. 1981. ISBN 90-247-2491-0.
Wagner GS, ed: Myocardial infarction: Measurement and intervention. 1982. ISBN 90-247-2513-5.
Meltzer RS, Roelandt J, eds: Contrast echocardiography. 1982. ISBN 90-247-2531-3.
Amery A, Fagard R, Lijnen R, Staessen J, eds: Hypertensive cardiovascular disease pathophysiology and treatment. 1982.
ISBN 90-247-2534-8.
Bouman LN, Jongsma HJ, eds: Cardiac rate and rhythm. 1982. ISBN 90-247-2626-3.
Morganroth J, Moore EN, eds: The evaluation of beta blocker and calcium antagonist drugs. 1982. ISBN 90-247-2642-5.
Rosenbaum MB, ed: Frontiers of cardiac electrophysiology. 1982. ISBN 90-247-2663-8.
Roelandt J, Hugenholtz PG, eds: Long-term ambulatory electrocardiography. 1982. ISBN 90-247-2664-8.
Adgey AAJ, ed: Acute phase of ischemic heart disease and myocardial infarction. 1982. ISBN 90-247-2675-1.
Hanrath P, Bleifeld W, Souquet, eds: Cardiovascular diagnosis by Ultrasound.
Transesophageal, computerized, contrast, Doppler echocardiography. 1982. ISBN 90-247-2692-1.
Roelandt J, ed: The practice of M-mode and two-dimensional echocardiography. 1983. ISBN 90-247-2745-6.
Meyer J, Schweizer P, Erbel R, ed: Advances in noninvasive cardiology. ISBN 0-89838-576-8.
Morganroth J, Moore EN, eds: Sudden cardiac death and congestive heart failure: Diagnosis and treatment. ISBN 0-89838-580-6.
Perry HM, ed: Lifelong management of hypertension. ISBN 0-89838-582-2.
BIOLOGY OF ENDOTHELIAL CELLS
edited by
ERIC A. JAFFE
Cornell University Medical College
Department of Medicine
Division of Hematology-Oncology
1984 MARTINUS NIJHOFF PUBLISHERS
a member of the KLUWER ACADEMIC PUBLISHERS GROUP
BOSTON / THE HAGUE / DORDRECHT / LANCASTER
Distributors
for the United States and Canada:
Kluwer Boston, Inc., 190 Old Derby Street, Hingham,
MA 02043, USA
for all other countries:
Kluwer Academic Publishers Group, Distribution Center,
P.O. Box 322, 3300 AH Dordrecht, The Netherlands
Library of Congress Cataloging in Publication Data
Main entry under tit1e:
Biology of endothe1ia1 cells.
(Developments in cardiovascUlar medicine)
Inc1udes index.
1. Endothe1l,\lIII.-Addresses, essays, 1ectures.
2. eytolbsi-Addresses, essays, lectures. I. Jaffe,
Eric A. II. Series. (DmH: 1. Endothelium.-Cyto1ogy.
2. Endothelium.--Physio1ogy. Wl DE997'\'ME v. 27 I QS
532.5.E7J
QP88.45.B57 1983 599'.0821 83-11464
ISBN-13: 978-1-4612-9786-4 e-ISBN-13: 978-1-4613-2825-4
DOl: 10.1007/978-1-4613-2825-4
Copyright
© 1984 by Martinus Nijhoff Publishers, Boston.
Softcover reprint of the hardcover 1s t edition 1984
All rights reserved. No part of this publication may be repro-
duced, stored in a retrieval system, or transmitted in any form or
by any means, mechanical, photocopying, recording, or other-
wise, without the prior written permission of the publisher,
Martinus Nijhoff Publishers, 190 Old Derby Street, Hingham,
MA 02043, USA.
Preface
The participation of endothelial cells in various physiologic and pathologic processes has been hypothesized
since before the turn of the century. However, until recently, direct evidence for endothelial involvement in
these processes has been extremely difficult to obtain due to the inability to study endothelial cell function in
vitro. Though the possibility of using cultured endothelial cells to study endothelial cell function in vitro was
recognized many years ago, the inability to culture unambiguously identifiable endothelial cells limited
investigators in their studies of endothelial function. As a result, the field of endothelial cell biology lay
relatively fallow for many years.
The development in the early 1970's of routine and easily implemented methods for culturing human
endothelial cells and the demonstration that cultured endothelial cells synthesized a physiologically relevant
protein, Factor VIII/von Willebrand Factor, quickly changed this state of affairs. Over the following decade
the scope of endothelial cell research rapidly widened, spreading in a number of directions. First, methods
were developed to culture endothelial cells from a variety of species. Second, methods were developed to
culture endothelial cells from different organs and types of blood vessels (arteries, veins, and capillaries)
within a single species. Third, and most important, investigators began using cultured endothelial cells as
tools to study the potential involvement of endothelial cells in a wide assortment of biologically interesting
processes. The net result has been a tremendous increase in our understanding of endothelial cell function.
This book summarizes our present knowledge of the major facets of endothelial cell physiology which, to
large extent, have been delineated in studies using cultured endothelial cells.
Eric A. Jaffe
Contents
Preface by the editor. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . V
List of contributors .... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . XI
PART ONE: TISSUE CULTURE OF ENDOTHELIAL CELLS
1. Culture and identification of large vessel endothelial cells
by Eric A. Jaffe. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
2. Culture of capillary endothelial cells
by Bruce R. Zetter. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14
3. Culture of endothelial cells from neural capillaries
by Phillip D. Bowman, A. Lorris Betz and Gary W. Goldstein. . . . . . . . . . . . . . . . . . . . . . . . . . . . 27
4. Culture of pulmonary endothelial cells on micro carrier beads
by Una S. Ryan . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 34
5. Construction of an artificial blood vessel wall from cultured endothelial cells
by Robert F. Taylor. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 51
PART TWO: DETERMINANTS OF ENDOTHELIAL AND SMOOTH MUSCLE CELL GROWTH
"6. Growth requirements for bovine aortic endothelium in vitro
by Corinne M. Gajdusek and Stephen M. Schwartz... . .... ..... ... . . .. ... . . ... . . .. . .. . . . 59
7. Contact inhibition in the endothelium
by Stephen M. Schwartz and Corinne M. Gajdusek.. . ..... .... . . . ... .... . ... . . .. . .. . ... . 66
8. Endothelial cell motility
by Christian C. Haudenschild and Sandra Harris-Hooker. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 74
9. Factors which stimulate the growth of human umbilical vein endothelial cells in vitro
by T. Maciag, G.A. Hoover, M.B. Stemerman and R. Weinstein.. .. . . . .. . .... . .... ... .. . . 87
10. Macrophages, neovascularization, and the growth of vascular cells
by Michael A. Glmbrone, Jr. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 97
VIII
11. The limited life-span of bovine endothelial cells
by Elliot M. Levine, Stephen N. Mueller, Judith B. Grinspan, James P. Noveral and Eliot M.
Rosen............................................................................. 108
12. Endothelium, heparin, and the regulation of vascular smooth muscle cell growth
by John J. Castellot, Jr., Robert D. Rosenberg and Morris J. Karnovsky . . . . . . . . . . . . . . . . . . . 118
PART THREE: MORPHOLOGY OF CULTURED ENDOTHELIAL CELLS
13. Morphology of vascular endothelial cells in culture
by Christian C. Haudenschild ........................................................ 129
14. The endothelial cytoskeleton
by Stephen H. Blose. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . 141
PART FOUR: SYNTHESIS OF CONNECTIVE TISSUE ELEMENTS BY ENDOTHELIAL CELLS
15. Metabolism of thrombospondin and fibronectin by endothelial cells
by Deane F. Mosher, Eliot C. Williams and Paula J. McKeown-Longo..................... 155
16. Collagen synthesis by endothelial cells in culture
by Helene Sage. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 161
17. Sulfated glycosaminoglycans and vascular endothelial cells
by P. Christer Busch. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 178
18. Elastin synthesis by endothelial cells
by Jerome O. Cantor, Mary S. Parshley, Ines Mandl and Gerard M. Turino . . . . . . . . . . . . . . . . 189
19. Gene mapping using hybrids of human endothelial cells and rodent fibroblasts
by Nicholas A. Kefalides. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 194
PART FIVE: INTERACTIONS OF ENDOTHELIAL CELLS WITH THE COAGULATION AND
COMPLEMENT SYSTEMS AND FORMED ELEMENTS IN BLOOD
20. Properties of plasminogen activators produced by endothelial cells
by David J. Loskutoff and Eugene Levin. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 200
21. Synthesis of Factor VIII by endothelial cells
by Eric A. Jaffe. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 209
22. Tissue factor activity of cultured human vascular cells
by James R. Maynard. ... . . . . ... .. . . . . . .. . .. .. . .. ... ... . . ... .. .... . .. . . . . . ... . ... . .. 215
23. Activation of Hageman factor by cultured rabbit endothelial cells
by David J. Loskutoff and Roger C. Wiggins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 224
24. Prostacyclin production by endothelial cells
by Richard I. Levin, Babette B. Weksler, Aaron J. Marcus and Eric A. Jaffe. . . . . . . . . . . . . . . 228
25. Regulation of endothelial cell function by cyclic nucleotides
by Andrew I. Schafer, Michael A. Gimbrone, Jr. and Robert I. Handin. . . . . . . . . . . . . . . . . . . . 248
26. Interactions of thrombin, antithrombin III, and protein C with endothelium
by Whyte G. Owen . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 259
27. Viral infection of endothelium and the induction of Fc and C3 receptors
by Harvey M. Friedman.. .. .... . .. ... ... . . .... . . . .. . .. ... .. . .. .... . .. . .. . . .. . .. . . . . . 268
IX
28. Adhesive interactions between polymorphonuclear leukocytes and endothelium
by Richard L. Hoover and Morris J. Karnovsky. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 277
29. Neutrophil endothelial interactions
by Charles F. Moldow. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 286
30. Synthesis of colony stimulating activity by endothelial cells
by Peter J. Quesenberry and Michael A. Gimbrone, Jr. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 298
PART SIX: INTERACTION WITH AND METABOLISM OF PLASMA COMPONENTS
BY ENDOTHELIAL CELLS
31. The metabolism of vasoactive peptides by human endothelial cells
by Alice R. Johnson. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 302
32. The metabolism of angiotensin I and bradykinin by endothelial cells
by James W. Ryan. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 317
33. Metabolism of serotonin and adenosine
by Jeremy D. Pearson and John L. Gordon. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 330
34. Receptors for insulin and multiplication stimulating activity (MSA) in endothelial cells
by Robert S. Bar . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 343
35. Binding of lipoprotein lipase to cultured endothelial cells
by Patsy Wang-Iverson. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 350
36. Role of lipoproteins in the regulation of cultured endothelial cell cholesterol metabolism
by Phoebe E. Fielding and Christopher J. Fielding . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 356
37. Quantitative aspects of endocytosis in cultured endothelial cells
by Peter F. Davies. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 365
PART SEVEN: IMMUNOLOGIC ASPECTS OF ENDOTHELIAL CELLS
38. The alloantigens of endothelial cells
by Peter Stastny and Gabriel Nunez. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 377
39. Accessory cell function of human endothelial cells: presentation of antigen to T cells
by Henry Hirschberg. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 385
40. Cell surface markers on endothelial cells: a developmental perspective
by Robert Auerbach and Jeymohan Joseph. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 393
PART EIGHT: ENDOTHELIAL CELLS AND VASCULAR PROSTHESES
41. Endothelial seeding of vascular prostheses
by Russell S. Dilley and Malcolm B. Herring. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 401
PART NINE: ENDOTHELIAL CELLS AND CANCER
42. Angiogenesis
by Judah Folkman. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 412
x
43. Synthesis of collagenase and plasminogen activator by endothelial cells
by David Moscatelli, Janet L. Gross, Eric A. Jaffe and Daniel B. Rifkin. . . . . . . . . . . . . . . . . . . 429
44. In vitro systems for studying the interaction of metastatic tumor cells with endothelial cells and
subendothelial basement membranes
by George Poste and Garth L. Nicolson. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 438
Index of subjects .... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 451
List of contributors
Robert AUERBACH Jerome O. CANTOR
Department of Zoology Department of Pathology
University of Wisconsin College of Physicians & Surgeons
Zoology Research Building of Columbia University
1117 West Johnson St. 630 West 168th Street
Madison, WI 53706, USA New York, NY 10032, USA
Robert S. BAR John J. CASTELLOT, Jr.
Department of Internal Medicine Department of Pathology
The University of Iowa Harvard Medical School
3E-21, VA Medical Center Building D2
Iowa City, IA 52240, USA 25 Shattuck Street
Boston, MA 02115, USA
A. Lorris BETZ
Pediatric Neurology Sect. Peter DAVIES
Department of Pediatrics & Neurology Department of Pathology
University of Michigan Medical Center Harvard Medical School
Ann Arbor, MI 48109, USA Brigham and Women's Hospital
75 Francis St.
Stephen H. BLOSE Boston, MA 02115, USA
Cold Spring Harbor Laboratories
P.O. Box 100 Russell DILLEY
Cold Spring Harbor, NY 11724, USA Department of Surgery
Indiana University School of Medicine
Phillip D. BOWMAN Emerson Hall 212
Pediatric Neurology Section 1100 West Michigan Street
Department of Pediatrics & Neurology Indianapolis, IN 46223, USA
University of Michigan Medical Center
Ann Arbor, MI 48109, USA Christopher J. FIELDING
Department of Physiology
Christer BUSCH Room M1315
Department of Pathology Cardiovascular Research Institute
University of Uppsala University of California Medical Center
Box 553 San Francisco, CA 94143, USA
S-75122 Uppsala. Sweden
