Biophysical Regulation of Vascular Differentiation and Assembly BIOLOGICAL AND MEDICAL PHYSICS, BIOMEDICAL ENGINEERING The fields of biological and medical physics and biomedical engineering are broad, multidisciplinary and dynamic. They lie at the crossroads of frontier research in physics, biology, chemistry, and medicine. The Biological and Medical Physics, Biomedical Engineering Series is intended to be comprehensive, covering a broad range of topics important to the study of the physical, chemical and biological sciences. Its goal is to provide scientists and engineers with text- books, monographs, and reference works to address the growing need for information. Books in the series emphasize established and emergent areas of science includingmolecular,membrane, and mathematical biophysics; photosynthetic energy harvesting and conversion; information processing; physical principles of genetics; sensory communications; automata networks, neural networks, and cellular automata. Equally important will be coverage of applied aspects of biological and medical physics and biomedical engineering such as molecular electronic components and devices, biosensors, medicine, imaging, physical principles of renewable energy production, advanced prostheses, and environmental control and engineering. Editor-in-Chief: Elias Greenbaum, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA Editorial Board: Masuo Aizawa, Department of Bioengineering, Judith Herzfeld, Department of Chemistry, Brandeis Tokyo Institute of Technology, Yokohama, Japan University, Waltham, Massachusetts, USA Olaf S. Andersen, Department of Physiology, Biophysics & Mark S. Humayun, Doheny Eye Institute, Los Angeles, Molecular Medicine,Cornell University, New York, USA California, USA Robert H. Austin, Department of Physics, Princeton Pierre Joliot, Institute de Biologie Physico-Chimique, University, Princeton, New Jersey, USA Fondation Edmond de Rothschild, Paris, France James Barber, Department of Biochemistry, Imperial Lajos Keszthelyi, Institute of Biophysics, Hungarian College of Science, Technology and Medicine, London, Academy of Sciences, Szeged, Hungary England Robert S. Knox, Department of Physics and Astronomy, Howard C. Berg, Department of Molecular and Cellular University of Rochester, Rochester, New York, USA Biology, Harvard University, Cambridge, Aaron Lewis, Department of Applied Physics, Hebrew Massachusetts, USA University, Jerusalem, Israel Victor Bloomf ield, Department of Biochemistry, Stuart M. Lindsay, Department of Physics and Astronomy, University of Minnesota, St. Paul, Minnesota, USA Arizona State University, Tempe, Arizona, USA Robert Callender, Department of Biochemistry, Albert David Mauzerall, Rockefeller University, New York, Einstein College of Medicine, Bronx, New York, USA New York, USA Britton Chance, Department of Biochemistry/ Eugenie V. Mielczarek, Department of Physics Biophysics, University of Pennsylvania, Philadelphia, and Astronomy, George Mason University, Fairfax, Pennsylvania, USA Virginia, USA Steven Chu, Lawrence Berkeley National Laboratory, Markolf Niemz, Medical Faculty Mannheim, University Berkeley, California, USA of Heidelberg, Mannheim, Germany Louis J. DeFelice, Department V. Adrian Parsegian, Physical Science Laboratory, of Pharmacology, Vanderbilt University, Nashville, National Institutes of Health, Bethesda, Maryland, USA Tennessee, USA Linda S. Powers, University of Arizona, Johann Deisenhofer, Howard Hughes Medical Institute, Tucson, Arizona, USA The University of Texas, Dallas, Texas, USA Earl W. Prohofsky, Department of Physics, Purdue George Feher, Department of Physics, University University, West Lafayette, Indiana, USA of California, San Diego, La Jolla, California, USA Andrew Rubin, Department of Biophysics, Moscow Hans Frauenfelder, Los Alamos National Laboratory, State University, Moscow, Russia Los Alamos, New Mexico, USA Michael Seibert, National Renewable Energy Ivar Giaever, Rensselaer Polytechnic Institute, Troy, Laboratory, Golden, Colorado, USA NewYork, USA David Thomas, Department of Biochemistry, Sol M. Gruner, Cornell University, Ithaca, University of Minnesota Medical School, Minneapolis, New York, USA Minnesota, USA For further volumes: http/www.springer.com/series/3740 Sharon Gerecht Editor Biophysical Regulation of Vascular Differentiation and Assembly Editor Sharon Gerecht Department of Chemical and Biomolecular Engineering Johns Hopkins Physical Sciences-Oncology Center Institute for NanoBioTechnology Johns Hopkins University Baltimore, MD 21218, USA [email protected] ISBN 978-1-4419-7834-9 e-ISBN 978-1-4419-7835-6 DOI 10.1007/978-1-4419-7835-6 Springer New York Dordrecht Heidelberg London © Springer Science+Business Media, LLC 2011 All rights reserved. This work may not be translated or copied in whole or in part without the written permission of the publisher (Springer Science+Business Media, LLC, 233 Spring Street, New York, NY 10013, USA), except for brief excerpts in connection with reviews or scholarly analysis. Use in connection with any form of information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed is forbidden. The use in this publication of trade names, trademarks, service marks, and similar terms, even if they are not identified as such, is not to be taken as an expression of opinion as to whether or not they are subject to proprietary rights. Printed on acid-free paper Springer is part of Springer Science+Business Media (www.springer.com) Preface I am pleased to present this book, Biophysical Regulation of Vascular Differentiation and Assembly in the series Biological and Medical Physics, Biomedical Engineering. The ability to grow stem cells in the laboratory and to guide their maturation to functional cells allows us to study the underlying mechanisms that govern vasculature differentiation and assembly in health and disease. Accumulating evidence suggests that early stages of vascular growth are exquisitely tuned by biophysical cues from the microenvironment, yet the scientific understanding of such cellular environments is still in its infancy. Comprehending these processes sufficiently to manipulate them would pave the way to controlling blood vessel growth in therapeutic applications. This book assembles the works and views of experts from various disciplines to provide a unique perspective on how different aspects of microenvironment regu- late the differentiation and assembly of the vasculature. In particular, it describes recent efforts to exploit modern engineering techniques to study and manipulate various biophysical cues. The book opens with a description of the emergence of blood and blood vessels during development; understanding their emergence increases our understanding of postnatal and disease processes (Sills and Hirschi). The following chapters describe the critical role of the three-dimensional extracellular matrix milieu in controlling tube morphogenesis and stabilization (Davis, Stratman, and Sacharidou), in directing vascular differentiation of human embryonic stem cells (Kraehenbuehl, Aday, and Ferreira), in affecting the intra- and extracellular microrheology of endothelial cells (Fraley, Hale, Bloom, Celedon, Lee, and Wirtz), and in modulating blood vessel formation through biophysical cues (Critser and Yoder). The book then details the hypoxic regulation of vascular remodeling through the mediation of hypoxia- inducible factor 1 (Sarkar and Semenza), in the context of the three-dimensional extracellular matrix during development and regeneration (Abaci, Hanjaya-Putra, and Gerecht), and as one of the complex microenvironmental factors in tumor angiogenesis (Infanger, Pathi, and Fischbach). The final chapters consider the design of biologically inspired culture systems to control multiple microenviron- mental factors during differentiation (Freytes and Vunjak-Novakovic), with a focus on understanding the effects of hemodynamic forces and their application to vascular graft engineering (Diop and Li). v vi Preface This book provides an interdisciplinary view of vasculature regulation by various biophysical cues and presents recent advances in measuring and controlling such parameters. I hope it will inspire life scientists, biophysicists, and engineers to pursue unconventional approaches to answering fundamental questions in vascular differentiation and assembly. I am grateful to all of the authors for their excellent contributions and thank Springer for implementing this project; especially, I want to thank Christopher Coughlin, the publishing editor of the book, for initiating and supporting this project and Ho Ying Fan for his excellent production work. Baltimore, 2010 Sharon Gerecht Contents 1 The Emergence of Blood and Blood Vessels in the Embryo and Its Relevance to Postnatal Biology and Disease .............................. 1 Tiffany M. Sills and Karen K. Hirschi 2 Molecular Control of Vascular Tube Morphogenesis and Stabilization: Regulation by Extracellular Matrix, Matrix Metalloproteinases, and Endothelial Cell–Pericyte Interactions ................................................................................................ 17 George E. Davis, Amber N. Stratman, and Anastasia Sacharidou 3 Scaffolding for Three-Dimensional Embryonic Vasculogenesis ........... 49 Thomas P. Kraehenbuehl, Sezin Aday, and Lino S. Ferreira 4 Intra- and Extracellular Microrheology of Endothelial Cells in a 3D Matrix ..........................................................................................