LUNG DEVELOPMENT

Clinical Physiology Series

Lung Development Edited by Claude Gaultier, Jacques R. Bourbon, and Martin Post

Flow-Dependent Regulation of Vascular Function Edited by John A. Bevan, Gabor Kaley, and Gabor M. Rubanyi

Pathophysiology of Hypertension in Blacks Edited by John C. S. Fray and Janice G. Douglas

Hyperglycemia, Diabetes, and Vascular Disease Edited by Neil Ruderman, Joseph Williamson, and Michael Brownlee

Endothelin Edited by Gabor M. Rubanyi

Hypoxia, Metabolic Acidosis, and Circulation Edited by Allen I. Arieff

Response and Adaptation to Hypoxia: Organ to Organelle Edited by Sukhamay Lahiri, NeilS. Cherniack, and RobertS. Fitzgerald

Clinical Physiology of Sleep Edited by Ralph Lydic and Julien F. Biebuyck

High Altitude and Man Edited by John B. West and Sukhamay Lahiri

LUNG DEVELOPMENT

Edited by

Claude Gaultier

Jacques R. Bourbon

Martin Post

Springer New York 1999

Copyright© 1999 by the American Physiological Society Originally published by American Physiological Society in 1999 Softcover reprint of the hardcover 1st edition 1999

http:! /www.oup-usa.org

All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, recording, or otherwise, without the prior permission of Oxford University Press.

Library of Congress Cataloging-in-Publication Data Lung development I edited by Claude Gaultier, jacques R. Bourbon, Martin Post. p. em.- (Clinical physiology series

ISBN 978-1-4614-7537-8 (eBook) DOI 10.1007/978-1-4614-7537-8 1. Lungs-Growth. I. Gaultier, C. (Claude) II. Bourbon, Jacques R. III. Post, Martin, 1952 IV. American Physiological Society (1887- ) V. Series. [DNLM: 1. Lung-growth & development. 2. Lung-embryology. 3. Lung-physiopathology. WF 600 L96329 1999] QP12l.L838 1999 612.6' 40124-dc21 DNLM/DLC for Library of Congress 98-44090

987654321

PREFACE

Lung development became a focal point of intensive research when M. E. Avery and J. Mead reported pioneering work on the mechanism of neonatal respiratory dis­tress syndrome (1). During the last two decades there has been an explosive increase in the number of publications on this subject.

Respiratory physiology was the first approach used to investigate the develop­ing lung. P. A. Auld, M. E. Avery, R. C. Bryan, C. D. Cook, K. W. Cross, F. Geubelle, P. Karlberg, L. S. Strang, and others laid the groundwork for an emerging under­standing of neonatal lung function during the transition from intrauterine to extrauterine life. Anatomical and morphometrical data were later reported by E. A. Boysen, P. H. Burri, J. L. Emery, S. Engel, L. Reid, W. Thurbeck, J. S. Wiggle­worth, E. R. Weibel, and others. All of these studies brought new insights into the processes underlying the development of bronchial, vascular, and alveolar structures. In 1975 and 1980, two reviews summarized knowledge of the relationships between structure and function in the developing lung in health and disease (2, 3).

Cellular biological studies of the lung concentrated initially on surfactant syn­thesis and metabolism. Investigators such as T. Akino, J. Clements, S. Hawgood, A. Jobe, W. Longmore, F. Possmayer, L. M.G. Van Golde, and J. A. Whitsett worked in this field. In 1991, J. R. Bourbon edited a book on pulmonary surfactant (4), and the following year another book on the same topic written by B. Robertson, L. M. G. Van Golde, and J. J. Batenburg was published (5). Data from the first decade of re­search on surfactant enabled intensive care physicians, neonatologists, and pediatri­cians to improve the treatment and survival of patients with respiratory distress syndrome.

Molecular studies of lung development started in the late 1980s and are cur­rently burgeoning. A picture is beginning to form of the complex series of controlled interactions involving genetic influences, hormonal stimulation, and cell-cell inter­actions that is required for lung development. The role of the time of injury in ab­normal development, first emphasized by L. Reid (6), remains important at the mo-

v

vi Preface

lecular level. Lung Development provides a comprehensive review of the multiple

facets of lung development in health and disease. To meet the challenge of reviewing

an ever-changing field, the editors obtained the participation of over 30 international

authorities on lung development. Each of these contributors took the standpoint that

the developing lung should be understood starting at the bedside and moving toward

gene dysfunction. As a result, each chapter brings new insights of clinical relevance

into the physiological and pathophysiological processes operative in neonatal and

pediatric respiratory disorders. Pediatric pulmonologists, neonatologists, intensive

care physicians, obstetricians, and chest surgeons now need to be aware of findings

from cellular and molecular as well as from anatomical and physiological studies.

The first four chapters deal with morphogenesis, elastogenesis, maturation of

airway epithelial cells, and gene expression in alveolar development. R. Keyzer and

M. Post provide a clear overview of the role of permissive and/or inductive growth

factors and the extracellular matrix in lung branching morphogenesis. T. J. Mariani

and R. A Pierce focus on the development of the lung elastic matrix and its significant

role in the development and maintenance of normal lung function; they also discuss

abnormal elastogenesis in bronchopulmonary dysplasia. D. Gaillard and E. Puchelle

provide a comprehensive review of the role of the extracellular matrix and of growth

factors in the differentiation and maturation of airway epithelial cells. J. R. Bourbon

covers the field of gene expression in pulmonary bronchiolar and alveolar epithelial

cells, providing information on the complex mechanisms of gene expression control,

including those involving transcription factors and mesenchymal-epithelial interre­

lationships. Chapters 5-7 review angiogenesis, pulmonary vasculature, and circulation.

P. H. Burri discusses the development of the lung and its vasculature, providing a

clear and well-illustrated overview, particularly regarding the pulmonary capillary

network, and he emphasizes the deleterious effects of glucocorticoid administration

on early postnatal lung development. N. W. Morrell, M. C. M. Weiser, and K. R.

Stenmark deal with the mechanisms controlling angiogenesis and vasculogenesis

and the development of pulmonary arterial smooth muscle. S. H. Abman, J.P. Kin­

sella, and J.-C. Mercier describe the role of NO and ET-1 in the developing pul­

monary circulation, review the mechanisms implicated in persistent pulmonary

hypertension of the newborn, and discuss therapeutic strategies.

Chapters 8-11 cover the developmental aspects of cellular host defense mecha­

nisms, lung epithelial ion transport, cell growth, and tissue repair, as well as the role

of bioactive peptides. S. P. Sorokin, R. F. Hoyt, and N. A F. McNelly describe local de­

fenses provided by resident cells and hematological defenses provided by leukocytes

and their products in the neonatal lung. 0. Pitkiinen and H. O'Brodovich discuss re­

cent work on lung epithelial ion transport and its dysfunction in neonatal lung dis­

eases, including bronchopulmonary dysplasia. A Clement and J. S. Brody deal with

the mechanisms of cell growth and tissue repair in a chapter that supplies a unique

overview of abnormal lung development after tissue repair, as in lung fibrosis.

M. E. Sunday follows with a comprehensive review of bioactive neuropeptides and

lung development.

Preface vii

The last part of the book, Chapters 12-16, centers on the pathophysiology of

neonatal and pediatric pulmonary disorders. T. R. Korfhagen and J. A Whitsett re­

view methods for introducing mutations that affect respiratory function. They con­

centrate on the SP-B knockout mouse, which provides a model for studying the role

of SP-B in lung function and for designing new therapies for surfactant deficiency.

M. Kalenga, C. Gaultier, and P. H. Burri review current knowledge on the role of nu­

trition in lung development, emphasizing alterations produced during the periods

characterized by the highest rates of remodeling of the gas exchange compartment.

R. Harding and C. Albuquerque cover research on fetal lung hypoplasia and the con­

trol of lung expansion in the fetus, discussing congenital diaphragmatic hernia, mus­

culoskeletal and neurological abnormalities, and other causes of lung hypoplasia.

R. L. Morton and C. W. White deal with pulmonary antioxidant defense mechanisms

and describe the pathogenic events involved in the development of oxygen toxicity

in bronchopulmonary dysplasia of premature infants. Finally, S. G. Haworth and

A A Hislop report their unique experience with lung development after transplan­

tation in immature rats. Their chapter is of obvious clinical relevance because lung

transplantation is now a therapeutic option in children with end-stage pulmonary or

vascular disease. C. G.

J. R. B. M.P.

REFERENCES

1. Avery, M. E., and J. Mead. Surface properties in relation to atelectasis and hyaline mem­

brane disease. Am]. Dis. Child. 97:517-523, 1959.

2. Gaultier, C., and F. Girard. Croissance pulmonaire normale et pathologique: relation struc­

ture-fonction. Bull. Eur. Physiopathol. Resp. 16:791-842, 1980.

3. Thurlbeck, W. M. Postnatal growth and development of the lung. Am. Rev. Respir. Dis.

111:803-844, 1975. 4. Bourbon, J. Pulmonary surfactant: biochemical, functional, regulatory, and clinical con­

cepts. Boca Raton, Fl: CRC Press, Inc., 1991.

5. Robertson, B., L. M.G. Van Golde, and J. J. Batenburg. Pulmonary surfactant from molecu­

lar biology to clinical practice. Amsterdam: Elsevier, 1992.

6. Reid, L. The embryology of the lung. In: Ciba Foundation Symposium: Development of the Lung. edited by A. V. S. De Reuk and Porter, R. Londres: Churchill, 1967, p. 109-112.

CONTENTS

Contributors, xi

1 Lung Branching Morphogenesis: Role of Growth Factors and Extracellular Matrix, 1 Richard Kejjzer and Martin Post

2 Development of Lung Elastic Matrix, 28 Thomas J. Mariani and Richard A. Pierce

3 Differentiation and Maturation of Airway Epithelial Cells: Role of Extracellular Matrix and Growth Factors, 46 Dominique Gaillard and Edith Puchelle

4 Gene Expression in Alveolar Development, 77 Jacques R. Bourbon

5 Lung Development and Pulmonary Angiogenesis, 122 Peter H. Burri

6 Development of the Pulmonary Vasculature, 152 Nicholas W. Morrell, Mary C. M. Weiser, and Kurt R. Stenmark

7 Nitric Oxide and Endothelin in the Developing Pulmonary Circulation: Physiologic and Clinical Implications, 196 Steven H. Abman, John P. Kinsella, and Jean-Christophe Mercier

8 Development of Cellular Host Defense Mechanisms, 221 Sergei P. Sorokin, Richard F. Hoyt, Jr., and Nancy A. F. McNelly

ix

X

9 Development of Lung Epithelial Ion Transport: Implications for Neonatal Lung Disease, 255 Olli Pitkiinen and Hugh O'Brodovich

10 Mechanisms of Cell Growth and Tissue Repair, 282 Annick Clement and Jerome S. Brody

11 Bioactive Peptides and Lung Development, 304 Mary E. Sunday

12 Transgenic Models of Lung Development and Disease, 327 Thomas R. Korfhagen and Jeffrey A. Whitsett

13 Nutritional Aspects of Lung Development, 347 Masendu Kalenga, Claude Gaultier, and Peter H. Burri

14 Pulmonary Hypoplasia: Role of Mechanical Factors in Prenatal Lung Growth, 364 Richard Harding and Cheryl Albuquerque

15 Pulmonary Antioxidant Defense Mechanisms, 395 Ronald L. Morton and Carl W White

16 Lung Development After Transplantation, 425 Sheila G. Haworth and Alison A. Hislop

Index, 441

Contents

Contributors

STEVEN H. ABMAN

Pediatric Heart-Lung Center Department of Pediatrics University of Colorado School of Medicine and The Children's Hospital Denver, Colorado

CHERYL ALBUQUERQUE

Department of Obstetrics and Gynecology University of California Davis, California

JACQUES R. BOURBON

INSERM Unite 319 Univerisite Denis Diderot-Paris 7 Paris, France

JEROME S. BRODY

Pulmonary Center Boston University School of Medicine Boston, Massachusetts

PETER H. BuRRI

Institute of Anatomy University of Berne Berne, Switzerland

ANNICK CLEMENT

Department of Pediatric Pulmonology Trousseau Hospital St. Antoine Medical School University of Paris Paris, France

xi

DOMINIQUE GAILLARD

INSERM Unite 314, IFR 53 Biologie du Developpement-Reproduction, UFR Medecine Reims, France

CLAUDE GAULTIER

Service de Physiologie-Explorations Fonctionnelles H6pital Robert Debre, Universite Paris 7 Paris, France

RICHARD HARDING

Department of Physiology Monash University Melbourne, Victoria Australia

SHELIA G. HAWORTH

Developmental Pharmacology and Vascular Biology Unit Institute of Child Health London, United Kingdom

ALISON A. HISLOP

Developmental Pharmacology and Vascular Biology Unit Institute of Child Health London, United Kingdom

RICHARD F. HoYT, JR.

Department of Anatomy and Neurobiology Boston University School of Medicine Boston, Massachusetts

xii

MASENDU KALENGA Service de Neonatologie Clinique Saint Vincent Rocourt, Belgium

RICHARD KEYZER Lung Biology Research Program Hospital for Sick Children Toronto, Canada

JoHN P. KINSELLA Section of Neonatology Department of Pediatrics University of Colorado School of Medicine and The Children's Hospital Denver, Colorado

THoMAS R. KoRFHAGEN Division of Pulmonary Biology Children's Hospital Research Foundation Cincinnati, Ohio

THOMAS J. MARIANI Department of Internal Medicine Washington University School of Medicine at Barnes-Jewish Hospital St. Louis, Missouri

NANCY A. F. McNELLY Department of Anatomy and Neurobiology Boston University School of Medicine Boston, Massachusetts

JEAN-CHRISTOPHE MERCIER Service de Reanimation Pediatrique Hopital Robert Debre and Laboratoire de Physiologie sur la Circulation Pulmonaire Faculte de Medecine Cochin Paris, France

NICHOLAs W. MoRRELL Developmental Lung Biology Department of Pediatrics University of Colorado Health Sciences Center Denver, Colorado and Department of Medicine Royal Postgraduate Medical School Hammersmith Hospital London, United Kingdom

RoNALD L. MoRTON Department of Pediatrics

Contributors

National Jewish Center for Immunology and Respiratory Medicine and University of Colorado Health Sciences Center Denver, Colorado

HuGH O'BRoDOVICH Medical Research Council Group in Lung Development Hospital for Sick Children Research Institute Department of Pediatrics University of Toronto Toronto, Canada

RICHARD A. PIERCE Department of Internal Medicine Washington University School of Medicine at Barnes-Jewish Hospital St. Louis, Missouri

0LLI PITKANEN Children's Hospital University of Helsinki Helsinki, Finland

MARTIN PosT The Medical Research Council Group in Lung Development Hospital for Sick Children Research Institute Department of Pediatrics and Physiology University of Toronto Toronto, Canada

EDITH PUCHELLE INSERM Unite 314, IFR 53 Biologie du Developpement-Reproduction, UFR Medecine Reims, France

SERGEI P. SoROKIN Department of Anatomy and Neurobiology Boston University School of Medicine Boston, Massachusetts

Contributors

KuRT R. STENMARK Department of Medicine Royal Postgraduate Medical School Hammersmith Hospital London, United Kingdom

MARY E. SUNDAY Brigham & Women's Hospital and Harvard Medical School Department of Pathology Boston, Massachusetts

MARY c. M. WEISER Developmental Lung Biology Department of Pediatrics University of Colorado Health Science Center Denver, Colorado

CARL w. WHITE Department of Pediatrics

xiii

National Jewish Center for Immunology and Respiratory Medicine and University of Colorado Health Sciences Center Denver, Colorado

JEFFREY A. WHITSETT Division of Pulmonary Biology Children's Hospital Research Foundation Cincinnati, Ohio

LUNG DEVELOPMENT