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VOLUME 2 KNOBIL AND NEILL’S PHYSIOLOGY OF REPRODUCTION FOURTH EDITION VOLUME 2 Editors-in-Chief T M. P a J. Z ony lanT and nThony eleZnik University of Pittsburgh, Pittsburgh, PA, USA Associate Editors d F. a avid lberTini Kansas University Medical Center, Kansas City, KS, USA r l. G oberT oodMan West Virginia University, Morgantown, WV, USA a e. h llan erbison Otago School of Medical Sciences, Dunedin, New Zealand M M. M c arGareT c arThy University of Maryland School of Medicine, Baltimore, MD, USA l J. M ouis uGlia Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, USA J a s. r o nne ichards Baylor College of Medicine, Houston, TX, USA AMSTERDAM • BOSTON • HEIDELBERG • LONDON NEW YORK • OXFORD • PARIS • SAN DIEGO SAN FRANCISCO • SINGAPORE • SYDNEY • TOKYO Academic Press is an imprint of Elsevier Academic Press is an imprint of Elsevier 32 Jamestown Road, London NW1 7BY, UK 225 Wyman Street, Waltham, MA 02451, USA 525 B Street, Suite 1800, San Diego, CA 92101-4495, USA The Boulevard, Langford Lane, Kidlington, Oxford OX5 1GB, UK Copyright © 2015, 2006 Elsevier Inc. All rights reserved. First Edition: Raven Press (1988) Second Edition: Lippincott Williams & Wilkins (1994) No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Details on how to seek permission, further information about the Publisher’s permissions policies and our arrangements with organizations such as the Copyright Clearance Center and the Copyright Licensing Agency, can be found at our website: www.elsevier.com/permissions. This book and the individual contributions contained in it are protected under copyright by the Publisher (other than as may be noted herein). Notices Knowledge and best practice in this field are constantly changing. As new research and experience broaden our understanding, changes in research methods, professional p ractices, or medical treatment may become necessary. Practitioners and researchers must always rely on their own experience and k nowledge in evaluating and using any information, methods, compounds, or experiments described herein. In using such information or methods they should be mindful of their own safety and the safety of others, including parties for whom they have a professional responsibility. To the fullest extent of the law, neither the Publisher nor the authors, contributors, or editors, assume any liability for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions, or ideas contained in the material herein. ISBN: 978-0-12-397175-3 (set) ISBN: 978-0-12-416594-6 (v1) ISBN: 978-0-12-416593-9 (v2) British Library Cataloguing-in-Publication Data A catalogue record for this book is available from the British Library Library of Congress Cataloging-in-Publication Data A catalog record for this book is available from the Library of Congress For information on all Academic Press publications visit our website at http://store.elsevier.com/ Typeset by TNQ Books and Journals www.tnq.co.in Printed and bound in the United States of America Illustration Credits Pair bonded prairie vole family from Chapter 48 (J. Balthazart and L. Young). Photo by Todd H. Ahern Relationship between gonadotropin releasing hormone GnRH (red) and kisspeptin neurons (green) in a coronal section of the monkey hypothalamus from Chapter 28 (A.J. Zeleznik and T.M. Plant). Mouse uterus showing vascular permeability at the sites of implantation detected after an intravenous injection of a blue dye on day 8 of pregnancy. From Chapter 38 (S.K. Dey). Per Dey, acknowledgement/credit not needed. Top back. Scanning electron micrograph of a bull sperm interacting with ciliated epithelium in the sperm storage reservoir of the oviduct (Chapter 5, Lefebvre et al., 1995). Middle back from David Albertini. Confocal micrograph of a horse oocyte based on collaboration between Elaine Carnevale, Colorado State University and David Albertini and John Bromfield of the Kansas University Medical Center. Lower back from Chapter 28 (A.J. Zeleznik and T.M. Plant). Pulsatile LH release from the pituitary and multi unit electrical activity in the mediobasal hypothalamus recorded from an intact (left panel) and ovariectomized (right panel) rhesus monkey. Contributors Kjersti M. Aagaard Department of Obstetrics and Gynecol- Gerard S. Conway Department of Endocrinology, University ogy, Division of Maternal-Fetal Medicine, Baylor College of College Hospitals, London, UK Medicine, Houston, TX, USA John F. Couse Taconic Farms, Albany Operations, Rensselaer, David F. Albertini Department of Molecular and Integrative NY, USA Physiology, Institute of Reproductive Health and Regenera- Geert J. de Vries Neuroscience Institute, Georgia State Uni- tive Medicine, Kansas University Medical Center, Kansas versity, Atlanta, GA, USA City, KS, USA Emily DeFranco Department of Obstetrics and Gynecology, Eugene D. Albrecht Departments of Obstetrics, Gynecology, University of Cincinnati College of Medicine, Cincinnati, and Reproductive Sciences and Physiology, University of OH, USA Maryland School of Medicine, Baltimore, MD, USA Francesco J. DeMayo Department of Molecular and Cellu- Steven M. Anderson University of Colorado Denver, lar Biology, Baylor College of Medicine, Houston, TX, USA Anschutz Medical Campus, Aurora, CO, USA Sudhansu K. Dey Division of Reproductive Sciences, Cincin- William E. Armstrong Department of Anatomy and Neuro- nati Children’s Research Foundation, Cincinnati Children’s biology, University of Tennessee Health Science Center, Hospital Medical Center, Cincinnati, OH, USA Memphis, TN, USA Juan M. Dominguez Department of Psychology, University Richard J. Auchus Division of Metabolism, Endocrinology, of Texas, Austin, TX, USA and Diabetes, Department of Internal Medicine, University Edward M. Eddy Laboratory of Reproductive and Develop- of Michigan Medical Center, Ann Arbor, MI, USA mental Toxicology, National Institute of Environmental Susan P. Bagby Department of Medicine, Division of Health Sciences, National Institute of Health, Research Tri- Nephrology and Hypertension, Center for Developmental angle Park, NC, USA Health, Knight Cardiovascular Institute, Oregon Health and Rafael A. Fissore Department of Veterinary and Animal Science University, Portland, OR, USA Science, University of Massachusetts, Amherst, MA, USA Jacques Balthazart GIGA Neurosciences, University of Liège, Loretta M. Flanagan-Cato Laboratory of Neuroendocrinol- Liège, Belgium ogy, Department of Psychology, University of Pennsylvania, April K. Binder Laboratory of Reproductive and Develop- Philadelphia, PA, USA mental Toxicology, National Institute of Environmental Harvey M. Florman Department of Cell and Developmental Health Sciences, NC, USA Biology, University of Massachusetts Medical School, Jeffrey D. Blaustein Center for Neuroendocrine Studies, Worcester, MA, USA Neuroscience and Behavior Program, University of Massa- chusetts, Amherst, MA, USA Nancy G. Forger Neuroscience Institute, Georgia State Uni- versity, Atlanta, GA, USA S. Marc Breedlove Neuroscience Program, Michigan State University, East Lansing, MI, USA Douglas L. Foster Departments of Obstetrics, Gynecology, and Ecology and Evolutionary Biology, University of Paula J. Brunton Division of Neurobiology, The Roslin Insti- Michigan, Ann Arbor, MI, USA tute and Royal (Dick) School of Veterinary Studies, Univer- sity of Edinburgh, Easter Bush, Midlothian, UK Stephen Franks Institute of Reproductive and Developmen- tal Biology, Imperial College London, Hammersmith Hospi- Jeeyeon Cha Division of Reproductive Sciences, Cincinnati tal, London, UK Children’s Research Foundation, Cincinnati Children’s Hos- pital Medical Center, Cincinnati, OH, USA Jennifer R. Gardiner Division of Cancer Biology, Institute of Cancer Research, London, UK Shawn L. Chavez Institute for Stem Cell Biology and Regen- erative Medicine, Stanford University, Stanford, CA, USA, Kathrin Gassei Department of Obstetrics, Gynecology and Department of Obstetrics and Gynecology, Stanford Univer- Reproductive Sciences, University of Pittsburgh School sity, Stanford, CA, USA, Division of Reproductive and of Medicine, and Magee-Womens Research Institute, Developmental Sciences, Oregon National Primate Research Pittsburgh, PA, USA Center, Oregon Health and Science University, Beaverton, George D. Giraud Department of Medicine, Center for OR, USA Developmental Health, Knight Cardiovascular Institute, Paula E. Cohen Department of Biomedical Sciences, Cornell Oregon Health and Science University, Portland VA Medical University, Ithaca, NY, USA Center, Portland, OR, USA xxxvii xxxviii CONTRIBUTORS Robert L. Goodman Department of Physiology and Pharma- Jon E. Levine Department of Neuroscience, School of Medi- cology, West Virginia University, Morgantown, WV, USA cine and Public Health, Wisconsin National Primate Research Center, University of Wisconsin, Madison, WI, USA Andrea C. Gore Division of Pharmacology and Toxicology, The University of Texas at Austin, Austin, TX, USA Xiao-Feng Li Academic Department of Anatomy and Human Sciences/Division of Women’s Health, School of Medicine, David R. Grattan Centre for Neuroendocrinology, Univer- King’s College London, Guy’s Campus, London, UK sity of Otago, Dunedin, New Zealand Hyunjung (Jade) Lim Division of Reproductive Sciences, Janet E. Hall Department of Medicine, Reproductive Endo- Cincinnati Children’s Research Foundation, Cincinnati Chil- crine Unit, Massachusetts General Hospital and Harvard dren’s Hospital Medical Center, Cincinnati, OH, USA; Medical School, Boston, MA, USA Department of Biomedical Science and Technology, Konkuk Kate Hardy Institute of Reproductive and Developmental University, Seoul, South Korea Biology, Imperial College London, Hammersmith Hospital, Mark Lindgren Department of Urology, University of Illinois London, UK at Chicago, Chicago, IL, USA Frances J. Hayes Department of Medicine, Reproductive Zhilin Liu Department of Molecular and Cellular Biology, Endocrine Unit, Massachusetts General Hospital and Baylor College of Medicine, Houston, TX, USA Harvard Medical School, Boston, MA, USA Joseph S. Lonstein Neuroscience Program and Department of David Hazlerigg Department of Arctic and Marine Biology, Psychology, Michigan State University, East Lansing, MI, USA University of Tromsø, Tromsø, Norway Paul S. MacLean University of Colorado Denver, Anschutz Mark P. Hedger Monash Institute of Medical Research, Medical Campus, Aurora, CO, USA Monash University, Melbourne, VIC, Australia Catherine A. Marler Neuroscience Training Program and Jon D. Hennebold Division of Reproductive and Develop- Department of Psychology, University of Wisconsin, mental Sciences, Oregon National Primate Research Center, Madison, WI, USA Oregon Health and Science University, Beaverton, OR, USA Kelly Mayo Department of Molecular Biosciences, Center for Allan E. Herbison Center for Neuroendocrinology and Reproductive Science, Northwestern University, Evanston, Department of Physiology, Otago School of Medical Sci- IL, USA ences, Dunedin, New Zealand Erik C. Mazur Department of Obstetrics and Gynecology, Sylvia C. Hewitt Laboratory of Reproductive and Develop- Baylor College of Medicine, Texas Children’s Hospital Pavil- mental Toxicology, National Institute of Environmental ion for Women, Houston, TX, USA Health Sciences, NC, USA Craig A. McArdle School of Clinical Sciences, Laboratories Stanley M. Hileman Department of Physiology and Phar- for Integrative Neuroscience and Endocrinology, University macology, West Virginia University, Morgantown, WV, USA of Bristol, Bristol, UK Barry T. Hinton Department of Cell Biology, University of Margaret M. McCarthy Departments of Pharmacology, Physi- Virginia Health System, Charlottesville, VA, USA ology, and Psychiatry, Program in Neuroscience, U niversity of J. Kim Holloway Department of Biomedical Sciences, Cornell Maryland School of Medicine, Baltimore, MD, USA University, Ithaca, NY, USA Neil J. McKenna Department of Molecular and Cellular Elaine M. Hull Department of Psychology, Florida State Uni- Biology, Baylor College of Medicine, Houston, TX, USA versity, Tallahassee, FL, USA James L. McManaman University of Colorado Denver, Joan S. Hunt Department of Anatomy and Cell Biology, Uni- Anschutz Medical Campus, Aurora, CO, USA versity of Kansas Medical Center, Kansas City, KS, USA Sam Mesiano Department of Reproductive Biology, Case Mary Hunzicker-Dunn School of Molecular Biosciences, Western Reserve University, Cleveland, OH, USA, Depart- Washington State University, Pullman, WA, USA ment of Obstetrics and Gynecology, University Hospitals of E. Keith Inskeep Division of Animal and Nutritional Sci- Cleveland, Cleveland, OH, USA ences, West Virginia University, Morgantown, WV, USA Joan I. Morrell Center for Molecular and Behavioral Neuro- Thomas Jansson Department of Obstetrics and Gynecology, science, Rutgers University, Newark, NJ, USA Center for Pregnancy and Newborn Research, University of Louis J. Muglia Center for Prevention of Preterm Birth, Texas Health Science Center at San Antonio, San Antonio, Cincinnati Children’s Hospital Medical Center, Cincinnati, TX, USA OH, USA Sherri L. Jones Center for Studies in Behavioral Neurobiol- Makoto C. Nagano Department of Obstetrics and Gynecol- ogy, Department of Psychology, Concordia University, Mon- ogy, Royal Victoria Hospital, McGill University, Montreal, tréal, QC, Canada QC, Canada Kenneth S. Korach Laboratory of Reproductive and Devel- Margaret C. Neville University of Colorado Denver, opmental Toxicology, National Institute of Environmental Anschutz Medical Campus, Aurora, CO, USA Health Sciences, NC, USA Kevin T. O’Byrne Academic Department of Anatomy and Michael J. Large Department of Molecular and Cellular Human Sciences/Division of Women’s Health, School of Medi- Biology, Baylor College of Medicine, Houston, TX, USA cine, King’s College London, Guy’s Campus, London, UK CONTRIBUTORS xxxix Peter O’Shaughnessy Institute of Biodiversity, Animal Mark S. Roberson Department of Biomedical Sciences, Health and Comparative Medicine, University of Glasgow, College of Veterinary Medicine, Cornell University, Ithaca, Glasgow, UK NY, USA Kyle E. Orwig Departments of Obstetrics, Gynecology Sarah A. Robertson Robinson Research Institute and School and Reproductive Sciences, and Molecular Genetics and of Paediatrics and Reproductive Health, University of Developmental Biology, University of Pittsburgh School of Adelaide, Adelaide, SA, Australia Medicine, and Magee-Womens Research Institute, Pitts- John A. Russell Centre for Integrative Physiology, Univer- burgh, PA, USA sity of Edinburgh, Edinburgh, UK Stephanie A. Pangas Department of Pathology and Immu- Yoel Sadovsky Department of Obstetrics, Gynecology, and nology, and Department of Molecular and Cellular Biology, Reproductive Sciences, Magee-Womens Research Institute, Baylor College of Medicine, Houston, TX, USA University of Pittsburgh, Pittsburgh, PA, USA Gerald J. Pepe Department of Physiological Sciences, Eastern Masayuki Shimada Laboratory of Reproductive Endocrinol- Virginia Medical School, Norfolk, VA, USA ogy, Graduate School of Biosphere Science, Hiroshima Uni- Mariana Pereira Center for Molecular and Behavioral Neu- versity, Higashi-Hiroshima, Hiroshima, Japan roscience, Rutgers University, Newark, NJ, USA Valerie Simonneaux Institut des Neurosciences Cellulaires Margaret G. Petroff Department of Anatomy and Cell et Intégratives, Strasbourg, France Biology, University of Kansas Medical Center, Kansas City, Lee B. Smith MRC Centre for Reproductive Health, The KS, USA Queen’s Medical Research Institute, University of Edin- James G. Pfaus Center for Studies in Behavioral Neurobiol- burgh, Edinburgh, UK ogy, Department of Psychology, Concordia University, Richard L. Stouffer Division of Reproductive and Develop- Montréal, QC, Canada mental Sciences, Oregon National Primate Research Center, Bart T. Phillips Departments of Obstetrics, Gynecology and Oregon Health and Science University, Beaverton, OR, Reproductive Sciences, and Molecular Genetics and Devel- USA opmental Biology, University of Pittsburgh School of Medi- Susan S. Suarez Department of Biomedical Sciences, cine, and Magee-Womens Research Institute, Pittsburgh, PA, College of Veterinary Medicine, Cornell University, Ithaca, USA NY, USA Tony M. Plant Department of Obstetrics, Gynecology and Melissa A. Suter Department of Obstetrics and Gynecology, Reproductive Sciences, University of Pittsburgh School of Baylor College of Medicine, Houston, TX, USA Medicine, and Magee-Womens Research Institute, Pitts- Amanda Swain Division of Cancer Biology, Institute of burgh, PA, USA Cancer Research, London, UK Vincent Prevot Laboratory of Development and Plasticity of Manuel Tena-Sempere Department of Cell Biology, Physiol- the Neuroendocrine Brain, Jean-Pierre Aubert Research ogy and Immunology, University of Córdoba, Córdoba, Center, School of Medicine, University of Lille, Lille, Spain, CIBER Fisiopatología de la Obesidad y Nutrición, France Instituto de Salud Carlos III, Spain, Instituto Maimónides de Gail S. Prins Department of Urology, University of Illinois at Investigaciones Biomédicas (IMIBIC)/Hospital Universita- Chicago, Chicago, IL, USA rio Reina Sofia, Córdoba, Spain Aleksandar Rajkovic Departments of Obstetrics, Gynecol- Ei Terasawa Department of Pediatrics, School of Medicine, ogy and Reproductive Sciences, Human Genetics, and and Wisconsin National Primate Research Center, Univer- Pathology, University of Pittsburgh, and Magee-Womens sity of Wisconsin, Madison, WI, USA Research Institute, Pittsburgh, PA, USA Kent L. Thornburg Department of Medicine, Center for Cyril Ramathal Institute for Stem Cell Biology and Regen- Developmental Health, Knight Cardiovascular Institute, erative Medicine, Stanford University, Stanford, CA, USA, Oregon Health and Science University, Portland, OR, USA Department of Obstetrics and Gynecology, Stanford Univer- Paul Le Tissier Center for Integrative Physiology, University sity, Stanford, CA, USA of Edinburgh, Edinburgh, UK Renee A. Reijo Pera Institute for Stem Cell Biology and Kiyotaka Toshimori Department of Reproductive Biology Regenerative Medicine, Stanford University, Stanford, CA, and Medicine and Department of Histology, Chiba Univer- USA, Department of Obstetrics and Gynecology, Stanford sity Graduate School of Medicine, Chuo-ku, Chiba, Japan University, Stanford, CA, USA Hanna Valli Departments of Obstetrics, Gynecology and JoAnne S. Richards Department of Molecular and Cellular Reproductive Sciences, and Molecular Genetics and Devel- Biology, Baylor College of Medicine, Houston, TX, USA opmental Biology, University of Pittsburgh School of Medi- Emilie F. Rissman Department of Biochemistry and Molecu- cine, and Magee-Womens Research Institute, Pittsburgh, PA, lar Genetics, Program in Neuroscience, University of Vir- USA ginia School of Medicine, Charlottesville, VA, USA William H. Walker Department of Obstetrics, Gynecology Bernard Robaire Departments of Pharmacology and Thera- and Reproductive Sciences, University of Pittsburgh School peutics, and Obstetrics and Gynecology, McGill University, of Medicine, and Magee-Womens Research Institute, Pitts- Montréal, QC, Canada burgh, PA, USA xl CONTRIBUTORS Wipawee Winuthayanon Laboratory of Reproductive and Larry J. Young Department of Psychiatry and Behavioral Developmental Toxicology, National Institute of Environ- Sciences, Center for Translational Social Neuroscience, and mental Health Sciences, NC, USA Yerkes National Primate Research Center, Emory University, Selma Feldman Witchel Department of Pediatrics, Univer- Atlanta, GA, USA sity of Pittsburgh School of Medicine, and Children’s Hos- Anthony J. Zeleznik Department of Obstetrics, Gynecology pital of Pittsburgh, Univeristy of Pittsburgh Medical Center, and Reproductive Sciences, University of Pittsburgh School of Pittsburgh, PA, USA Medicine, and Magee-Womens Research Institute, Pittsburgh, PA, USA Introduction This, the fourth edition of “Knobil and Neill’s Phys- molecular, cellular, and organismic levels. This is not iology of Reproduction,” is a major departure from its surprising given the excellent past records of the two first three editions by having Editors in Chief not pre- Editors in Chief. viously involved in managing the production of this Ernst Knobil and I believed strongly that any work work. Before his death in the year 2000, Ernst Knobil claiming to be comprehensive and hewing to the highest and I had made plans for the transition to an Editor principles of scholarship must include a summary of the in Chief who had been trained at the postdoctoral founding and the founders of the field. Because Dr Roy level in one of our laboratories. Dr Tony M. Plant was O. Greep was one of the leading founders of the field, we chosen from among several excellent candidates who requested that he provide that information together with had the requisite characteristics needed to continue an overview of the future of the field in his Foreword for production of a work that would have the same high the first edition in 1988. Thus, the original Foreword had standards we hoped to have maintained in the earlier the great strength of being written by one of the last sur- editions. I first met Tony in the early 1970s while I was a viving founders in the field, and thus avoided the greatest young faculty member at Emory University in Atlanta, weakness of all historical analysis, namely that history is Georgia, and he was employed at the Georgia Mental defined as what professional historians define it to be. Health Institute also located in Atlanta. I received a A new Foreword has been prepared by Dr M. Susan letter from Ernst Knobil inquiring about my impres- Smith to address, in part, Greep’s predictions of prog- sion of Tony, who had applied for a postdoctoral fel- ress that might occur in the field in the succeeding years lowship in Ernst’s laboratory where I had trained as a after his Foreword first appeared. Susan is a prominent fellow but had recently relocated to Emory. My reply leader in reproductive physiology due, for example, to was a strong endorsement of Tony, which was borne her Presidency of the Endocrine Society, Directorship of out in subsequent years. Tony Plant chose Dr Tony the Oregon National Primate Research Center, and main- Zeleznik as a Co-Editor in Chief to share with him taining an National Institutes of Health (NIH)-funded the demanding tasks of editorship requiring a broad laboratory running for several decades. I am pleased base of information in the field and a high level of aca- that her fellowship training occurred in my laboratory at demic rigor. My perusal of the list of authors and their Emory University during which we published the most chapter titles suggests that the information presented highly cited paper of my career, of which she was the in this edition will rival in quality that presented in senior author. the first three editions, i.e., the work is a modern syn- thesis of reproductive physiology of mammals at the Jimmy D. Neill xli Preface Having had the fortune of being mentored by Ernst and to identify the burning questions that remain to be Knobil in the early stages of our careers and serving addressed. as assistant professors in his faculty in the Department In this 4th edition, Volume 1 focuses on basic pro- of Physiology at the University of Pittsburgh School of cesses of male and female reproduction while the Medicine, we were greatly honored by the invitation to thrust of Volume 2 is on the physiological control sys- serve as Editors in Chief for the 4th edition of this book tems that govern reproductive processes, including that has come to be recognized by many as the “Bible of those regulating sexual behavior. A chapter on meio- Reproduction.” At the same time, we undertook the task sis has been included for the first time, and discus- with considerable trepidation, being fully aware of how sions of epigenetic mechanisms that are emerging as difficult it would be to fill the shoes of Professors Knobil important regulators of reproduction, as well as fetal and Neill, who, with their utmost attention to scientific origins of adult diseases, have been expanded. New rigor, had, together or individually, guided the previous chapters on spermatogonial stem cells and hormone three editions. signaling in the testis that provide contemporary views Given the foregoing challenge, we began by evaluat- of the control of testicular function replace the more ing whether the structure and content of the previous classical approach to the control of spermatogen- edition needed to be refocused. It quickly became obvi- esis that was presented in prior editions of the text. ous that this was indeed the case because of the rapidly We have also expanded the discussion of the regula- growing use of “omics” approaches in most, if not all, tion of reproductive behavior, which, having moved areas of reproductive biology. In this regard, it is note- far away from its origins in ethology, is now domi- worthy that the first edition of this text was published nated by genomic, epigenetic, cellular, and molecular in 1988, a year before the first use of the “gene knock- approaches to the understanding of sexual motivation, out” approach in mice was described. Over the course partner preference, and parental behavior. For those of the 25-year history of this text, the ability to delete or chapters that have been updated, we are confident that modify individual genes has increasingly and signifi- these new versions present the most current discussion cantly added to the classical armamentarium of organ of the subject material. ablation/hormone replacement paradigms previously Such restructuring of this book would not have been available to investigators studying reproduction. In possible without the enthusiasm and commitment of our addition, the application of genetics/genomics to eluci- section editors, to whom we are greatly indebted. A fea- date the etiology of human disease has increased in par- ture of the 3rd edition that has been maintained is the allel to the use of transgenesis in experimental animals. inclusion of the Foreword by Professor Roy O. Greep that Collectively, these powerful approaches have provided was written for the 1st edition, published in 1988. As rec- new, and often serendipitous, information on the regu- ognized by Professor Neill, the Editor in Chief of the pre- lation of reproduction. For example, our view of the vious edition, Greep’s account of the future of research neuroendocrine control of the hypothalamic–pituitary– on the physiology of reproduction continues to remain gonadal axis is now completely dominated by kisspeptin. remarkably relevant, now 26 years after it was written. This hypothalamic peptide, which, in the context of We are pleased to include a second Foreword that was reproduction, was unheard of before 2003, surfaced written by Dr M. Susan Smith, who worked with Jimmy because mutations of its receptor, then known as GPR54, Neill as a postdoctoral scholar and was also a member of were identified in individuals with delayed puberty. Ernst Knobil’s Department of Physiology at the Univer- Accordingly, our authors were confronted with the sity of Pittsburgh School of Medicine. Dr Smith’s broad need to integrate information gleaned from “classical” understanding of both whole animal and molecular whole animal studies with results generated by con- approaches used in the study of reproductive processes temporary “omics” approaches in order to provide a makes her uniquely qualified to comment on how the holistic overview of reproductive processes. In keeping study of reproduction has progressed since Greep’s with this approach, we encouraged authors to discuss original Foreword in 1988, as well as to identify the the historical underpinnings of their respective fields challenges to be met in future years. xliii

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The Fourth Edition of Knobil & Neill continues to serve as a reference aid for research, to provide the historical context to current research, and most importantly as an aid for graduate teaching on a broad range of topics in human and comparative reproduction. In the decade since the publication o
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