Results and Problems in Cell Differentiation
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1 Results and Problems in Cell Differentiation Volume 58 Series editors Jacek Z. Kubiak, Rennes CX, France Malgorzata Kloc, Houston, TX, USA
2 More information about this series at
3 Rafal P. Piprek Editor Molecular Mechanisms of Cell Differentiation in Gonad Development
4 Editor Rafal P. Piprek Institute of Zoology Jagiellonian University Krakow Poland ISSN ISSN (electronic) Results and Problems in Cell Differentiation ISBN ISBN (ebook) DOI / Library of Congress Control Number: Springer International Publishing Switzerland 2016 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, express or implied, with respect to the material contained herein or for any errors or omissions that may have been made. Printed on acid-free paper This Springer imprint is published by Springer Nature The registered company is Springer International Publishing AG Switzerland
5 Preface The Gonad: A Complex Organ Containing Cells of Diverse Origin The sex is a set of structural and functional features that classify an individual as a male or female. In males, the testes produce sperm and androgens, which orchestrate the creation of male sex traits. In females, the ovaries produce eggs and estrogens, which drive the female sex features. In the majority of vertebrates, anatomically recognized gonads form late during embryogenesis; thus, the sex of an early embryo is defined exclusively by the presence of sex chromosomes. Interestingly, although the testes and ovaries have different structure and perform diverse functions, they develop from a common sexually undifferentiated bipotential anlage. In addition, the gonads consist of several cell types, which originate and migrate from different embryonic germ layers. Studies of gonadal development are fascinating because they reveal how the distinct cell lines mix and organize into a unique male or female structure. In this book, we describe how various cell types create the gonad and what is the molecular and cellular machinery driving these processes. Figure 1 summarizes key processes in mouse gonadal development. Summary of Gonadal Development in Mammals At the earliest stages of gonadogenesis, the gonadal primordia, termed the genital ridges, are sexually undifferentiated. In all vertebrates, the genital ridges form at the ventral surface of mesonephroi and the first cells in the gonadal primordium originate from the coelomic epithelium (Chap. 1). Mutational analyses revealed a series of genes (e.g., Gata4, Wt1, Sf1, and Lhx9) key for the formation of genital ridges in mice. The first morphological sign of gonadogenesis is the thickening v
6 vi Preface Fig. 1 Mouse timeline for major processes of male and female gonadal development. This diagram summarizes various processes occurring in germ cells and gonadal soma during the fetal development in mice starting from PGC specification to follicle assembly and spermatogonia reproliferation just after birth. Abbreviations: b member basement membrane, co. epith. coelomic epithelium, dpc days post coitum, dpp days postpartum, FLC fetal Leydig cells, GR genital ridge, PMC peritubular myoid cells, prosg prospermatogonia (proliferation) of coelomic epithelium, accompanied by disintegration of its basement membrane. These processes transform the monolayer epithelium into a cluster of coelomic epithelium-derived cells, called the genital ridge. These first gonadal cells, called the gonadal precursor cells or GREL cells, express SF1 protein and during further development of the gonad will differentiate into supporting cells, i.e.,
7 Preface vii the Sertoli cells in the testes and follicular cells (granulosa) in the ovaries that assist the germ cells in the process of spermato- or oogenesis, respectively. The second cell type present in developing gonad are the primordial germ cells (PGCs) that immigrate to the genital ridges (Chap. 2) from the distant embryonic locations. In mice, the germ line is established by epigenetic mechanisms in extraembryonic tissues before gonads develop and acquires totipotency through genetic and epigenetic regulation of genome function. We discuss the molecular and cellular mechanisms underlying the formation of PGCs in extraembryonic tissues and their migration toward the genital ridges. After reaching the genital ridges, the PGCs settle and become enclosed by coelomic epithelium-derived gonadal precursor cells. Battle between male sex-determining genes (Sry, Sox9, and Fgf9) and female sex-determining genes (Rspo1, Wnt4, and Foxl2) decides on the differentiation of these somatic cells into Sertoli or follicular cells, i.e., the male or female supporting cells (Chap. 3). Subsequently, in the testes, the Sertoli cells gather into groups enclosing the germ cells; these groups are organized into the testis cords that give rise to the sperm producing seminiferous tubules. In the ovaries, gonadal precursor cells enclose the oocytes and differentiate into granulosa. The third cell type present in developing gonad are cells immigrating from the embryonic kidney (mesonephros) (Chap. 4). The migration of mesonephrosderived cells seems critical for the formation of testes. In mice, the majority of cells immigrating from the mesonephros give rise to the endothelial cells contributing to the formation of blood vessels that are key for the establishment of testis cord structure and number. The VEGF, PDGF, and neurotrophins seem to be signaling factors crucial for the migration of mesonephros-derived cells to developing gonads. It has been suggested that mesonephros or gonad mesonephros border region is also a source of the peritubular myoid cells and steroidogenic cells of the gonad. The next step in gonadogenesis is the differentiation of the steroidogenic cells (Chap. 5). This cell line differentiates into the interstitium of the gonad, i.e., the region located outside of the testis cords/seminiferous tubules. While steroidogenic cells of the male gonad, termed Leydig cells, originate during fetal development, steroidogenic cells of the ovary, termed theca cells, differentiate around ovarian follicles at perinatal stages at the beginning of follicle formation. The origin of steroidogenic cells is still obscure. The potential sources of steroidogenic cells include the coelomic epithelium, mesonephros, adrenogonadal primordium, neural crest cells, gonad mesonephros border region, and perivascular cells. Several factors (such as DHH and PDGF) are believed to play a role in steroidogenic cell differentiation. After the onset of sexual differentiation of somatic cells in the gonads, the germ cells commit to the male or female pathways of gametogenesis (Chap. 6). In the developing female gonads, the germ cells enter meiosis just after the beginning of ovarian differentiation; thus, the oocytes form before birth. In the fetal testes, the germ cells are mitotically arrested in the spermatogonial stage, and in the male gonad, the meiosis is triggered during puberty. It seems that retinoic acid is a
8 viii Preface meiosis-inducing substance in both male and female gonads, but the difference in the pattern of expression of enzymes synthesizing and inactivating retinoic acid in the developing testes and ovaries causes sex-specific differences in meiotic entry. The final process of ovarian cells assembly occurs during folliculogenesis (Chaps. 7 and 8). The oocytes in the fetal ovaries gather to form germ cell clusters. Around birth, the clusters break down to form primordial follicles, each containing a single oocyte enclosed by flat follicular (granulosa) cells. Most of the primordial follicles remain quiescent; however, a selected subpopulation develops into primary follicles containing oocytes enclosed by cuboidal granulosa cells. The transition from primary to secondary follicles occurs when a single-layer granulosa proliferates to form a multilayer granulosa and the theca cells differentiate around the secondary follicle. Subsequently, the antrum forms within the secondary follicle. Signaling between oocyte and granulosa regulates oocyte growth and maturation. After ovulation, the remaining granulosa cells and theca cells undergo terminal differentiation into corpus luteum. The final assembly of cells in developing testes is the formation of elongated tubular structures termed the testis cords containing germ cells enclosed by pre-sertoli cells (derived from the aggregate of SF1-positive cells). The pre-sertoli cells commit to epithelial differentiation and polarize and gather into groups surrounding the germ cells. A basement membrane is deposited outside of the cords. Peritubular myoid cells differentiate outside the basement membrane of the testis cords. Soon after birth, the cords transform into seminiferous tubules when a lumen appears inside. Sertoli cells assist in spermato- and spermiogenesis which transform spermatogonial stem cells (SSCs) into spermatozoa (Chaps. 9 and 10). Specific cell junctions of Sertoli cells form a testis blood barrier that is critical for the process of spermatogenesis. The continuity of function of the testes and ovaries is ensured by stem cells which, owing to their abilities of self-renewal, constitute a source of somatic and germ cells in developing and adult gonads (Chap. 11). The continuity of spermatogenesis is ensured by the aforementioned spermatogonial stem cells (SSCs). Interestingly, despite the general belief that the number of oocytes is determined during the perinatal period, there is evidence that ovaries may have regenerative capability in adult females, ensured by the presence of female germline stem cells (FGSCs). Among somatic stem cells in the adult testes, stem Leydig cells (SLCs) have been described; however, so far, there is no evidence for the presence of stem cells for Sertoli or peritubular myoid cells. In adult ovaries, granulosa stem cells and thecal stem cells have been found. In this book, we also present information on the complex molecular machinery regulating gonad development. One of the important regulators are micrornas (mirnas), i.e., small noncoding RNAs with a major role in posttranscriptional regulation of gene expression. mirnas are differentially expressed in the developing male and female gonads, and thus, these molecules may be responsible for sexual differentiation (Chap. 12). mirnas have crucial roles in gonad development by either directly silencing the expression of proteins in somatic or germ cells or indirectly acting at the hypothalamus pituitary level. The fundamental role of
9 Preface ix mirnas in follicle assembly, growth, differentiation, and ovulation is especially well documented. The molecular mechanisms driving sex determination and sexual differentiation, i.e., creation of the testis vs. ovarian structure and function, constitute a cascade of factors, and the action of genes involved in these processes is interconnected in a complex network. Any disturbance in this complex cascade can lead to far-reaching consequences such as gonadal dysgenesis or sex reversal. Although a number of human sexual developmental disorders have been traced to various known mutations, the genetic causes for many disorders still remain unknown. The effects of genes involved in sex determination are discussed in Chap. 13. Much is known about the mechanisms of gonadogenesis; however, the further one delves into this area, the more complicated it becomes. The first descriptions of gonad development made in the nineteenth century were based on a simple histological staining and light microscopy observations. The development of molecular techniques in the second half of the twentieth century greatly contributed to the study of the genetic control of gonadogenesis. In Chap. 14, the history of gonad development studies is presented and techniques that launched work on the origin of cell lineages and the roles of molecular and cellular mechanisms driving the creation of testis vs. ovarian structure are described. Krakow, Poland Rafal P. Piprek
10 ThiS is a FM Blank Page
11 Contents 1 Early Development of the Gonads: Origin and Differentiation of the Somatic Cells of the Genital Ridges... 1 Rafal P. Piprek, Malgorzata Kloc, and Jacek Z. Kubiak 2 The Formation and Migration of Primordial Germ Cells in Mouse and Man Massimo De Felici 3 The Gonadal Supporting Cell Lineage and Mammalian Sex Determination: The Differentiation of Sertoli and Granulosa Cells Gwenn-Aël Carré and Andy Greenfield 4 Mesonephric Cell Migration into the Gonads and Vascularization Are Processes Crucial for Testis Development Sarah M. Romereim and Andrea S. Cupp 5 Origin and Differentiation of Androgen-Producing Cells in the Gonads Sarah J. Potter, Deepti Lava Kumar, and Tony DeFalco 6 Germ Cell Commitment to Oogenic Versus Spermatogenic Pathway: The Role of Retinoic Acid Kellie S. Agrimson and Cathryn A. Hogarth 7 Ovarian Folliculogenesis Nitzan Rimon-Dahari, Lia Yerushalmi-Heinemann, Liat Alyagor, and Nava Dekel 8 Control of Oocyte Growth and Development by Intercellular Communication Within the Follicular Niche Stephany El-Hayek and Hugh J. Clarke xi
12 xii Contents 9 Biology of the Sertoli Cell in the Fetal, Pubertal, and Adult Mammalian Testis Katarzyna Chojnacka, Marta Zarzycka, and Dolores D. Mruk 10 Mechanisms Regulating Spermatogonial Differentiation Jennifer M. Mecklenburg and Brian P. Hermann 11 Stem Cells in Mammalian Gonads Ji Wu, Xinbao Ding, and Jian Wang 12 A Role of MicroRNAs in Cell Differentiation During Gonad Development Hadas Grossman and Ruth Shalgi 13 The Battle of the Sexes: Human Sex Development and Its Disorders Anna Biason-Lauber 14 Methods for the Study of Gonadal Development Rafal P. Piprek Index
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