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Review Article Physiologic Course of Female Reproductive Function: a Molecular Look Into the Prologue of Life

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Review Article Physiologic Course of Female Reproductive Function: a Molecular Look Into the Prologue of Life Hindawi Publishing Corporation Journal of Pregnancy Volume 2015, Article ID 715735, 21 pages http://dx.doi.org/10.1155/2015/715735 Review Article Physiologic Course of Female Reproductive Function: A Molecular Look into the Prologue of Life Joselyn Rojas, Mervin Chávez-Castillo, Luis Carlos Olivar, María Calvo, José Mejías, Milagros Rojas, Jessenia Morillo, and Valmore Bermúdez Endocrine-Metabolic Research Center, “Dr. Felix´ Gomez”,´ Faculty of Medicine, University of Zulia, Maracaibo 4004, Zulia, Venezuela Correspondence should be addressed to Joselyn Rojas; [email protected] Received 6 September 2015; Accepted 29 October 2015 Academic Editor: Sam Mesiano Copyright © 2015 Joselyn Rojas et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The genetic, endocrine, and metabolic mechanisms underlying female reproduction are numerous and sophisticated, displaying complex functional evolution throughout a woman’s lifetime. This vital course may be systematized in three subsequent stages: prenatal development of ovaries and germ cells up until in utero arrest of follicular growth and the ensuing interim suspension of gonadal function; onset of reproductive maturity through puberty, with reinitiation of both gonadal and adrenal activity; and adult functionality of the ovarian cycle which permits ovulation, a key event in female fertility, and dictates concurrent modifications in the endometrium and other ovarian hormone-sensitive tissues. Indeed, the ultimate goal of this physiologic progression is to achieve ovulation and offer an adequate environment for the installation of gestation, the consummation of female fertility. Strict regulation of these processes is important, as disruptions at any point in this evolution may equate a myriad of endocrine- metabolic disturbances for women and adverse consequences on offspring both during pregnancy and postpartum. This review offers a summary of pivotal aspects concerning the physiologic course of female reproductive function. 1. Introduction for a second wave of structural and functional modifications inherent to the ovarian cycle, which in turn finalizes with the Historically, the phenomenon of human reproduction has crucial event in female fertility: ovulation [4]. In ensemble, awakened great interest. One of its first scientific descriptions, these processes permit generation of new life, reproduction. authored by Hippocrates, dates back to the fifth century Indeed, female reproductive physiology entails intricate BC, suggesting generation of new beings to stem from the interactions among hormonal, metabolic-energetic, genetic- union of the male’s ejaculate and the female’s menstrual epigenetic, and intra- and extraovarian factors, which in bleeding. More than two millennia after, we now know that coordination modulate the successive development of the reproduction derives from a complex succession of biologic female gamete [5]. Disruptions in any of these components events,wheretheunionofthegametes,spermatozoaand mayleadtoinfertility,analarmingprobleminwomen’sglobal oocytes, plays a fundamental role [1]. health, currently affecting 48.5 million females aged 20– In their earliest stage, gametes originate from specific 44 years [6]. Moreover, alterations of female reproductive cells that abandon their somatic lineage to differentiate into physiology often bear implications in other organ systems, primordial germ cells (PGC), key components in repro- as in the classical example of polycystic ovary syndrome [7]. duction [2]. In female humans, the ovary represents an Beyond the physical and mental implications in women [8], essential structural support for the development of PGC these alterations may also reflect on the ulterior health of their throughout their evolution [3]. Once they have matured into potential offspring [9]. Due to this profound impact in female primordial follicles, a stage reached before birth, and once the well-being and their progeny, this review aims to describe the subject has reached puberty, folliculogenesis begins, a series physiological and molecular phenomena implicated in female of cellular changes necessary for maturation and preparation fertility. 2 Journal of Pregnancy ACT I Prenatal development of ovaries and germ cells (i) Gonadal differentiation (iii) Specification of PGC (v) Formation of final oocyte pool (ii) Migration of PGC (iv) Oogenesis (vi) Entry into oocyte quiescence ACT II Onset of reproductive maturity (i) Adrenarche (iii) Gonadarche Chronology (ii) Pubarche (iv) Thelarche ACT III Folliculogenesis, the ovarian cycle, and menarche PGC: primordial germ cells Figure 1: Main events in the physiologic life course of female reproductive function. Table 1: Approximate values for serum levels of various endocrine mediators at distinct stages in the physiologic life course of female reproductive function. Stage LH FSH Estradiol DHEAS Testosterone Leptin IGF-I (IU/L)a (IU/L)a (pg/mL)a (g/dL)a (ng/dL)a (ng/mL) (g/dL) Prepubertal >0.3 <4 <10 5–40 <20 0.5–11.7b 115–208d Premenarchal ≤12 1–12 <50 35–130 13–44 1.6–12.6c 232–363e Postmenarchal (early follicular phase) 2–11 1–12 20–85 75–255 15–59 5.8–19.2c 251–440e Postmenarchal (midcycle) ≤85 ≤19 ≤350 — — — — LH: luteinizing hormones; FSH: Follicle-Stimulating Hormone; DHEAS: dehydroepiandrosterone sulfate. aBordini and Rosenfield [91]. bEllis and Nicolson [228]. cBandini et al. [229]. dYuksel¨ et al. [230]. eZumbado et al. [10]. 2. Overview of Female Reproductive Function: 3. Act I: The Setup—Prenatal Development of Fertility as a Three-Act Theatre Piece Ovaries and Germ Cells The ovary goes through a wide array of structural and In mammals, the prenatal period is a critical stage for the functional modifications throughout a female’s life, in order functional development of all organ systems. Within the to provide reproductive potential [4]. Figure 1 chronologi- female reproductive sphere, it comprises sexual differentia- cally summarizes the principal events in this timeline. These tion, according to the chromosomal load inherited in syn- processes are subject to regulation by multiple endocrine sig- gamy, and formation of the future female gametes (Figure 2), nals, as reflected in the ample fluctuations in gonadotropin, both coordinated by successive genetic interactions [11]. sex hormone, and other mediators’ serum concentrations throughout various stages of life (Table 1). Nonetheless, 3.1. Gonadal Differentiation. Gametes, spermatozoa and sec- these molecules are only selected representatives from the ondary oocytes, are haploid cells responsible for generation abundance of mediators from many interconnected and of offspring through fecundation, which culminates in the overlapping neuroendocrine regulation systems, where both formation of a single cell, the zygote, whose genome proceeds reproductive and metabolic signals are integrated [10]. from the conjugation of its predecessors’ genomes. From Much like a theatrical play, this sequence may be schema- this pivotal step, zygotes inherit a pair of sex chromosomes tized in three elemental parts or “acts”: (1) the setup: (XX or XY) which will drive the transformation of this embryonic origin and in utero development of the ovary, and cellular unit into a multicellular organism with a sex-specific infantile quiescence; (2) the buildup: ovarian and adrenal phenotype [12]. Once the embryo has attained the definitive reactivation in puberty and neuroendocrine cues initiating organization of germ layers, the urogenital ridge, a thickening sexual maturation; and (3) the climax: molecular mechanisms of coelomic epithelium superimposed on the anterior portion in folliculogenesis and the normal ovarian cycle. of the mesonephros, becomes the gonadal primordium and Journal of Pregnancy 3 Weeks 1-2 Week 3 Weeks 4–6 Gastrulation EM Implantation Specification, migration, and proliferation of PGC Epiblast Epigenetic reprogramming Segmentation DNA demethylation-histone modifications blastulation reactivation of totipotentiality Syngamy Gastrula Blastula Somatic lineage Morula cells Zygote Weeks 7–9 Weeks 10–20 Weeks 21–40 SRY pathway Sertoli cells XY Inhibition of PGC FGF9-CYP26 Mitosis of PGC G1/G0 arrest meiosis Testicular differentiation Sex chromosomes RA Wave of apoptosis Primordial follicles Ovarian differentiation Entry into meiosis XX Meiotic arrest Germ nest formation FOXL2/RSPO1 Arrest in prophase I- pathway diplotene Figure 2: Overview of gonadal differentiation and germ cell development. CYP26: retinoic acid hydroxylases; EM: extraembryonic mesoderm; FGF9: fibroblast growth factor-9; PGC: primordial germ cells. RA: retinoic acid. Syngamy yields a single totipotent cell, the zygote, which subsequently undergoes several proliferative and reorganizational processes. After gastrulation, arrangement into a three-layered embryonic structure, has occurred, nascent PGC undergo induction into pluripotent cells, specification, by EM. PGC also begin migration towards their final residence, the gonadal ridges, whilst simultaneously suffering epigenetic reprogramming essential for reactivation of totipotentiality. Afterwards, according to the sex chromosome load, both PGC and gonads undergo differentiation.InXYsubjects,SRY induces differentiation of Sertoli cells, which thereafter drive testicular differentiation. Likewise, FGF9 and RA hydroxylases inhibit meiosis in these PGC, instead
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