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«Chapter 12 The Oocyte-to-Embryo Transition Scott Robertson and Rueyling Lin Abstract The oocyte-to-embryo transition refers to the process whereby a ...»

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Chapter 12

The Oocyte-to-Embryo Transition

Scott Robertson and Rueyling Lin


The oocyte-to-embryo transition refers to the process whereby a fully

grown, relatively quiescent oocyte undergoes maturation, fertilization, and is converted into a developmentally active, mitotically dividing embryo, arguably one of

the most dramatic transitions in biology. This transition occurs very rapidly in

Caenorhabditis elegans, with fertilization of a new oocyte occurring every 23 min

and the first mitotic division occurring 45 min later. Molecular events regulating this transition must be very precisely timed. This chapter reviews our current understanding of the coordinated temporal regulation of different events during this transition. We divide the oocyte-to-embryo transition into a number of component processes, which are coordinated primarily through the MBK-2 kinase, whose activation is intimately tied to completion of meiosis, and the OMA-1/OMA-2 proteins, whose expression and functions span multiple processes during this transition.

The oocyte-to-embryo transition occurs in the absence of de novo transcription, and all the factors required for the process, whether mRNA or protein, are already present within the oocyte. Therefore, all regulation of this transition is posttranscriptional. The combination of asymmetric partitioning of maternal factors, protein modification-mediated functional switching, protein degradation, and highly regulated translational repression ensure a smooth oocyte-to-embryo transition. We will highlight protein degradation and translational repression, two posttranscriptional processes which play particularly critical roles in this transition.

Keywords Oocyte maturation • Oocyte-to-embryo transition • OMA-1 • MBK-2

• Asymmetric partitioning • Protein degradation • Translational repression • ZIF-1 • 3¢UTR • RNA binding S. Robertson (*) • R. Lin Department of Molecular Biology, University of Texas Southwestern Medical Center, 5323 Harry Hines Blvd, Dallas, TX 75390-9148, USA e-mail: scott.robertson@utsouthwestern.edu T. Schedl (ed.), Germ Cell Development in C. elegans, Advances in Experimental 351 Medicine and Biology 757, DOI 10.1007/978-1-4614-4015-4_12, © Springer Science+Business Media New York 2013 352 S. Robertson and R. Lin

12.1 Introduction The oocyte-to-embryo transition refers to the process whereby a fully grown, relatively quiescent oocyte undergoes maturation, fertilization, and is converted into a developmentally active, mitotically dividing embryo. These events occur in rapid succession and without any apparent delay in Caenorhabditis elegans, suggesting that the molecular events controlling the oocyte-to-embryo transition must be very precisely regulated. The details of oocyte maturation, ovulation, and fertilization are described elsewhere in this issue (Kim et al. 2012, Chap. 10; Marcello et al. 2012, Chap. 11). Our aim in this chapter is not to repeat describing each event occurring during this transition, but instead to focus more on the coordinated temporal regulation of these events. We will discuss selected events associated with oocyte maturation, fertilization, and early embryonic development in order to highlight our current understanding of the complex regulation of this rapid transition and the coordination between processes. We will also take a somewhat “extended” view into embryonic development, up to approximately the 4-cell embryo (Fig. 12.1), in order to incorporate a brief discussion of the transition from maternal-to-zygotic control of development, which we consider the final phase of the oocyte-to-embryo transition.

In C. elegans, an oocyte matures, and then is ovulated and fertilized approximately every 23 min in young hermaphrodites (McCarter et al. 1999). Soon after fertilization, the oocyte-derived nucleus completes two rounds of meiotic division and then replicates its haploid genome (Fig. 12.2) (Begasse and Hyman 2011). The oocyte-derived pronucleus fuses with the sperm-derived pronucleus, which has also just replicated its haploid genome, and the resulting nucleus immediately enters metaphase of the first mitotic cycle. Because C. elegans oocytes do not undergo an arrest in meiosis II after maturation, a stage equivalent to the vertebrate “egg” does Fig. 12.1 Schematic of the oocyte-to-embryo transition in C. elegans. One arm of the bilobed adult gonad is expanded below a cartoon of an adult hermaphrodite. In this chapter, the oocyte-toembryo transition refers to the conversion of a −1 oocyte to a 4-cell stage embryo. Germline and germline blastomeres are shaded in red 12 The Oocyte-to-Embryo Transition 353 Fig. 12.2 Schematic of various events in newly fertilized C. elegans embryos. Morphologically distinct stages between the newly fertilized embryo and the 4-cell embryo are displayed beside a timeline indicating minutes post-fertilization. Germline blastomeres are shaded in red. Small black ovals = polar bodies; stars = centrosomes. Astral microtubules in the first mitotic metaphase embryo are not shown. The time it takes for each step depends on the temperature. Times shown here are at 20–22°C and are derived from Albertson (1984) and McCarter et al. (1999). All embryos are orientated with the anterior to the left in all figures not exist. Therefore, it is more appropriate to use the term “oocyte-to-embryo,” rather than “egg-to-embryo,” transition to describe events in this chapter. Within less than 30 min of fertilization, the 1-cell embryo switches from meiotic divisions to mitotic divisions. Certain meiotic spindle-specific proteins are “toxic” for mitotic spindle formation. Therefore, the proper transition from meiosis to mitosis requires precisely timed turnover of meiosis-specific regulators and synthesis of mitosisspecific regulators. This requires the reproducible execution of a number of interconnected processes in precisely the right sequence within a short period of time, necessitating very tight regulation and coordination.

354 S. Robertson and R. Lin Fig. 12.3 Partitioning of developmental fate during the first two mitotic cycles. Left: A lineage diagram of the first few embryonic divisions. Lineage branches expressing anterior proteins are shown in yellow, posterior proteins in blue, and germline proteins in red. Two sets of schematic drawing of early blastomeres are shown on the right. The first set highlights the separation of germline blastomeres (red) from somatic blastomeres (white). The second set highlights the separation of AB-derived, anterior blastomere fates (yellow) from the P1-derived, posterior blastomere fates (blue). Sister blastomeres are connected by a short black line. Germline blastomeres P0, P1, and P2, as well as the anterior blastomere AB are labeled While zygotic transcription can be detected as early as the 4-cell stage, embryos depleted of the large subunit of RNA polymerase II, AMA-1, exhibit no observable defects in cell divisions until the 28-cell stage (Powell-Coffman et al. 1996).

Therefore, maternally provided proteins and RNAs control the characteristic asymmetric early cleavages, orientation of cleavage planes, and lineage-specific timing of early divisions, as well as all events during the oocyte-to-embryo transition.

The first mitotic division occurs at about 45 min post fertilization and is asymmetric: it always aligns along the long embryonic axis (the anterior-posterior axis) and gives rise to two daughters of different size, molecular make up, and cell fate (Gönczy and Rose 2005) (Fig. 12.3). The site of sperm entry determines the posterior end (Goldstein and Hird 1996). The sperm provides a cue(s) for the asymmetric localization of cortical polarity proteins (PAR), which asymmetrically localize in complexes at the cortex (Wang and Seydoux 2012, Chap 2). Asymmetric distribution of PAR protein complexes determines the position of the mitotic spindle along the A-P axis, as well as the differential localization of many maternally provided proteins. Among these are key regulators for the specification or differentiation of individual tissues as well as regulators guiding cell division patterns. Following the first asymmetric cell division, the posterior daughter, P1, also divides asymmetrically and gives rise to all body-wall muscles but one, the entire intestine, pharyngeal tissues, and germ cells. The anterior daughter, AB, on the other hand, divides symmetrically and goes on to produce mostly skin and neuronal cells. Mislocalization 12 The Oocyte-to-Embryo Transition 355 of these key maternal regulators usually results in abnormal cell specification and embryonic lethality (Draper et al. 1996; Guedes and Priess 1997; Kemphues et al.

1988; Mello et al. 1992; Schubert et al. 2000; Tabara et al. 1999).

The first mitosis is also the first segregation of strictly somatic (AB) versus germline/somatic fate (P1) (Fig. 12.3). The single germline precursor in the C. elegans embryo, P4, is specified very early (reviewed by Wang and Seydoux 2012, Chap. 2; Strome 2005; Strome and Lehmann 2007). After four rounds of asymmetric divisions that begin with the 1-cell embryo, with each division generating a germline blastomere and a somatic sister, P4, along with intestinal precursors, moves into the center of the embryo during gastrulation. Following gastrulation, P4 divides one more time, symmetrically, to produce Z2 and Z3, at the ~100-cell stage. Z2 and Z3 do not divide further until halfway through the first larval stage, and will eventually give rise to the ~2,000 germ cells in the adult. As in all animals, primordial germ cells in C. elegans are subject to transcriptional repression. This repression begins with the first germline blastomere, the 1-cell embryo (Seydoux et al. 1996). Only after the first mitotic division is a blastomere generated (AB) with strictly somatic developmental fate. Therefore, the 1-cell embryo has to retain germline fate (totipotency), which requires that it be transcriptionally silenced, while simultaneously preparing its somatic daughter for activation of lineage-specific zygotic transcription.

Before the first mitotic division, potent regulators for anterior blastomere fates, posterior blastomere fates, and germline blastomere fates coexist within a common cytoplasm. In fact, these maternally provided regulators, with a few important exceptions, are proteins translated in oocytes from maternally provided mRNAs and deposited into the newly fertilized embryo. The 1-cell embryo is therefore faced with the unique problem of keeping the activity of these potent regulators in check before they are segregated to their appropriate blastomere(s) or lineage. The solution to this problem seems to shape much of how C. elegans regulates its oocyte-to-embryo transition.

Molecular events regulating the oocyte-to-embryo transition must be very precisely timed. While we do not have a complete understanding for how these events are coordinated, what has emerged over the last several years is that a relatively small number of key players regulate this process, as well as a clear understanding of the importance of both translational control and protein degradation in regulating this transition. In addition, protein phosphorylation by several maternally supplied kinases plays a pivotal role at multiple points in this transition. These phosphorylation events not only mark several proteins for immediate proteasomal degradation, but also coordinate events by regulating the timing of degradation relative to other parallel processes, such as the cell cycle, during the oocyte-to-embryo transition.

Finally, a protein with multiple distinct functions throughout the oocyte-to-embryo transition is switched from one state to another by a specific phosphorylation.

In this chapter, we divide the oocyte-to-embryo transition into three key components: (1) oocyte maturation, ovulation, and fertilization; (2) the transition from meiosis to mitosis: degradation of MEI-1; and (3) transition from a single-cell embryo to a multicell embryo, and we review our current understanding of these processes.

356 S. Robertson and R. Lin We will emphasize two key factors whose activities are crucial not just for individual processes, but also for coordinating multiple steps within the oocyte-to-embryo transition. In addition, we summarize our current understanding of the roles that protein degradation and translational regulation play during this transition.

12.2 Three Key Components of the Oocyte-to-Embryo Transition 12.2.1 Oocyte Maturation, Ovulation, and Fertilization These topics are described in considerable detail elsewhere in this volume (Kim et al. 2012, Chap. 10; Marcello et al. 2012, Chap. 11), and we direct readers there for a more complete discussion on these topics. Following induction to undergo maturation by the sperm MSP (major sperm protein) signal, the oocyte immediately adjacent to the spermatheca enters meiotic metaphase I, is ovulated through the spermatheca, and is fertilized. After fertilization, the oocyte-derived nucleus completes both meiotic divisions. Two molecular events occur during this stage that are crucial for a proper oocyte-to-embryo transition. First, MBK-2 kinase, a key coordinator for the oocyte-to-embryo transition (see Sect. 12.3.2), is activated (Cheng et al. 2009; Pellettieri et al. 2003; Stitzel et al. 2006). The activation of MBK-2 is dependent upon the completion of meiosis I, and not sperm entry. Upon activation, MBK-2 phosphorylation of several substrates during meiosis II is critical in coordinating the oocyte-to-embryo transition. Sperm entry does trigger many other events, including the block to polyspermy, cortical vesicle release, calcium fluxes, and the second meiotic division (reviewed in Chap. 11, Marcello et al. 2012). Sperm entry also provides the first polarity cue in the embryo (Goldstein and Hird 1996).

C. elegans oocytes do not have inherent polarity. It was shown that sperm entry, by destabilizing the actomyosin network in the surrounding cortex, initiates a flow of cortically localized non-muscle myosin and actin. This cortical flow carries other cortical proteins, including some PAR proteins, to the opposite cortex (Munro et al.

2004). Establishment and maintenance of opposing PAR complexes on the cortex (see Wang and Seydoux 2012, Chap. 2) is crucial for a proper oocyte-to-embryo transition.

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